Advances in Agronomy, Volume 25

ADVANCES IN AGRONOMY VOLUME 25 CONTRIBUTORS TO THIS VOLUME K. BAEUMER W. A. P. BAKERMANS C. BLOOMFIELD J. K. COULT...

Author: N. C. Brady (Editor)

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ADVANCES IN

AGRONOMY VOLUME 25

CONTRIBUTORS TO THIS VOLUME

K. BAEUMER W. A. P. BAKERMANS

C. BLOOMFIELD J. K. COULTER A. E. FOSTER

R. F. HARRIS T. K. HODGES

E. A. HOLLOWELL W. E. KNIGHT G. A. PETERSON

MOSHEJ. PINTHUS J. R. QUINBY J. C. RYDEN

J. K. SYERS

ADVANCES IN

AGRONOMY Prepared under the Auspices of the AMERICAN SOCIETY

AGRONOMY

OF

VOLUME 25

Edited by N. C. BRADY International Rice Research Institute Manila, Philippines ADVISORY BOARD

D. G . BAKER

H. M. LAUDE

G. R. DUTT G . W. KUNZE

M. A. MASSENGALE

D. E. WEIBEL

1973

ACADEMIC PRESS

New York

San Francisco London

A Subsidiary of Harcourt Brace Jovanovich, Publishers

COPYRIGHT 0 1973, BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. N O PART O F THIS PUBLICATION MAY BE REPRODUCED OR TRANSMImED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER.

ACADEMIC PRESS, INC.

111 Fifth Avenue, New York, New York 10003

United Kingdom Edition published by ACADEMIC PRESS, INC. (LONDON) LTD. 24/28 Oval Road, London NWI

LIBRARY OF CONGRESS CATALOG CARDNUMBER:50-5598

PRINTED IN THE UNITED STATES OF AMERICA

CONTENTS CONTRIBUTORS TO VOLUME25 . . . . . . . . . . . . . . . . . . . . . , . . . . . . , . . . . . . . . . . . .

ix

PREFACE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

xi

PHOSPHORUS IN RUNOFF AND STREAMS

J. C. RYDEN,J. K. SYERS,AND R. F. HARRIS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1

11. Terminology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Factors Affecting the Dynamics of Phosphorus in Runoff and Streams . .

2

.

IV. Phosphorus Loads in Runoff and Streams . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Impact of Phosphorus Carried in Streams on Standing Waters . . . . . . . . . VI. Present Status and Outlook . . . , . , . . . . . . . . , . . , . . . . . , . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

4

20 37 38 41

CRIMSON CLOVER

W. E. KNIGHTAND E. A. HOLLOWELL

I. 11. 111.

...............................................

Morphology . . . . . . . . . . . . . . . . . . . ................. . . . . ... .. .. .. .. Physiology . , . . . . . . . . . . . . . , . . . Culture . . . . . . . ... . . .. . ............... .. Utilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

IV. V. VI. VII. VIII. Conclusions

..,............

48 50 52

57 65 68

....................................

. . . . .. . . . . . .. . .. . . .

........................ ...............................................

12 73

ZERO-TILLAGE

K. BAEUMERAND W. A. P. BAKERMANS 1. Introduction: The Concept of Zero-Tillage

. . . . . . . . . . . . . . . . . ... . . . . . .

11. Comparison of Environmental Conditions in Tilled and Untilled Soils . . . 111. Effects of Zero-Tillage on Plant Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . .

IV. Crop Husbandry . . . . . , . . . . . , . . . , . . . . . . . . . , . . . . , . . . . . . . . . . . . . . . . . V. Evaluation of Zero-Tillage in Farming Systems . . . . . . . . . . . . . . . . . . . . . . VI. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V

78 80 95 103 113 119 120

vi

CONTENTS

THE GENETIC CONTROL OF FLOWERING AND GROWTH IN SORGHUM

J. R. QUINBY

................

I. 11. 111. The Floral Stimulus

IV. V. VI. VII. VIII. IX. X. XI. XII.

..

Implications to Plant Breeding References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

160

ION ABSORPTION BY PLANT ROOTS

T. K. HOLXES I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Overview of Nutrient Absorption by Roots . . . . . . . . . . . . . . . . . . . . . . . . . Energy-Dependent and Active Ion Transport . . . . . . . . . . . . . . . . . . . . . . . Kinetics and Selectivity of Ion Absorption . . . . . . . . . . . . ......... Energetics of Ion Transport . . . . . . . . . . . . . . . . . . . . . . . . Proposed Model for Ion Absorption by Roots . . . . . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . ................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

11. 111. IV. V. VI. VII.

163 164 167 180

198 201 202

LODGING IN WHEAT, AND OATS: THE PHENOMENON, ITS CAUSES, AND PREVENTIVE MEASURES

MOSHEJ. PINTHUS I. 11. 111. IV. V. VI. VII. VIII.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Description and Causes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Effects of Lodging on Crop Development and Yield . . . . . . . . . . . . . . . . Plant Characters Associated with Lodging . . . . . . . . . . . . . . . . . . . . . . . . . Environmental and Agronomic Factors Affecting Lodging . . . . . . . . . . . Prevention of Lodging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Breeding for Lodging Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Increased Exploitation of Yield-Promoting Factors Due to the Prevention of Lodging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References ...................................................

210 21 1 217 223 23 1 23 8 246 254 256

vii

CONTENTS

GENESIS AND MANAGEMENT

OF ACID SULFATE SOILS

C. BLOOMFIELDAND J. K. COULTER

I. Introduction . . . . . . . . . . . . . . . . . . . . ..................... 11. The Formation of Sulfides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Oxidation of Sulfides . . . . . . . . . . ........... IV. Mining and Corrosion Problems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Classification and Mapping . . . . . . .............. VI. Conditions for Plant Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VII. Management for Agriculture ......... VIII. Analysis of Pyritic Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IX. Conclusions . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

266 267 278 290 292 296 3 08 3 15 318 319

MALTING BARLEY I N THE UNITED STATES G. A. PETERSON AND A. E. FOSTER

I. 11. 111.

IV. V. VI. VII. VIII. IX. X. XI. XII.

Classification of Cultivated Barleys of the United States

Quality Testing P Barley Varieties XI11. Malting Barley Pr References . .

cceptable Malting

.............................. .........................

364 375

AUTHORINDEX . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . SUBJECTINDEX . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

379 398

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CONTRIBUTORS TO VOLUME 25 Numbers in parentheses indicate the pages on which the authors' contributions begin.

K. BAEUMER(77), Faculty of Agriculture, University of Goettingen, Goettingen, Federal Republic of Germany W. A. P. BAKERMANS (77), Institute for Biological and Chemical Research of Field Crops and Herbage, Wageningen, The Netherlands C. BLOOMFIELD (265 ) , Rothamsted Experimental Station, Harpenden, Herts, England J. K. COULTER( 2 6 5 ) , Rothamsted Experimental Station, Harpenden, Herts, England A. E. FOSTER(327), Department of Agronomy, North Dakota State University, Fargo, North Dakota R. F. HARRIS( 1 ) , Department of Soil Science, University of Wisconsin, Madison, Wisconsin T. K . HODGES(163), Department of Botany and Plant Pathology, Purdue University, Lafayette, Indiana E. A. HOLLOWELL (47), W.S. Department of Agriculture, Beltsville, Maryland W. E. KNIGHT (47), U.S. Department of Agriculture, Mississippi State, Mississippi 0.A. PETERSON (327), Department of Agronomy, North Dakota State University, Fargo, North Dakota MOSHEJ. PINTHUS(209), The Hebrew University of Jerusalem, Faculty of Agriculture, Rehovot, Israel J. R. QUINBY ( 125 ) , Pioneer Hi-Bred Company, Plainview, Texas J. C. RYDEN(1 ), Department of Soil Science, University of Wisconsin, Madison, Wisconsin" J. K. SYERS( I ) , Department of Soil Science, University of Wisconsin, Madison, Wisconsin"

* Present address: Department of Soil Science, Massey University, Palmerston North, New Zealand. ix

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PREFACE

Dramatic reductions during the past two years in the world food supply have jolted a complacent world into the realization that the food-population race remains unquestionably the most critical problem facing mankind. Population growth continues at alarming rates in those countries where food supplies are already inadequate. Food shortages are plaguing not only the poor countries where hunger, malnutrition, and starvation are a way of life, but have now reached the more affluent nations. Even the United States which for a generation has sought through public programs to limit crop production is now concentrating on programs to increase food supply. Once again tillers of the soil, and the crops and animals which supply our food have high national priorities. In this time of international concern over food supply, reviews of scientific advancement such as those contained in this volume are most reassuring. Papers contained in this volume are concrete evidence of the contribution of crop and soil scientists to mankind’s efforts to feed himself. Four of the papers deal with crops. One is concerned with research on crimson clover, a legume grown in the southern part of the United States and a plant which is most important to a growing animal industry in this area. Remarkable progress is reported on knowledge gained from the breeding of sorghum, a plant which is rapidly becoming a major crop in the semi-arid regions throughout the world. Factors affecting the lodging of small grains is the subject of one review. Recent advances in research on malting barley, a crop of expanded acreage and of increasing quality expectations is the subject of the fourth crops article. The reviews of advances in soil science are certainly not unrelated to crop production. The mechanisms of ion absorption by plant roots are the subject of one review. Plant root growth is one of the phenomena considered in the critical analysis of the practice of zero-tillage made by scientists who have devoted much of their research efforts to this cultural practice. Phosphorus accumulation in streams and lakes fed by runoff from agricultural lands is the subject of another review. The need to prevent environmental contamination from agricultural chemicals is considered. The genesis and management of acid sulfate soils, which occupy millions of acres of coastal areas in warm and hot humid climates are discussed. These soils are important especially to the rice growing areas of the world. The international focus of this journal is maintained not only by the nature of the subjects covered but by the selection of authors to write the reviews. Food production is truly an international problem to which crop and soil scientists throughout the world are addressing their attention.

N. C . BRADY xi

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PHOSPHORUS IN RUNOFF AND STREAMS J. C. Ryden,' J. K. Syers,' and R. F. Harris Department of Soil Science, University of Wisconsin, Madison, Wisconsin

I. Introduction 11. Terminology

..................................................... . ...................... .............................

......................

B. Forms of 111. Factors Affecting

in Runoff and Streams

......................

B. Chemical Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Phosphorus Loads in Runoff and Streams . A. Influence of Point Sources on Phosphorus in Streams . . . B. Runoff from Forest Watersheds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Runoff from Agricultural Watersheds D. Runoff from Land Associated with Ani E. Urban Runoff . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Impact of Phosphorus Carried in Streams on Standing Waters . . . . . . VI. Prcsent Status and Outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I.

1 2 2 4 4 4

7 20. 21 22 25 32 33 37 38 41

Introduction

Increasing evidence suggests that phosphorus ( P ) in surface waters is a primary factor controlling the eutrophication of water supplies (Ohle, 1953; Mackenthun, 1965; Stewart and Rohlich, 1967; Vollenweider, 1968; Lee, 1970). Assessment of the relative contribution of the different sources of P to surface waters (Fig. 1 ) is of critical importance for implementation of control measures to prevent or reverse P-induced eutrophication. Although the importance of runoff and streams as major sources of P to standing waters is well recognized, little attempt has been made to differentiate between and quantify the P forms in runoff and streams which are of potential importance with respect to their impact on the biological productivity of standing waters. Furthermore, little emphasis has been placed on the reactions that may occur between dissolved inorganic P and Present address: Department of Soil Science, Massey University, Palmerston

North, New Zealand. 1

2

J. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

the solid phases with which it is in contact in runoff and streams, as pointed out by Taylor ( 1967) and Biggar and Corey (1969). Critical concentration limits have been suggested for P in surface waters which, if exceeded, will lead to excessive biological productivity (Sawyer, 1947; Mackenthun, 1968). In this review, however, rather than emphasizing critical concentrations, P in runoff and streams will be discussed mainly from the standpoint that any P load constitutes a potential increase in the P fertility of surface waters.

II.

Terminology

A. HYDROLOGY AND PHOSPHORUS SOURCES This review will use essentially the definitions proposed by Langbein and Iseri ( 1960). Watershed (drainage basin; catchment area). A part of the surface of the earth that is occupied by a drainage system, which consists of a surface stream, or a body of standing (impounded) surface water, together with all tributary surface streams and bodies of standing surface water. Stream. A general term for a body of flowing water. In hydrology the term is usually applied to the water flowing in a natural channel. Stream flow. The discharge (of water) that occurs in a natural channel. Runoff.That part of precipitation that falls on land and ultimately appears in surface streams and lakes. Runoff may be classified further according to its source. Surface runoff (overland flow). That part of rainwater or snowmelt which flows over the land surface to stream channels. Surface runoff may also enter standing waters directly or be consolidated into artificial channels, e.g., storm sewers in urban areas (urban runoff), before entering a stream or body of standing water. Subsurface runoff (storm seepage). That part of precipitation which infiltrates the surface soil and moves toward streams as ephemeral, shallow, perched groundwater above the main groundwater level. In many agricultural areas subsurface runoff may be intercepted by artificial drainage systems, e.g., tile drains, accelerating its movement to streams. Groundwater run08 (base runoff). That part of precipitation that has passed into the ground, has become ground water, and is subsequently discharged into a stream channel or lake as spring or seepage water. In addition to runoff, the other potential contributors to streams and standing waters are precipitation incident on the water surface and industrial and sewage effluents (Fig. 1 ) .

PHOSPHORUS IN RUNOFF AND STREAMS

3

McCarty (1967) and Vollenweider ( 1968) have made a useful division of sources of P to surface waters based on the ease of quantification. Point sources enter at discrete and identifiable locations and are therefore amenable to direct quantification and measurement of their impact on the receiving water. Major point sources include effluents from indus-

FIG. 1. Schematic representation of the relationships between phosphorus sources and runoff, streams, and standing waters.

trial and sewage-treatment plants (Fig. 1) . Diffuse .wurces may be defined as those which at present can be only partially estimated on a quantitative basis and which are probably amenable only to attenuation rather than to elimination. Diffuse sources require the most investigative attention. Vollenweider ( 1968) further divided diffuse sources into: 1. Natural sources such as eolian loading, and eroded material from virgin lands, mountains and forests. 2. Artificial or semiartificial sources which are directly related to human activities, such as fertilizers, eroded soil materials from agricultural and urban areas, and wastes from intensive animal rearing operations. The loads of P imparted to runoff and streams from natural diffuse sources provide a datum line against which the magnitude of P loads from artificial sources may be compared.

4

J. C. RYDEN, J. K.

SYERS, AND

R. F. HARRIS

B. FORMS OF PHOSPHORUS

In natural systems, P occurs as the orthophosphate anion (Pod3-)which may exist in a purely inorganic form (H2P0,- and HP0,2-) or be incorporated into an organic species (organic P ) . Under certain circumstances inorganic orthophosphate may exist as a poly- or condensed phosphate. A secondary distinction is made between particulate and dissolved forms of P, the split conventionally being made at 0.45 pm. Other terminology used is as follows: Total P . All forms of P in a runoff or stream sample (dissolved and particulates in suspension) as measured by an acid-oxidation treatment (e.g., acid ammonium persulfate). Dissolved inorganic P . P in the filtrate after 0.45 pm separation determined by an analytical procedure for inorganic orthophosphate. Organic P . P that may be determined within the dissolved and particulate fractions by the difference between total P and inorganic P. Ill.

Factors Affecting the Dynamics of Phosphorus in Runoff and Streams

Before evaluating the magnitude of various P sources in terms of the loads of P in runoff and streams, and the extent to which previous studies of P loadings enable an adequate definition of P sources, it is important to understand the physical and chemical factors affecting the dynamics of P in runoff and streams. These factors determine not only the movement of P into runoff and streams, but also its distribution between the aqueous and particulate phases. A.

PHYSICALFACTORS

All terrestrially derived diffuse sources of P are associated with the movement of water in contact with a solid phase. The solid phase may be stationary with respect to water flow, or may move in the flow at some speed equal to or less than the flow. Precipitation disposed of as subsurface or groundwater runoff is primarily in contact with a stationary solid phase, namely the soil profile and, in the case of groundwater runoff, possibly the bedrock. Consequently, the amounts and concentrations of P carried in subsurface and groundwater runoff will be influenced by the time of contact with any component in the soil profile capable of interacting with dissolved P in the percolating water and by the concentration of dissolved P that the soil components maintain in the soil solution. Time of contact between the percolating solution and any soil component will in turn depend on the rates of infiltration and percolation into and through the soil.

PHOSPHORUS IN RUNOFF AND STREAMS

5

Some of the theories developed to describe water movcment in soils can be applied to evaluate the potential loss of P from various soil types as a result of subsurface runoff. Gardner (1965) developed equations to describe the movement of nitrate in the soil profile due to leaching. The chemical interactions that occur between dissolved inorganic P and soil components (discussed later), when water percolates through the soil, must also be taken into consideration. Inclusion of a term in the equations developed by Gardner (1965) to describe the relationship between P in particulate and aqueous phases is therefore necessary. This could take the form of a linear adsorption isotherm relevant to the concentrations of dissolved inorganic P maintained in the solution of a particular soil. Biggar and Corey (1969) have also reviewed the literature on infiltration and percolation of water in agricultural soils as it pertains to nutrient movement. The movement of solid phase material in contact with natural waters occurs during surface runoff and in streams. The amounts of solid material capable of entering surface runoff will depend on the intensity of rainfall, physical and chemical attachment between various solid components, and the amounts and energy of runoff waters (Guy, 1970). It is the energy of surface runoff or stream water, however, that governs the amounts of a specific size fraction of particulate materials which will remain in suspension during water flow. The primary source of particulate material to surface runoff and streams is eroding soil (Guy and Ferguson, 1970), although in urban areas with little ongoing development, particulates may be dominated by specifically urban detrital material (e.g., street litter and dust) and organics derived from urban vegetation. The total on-site losses of soil due to sheet and rill erosion are not necessarily delivered to streams. The amount of sediment that travels from a point of erosion to another point in the watershed is termed the sediment yield (Johnson and Moldenhauer, 1970). Consequently the Universal Soil Loss Equation used to predict field soil losses on an average annual basis (Wischmeier and Smith, 1965) must be corrected when used to predict sediment loads in streams because deposition of particulates may occur on the land surface as a result of slope variations before surface runoff reaches a stream. It is for this reason that estimates of soil loss in surface runoff from sites within a particular watershed cannot be translated into total P losses through a knowledge of the total P content of the soil, if the P loss is to be related to P enrichment of surface waters. An associated complication arises from the fact that soil P is primarily associated with the solid phase. As soil erosion is a selective process with respect to particle size, selectivity has been observed for P loss in surface

6

J. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

runoff. The extent of the selectivity depends on the particle sizes with which most of the soil P is associated. This observation has led to the concept of enrichment ratios (ER) , which for P are calculated as the ratio of the concentration of P in the particulate phase of surface runoff to the concentration of P in the source of the particulate phase. This effect was first considered by Rogers (1941), who observed ER values of 1.3 for total P and 3.3 for “0.002 N H,SO, extractable” P for a silt loam situated on a 20-25% slope. Other values range from 1.5 to 3.1 for total P (Knoblauch et al., 1942; Neal, 1944; Stoltenberg and White, 1953), whereas Massey and Jackson (1952) observed values between 1.9 and 2.2 for “water-soluble plus pH 3 extractable” P for silt loams in Wisconsin. The selective nature of surface runoff with respect to P is due to selective removal of fine soil particulates as a result of the energy limitations of runoff and the fact that a large percentage of total soil P is frequently associated with clay-sized material (Scarseth and Chandler, 1938; Williams and Saunders, 1956; Syers et al., 1969). Greater selectivity of fines and consequently particulate P will occur as the energy of surface runoff decreases. Stoltenberg and White (1953) observed that as precipitation disposed of through surface runoff decreased from 70 mm to 0.25 mm per hour, the clay content of eroded material from a soil with a clay content of 16-18% increased from 25% to 60%. This has obvious implications in relation to the nature of the sediment load carried by a stream and the interactions of P between the solid and aqueous phases, particularly during periods of surface runoff. It should be pointed out, however, that although the P content of the sediment load may increase as surface runoff diminishes, as may be predicted from the work of Stoltenberg and White (1953), the total P load may not change, or may even decrease, owing to lower sediment loads. The particulate material carried in streams may be divided into bed load and wash or suspended load. The bed load, which may also have a contribution from existing stream sediment, is that which moves along or close to the stream bed, whereas the wash load is maintained in the flow by turbulence (Johnson and Moldenhauer, 1970). By inference from the selectivity of surface runoff for fine soil particulates, the wash load will be high during surface runoff events. Furthermore, Johnson and Moldenhauer (1970) suggested that the wash load travels at about the same velocity as the water with which it is in contact. Consequently, P associated with the clay- and silt-sized particulates constituting the wash load will move between any two points in the stream profile at the same speed as the ambient dissolved forms of P. Increased turbulence in streams during high flow, or arising from an increasing gradient, will tend to maintain in suspension particle sizes more

PHOSPHORUS IN RUNOFF AND STREAMS

7

characteristic of the bed load, and may even resuspend existing stream bed sediment. In a study of total P loads in the Pigeon River, North Carolina, Keup (1968) noted that an increase in gradient from 2.81 to 4.35 m/km, over which no tributaries entered the main stream, resulted in a 90.8 kg/day increase in the total P load carried. It appears that in the majority of cases a large proportion of particulate P in streams arises from soil erosion. Phosphorus may be stored in stream bed sediments, but unless the stream is actively aggrading, the amount of P stored will be less than the inflow (Keup, 1968). That which is stored is liable to resuspension and transport owing to turbulence during periods of high flow.

B. CHEMICAL FACTORS 1 . Nature of Soil P Soil P may be divided into two broad categories: inorganic P, namely, that associated with soil mineral particles; and organic P, which forms an integral part of the soil organic matter fraction. a. Inorganic P . O n the basis of solubility product criteria, it has been postulated that discrete phase crystalline Fe and A1 phosphates exist in noncalcareous soils (Kittrick and Jackson, 1956; Hemwall, 1957; Chakravart and Talibudeen, 1962). The general occurrence of discrete Fe and A1 phosphates seems doubtful on the basis of the ion product data presented by Bache (1964) and the experimental observations of Hsu (1964). It is now generally accepted that secondary inorganic P in many soils exists primarily in association with oxides and hydrous oxides of Fe and Al, as surface-bound forms or within the matrices of such components. However, that discrete Fe and A1 phosphates are formed as temporary phases in the vicinity of phosphate fertilizer particles due to conditions of localized high acidity and P concentration is well established (Lindsay and Stephenson, 1959; Huffman, 1969). Such compounds will not be stable as the dissolved inorganic P concentration in the soil solution or aqueous portion of other soil-water ecosystems decreases. The calcium phosphate mineral, apatite (Shipp and Matelski, 1960) and calcic fertilizer-soil reaction products (Huffman, 1969) have been identified in soils. The amounts of apatite are appreciable only in weakly weathered soils (Williams et al., 1969), as predicted by the weathering indices of Jackson ( 1969). Calcic fertilizer-sail reaction products may be present in neutral and calcareous surface soil horizons, and their importance in maintaining high concentrations of dissolved inorganic P in soil-water ecosystems should not be overlooked.

8

J. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

Consequently three basic forms of inorganic P may exist in unfertilized soils (Syers and Walker, 1969; Williams and Walker, 1969): apatite, which is a discrete phase P compound; P sorbed on the surfaces of Fe, Al, and Ca soil components (nonoccluded); and P present within the matrices of Fe and A1 components (occluded). In fertilized soils, a variety of P fertilizer-soil reaction products may exist as transient phases. As the solubility product of pure apatite in water is low (0.03 pg per milliliter at pH 7, Stumm, 1964) and the P held within the matrices of Fe and A1 components is virtually chemically immobile, except under reducing conditions in the case of Fe, major emphasis should be directed toward the reactions involving P in solution and that sorbed on the surfaces of Fe, Al, and Ca components as well as the release of P due to dissolution of fertilizer-soil reaction products. b. Organic P. Elucidation of the composition of soil organic P is restricted by lack of extractants capable of removing organic P from soils in a relatively unaltered form and by the inadequacy of current methods for mildly degrading extracted organic P-organic matter complexes. Existing data indicate that most of the organic P in soils is associated, in an ill-defined manner, with the humic and fulvic acid complex of soil organic matter (Anderson, 1967). Of the specific forms of organic P that have been identified in soils, inositol phosphates are present in largest relative amounts, comprising up to 60% of the total organic P (Anderson, 1967; Cosgrove, 1967; McKercher, 1969). Other specific organic P compounds are present in soil in much lower quantities: nucleic acids account for 5-lo%, and other phosphate esters, such as phospholipids, sugar phosphates, and phosphoproteins, for less than 1-2% (McKercher, 1969). 2. Sorption of Dissolved P by Soils Whenever water containing a particular concentration of dissolved P comes into contact with soil material, there is a possibility for sorption, desorption, or dissolution reactions to take place. The types of reactions are the same regardless of whether they occur under conditions existing in the soil profile, surface runoff, or streams. Although in some cases biological assimilation may initially affect the distribution of P between dissolved and particulate phases of soil-water systems, the distribution of P between these phases will be determined by the nature of the inorganic particulates and the concentrations of dissolved P in solution (Keup, 1968; McKee et al., 1970; Ryden et al., 1972b). a. Inorganic P. It has been demonstrated that the uptake or sorption of P from solution by soils is significantly related to the presence of shortrange order (amorphous) oxides and hydrous oxides of Fe and A1 (Williams et al., 1958; Gorbunov et al., 1961; Bromfield, 1965; Hsu, 1964; Saunders, 1965; Syers et al., 1971). Furthermore, “pure” oxides and hy-

PHOSPHORUS IN RUNOFF AND STREAMS

9

drous oxides of Fe and Al, and short-range order aluminosilicates have also been shown to be particularly effective in the sorption of inorganic P from solution (Gastuche et al., 1963; Muljadi et al., 1966; Hingston et al., 1969). The sorption of inorganic P by Fe and A1 oxides and hydrous oxides is known to be rapid, as is the sorption of P by soils. Furthermore, short-range order Fe and A1 oxides and hydrous oxides are ubiquitous in soils (Hsu, 1964), their relative amounts depending on parent material, climatic and drainage conditions, and occur mainly as coatings on other soil components. Shen and Rich (1962) and Jackson (1963) have noted the occurrence of A1 hydroxypolymers and Dion (1944), and Roth et al. ( 1969) have reported the presence of F e oxide and hydrous oxide coatings on clay mineral surfaces. Such coatings, in conjunction with the greater surface area of the clay fraction compared to that of the other particle-size fractions in a soil, explain the observation of Scarseth and Chandler (1938) that up to 50% of the total P in soils may be associated with the the clay fraction, as well as the enrichment ratio effect for P as a result of soil erosion. Attempts have been made to correlate P sorption with the clay content of soils (Williams et al., 1958). Correlations between P sorption and clay content after removal of Fe and A1 oxides and hydrous oxides often have been poor. Better correlations may be expected if P sorption is related to the content of water-dispersed clay. The sorption of P by water-dispersed clay and silt of soils has obvious implications to reactions occurring between dissolved and particulate P in surface runoff and streams. Sorption of inorganic P by CaC03 has also been demonstrated (Cole et al., 1953). The nature of the surfaces of calcite in calcareous soils may be very different from those of pure calcite (Buehrer and Williams, 1936; Lahav and Bolt, 1963; Syers et al., 1972). The sorption of dissolved inorganic P by soils may be described by sorption isotherms similar to that shown in Fig. 2. Numerous workers have also shown that sorption may be described by some of the adsorption isotherms developed to describe gas adsorption by solids (Russell and Prescott, 1916; Olsen and Watanabe, 1957; Rennie and McKercher, 1959; Syers et al., 1973). Similar observations have been made for the sorption of inorganic P by soil components such as kaolinite and short-range order Fe and A1 oxides and hydrous oxides (Gastuche et al., 1963; Muljadi et al., 1966; Kafkafi et al., 1967). Although these studies have been useful in describing relationships between various soils and soil components with respect to their P sorption capacities, they have provided little information regarding P sorption behavior from solutions containing the low dissolved inorganic P concentrations characteristic of most soil-water ecosystems, largely because of the high levels of added P used (Ryden et al., 1972b). Furthermore, Syers et al. (1973) obtained two linear Langmuir relation-

10

J. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

sorbed ( f )

APon sol I

released (3

FIG.2. Typical isotherm for the sorption of added inorganic phosphorus by a soil. E = equilibrium P concentration. (From White and Beckett, 1964.)

ships which intersected at equilibrium P concentrations varying from 1.5 to 3.2 pg P/ml, for three contrasting soils-an observation that probably invalidates interpretations of P sorption made from many previous studies where high levels of added P were used. The study of White and Beckett (1964), conducted at initial dissolved inorganic P concentrations, comparable to those existing in soil-water ecosystems, provides a useful basis for understanding the interactions between aqueous and particulate phases of P in runoff and streams. Figure 2 illustrates the principle of the approach used. White and Beckett (1964) defined the intersection of the P sorption isotherm and the abscissa, the “equilibrium phosphate potential” ( 5 p C a pH,PO,) , abbreviated to “equilibrium P concentration” by Taylor and Kunishi ( 1971) . The intersection is equivalent to the inorganic P concentration in the ambient aqueous phase when there is no net sorption or release of P, i.e., AP = 0. This is a point of reference which provides a predictive estimation of sorption or release of P should the P concentration in solution change. Furthermore, the average slope of the sorption curve over a given final P concentration range provides information on the ability of the soil to maintain the P concentration at the equilibrium P concentration. The steeper the slope, the closer will the final P concentration be to the equilibrium P concentration. The slope of the curve, although not related to total P sorbed, is related to the extent to which that soil may sorb P over the concentration range considered. The potential of this approach in predicting the chemical mobility of P in soil-water systems is clearly evident and has been used with regard to streams by Taylor and Kunishi (1971) and Ryden et al. (1972a,b) for rural and urban soils, respectively. The desorption of sorbed P from soils is not as simple as may be inferred from the sorption-release relationships obtained by White and

+

PHOSPHORUS I N RUNOFF AND STREAMS

11

Beckett (1964). In fact very few studies have been reported regarding the desorption of sorbed P, and those reported by Syers et al. (1970) and Ryden et al. (1972a), involved desorption following sorption of P from solutions containing P concentrations in excess of those commonly found in soil-water ecosystems. In studies involving the sorption of P by kaolinite from solutions containing realistic inorganic P concentrations, Kafkafi et al. (1967) observed that initially all the sorbed P was isotopically exchangeable. During a subsequent washing or desorption step, however, a portion of the sorbed P became nonexchangeable, or “fixed,” this portion being dependent upon the amount of P sorbed, the number of washings, and the nature of the previous P sorption cycle. Sorption of P was represented by either onestep sorption from a range of solutions of different initial P concentration or by successive additions of small amounts of dissolved inorganic P. Both these types of P sorption, as well as an effect analogous to washing, could occur in soil-water ecosystems. 6. Organic P . Although the mechanisms involved in the retention of organic P by soils have not been established fully, there is evidence that inositol hexaphosphate, and possibly other organic P compounds, are retained by a precipitation rather than a sorption reaction. Nevertheless, removal of dissolved organic P from solution appears to be a rapid process. Pinck et al. (1941 ) reported that many commonly occurring water-soluble organic phosphates, e.g., salts of glycerophosphate, hexose diphosphate, and nucleic acids, become nonextractable with water at almost the same rate and as completely as dissolved inorganic P. The retention of water-soluble organic P by sorption reactions may occur by at least two basically different mechanisms (Sommers et al., 1972). Goring and Bartholomew (1950) observed that removal of “free iron oxides” considerably reduced the amount of fructose 1,6-diphosphate sorbed by subsoil material, suggesting that the sorption of organic P may occur through orthophosphate groups by a similar mechanism to that for inorganic P. It is also possible that organic P can be retained by interaction of the organic moiety of the phosphate ester with inorganic soil components. For example, nucleic acids and nucleotides are protonated at pH 5 (Jordan, 1955) and could consequently be retained on clay surfaces by displacement of exchangeable cations. Furthermore, physical adsorption, also through the organic portion of the molecule, is possible, particularly if the molecular weight of the compound is high, as suggested by Greenland (1965). In such cases retention is weak and is accomplished by van der Waals and ion-dipole forces. Greaves and Wilson (1969) have implicated physical adsorption in the retention of nucleic acids by montmorillonite. It is also possible that retention occurs indirectly through other

12

J. C . RYDEN, J. K. SYERS, AND R. F. HARRIS

soil organic compounds such as fulvic and humic acids after interaction of organic phosphates with these species (Martin, 1964). The desorption of sorbed organic P has not been extensively studied. The hypothesis that inorganic P added to soils displaces sorbed organic P to solution (Latterell et al., 1971) was not supported by the data presented by Wier and Black (1968). Although organic P may be leached from soils, it appears that a large proportion of that removed may not be in a dissolved form. After incubating sucrose with ammonium nitrate in the upper portion of a calcareous soil, Hanapel et al. (1964) found that most of the organic P removed by leaching was present in a particulate rather than a dissolved form. 3. Chemical Aspects of P in Subsurface and Groundwater Runoig Losses of P in subsurface and groundwater runoff have been considered minimal in the past, but, as will be discussed later, such losses can amount to a significant proportion of losses from agricultural land, and possibly a major proportion from forest lands. The supposition that P losses in subsurface and groundwater runoff are low probably stems from the concept of P immobility based on the P sorption properties of soils using added inorganic P concentrations far in excess of those normally present in the soil solution. It is of interest to note that many of the reported mean concentrations of dissolved inorganic P in subsurface runoff are within the range of values expected to be maintained in the soil solution. Pierre and Parker (1927) reported values ranging from 0.020 to 0.350 pg P/ml, with an average of 0.090 pg/ml, for several surface soils from the southern and midwestern states of the United States. These workers also noted that dissolved inorganic P concentrations could be maintained at a fairly constant level. Barber et al. (1963) reported similar values for the upper 15 cm of 87 soils from the midwestern United States, with an average of 0.180 pg of P per milliliter; the frequency distribution of the values obtained, however, suggested a mode of between 0.040 and 0.060 pg of P per milliliter. As water percolates through the soil profile, there tends to be a “chemical sieving” of dissolved inorganic P (Black, 1970). This arises as a result of the sorption of inorganic P by soil components. The low concentrations of P found in groundwater runoff, which has experienced the maximum effects of deep percolation with concomitant increase of contact with P-deficient particulates of the subsoil, are undoubtedly a direct result of the chemical sieving effect. The principle of this effect is illustrated by other data presented by Barber et al. (1963). For the same 87 soils mentioned previously, the average dissolved inorganic P concentration at a depth of 46-61 cm was 0.089 pg/ml, less than half that for the upper

PHOSPHORUS IN RUNOFF AND STREAMS

13

0-15 cm. Another illustration is observed in results presented by Ryden et al. (1972a) for the P sorption properties of successive soil horizons of a Miami silt loam profile. The concentrations of dissolved inorganic P maintained in solution after shaking with solutions of different initial added inorganic P concentrations at a solution: soil ratio of 40: 1 are given in Table I. TABLE I Dissolved Inorganic Phosphorus (P) Concentrations Maintained by Soil IIorizoiis of Miami Silt Loam after Equilibration with Solutions of Different Initial Added Inorganic P Concentrationsn

Horizon

Depth (cm)

Initial P conc. (ccg/ml)

Final P coiic. (/*g/mU

A1

0-15 15-38 56-66

0.0 0.471 0.030

0.471 0.030 0.007

B1 3C1

~

Data extrapolated from Ryden et

(11.

(197‘2a).

The concentration of dissolved inorganic P in subsurface and groundwater runoff will depend on the nature and amounts of P-retaining components in the profile, the surface area exposed to percolating waters, and the ease of percolation which affects the contact time of dissolved inorganic P with the retaining components. In studies of P leaching through columns of organic soils in the laboratory, Larsen et al. (1958) observed that P retention, measured by srP autoradiographs, was closely correlated with the total hydrous Fe and A1 oxide (“sesquioxide”) content. Similarly, losses of P due to leaching through a deep siliceous sandy soil were demonstrated in W. Australia by Ozanne (1963). When 225 kg/ha of 32P-labeled superphosphate was broadcast during winter on a fallow sandy soil, over 50% of the P had penetrated to more than 1 m below the surface within 38 days, during which 230 mm rain had fallen. Ozanne (1963) also demonstrated that the potentially large losses of P to subsurface and groundwater runoff from sandy soils compared to that from loamy soils were due to quantitative rather than qua1itativ.e differences in P-retaining components. Although major emphasis has been placed on P losses in surface runoff, it appears that losses of P to subsurface and groundwater runoff, although of little significance from an agricultural standpoint, may under certain conditions constitute a significant loss of P from agricultural watersheds in terms of the P enrichment of surface waters, as will be discussed

14

J. C. RYDEN, J . K . SYERS, AND R. F. HARRIS

later. Losses of P to subsurface and groundwater runoff are even more difficult to evaluate than those in surface runoff and demand further investigative attention.

4 . Chemical Aspects of P in Streams As discussed previously, surface runoff from agricultural land constitutes a heterogeneous and relatively short-lived system. Any attempt to consider the distribution and chemical mobility of P between solid and aqueous phases before entry into the receiving stream would be pointless as a new and more homogeneous system is rapidly established. Surface runoff in urban areas is somewhat different because in most cases it is channelized shortly after origin by alteration of surface drainage patterns; under such circumstances it is analogous to a stream in an artificial channel. Consequently, the chemical mobility of P will be discussed from the standpoint of the stream environment. The potential of suspended particulates derived from eroding soil to modify the dissolved inorganic P concentration of streams has been suggested by Taylor ( 1967) and Biggar and Corey (1969). Wang and Brabec (1969) also implied that inorganic P was sorbed by suspended particulate material from observations of dissolved inorganic P concentrations in the Illinois River at Peoria Lake. An evaluation of the possible effects of eroded soil materials on the dissolved inorganic P concentrations of streams may be obtained from P sorption studies (Taylor and Kunishi, 1971; Ryden et al., 1972a,b). It is essential, however, that conditions realistic of those existing in streams are used if meaningful results are to be obtained (Ryden et al., 1972a). Widely differing interpretations can be made as solution: soil ratios and initial dissolved inorganic P concentrations are changed from those conventionally used in P sorption studies to those realistic in terms of the stream environment (Fig. 3 a-c). The data in Fig. 3a suggest that inorganic P released from the A1 horizon, which contained a P fertilizer-soil reaction product, would be largely resorbed by the noncalcareous B1 horizon and to some extent by the calcareous 3C1 horizon, should the horizons erode together. Sorption studies employing low initial added inorganic P concentrations and a wide (400: 1 ) so1ution:soil ratio (Fig. 3c) indicate that the B1 horizon has a much lower ability to remove dissolved inorganic P from solution than expected, this being equal to or only slightly greater than that of the 3C1 horizon. In fact for mixtures of varying ratios of A1 and B l , and A1 and 3C1 horizons, it was found (Ryden et al., 1972b) that the latter mixtures were able to maintain lower dissolved inorganic P concentrations than the former. The conditions used by Ryden et al. (1972a,b) to predict the potential of eroding soils to modify the dissolved

PHOSPHORUS IN RUNOFF AND STREAMS

15

+loo

+I00

’:; 0 1000

1000

3000

-SO

5-

+ Ir

+4

._ -

s

o

c O

n

Q

-1

.30

10

10

0

-

10

Final dissolved inorganic P Concentration Wgll)

FIG. 3. Sorption of added inorganic phosphorus by horizons of a Miami silt loam profile from solutions of varying initial dissolved inorganic P concentrations and at varying so1ution:soil ratios. ( a ) High added P (0-6 pg/ml) and narrow so1ution:soil ratio (50: 1 ) . ( b ) Low added P (0-0.2 pg/ml) and narrow solution:soil ratio ( 4 0 : l ) . (c) Low added P (0-0.2 pg/ml) and wide so1ution:soil ratio ( 4 0 0 : l ) . [From Ryden et al. (1972a), reproduced with permission of the American Society of Agronomy.]

inorganic P concentrations of streams, gave results comparable to those obtained in simulated stream systems using a solution: soil ratio of 1000:1 This is equivalent to a sediment concentration of 1000 mg/liter, which lies well within the range of values cited by Guy and Ferguson (1970) and Johnson and Moldenhauer ( 1970). The P sorption studies reported by Taylor and Kunishi (197 1) and Ryden et al. (1972a,b) involved closed systems, i.e., soil in contact with the same aqueous phase. This may be justified on the grounds that the wash load of a stream travels at the same velocity as the water in which it is suspended (Johnson and Moldenhauer, 1970), as discussed previously.

16

J. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

Sorption studies may be used to provide reasonable estimates of dissolved inorganic P concentrations in streams, under various flow conditions, draining rural watersheds. Taylor and Kunishi (1971 ) observed that dissolved inorganic P concentrations during base flow of a stream draining a small agricultural watershed in Pennsylvania, were in the range of 0.040 to 0.060 pg P/ml, values which were close to those predicted from P sorption studies using stream bank sediment and subsoil material. During periods of surface runoff, predicted dissolved inorganic P concentrations would be in excess of 0.200 pg of P per milliliter for the surface soil used by Taylor and Kunishi (1971) and 0.100 pg of P per milliliter for that used by Ryden et al. (1972a) due to release of P from eroded surface soil; however, predictions from the work of Taylor and Kunishi (1971) are based on the use of a narrow (10: 1 ) so1ution:soil ratio. The ability of eroding stream bank material or resuspended stream bed sediment to resorb inorganic P released to solution should not be ignored (Taylor and Kunishi, 1971 ) . In a more recent study of the same watershed in Pennsylvania, Kunishi et al. (1972) observed that during a heavy summer rainstorm only 31% of the total “available” P (total dissolved plus resin-extractable P on the suspended sediment) was in the resin-extractable form in a stream draining an agricultural subwatershed. At the outflow of the main watershed, however, over 50% of the total “available” P was in the resin-extractable form. Kunishi et al. (1972) suggested that for this watershed, as suspended material moves downstream and mixes with material from other parts of the watershed as well as that eroded from the stream banks, dissolved P is actively sorbed. During a second less intense storm, however, when stream bank erosion was less severe, the proportion of total “available” P associated with the sediment was virtually the same at both monitoring stations. A similar hypothesis might also explain the observation of White ( 1 972) at Taita, New Zealand, that the concentration of dissolved inorganic P at the outflow of small watershcds during base flow was lower than that recorded for groundwater seepage giving rise to the stream flow. It is important to distinguish between the quantities of various types of soil materials expected to enter streams in urban as opposed to agricultural surface runoff. In agricultural areas, surface runoff will carry primarily surface soil material to receiving streams. Surface soils may contain P fertilizer-soil reaction products capable of producing significant increases in dissolved inorganic P concentrations, due to their dissolution (Ryden et al., 1972a). In urban areas, however, land under development, which is prone to severe erosion, is frequently graded, exposing some or all horizons of the area profile to potential erosion. Dissolved inorganic P concentrations of receiving streams in urban areas may be sufficiently high that

PHOSPHORUS IN RUNOFF AND STREAMS

17

the addition of eroded soil material may cause a reduction in the dissolved inorganic P concentration. An approach similar to that used by Taylor and Kunishi (1971) and Ryden et al. (1972a,b) could be used to identify other diffuse sources of potential P enrichment within a watershed. The approach would be particularly useful for estimating the potential of various forms of urban detrital material to influence the dissolved inorganic P concentrations of surf ace runoff. One diffuse source of considerable importance is the leachate from leaves, particularly during the autumn. An appreciable percentage of the total P in leaf tissue may be in a water-soluble form. Ash leaves may contain 62% of total P as water-soluble inorganic P (Nykvist, 1959). Cowen and Lee (1972) observed that 44 and 120 pg soluble inorganic P per gram air-dry weight of fallen oak and poplar leaves, respectively, could be leached by 1 liter of distilled water percolating at a rate of 8.4 ml per minute. Greater amounts of P were released from oak leaves during consecutive leaching cycles and after fragmentation of whole leaves. Similar experiments were conducted by Timmons et al. (1970) using agricultural crop residues. These were leached in a fresh condition and after drying, and freezing and thawing cycles. The data suggest that the leaching of crop residues is most likely to contribute to the dissolved inorganic P concentration of streams during spring thaw in certain areas when, after numerous freezing and thawing cycles, the residues will be carried over frozen ground in surface runoff. When greater infiltration can occur, a portion of the leached P may be retained in the soil due to sorption.

5 . P Chemistry of Stream-Bed Sediment Little is known of the chemistry of stream-bed sediment although it is conceivable that it is similar to that of the subsoil of the surrounding area (Taylor and Kunishi, 1971 ) . Consequently, P sorption studies using subsoil material may provide some information on the role of stream-bed sediment in regulating the dissolved inorganic P concentration due to its suspension during turbulence. This would be particularly true in watersheds with little contribution to stream-bed sediment as a result of surface runoff. In watersheds where surface runoff is a regular occurrence, however, stream-bed sediment is expected to have a significant contribution from surface horizon soil material, and the latter could contribute to base flow concentrations of inorganic P. Care should be taken, however, in the extension of the P sorption properties of field soils to stream-bed sediment. Hsu (1964) observed that the amount of inorganic P sorbed by soil after storage for 1 year in a continuously wet condition, increased from 69 to 99 pg of P per gram of soil.

18

J. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

The increased sorption was attributed to release of Fe to solution from crystalline phases due to the development of localized reducing conditions during storage, and reprecipitation of “ferric hydroxide” on contact with more aerobic conditions. The redox status of stream-bed sediments does not appear to have been studied, but it is reasonable to suggest that reduction occurs at depth in the sediment with the possibility of crystalline ferric components being transformed to short-range order ferrous forms. The importance of short-range order oxides and hydrous oxides of Fe in the sorption of inorganic P has already been discussed. The possible transformation of Fe from crystalline to short-range order forms represents the first stage of the more aggressive transformations which occur in lake sediments under anaerobic conditions (Shukla et al., 1971). The observation of Kafkafi et al. (1967) that the washing of kaolinite, on which P had been sorbed, produces a “pool” of nonexchangeable P is also of direct relevance to the P chemistry of stream-bed sediments, assuming a similar effect occurs. Stream-bed sediment with associated sorbed P could undergo a series of steps equivalent to sequential washing due to resuspension and settling as a result of minor turbulence. The observations of Kafkafi et al. (1967) suggest that sorbed P could become progressively less exchangeable and may constitute an essentially permanent removal of dissolved inorganic P from streams. When stream-bed sediment contains eroded fertilized soil materials, however, a different situation may prevail. Ryden et al. (1972a) showed that release of P from a surface soil horizon by repeated washing with P-free 0.1 M NaCl initially followed first-order kinetics, suggesting that release was due to the dissolution of solid phase P, probably a fertilizer-soil reaction product. 6 . Forms of P in Runoffand Streams

In many studies concerned with various aspects of P in runoff and streams there has been a tendency to measure total P. The measurement of total P discharged by streams does not provide any indication of the amounts of P available for aquatic plant growth. Consequently, the forms of P measured in streams that enter a lake or reservoir are of direct importance in assessing the impact of runoff- and stream-derived P on a body of standing water. Dissolved inorganic P is one of the obvious choices because this form of P is directly available for biological utilization. Objections to the measurement of dissolved inorganic P, as it is conventionally determined, have been raised by Frink (1971 ) on the basis that distinction between dissolved and particulate forms is based on filtration through a 0.45 pm filter. Although it is possible that filtration does not strictly differentiate between dissolved and particulate P, it provides a more

PHOSPHORUS IN RUNOFF AND STREAMS

19

realistic measure in terms of the effects of runoff- and stream-derived P on the biological productivity of standing waters than the measurement of total P. Vollenweider ( 1968) has also pointed out the necessity to distinguish between total P and dissolved forms of P because it is possible that P exports from some watersheds occur mainly in biologically unavailable forms, such as apatite. This work showed that P exports from the Alpine portion of the Rhine Basin amount to 1.45 kg/ha per year. As this is mainly in the form of apatite, however, the contribution of biologically available P to Lake Constance is relatively small. In other regions it appears that a high proportion of particulate inorganic P in streams draining urban and rural watersheds may in fact be apatite. Eroding urban soils in the Lake Mendota watershed, Wisconsin, contain between 6 and 80% of the total inorganic P as apatite, with amounts exceeding 50% in the lower B and C horizons (J. K. Syers, J. C. Ryden, and J. G. Thresher, unpublished data). For the same soil materials, Sagher and Harris (1972) observed that algal cultures suffered P starvation when the sole P source in the growth medium was C horizon material, indicating the very low biological availability of the P present in apatite. Chemical fractionation schemes have been used to determine the forms of inorganic P in soils. These schemes evolved from the observations of Chang and Jackson (1957) that certain chemical reagents were able to solubilize inorganic P contained in various synthetic phosphates and phosphate minerals. Recent workers (Bromfield, 1967; Williams et al., 1967, 1971a,b; Syers et al., 1972) have questioned the validity of the separation of inorganic P into Al-, Fe-, and Ca-bound forms, as proposed by Chang and Jackson ( 1957). Providing that the problems inherent in inorganic P fractionation schemes are recognized, useful interpretations may be drawn from the data obtained. The form of particulate inorganic P which is expected to have the greatest potential impact on the biological productivity of standing waters is that which is nonoccluded. Part of the nonoccluded and even some of the occluded inorganic P associated with ferric components is released into solution when anaerobic conditions develop subsequent to sedimentation. Appropriate inorganic P fractionation schemes applied to suspended stream sediments may provide a more meaningful measure of the forms and amounts of particulate inorganic P carried in streams. As pointed out by Taylor et al. (1971), suspended sediment concentrations are frequently not high enough to provide adequate amounts of xaterial in a manageable volume of water. Evaluation of the forms of P in soil materials which are known to be transported to streams in surface runoff may overcome this problem to some extent. In the case of eroding soil materials, the inorganic P fractionation schemes should not

20

J. C. RYDEN, J. K. SYERS, A N D R. F. HARRIS

be applied to the whole soil, due to the ER effect resulting from erosion. Water-dispersed particle-size separates should be used. In spite of the possible errors involved in a dissolved-particulate P split based on filter pore size, it seems that in the majority of cases the most meaningful and useful measurements of P in runoff are dissolved forms, particularly dissolved inorganic P. Frequently dissolved forms of P account for a major percentage of total P (Sylvester, 1961; Sullivan and Hullinger, 1969), whereas dissolved inorganic P in many cases constitutes a major proportion of the total dissolved P. It should be noted that dramatic changes can occur in the concentration of dissolved inorganic P and other P fractions after sample collection, even after only a short period of time . some cases when samples are not analyzed im(Ryden et al., 1 9 7 2 ~ )In mediately after collection, the only valid P parameter that can be measured is total P.

IV.

Phosphorus loads in Runoff a n d Streams

The P content of precipitation reflects the amount of P subject to washout from the atmosphere at the time of the precipitation event. The amounts of P carried in precipitation rarely exceed 1 kg/ha per year as total P (Miller, 1961; Weibel et al., 1966; Allen et al., 1968; Gore, 1968). Weibel et al. (1966) reported that the average concentration of total acidhydrolyzable P in precipitation falling on Cincinnati, Ohio, was 0.080 pg/ml, whereas Taylor et al. ( 197 1 ) reported an average concentration of 0.020 pg/ml for total dissolved P in precipitation collected at rural Coshocton, Ohio. Data for the P content of precipitation should be viewed with some skepticism unless adequate precautions have been taken to guard against contamination of the collection vessel (Gore, 1968; White, 1972). White (1972) found that although rainwater collected over an extended period indicated a mean dissolved inorganic P concentration of 0.020 pg/ml, a mean concentration of 0.003 pg/ml, based on specific showers, might be a more accurate estimate. It is difficult to evaluate the effect of P carried in precipitation on P loads in runoff and streams. Phosphorus contained in precipitation which becomes a part of any soil-water ecosystem may undergo considerable change in form, depending primarily on the chemical factors discussed previously, and will become an integral part of the P forms in runoff and streams. Surface runoff water is the carrier of not only the P initially present in precipitation but also any P which enters surface runoff water because

PHOSPHORUS IN RUNOFF AND STREAMS

21

of chemical interactions or the energy of the water itself. Several factors affect the amount and energy of surface runoff water at any particular location and, therefore, the amount of additional P entering and carried by it. These include nature of land use, extent of vegetative cover, slope, intensity of rainfall, and permeability of the land surface. The quantity of precipitation entering subsurface and groundwater runoff is inversely related to that disposed of in surface runoff and evapotranspiration. It is consequently affected by the factors listed above for surface runoff. The major portion of P in subsurface and groundwater runoff is expected to be in dissolved forms. If subsurface runoff is accelerated by artificial drainage systems, however, soil colloids, with associated P, may appear in the water as it enters streams. The P load carried by a stream under given flow conditions will represent the relative contribution of P loads in each of the runoff components, as well as the influence of any point source of P. A.

INFLUENCE OF POINT SOURCESON PHOSPHORUS IN STREAMS

Estimates of the contribution of P to surface waters from domestic wastes in the United States range from 91 x loo to 227 x l o G kg per year with total P concentrations ranging from 3.5 to 9.0 pg/ml (McCarty, 1967; Ferguson, 1968). Weibel et al. ( 1964) estimated that P discharged as raw sewage from combined storm sewers in Cincinnati, Ohio, amounted to 3.4 kg/ha per year as total dissolved P. In the area of Madison, Wisconsin, the per capita contribution of P to surface waters from treated domestic waste was estimated to be 0.544 kg/capita per year (Sawyer, 1947), whereas an estimate of 1 kg/capita per year was given by Metzler et al. (1958) for Chanute, Kansas. The difference between the estimates of Sawyer (1947) and Metzler et al. (1958) may reflect the increased use of P in domestic products, particularly detergents. The impact of sewage outfall on the dissolved inorganic P concentration of streams and rivers was studied by Brink and Gustafsson (1970). Their results are summarized in Table 11. Obviously the impact of the outfall is dependent on factors which include flow rate of the receiving stream and the P content of the effluent. Under certain agricultural management conditions animal excrement may constitute a point source of P to streams. Excrement may enter streams during surface runoff from feedlot operations or by the cleaning of milking sheds into open drains. The magnitude of these sources of P will be discussed later. McCarty (1967) was unable to estimate the magnitude of contributions of P made to streams from industrial wastes. The amounts of P discharged

22

J. C. RYDEN, J. K. SYERS, AND R. F . HARRIS

TABLE I1 Effect of Sewage Outfall on tllc Dissolved Inorganic Phosphorus Concentration of the Receiving Water" IXssolved inorganic P concentration

(pg

P/ml)

Receiving water

Before outfall

After outfall

River Stream Stream Ditch

0.09 0.05 0.11 0.01

0 4% 0.18 4.30 0.75

Data from Brink and Gustafsson (1970).

to streams will depend on the industrial process concerned and local legislation covering the discharge of industrial effluent. Mackenthun et al. (1968), for example, estimated that a potato canning factory and a woollen mill contributed 3446 and 835 kg of P per year, respectively, to the East Branch of the Sebasticook River, Maine. Domestic and many industrial wastes not only supply large amounts of total P to streams but also have a pronounced effect on the concentrations of dissolved forms of P in the receiving stream. Because domestic and industrial wastes are point sources, they are easily recognized within a watershed and are amenable to direct manipulation.

B. RUNOFFFROM FORESTWATERSHEDS A compilation of data from several studies of the quantities of P lost in streanis from stable forest and woodland watersheds is presented in Table 111. Exports of P in streams from long-established and stable forest watersheds provide a useful datum line against which losses of P from other land-use areas may be compared. The data in Table I11 show a considerable degree of uniformity. Total P losses range from 0.68 to 0.02 kg/ha per year with three out of the four values being less than or equal to 0.1 kg/ha per year. Only a few measurements have been made of the dissolved inorganic P concentration of stream water in forested watersheds. The values reported by Brink and Gustafson (1970) in Sweden show a mean of 0.015 pg/ml, with this fraction amounting to 33% of the total annual loss of P. The data suggest that total P and dissolved inorganic P concentrations rarely exceed 0.115 and 0.025 pg/ml, respectively. Two interesting points arise from the data in Table 111. From the study of a stream draining a

z

TABLE I11 Losses of P in Streams Draining Forest Watersheds

P concentration in streamwater (pg P/ml) Study

Location

Form measured

P loss (kg/ha/yr)

Range

Mean

El z 8 2 2 0

Bormann et al. (1968) Brink and Gustafsson (1970)

New Hampshire Sweden

Cooper (1969) Jaworslii and Hetting (1970) Sylvester (1961)

N. Minnesota Potomac River Basin Washington

Taylor et al. (1971)

Coshocton, Ohio

Total P Total P Dissolved inorganic P Not specified Total P Total P Dissolved inorganic P Total soluble P

0.02 0.06 0.02 0.1s 0.1 0.68 0.07 0.05

-

-

0.008-0.053 0.002-0.026 0.043-0.060

0.048 0.015 0.041

-

-

0.024-0.115 0.004-0.009

0.069 0.007 0.015

0.011-0.OPO

c.4 q

+

3 v)

+I

b

24

J . C. RYDEN, J . K. SYERS, A N D R. F. HARRIS

woodland area at Coshocton, Ohio, to which no fertilizer P had been applied for over 30 years (Taylor et al., 1971), it would appear that the woodland is conservative of P. The average total soluble P content of rainfall was 0.020 pg/ml, whereas that in the stream draining the watershed was 0.015 pg/ml. The extent of addition of total dissolved P to the woodland can be calculated from precipitation data given by Taylor et al. (1971 ) ; a value of 0.17 kg/ha per year is obtained. This value is more than three times greater than the annual P loss in the stream. The conservative nature of forests for P is further borne out by the fact that the annual contributions of P to the land surface in precipitation, quoted previously, are in most cases considerably greater than annual exports of P in streams from forest watersheds. In many cases there is an order of magnitude difference. This hypothesis assumes that data covering the P content of precipitation are correct. The second point of interest relates to the “background” P concentration in forest streams. The data suggest only minor seasonal fluctuations in P concentrations, particularly that of dissolved inorganic P. As a major portion of streamflow is considered to have a groundwater origin (Biggar and Corey, 1969; Johnson and Moldenhauer, 1970), it is conceivable that the dissolved inorganic P load in streams of forested areas is primarily due to that in groundwater runoff. If the reported mean P concentrations of forest streams are compared to those for groundwaters, a marked similarity is observed. Juday and Birge ( 193 1) found that the total dissolved P concentrations of 19 wells in northern Wisconsin, an extensively forested area, ranged from 0.002 to 0.197 pg/ml, with an average of 0.018 pg/ml when the highest value is omitted. This mean value is, if anything, slightly higher than the mean concentrations for dissolved fractions of P reported in Table 111. The higher mean concentrations of total P probably arise from suspended inorganic and organic solids that enter streamflow due to turbulence, especially during high flow. The minor fluctuations in P concentrations reported for forest streams suggest that P export is minimally affected by P input from surface runoff. Amounts of surface runoff in forest watersheds will be low owing to the protection afforded by canopy cover and/or forest floor vegetation. The “background” P export in forest streams is a direct reflection of the chemical and physical factors that affect P concentrations in groundwater and subsurface runoff. Because larger amounts of stream flow from forest watersheds will arise from groundwater and subsurface runoff, the “chemical sieving” action of the soil plays a major role in maintaining the consistently low dissolved inorganic P concentrations in forest streams and may also account in part for the apparent conservative nature of forest watersheds for P.

PHOSPHORUS IN RUNOFF AND STREAMS

25

C. RUNOFFFROM AGRICULTURAL WATERSHEDS The loss of P in streams draining agricultural (in most cases arable) watersheds is far less well defined than that for forest streams. This is probably due to the fact that in studies designed to estimate this loss, little differentiation has been made with respect to the forms of runoff. Consequently, there are major problems in estimating P loss from agricultural watersheds using many of the data presented in the literature. Losses of P from agricultural land have not only been based on analyses of streams draining a specific watershed (Campbell and Webber, 1969; Taylor et al., 1971 ), but have also been estimated from data obtained in surface runoff studies (Timmons et al., 1968). Many previous reviews of this subject have relied on such data (Taylor, 1967). Losses of P in streams draining various agricultural watersheds are summarized in Table IV. The lowest loss of total P is from rangeland in Ontario, Canada (Campbell and Webber, 1969) which had received no P fertilizer in living memory. This loss is very similar to losses of total P from forest watersheds, suggesting a minimal contribution if P from surface runoff. Similarly, the total P carried in the base flow, primarily attributable to groundwater runoff, of several streams draining arable agricultural watersheds in S.W. Wisconsin (Minshall et al., 1969) is also little different from total P loads in streams draining forest watersheds. Minshall et al. (1969) reported the total P loss in base flow to be less than 0.12 kg/ha per year. If stream flow during periods of surface and subsurface runoff is included, however, the estimated annual loss of total P increases by one order of magnitude, as indicated by the data of Witzel et al. (1 969) for the same area of S.W. Wisconsin (Table I V ) . These studies suggest that the groundwater runoff or base-flow component of streams draining agricultural watersheds is little different from the total P load of forest streams. It is therefore necessary to estimate the extent to which the P load of streams draining agricultural watersheds may be augmented by P loads of surface and subsurface runoff. The major factors affecting the loads of P in surface runoff from agricultural land include time, amount, and intensity of rainfall, rates of infiltration and percolation, slope, soil texture, nature and distribution of native soil P, P fertilization history, cropping practice, crop type, and crop cover density. A selection of reported losses of P in surface runoff from arable land of various slopes and cropping practices is summarized in Table V. Losses range from the extremely high values of 67 kg/ha per year to almost zero. Losses of P in all studies listed in Table V have been based on the collection of surface runoff (water and particulates) from small experimental

TABLE I V Losses of P in Streams Draining Agricultural Watersheds

Study Campbell and Webber (1969) Fippin (1945) Taylor d al. (1971)

Witzel d al.

Location

S. Ontario, Canada Tennessee Valley Coshoeton, Ohio

S.W. Wisconsin

(1969)

a

January through September 1967.

Soil texture

Form of P measured

Slope (%)

I-r

P Crop

P applied (kg/ha/yr)

P lost (kg/ha/yr)

-

Total P

-

90% Rangeland

0

0.08

-

Total P

-

Row crops, open farmland 50% Permanent pasture; 50% winter wheatmeadow 100% Pasture cultivation-haypasture

-

6.26

3.5

0.07

Silt loam

Total dis-. solved P

Silt loam

Total P

12-18

6-8

1.88

4.08

1.000

9.64 4.27

1.51 1.20

I-r ?c

PHOSPHORUS IN RUNOFF AND STREAMS

27

plots frequently no larger than 30 x 6 m, with subsequent analysis for one or more forms of P. Although this approach was originally developed to investigate soil fertility losses due to soil erosion, it is still used to estimate P loads in surface runoff as it relates to the fertility of surface waters (Timmons et al.,1968; Nelson and Romkens, 1969). It is difficult to make any generalizations regarding the P loads carried in surface runoff or to draw conclusions from them in terms of how agricultural practices and natural variables affect P loads in streams draining agricultural watersheds. This is due to the differences in forms of P measured and the lack of comparative studies with respect to slope, soil texture, cropping, and climatic variables. One of the few studies from which meaningful interpretations of P loss in surface runoff can be made in relation to degree of slope and cropping practice is that by Massey et al. (1953) in Wisconsin (Table V ) . As expected, greater “available” (water-soluble plus pH 3 extractable) P losses to surface runoff occurred on the steeper slopes when cropping practice was kept constant. The introduction of two years hay into the rotation reduced the P loss by a factor of approximately four. The value of “improved” or “conservative” agricultural practices in reducing the magnitude of P losses is illustrated in the studies at Coshocton, Ohio (Weidner et al., 1969) and at Lafayette, Indiana (Stoltenberg and White, 1953). It should be noted, however, that although the “improved” practice reduced the total amounts of acid-hydrolyzable P lost in surface runoff at Coshocton, the concentration of this fraction during surface runoff increased from 0.43 to 0.59 pg/ml. Attempts have been made to measure the relative contributions of the aqueous and particulate fractions of surface runoff to the total loss of a measured form of P. In a plot study using simulated rainfall, Nelson and Romkens ( 1969) obtained dissolved inorganic P concentrations of 0.05, 0.30, and 0.50 pg of P per milliliter in the aqueous phase of surface runoff from fallow plots 12 days after 0, 56, and 1 1 2 kg of P per hectare, respectively, had been disked into the soil, with only slight decreases in concentrations up to 75 days after fertilizer application. Although very high artificial rainfall rates were employed (up to 73.5 mm/hr), indications are that high concentrations of dissolved inorganic P may be maintained in surface runoff water. Timmons et al. (1968) determined the distribution of total P loss in surface runoff between the aqueous and particulate phases from plots under natural precipitation. Although these workers did not report P concentrations, losses of total P in the aqueous phase of surface runoff arising from snowmelt far o.utweighed those in the particulate phase. In contrast, total P loss in the aqueous phase varied in most cases between 5 and 40% of the loss in particulates in surface runoff arising from rainfall.

TABLE V Losses of Phosphorus in Surface Runoff from Field Plots Study

Location

Knoblauch et al.

New Jersey

(1942)

Massey et al.

Wisconsin

(1953)

Soil texture

Form of P measured

(%I

Sandy loam

Total P

Silt loam

Soluble pH 3 extractable P (available)

3.5

3 3

11

20

Lafayette, Indiana

Silt loam

0.5 M N H 4 F 0.1 N HCI

+

00 0.5

extractable P (“available”)

Thomas et al. (1968)

Tifton, Georgia

Sandy loam

Crop

+

0.05 N HCI 0.025 N H ~ S O I

extractable P

3

P lost (kg/ha/yr)

+

Vegetables (i) No manure (ii) Manure (iii) Cover crop (iv) Cover crop manure Corn-oats Corn-oats2 yr hay Corn-oats Corn-oats-? yr hay Corn-oats-4 yr hay Oats-5 yr hay Coma Cornh Soybeansa Soybeansb Wheat” Wheat* Meadow“ Meadow* corn Rye-peanuts-rye Rye-corn-oats Oats-rye

+

+

11

Stoltenberg and White (1953)

P applied (kg/ha/yr)

Slopc

40 06 67 07 59 66 49 65 0 91 0 24 2 91

0 73 0 75 0 13 2 86 0 86

3 82 1 93 0 0 0 0 0 0 0 0

84 48 99 74 02 07 05 02

Timmons et al. (1968)

W. Central Minnesota

Loam

Weinder et al. (1969)

Coshocton, Ohio

Silt loam

a

Total P

Total acidhydrolyzable P

6

-

Fallow Corn-continuous Corn-rotation Oats-rotation Hay-rotation Cornc Cornd Wheat" Wheatd

29.1 99.1 30.2

4.82 17.34 4.83 17.34

0.2-0.6 0.1-0. 2 0.1 0.0-0.1 0.1-0.3 10.24 3.11 1.33 0.41

Prevailing practice: moderate fertilizer levels; liming t o p H 6.0; straight row planting and cultivation.

* Conservation practice: higher fertilizer levels; liming t o p H 6.5; manure before corn; contour planting and cultivation. c

Prevailing practice: straight row tillage across slope; low P fertilizer level; alsike-red clover-timothy meadow mixture; liming t o p H 5.4. Improved practice: contour tillage; high P fertilizer level; clover-alfalfa-timothy meadow mixture; liming t o p H 6.8.

0

2 ? w

C

30

J. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

These observations are not unexpected because rainfall tends to loosen soil particles by drop impact, facilitating their entry into surface runoff waters. It is apparent that an appreciable dilution of dissolved P may occur when surface runoff augments base flow in streams. Taylor et al. (1971) reported a mean total dissolved P concentration of 0.022 pg/ml in a stream draining an agricultural watershed at Coshocton, Ohio; concentrations never exceeded 0.100 ,g/ml even under conditions of high stream flow when surface runoff was occurring. It is generally considered that P is retained sufficiently strongly by soil particulates that movement out of the soil profile in percolating waters is minimal (Way, 1850; Black, 1970). Subsurface runoff from agricultural land, however, may contain significant concentrations of dissolved inorganic P in relation to those present in surface waters (Table VI) . It should be noted, however, that the data in Table VI represent losses of dissolved inorganic P in tile and irrigation return flow drains. Artificial drainage systems increase the rates of infiltration and percolation, reducing contact times between the soil solution and soil components capable of sorbing inorganic P from solution. Furthermore, tile drains will remove water from surface horizons of the soil profile, diminishing the possibility for contact between percolating waters and more P-deficient subsoil material. Not all the data in Table VI, however, indicate a net loss of P from the soil profile to subsurface runoff. In the Snake River Valley, Idaho, Carter et al. (1971) found that only 30% of the dissolved inorganic P in irrigation water left an irrigation tract by return flow. When the dissolved inorganic P concentration in irrigation water exceeded 0.010-0.020 pg/ml, irrigation decreased the downstream P load, a useful field example of the chemical sieving action of soils. Johnston et al. (1965), however, reported a net loss of 3% at an applied P fertilizer rate of 51.9 kg/ha on irrigated land in the San Joaquin Valley, California. The data in Table VI indicate that a reasonable proportion of P loss to streams draining arable watersheds can be due to subsurface runoff. Although no data are available to compare P loads due to surface and subsurface runoff, Sylvester (1961) reported that total P loss by irrigation return flow in the Yakima Valley, Washington, ranged from 3.8 to 14.3 kg/ha per year, values higher than many reported for surface runoff losses. Under a nonirrigated farming system, Bolton et a!. (1970) observed losses of dissolved inorganic P in tile drain effluent ranging from 0.13 to 0.29 kg/ha per year at a fertilization rate of 28.9 kg of P per hectare per year. It would appear, therefore, that losses of P in subsurface runoff can be similar or even greater than those in surface runoff. Furthermore, subsurface runoff will occur not only during periods of surface runoff, but also when evapotranspiration is less than infiltration.

TABLE VI Losses of Dissolved Inorganic Phosphorus in Subsurface Runoff Dissolved inorganic P concentration (pglml) Study

Location

Bolton et al. (1970)

Ontario, Canada

Brink and Gustafsson (1970) Carter et al. (1971)

Sweden

Cooke and Wlliams (1970)

Soil texture

Drainage system Tile drains

Clay

-

Snake Valley, Idaho

Calcareous silt loam

Irrigation return flow

Woburn, England

Sandy

Tile drains

Voelecker (1874)

a

S. Central Michigan San Joaquin Valley, California Yakima Valley, Washington

Rothamsted, England

No P fertilizer applied. 28.9 kg P applied per hectare per year.

Clay to sandy loams Heavy silty clay Sandy loam

Clay loam

Range

Mean

Corn, oats Alfalfa, bluegrass

0.200-0.170 0,190-0.270 0.045-0.140

0.180" 0 . 210b 0.079

Alfalfa, corn, root crops, pasture Arable and grassland Arable grassland Root crops

0.007-0.23

0.012

0-0.300

0 . 0uo

0-0.700 0-0.750 0.010-0.300

0.440 0.080

0.053-0.230

0.079

-

Tile drains

Sandy drift Erickson and Ellis (1971 Johnston et al. (1965) Sylvester (1961)

Crop

Tile drains and ditches Irrigation return flow drains Surface return flow drains Subsurface return flow drains Tile drains

Cotton, rice, alfalfa

0.072-0.300

Wheat

-

0.161

0.029-0.460

0.182

0.054-0.802

-

32

J. C. RYDEN, J. K. SYERS, AND R. F . HARRIS

D. RUNOFFFROM LANDASSOCIATED WITH ANIMAL REARING Animal excrement is a source of P to surface waters (McCarty, 1967). Little direct information is available on the P load this source imparts to streams. Although some loss of P to subsurface and groundwater runoff can be expected, the two major ways in which animal excrement may enter streams are by surface runoff from land upon which manure has been spread and by surface runoff from feedlot operations. Manure spread on land in certain areas during the winter months is subject to transport in surface runoff waters. The amounts of surface runoff during spring thaws are particularly great owing to the combined effects of snowmelt and rainfall on frozen ground. A study of P loss from land manured during winter was conducted by Midgley and Dunklee (1 945). Manure was applied to study plots in Vermont during winter for a period of 6 years at a rate of 22.5 tonnes/ha. Losses of total dissolved P amounted to 2.1 and 2.5 kg/ha for 20 and 10% slopes, respectively. It was concluded that P losses were little affected by slope but more by the amount of snow. Using the data of Midgley and Dunklee (1945), Lee et al. (1969) estimated that 6810 kg of P is lost in surface runoff to streams in the Lake Mendota watershed, Wisconsin, from agricultural lands on which manure is spread during 5 months of the year when the ground is frozen. This amounted to approximately 60% of the total P losses from rural land in the watershed. Concern has also been shown in countries where large areas of land are used for pasture and high intensity grazing, such as in New Zealand, that dung pats may be carried in surface runoff and contribute significantly to the P loading of streams (Elliott, 1971). The magnitude of this problem is obviously very difficult to estimate, and its control virtually impossible, unless restrictions are placed on the proximity to streams that stock are allowed to graze. Again, there are few data from which the magnitude of P loss to streams via surface runoff from feedlot operations can be estimated. Surface runoff from feedlots could almost be regarded as a point source of P because such operations are highly concentrated and the area occupied is generally insignificant in relation to the area of the region in which they are located. In Nebraska the total area of concentrated feedlots amounts to no more than 5670 ha (Swanson et al., 1970). When it is considered, however, that cattle of 454 kg average weight excrete 7.7 kg of P per year (Millar and Turk, 1955), of which 60-80% may be in an inorganic form (Peperzak et al., 1959) and that 1.5 million cattle may be on feed at any one time, each occupying an area of 37 m? (Swanson et al., 1970), it is probable that the local impact of surface runoff from these operations on the

33

PHOSPHORUS IN RUNOFF AND STREAMS

P status of streams in the area is considerable. The magnitude of this source of P to streams may result in a spread of effects far beyond the immediate vicinity. Data presented by Gilbertson et al. (1970) for the effect of slope and cattle density on the total P losses from unpaved feedlots in Nebraska are presented in Table VII. The greatest total P losses occurred during snowTABLE VII Effect of Slope and Cattle Density on Total P Loss from ITnpaved Fcedlotsn

Slope 9 6

3

Cattle density (in2/animal) 18.6 9.3 18.6 9.3 18.6 9.5

I,

P loss in winter runoff I, (kg/lla)

P loss i n rain-

80.5 469.3 146.4

58.5 34.2 36.6 29.3 34.2 29.3

256.9

78.1 514.5

storm runoff c (kg/W

Data from Gilbertson et al. (1970). January through April, 1969. April through July, 1969.

melt with a large effect of cattle density but only minor effects due to slope. The latter finding is in agreement with that of Midgley and Dunklee (1945), despite the different purpose of the two studies. The concentrations of total P in surface runoff ranged from 6.8 to 753.2 pg/ml during winter and from 13.9 to 46.6 pg/ml in rainstorm surface runoff. These concentrations are extremely high and would be expected to produce a significant change in the total P concentration of receiving streams.

E. URBANRUNOFF The load of P in streams draining urban watersheds which have a negligible contribution of P from point sources will generally be dominated by that carried in surface runoff. Drainage patterns in urban areas are, in most cases, altered so drastically by paving, the installation of storm sewers, and the channelization of water courses, that contributions from subsurface and groundwater runoff are probably small. It is probable that a large proportion of precipitation in an urban area, which in a rural area would con-

34

J . C. RYDEN, J. K. SYERS, AND R. F. HARRIS

tribute to subsurface and groundwater runoff, is intercepted by drains and becomes indistinguishable from urban surface runoff. Because many of the studies of surface runoff from urban areas have been conducted in areas served by combined sewer systems it is difficult to estimate the contribution of surface runoff to the P load carried by streams. It is virtually impossible to separate the component appearing in stormwater outlets due to overloading of sanitary sewers during wet weather flow from that due to urban surface runoff (Weibel, 1969). Several studies, however, have been conducted recently with the sole objective of determining the quality of urban surface runoff. A summary of these data is given in Table VIII. One of the first studies conducted was that by Weibel et al. (1964) in an 1 1 ha residential and light commercial section of Cincinnati, Ohio. The maximum mean total dissolved P concentrations were observed during the summer (0.36-0.39 pg/ml) whereas minimum values were observed in winter (0.16 pg/ml). By far the most extensive study of the quality of urban surface runoff took place in Tulsa, Oklahoma (Avco Corporation, 1970). The proportion of unused land, arterial streets, and industrial land were all found to be important in relation to the mean dissolved inorganic P concentrations observed in monitored storm Sewers. The highest annual load of 8.8 kg/ha was for urban surface runoff from a light industrial area, a large proportion of which was still under development. Other test areas, all except one including residential property, gave rise to dissolved inorganic P losses of 1.1 to 3.3 kg/ha per year. The largest loads of P per impervious area were from districts where tree cover was dense. This is probably due to the leaching of dissolved inorganic P from leaves, discussed previously. As reported by Kluesener (1972) and Harris et al. (1972), for urban watersheds in Madison, Wisconsin, leaching of leaves and seeds, coupled with the considerably reduced infiltration characteristics of urban areas, can be expected to result in high concentrations of dissolved inorganic P in urban surface runoff in the spring and autumn. Storm sewers draining runoff from residential areas into Lake Wingra, Madison, were monitored intensively during snowmelt, and spring, summer, and autumn storm runoff events; samples were taken every 2-5 minutes during peak flow and at longer intervals over the entire length of a storm to enable determination of the frequency of sampling needed to obtain, in conjunction with flow data, a reliable estimate of P input loads (Harris et al., 1972). Dissolved inorganic P generally constituted more than 80% of the total dissolved P in runoff at all times of the year. Although dissolved inorganic P was highest in the autumn (up to 2.4 pg/ml) and spring (up to 2.1 pg/ml), immediately following leaf and seed fall, respectively, the relative input

wz

TABLE VIII Losses of Phosphorus in Surface Runoff from Urban Areas

meable area Study Avco Corporation

Sylvester (1961)

Weihel et al. (1964)

X 0

runoff waters (pg/ml)

P loss

?? 1 vl

(%)

Form measured

(kg P/ha/yr)

Range

Mean

2

Tulsa, Oklahoma

37

2 80

0 54-3 49

1 15

Ez

Durham, North Carolina Seattle, Washington

29

Dissolved inorganic P Total P

3 4

0 15-52 50

0 55

;

Dissolved inorganic P Total P Total dissolved

-

Trace-0 78

0 08

-

0 01-1 40 0 052-1 452

Location

(1970)

Bryan (1971)

V

P concentration in

Imper-

Cincinnati, Ohio

Z

-

37

P

4

0.92

o

21 0 '26

P m

>

5

36

J . C. RYDEN, J . K. SYERS, AND R. F . HARRIS

loading of dissolved inorganic P was greater during the snowmelt period (levels of 0.4 to 0.9 pg/ml) because of the large volumes of water discharged in this period. Particulate inorganic P varied from 10 to 80% of the total particulate P and showed no consistent relationship to time of year. Levels of total particulate P tended to increase with increasing runoff flow. A substantial proportion of this particulate P was of sufficiently high density to settle rapidly out of the biologically active lake surface waters and probably have minimal effect on lake P fertility status. On the other hand, low density runoff particulate P may provide an important reservoir of biologically available P in lake waters, especially in late spring and summer when P-deficient algae and aquatic plants will tend to accelerate release of dissolved P from such suspended runoff particulates. Although total P levels during a specific runoff event tended to be highest during the initial flush, total P load was dictated essentially by flow rather than by fluctuations in P composition (Harris et a!., 1972). If these trends recur for runoff from different land-use areas, limited sampling of runoff from representative flow-gauged storm sewers during periods of high Row, and analysis of these samples for dissolved inorganic P and low-density particulate P should provide valid estimations of the loads of biologically important P components in urban runoff. Another potentially important source of P to urban surface runoff is that associated with eroding soil. During urban development, particularly on the fringes of urban areas, large tracts of land are frequently stripped of vegetation and graded, maximizing the possibility of erosion should surface runoff occur. There are no reported studies of P losses from such development projects, but Guy and Ferguson (1970) cite soil loss from highway construction in a watershed in the Potomac River basin. This averaged 1710 tonnes/km' per year over a three-year period. The amount of a specified form of P lost to flowing waters by such severe erosion will depend to a large extent on previous land use. As extensive construction programs frequently utilize land previously under agricultural management, high P losses can be expected, the distribution of inorganic P between the solid and aqueous phases being primarily determined by the nature of the inorganic particulates and the concentrations of dissolved inorganic P in solution (Ryden et al., 1972a,b). There is reasonable agreement between the estimates of the P loads carried in urban surface runoff. In many situations, however, urban surface runoff probably only amounts to a small percentage of that contributed by municipal and industrial wastes. As the amounts of P discharged to streams from the latter sources are reduced, urban runoff will become a much more significant source of P to receiving streams (Weibel et al., 1964).

PHOSPHORUS IN RUNOFF AND STREAMS

V.

37

Impact of Phosphorus Carried in Streams on Standing Waters

The overall, short-term impact of surface runoff-derived P on standing waters is expected to be high because a large proportion of the average annual discharge of P occurs over only short periods of time during the annual cycle. Bryan (1971) pointed out that in Durham, North Carolina, there was an annual average of 40 day-long surface runoff cycles. Consequently, the major portion of the annual stream loading of P is concentrated into only 40 days, which potentially amplifies its effects by a factor of approximately nine. Furthermore, the impact of the P load carried in streams is expected to be greater during late spring and early summer when aquatic microorganisms are in the potentially active growth phase. The extent of any evaluation of the impact of P carried in streams on standing waters with respect to their biological productivity will also depend on the forms of P measured. If the only form measured is total P, then evaluation may be no more than one segment in a nutrient budget for the body of standing water. This is the easiest approach but one which allows no interpretation of the effects on biological productivity. Even when forms of P relevant to biological productivity are measured, a major unknown factor centers around the effects of mixing as streams enter standing waters. It is reasonable to suggest that temperature differences between stream water and standing water will have some effect on the degree of mixing. Stream water of a lower temperature than surface lake water would be expected to sink below the surface (Twenhofel, 1950), possibly minimizing effects on the photic zone. Such a situation may occur in summer and autumn when tcmperature differences will be the greatest. Furthermore, the effect of overall stream water density arising from sediment concentration, particularly during periods of surface runoff, causes entering water to sink to a lower level (Twenhofel, 1950). Temperature and density effects would tend to contribute P to deep waters and sediments, removing the P load from an immediately usable location. When minimal temperature and density differences exist between streams and standing waters, then a direct dilution effect will probably operate, providing entering waters produce enough turbulence to facilitate mixing. Under such circumstances the biological ‘availability of particulate forms of P will also depend on settling times which ultimately remove them from the photic zone. If the standing waters are in a stratified condition, however, entering stream waters could override the thermocline. In this case dilution would be limited by the amounts of epilimnetic waters. In spring-fed lakes, the primary source of water is groundwater runoff. The amount of water entering a lake from this source is difficult to eval-

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5. C. RYDEN, J. K. SYERS, AND R. F. HARRIS

uate. The P load of groundwater runoff has traditionally been regarded as minimal (Taylor, 1967; Keup, 1968), and there is considerable evidence to support this contention. Rarely do P concentrations (in most cases dissolved inorganic P ) exceed 0.020-0.030 pg of P per milliliter (Juday and Birge, 1931; White et al., 1963; Mackenthun et al., 1968; Cooke and Williams, 1970). The importance of groundwater runoff as a P source to bodies of standing water has been based on flow rates and P concentrations of land springs and wells. Although it seems unlikely that groundwater runoff itself will contribute significant quantities of P to standing waters, the upward movement of ground water through the sediment may cause redistribution of P within the sediment and even release of dissolved P to the overlying water. The magnitude of this effect will depend on the P status and redox status of the sediment, the nature of the P-retaining components, the nature of groundwater entry (point or diffuse) into the lake, and its amount. The relocation of sediment P to groundwater runoff may be why Millar and Tash (1967) estimated that groundwater runoff or springs contributed 24.9% of the P inflow to Upper Klamath Lake, Oregon. At present it is difficult to estimate the impact of runoff- and streamderived P on standing waters, and such considerations can only be made if the forms of P relevant to biological productivity are measured. Furthermore, the mixing effects that occur as flowing waters enter lakes and reservoirs, as well as the potential of bottom sediments for the P enrichment of groundwater runoff, require further investigation.

VI.

Present Status and Outlook

The preceding discussion of the factors affecting the dynamics and loads of P in runoff and streams reveals various gaps in our knowledge and illustrates the problems in interpreting the data thus far obtained. The first and major difficulty in data interpretation and comparison is the lack of uniformity in the forms of P measured. In many cases this makes comparison between different studies virtually impossible, thereby prohibiting estimations of the relative importance of any particular source. In many studies, particularly those relating to surface runoff from agricultural land, the measurement of total P has been favored. This has led to the concept of nutrient budgets for P, whereby nutrient input and output for an ecosystem are used to determine whether P is lost. This approach is favored by Frink (1967, 1971). If the estimates of P input and output are based on measurements of total P, little information is gained because such deter-

PHOSPHORUS IN RUNOFF AND STREAMS

39

minations override any knowledge of the distribution of P between various forms in runoff and streams, some of which will have a greater or lesser effect on the biological productivity of surface waters. Although relatively few studies have been conducted on the P loads of streams and surface runoff from forest and urban watersheds respectively, there is considerable agreement in the results so far obtained. The situation is quite different for P loads in runoff and streams from agricultural watersheds. Frink (1971) stated that an “average” agricultural watershed with respect to P loss is a “useless fabrication.” It would appear, however, that the major problem arises from the lack of relevant information upon which reliable estimates can be made, a situation which has arisen largely because of an apparent lack of definition of the system being investigated. The use of surface runoff plots to determine losses of P from agricultural watersheds presents several problems. Surface runoff is a spasmodic rather that a continuous phenomenon, its composition at any location being highly heterogeneous and likely to change over short distances because the energy of the aqueous component, and therefore its ability to carry particulate material, varies with slope. The studies cited previously (Timmons et al., 1968; Nelson and Romkens, 1969), in which attempts were made to measure the distribution of the P load between the solid and aqueous phases of surface runoff appear to have limited value. When surface runoff enters streams, a much greater degree of homogeneity will be assumed, resulting in a new and probably more stable distribution of P between the aqueous and sediment phases, as discussed previously. Measurement of dissolved P fractions in surface runoff itself may lead to erroneous conclusions regarding its impact on the dissolved P status of streams due to the transitory nature of surface runoff. In order to obtain more meaningful estimates of P loss from agricultural watersheds, detailed studies of the P load of streams draining the watersheds are required. Some such studies have been conducted (Minshall et al., 1969; Witzel et al., 1969; Campbell and Webber, 1969; Taylor et al., 1971); these will be referred to as watershed analyses herein. None of the watershed analyses cited, however, covered more than a 2-year period of monitoring; the duration of the study could lead to considerable variation in P loss estimates, due to yearly differences in weather patterns as noted by Timmons et al. (1968) for surface runoff studies. Future studies must be based on the watershed analysis approach in order to avoid bias in estimates of the P loss obtained in plot studies due to differences in the energy of surface runoff imparted by slope variations within the watershed. Furthermore, it is essential that studies be long-term to minimize yearly variation in weather patterns and that the forms of P measured be standardized. Although watershed analyses combine the P

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J . C. RYDEN, J. K. SYERS, A N D R. F. HARRIS

loads of surface, subsurface, and groundwater runoff, these may be separated by determining P loads under various flow conditions in a way similar to that used by Minshall et al. (1969) and to some extent Taylor et al. ( 1971 ) . With careful selection of small watersheds in the same geographic and climatic area, accurate records of fertilizer practice, and cognizance of less diffuse or even point sources of P (e.g., effluent from animal-rearing or industrial operations) within the watershed, it should be possible to obtain meaningful estimates of the effects of various land use and fertilizer practices as well as physical variables on the loss of P from agricultural watersheds. This approach is similar to that which has been used to evaluate P loads in streams draining forest watersheds. It is also important that this be coupled with investigation to define diffuse sources of P more adequately in terms of the components which constitute such sources. Attempts have been made in this direction, as illustrated in the studies conducted by Taylor and Kunishi (1971), Cowen and Lee (1972), and Ryden et al. (1972a,b). Studies similar to these are necessary if any remedial steps are to be taken to reduce the magnitude of man-induced diffuse P sources and will be particularly valuable if carried out in conjunction with watershed analyses. Only by adopting such an approach will it be possible to provide adequate estimates of the potential of soil and fertilizer P for the P enrichment of streams; a topic which is currently surrounded by considerable controversy. Comparative tables of the relative magnitude of various P sources have been drawn up for individual watersheds (Miller and Tash, 1967; Lee et al., 1969; Jaworski and Hetting, 1970). Although such tables are useful for identification of problems within a specific watershed, extrapolation of this concept to a national basis is dangerous. Local and regional variations in land use can seriously distort the relative impact of any source of P on water quality. The way in which P source data are presented can also lead to different conclusions as to the impact of one source as opposed to another. This is particularly true for comparative tables of P sources compiled on a nationwide basis. McCarty (1967) estimates that in the United States, 4.9 X loGto 77.2 X loGkg of P per year is lost to surface waters through urban surface runoff, whereas 54.5 x lo6 to 544.8 x loG kg of P per year originates from agricultural runoff. If losses are expressed on a per area basis, relative contribution estimates are very similar if not reversed, losses being 0.23 to 3.59 and 0.12 to 1.23 kg/ha per year, respectively. These figures show the need for careful evaluation of problems within any given watershed or group of watersheds. Watershed analyses will provide more useful data than estimations of the magnitude of various P sources from a national standpoint.

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ACKNOWLEDGMENTS Research supported by the College of Agricultural and Life Sciences, University of Wisconsin, Madison, by the Office of Water Resources Research Project No. WRC 71-10 (OWRR A- 038- WIS), and by the Eastern Deciduous Forest Biome Project, International Biological Program, National Science Foundation subcontract 3351, under Interagency Agreement AG-199, 40-193-69, with the Atomic Energy Commission, Oak Ridge National Laboratory.

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CRIMSON CLOVER W . E . Knight and E . A . Hollowell .

U S Department of Agriculture. Mississippi State. Mississippi. and U.S. Department of Agriculture. Beltsville. Maryland

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C . Economic Importance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1. Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Root. Stem. and Leaf ...................................... B. Flower . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C . Pollination and Seed Development ........................... I11. Physiology ........................ ....................... A . Growth and Development . . . . . . . B. Flowering . . . . . . . . . . . . . . . . . . . C . Seed . . . . . . . . . . . . . . . . . ............................... IV . Culture ......................... A. Adaptation . . . . . . . . . . . . . . . . . . B. Soils and Soil Fertility . . . . . . . . C. Inoculation ............................................... D . Establishment . . . . . . . . . . . . ............................. E . Companion Grasses and Cro uences ...................... F . Weed Control ..................... .................... G . Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . H. Insects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I . Seed Production . . . . . . . . . . . . . . . . . . . . . . . . V. Utilization . . . . . . . . . . . ................................. A . Pasture . . . . . . . . . . ................................. B. Hay and Silage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Green Manure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D . Seed ..................................................... VI . Genetics and Cytology . . . . ................................. A . Cytology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Inheritance of Characters .............................. VII . Breeding . . . . . . . . . . . . . . . . A . Objectives . . . . . . . . . . . . . . . . . . B. Variability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C . Seed Shattering . . . . . . . . . . . . . D . Seedling Vigor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Inbreeding and Hybridization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. Cultivars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VIII . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47

48 48 48 49 50 50 50 51 52 52 54 55 57 57 57 59 59 61 62 63 63 64 65 65 66 66 67 68 68 68 69 69 70 70 70 70 71 72 73

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I.

Introduction

A.

ORIGIN

Crimson clover, Trifolium incarnatum L., of the section Trifolium, belongs to the Leguminosae (Ascherson and Graebner, 1906-1910; Coombe, 1968; Zohary, 1970). Numerous botanists have recognized many varieties, based on wild populations. The authors believe, however, that these are nothing more than variations of morphological characteristics found in large populations of plants. Crimson clover is a winter-annual clover. It is native to Europe, where it was cultivated as a forage and green-manuring crop in Italy, France, Spain, Germany, Austria, and Great Britain during the eighteenth century. In 1818, this clover was introduced into the United States. By 1855, seed was widely distributed by the United States Patent Office (Kephart, 1920). This clover has been called “scarlet clover” because of the rich scarlet flowers. It is also known as “French clover,” “Italian clover,” “German clover,” “incarnate clover,” and “annual clover” (Westgate, 1913, 1914). Foury (1950) lists more than twenty common names by which crimson clover is known throughout the world.

B.

DISTRIBUTION

The genus Trifolium consists of some 250 described species of annual, and perennial forms that are widely distributed. Pieters and Hollowell (1937) listed crimson clover, Trifolium incarnatum L.; with red, T. pratense L.; alsike, T . hybridum L.; and white, T , repens L.; as one of the four Trifolium species of primary importance in the United States. Crimson clover is grown widely as a winter annual from the Gulf Coast region, except peninsular Florida, and as far northward as Maryland, southern Ohio, and Illinois. It spread rapidly throughout the southeastern states after 1880. By 1900, it was considered a good crop as far north as Kentucky. It also is grown in the Pacific Coast states and is an important seed crop in Western Oregon (Rampton, 1969; Williams et af., 1957; Williams and Elliott, 1960). If planted late in May or early in June, it can be grown as a summer annual in northern Maine (Westgate, 1924; Kephart, 1920) and is a promising crop for high altitudes. Initially, crimson clover was used as a winter cover and green manure crop (Duggar, 1897; von Horn, 1936; Westgate, 1914; Kephart, 1920). Since it grew during the off-season of the year, it was considered to be one of the most economical legumes for green-manuring (Duggar, 1897; Kephart, 1920).

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Before 1942, the largest acreage of crimson clover was located in Tennessee, Georgia, Alabama, Kentucky, and Oregon (Hollowell, 1943-1 947, 1947, 1950). After 1942, a rapid increase in use of crimson clover occurred. Contributing to this increase are: ( a ) the development of reseeding or volunteering varieties, ( b ) recognition of the requirements of crimson clover for substantial amounts of mineral fertilizers for rapid stand establishment and vigorous growth, (c) an appreciation of its value for winter grazing, and (d) an understanding of its need for thorough inoculation (Hollowell, 1951; Hollowell and Knight, 1962). C.

ECONOMIC IMPORTANCE

Crimson clover is probably the most important annual legume in the rapidly expanding winter grazing program of the South (Stewart and Boseck, 1947; Hollowell and Knight, 1962). One of the most important characteristics of crimson clover is its ability to grow rapidly during the fall and early spring when the land is not occupied by the ordinary summer-grown crops. It, therefore, fits well into cropping systems and sequences. Other characteristics that make crimson clover the most important winter-annual legume in the South are: ( a ) it will grow under a wide range of climatic and soil conditions; ( b ) it has many uses; ( c ) it produces large yields of easily harvested seed; and ( d ) it thrives in association with other crops (Hollowell, 1951 ;Hollowell and Knight, 1962). The total acreage of crimson clover is not known. The domestic disappearance of seed reached a peak in 1951 with 37,812,000 pounds of seed used in the United States. Since 1960, domestic use of seed has declined from an annual disappearance of 16,724,000 pounds to 10,116,000 pounds in 1970. Several factors contribute to this decline: ( a ) a sudden increase in seed losses in the mid 1950’s from clover seed weevils, ( b ) more than 60% of the crimson clover acreage was in reseeding cultivars that did not require annual reseeding, thus reducing demand for seed, (c) a decline in price of seed as seed production moved to the West and peracre yields of seed increased, and ( d ) an emphasis during the 1960’s on high per-acre yields of grass forage produced with mineral nitrogen. Since 1965, considerable emphasis has been placed on arrowleaf clover. This has resulted in a shift in acreage formerly in crimson clover to arrowleaf clover. Unless some of the hazards involved in the production of arrowleaf clover are overcome, crimson clover will continue to be the reliable standby in the winter-grazing program in the South (Kight and Wellhausen, 1968). Crimson clover has several advantages over arrowleaf, Trifolium vesiculosum Savi. (Beaty and Powell, 1969; Hoveland et al., 1569; Knight

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et al., 1969). Crimson is ( a ) easier to establish, ( b ) it is easier to get effectively inoculated, (c) it will make more fall and winter forage if planted at the optimum time, (d) it reseeds more reliably under use, and (c) the seed is less expensive (Knight, 197 1 a,b) . II.

A.

Morphology

ROOT, STEM,

AND

LEAF

Crimson clover, T . incurnuturn L., has a central taproot, supported by many fibrous roots. Root development is influenced to a great extent by soil moisture and tilth. Under favorable soil-moisture conditions, seedlings make rapid growth, forming a dense crown or rosette type of leaf development. The leaves and stems resemble those of red clover, but are distinguished by the rounded tips of the leaves. The soft pubescent lower and median leaves usually have long petioles with cuneate-obovate emarginate leaflets. The leaflets of common crimson clover are essentially sessile. When crimson clover is inbred, considerable variation in leaf and stem morphology is observed (Knight, 1969b). Size, shape, and pubescence of stems and leaves vary greatly among different genotypes. Multifoliolate leaves, glabrous leaves, and petiolulate leaflet attachment were found to be characters recessive to trifoliolate leaves, pubescence, and sessile leaflet attachment (Knight, 1969b). Favilli (1952-1953) also reported a glabrous form of crimson clover. The number of stems depends greatly on stand density. In thin stands, plants tend to compensate by producing a larger rosette and more stems (Knight and Hollowell, 1959; Knight, 1967). Stem and petiole elongation are directly related to stand density (Knight and Hollowell, 1959). Earlier growth is produced from dense stands than from thin stands. B.

FLOWER

When daylength is more than 12 hours, erect hairy flower stems elongate, with many nodes and leaves. Growth is terminated by the formation of a pointed, conical flower head composed of 75-125 florets (Fig. 1 ) . The corolla is usually scarlet or deep red and extends beyond the calyx. The florets open in succession from the bottom to the top of the head. Reproductive parts of the flower consist of ten stamens and a simple pistil. One stamen is more or less separate, while the other nine stamens have fused filaments that form a tube surrounding the ovary. The legume, or pod, is included in the calyx and is usually one-seeded. The stigma extends

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FIG. 1. Flower head and leaflets of crimson clover.

beyond the stamens and is held under tension by the keel. The pollen is brought into contact with the stigma when the flower is tripped.

C . POLLINATION AND SEEDDEVELOPMENT Generally, crimson clover flowers are self-fertile, but not self-pollinating (Pieters and Hollowell, 1937). Bees in search of nectar, pollen, or both, trip the flowers and bring about pollination (Amos, 1951). The flowers produce considerable nectar available to all kinds of bees (Anonymous, 1971; Hollowell, 195 1; Hollowell and Knight, 1962). After pollination, fertilization takes place in about 18 hours, at which time the corolla wilts. The seed matures in about 24 to 30 days, and the plant dies.

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Although self-fertility is the general rule for crimson clover, self-sterile, or self-incompatible, plants were reported by James (1949) and were found in genetic studies in Mississippi (Knight, 1969a,b). Crimson clover is a highly cross-pollinated crop. James (1949) grew red and white-flowered crimson clover in close proximity and obtained 68.4% outcrossing. Similar results were obtained by Rogers ( 195 1 ) . White-flowered plants were used by Knight (1969b) to determine the effectiveness of hand pollination without emasculation. When red-flowered plants were crossed with white-flowered plants, cross-pollination varied from 54 to 86%, with an average of 75 % cross-pollination. Ill.

A.

Physiology

GROWTHAND DEVELOPMENT 1. Time of Seeding

Earliest growth of crimson clover is produced by planting annually on a well-prepared seedbed (Stewart and Boseck, 1947). If fall and winter growth is desired, the clover must be planted sufficiently early for strong plants to develop before the advent of cold weather. Naftel (1950) considered 6 weeks prior to the average date of first frost as the optimum planting time. At State College, Mississippi, crimson clover planted August 15 produced highest yields over a 6 year-period. Planting delayed until November 15 produced only 25 % as much dry forage as planting August 15. Although July planting has given early fall grazing at some locations, stand failures frequently result from severe virus infections. Moisture was the primary limiting factor to stand establishment and growth through November 1, when temperature became the critical element until about February 15. 2. Rate of Seeding

Knight and Hollowell (1959) found a close relationship between stand density and early growth (Fig. 2 ) . Crimson clover in dense stands produced earlier fall and winter growth and greater forage yields than clover in thin stands. In general, minimum soil temperature readings were higher and maximum temperature readings were lower under dense stands than under thin stands. Donnelly and Cope (1961) reported increased yields and earlier growth of crimson clover as seeding rate was increased from 10 to 30 pounds per acre. The seeding rate for crimson clover depends on the condition of the seedbed, the purpose for which the clover is grown, and the equipment used in seeding.

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Fro. 2. Comparative growth of crimson clover in spacings of % : inch (left) and 6 inches (right) on November 27, 1956 at the Mississippi Agricultural and Forestry Experiment Station.

3. Defoliation Management studies on crimson clover indicate that thick stands grow more rapidly from the start than thin stands, but do not necessarily produce highest seed yields (Knight, 1967; Knight and Hollowell, 1959; Rampton, 1969). Mowing is practiced in Oregon to remove excess growth and reduce lodging (Rampton, 1969). In Mississippi and in Oregon, early mowing had little influence on seed yields, but late mowing reduced plant recovery and seed yields (Knight and Hollowell, 1962; Rampton, 1969). Rampton ( 1969) found that mowing crimson clover decreased lodging, delayed flowering, and reduced the bulk of plant material for threshing. Mowing reduced seed size and increased the percentage of hard seed (Knight and Hollowell, 1962; Rampton, 1969). Knight and Hollowell (1962) concluded that crimson clover forage can be grazed until April without reducing total forage appreciably, and that regrowth will produce an adequate supply of seed to establish a volunteer stand. Donnelly and Cope (1961) recommended removal of grazing animals by April 1 in southern Alabama and April 15 in northern Alabama to allow reseeding. Overgrazing can prevent reseeding, because cattle will eat the seedheads if the stocking rate

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is excessive. Crowder et al. (1955) determined the effect of clipping intensity on a mixture of Arlington oats, ryegrass, and crimson clover. Dry matter yields were greatest with an 8-week interval between clippings compared to yields with 2- and 4-week intervals. Mowing or grazing during the winter months reduced the incidence of crown rot, Sclerotinia trifoliorum Eriks (Knight and Hollowell, 1959; Knight, 1959). 4 . Moisture and Temperature

Crimson clover does not withstand either extreme cold or extreme heat. Its culture is therefore limited to regions with a long period of relatively mild, moist weather (Kephart, 1920). Reports from South Carolina indicate that crimson clover is killed by 10°F (Buie, 1929). However, preconditioning of the plants by cold weather usually prevents serious winter injury to crimson clover in the Southeast. In Alabama, Frontier crimson clover, the least winter hardy variety, survived temperatures of OOF during two winters (Hoveland et al., 1964). After seedlings become well established, crimson clover makes more growth at lower temperatures than most other clover species (Hollowell and Knight, 1962). B.

FLOWERING

1. Photoperiod and Temperature Photoperiodism, conditioned by temperature, occurs in crimson clover. Differences in maturity of crimson clover genotypes have been used to distinguish cultivars described as “early” and “late” (Westgate, 1913, 1914; Kephart, 1920). The vernalization requirement for several winter annual legumes was demonstrated by McKee ( 1935b). Moistened crimson clover seed, kept for 40 days at OOC, came into flower when subsequently planted in the greenhouse, while plants from untreated seed remained vegetative. Von Gliemeroth (1943) studied the effect of germination temperature and length of day on the development of crimson clover. He found that low germination temperature accelerated plant development, shortened the vegetative phase, caused earlier flowering and maturity, and accelerated formation of generative organs. In the same study, short daylength caused a markedly prolonged vegetative phase and intensive branching, which resulted in bushy plants. Crimson clover flower stems usually elongate when the length of day exceeds 12 hours (Hollowell, 1951; Hollowell and Knight, 1962). However, date of planting experiments conducted in the field at State College, Mississippi indicate that vernalization is required before stem elongation and flowering will occur. Crimson clover planted April 1, May 1 , and June 1 flowered in April of the following

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year. In greenhouse studies conducted by Knight and Hollowell (1958), date of flowering in crimson clover was greatly affected by temperature. Earliest flowering occurred when plants 6 weeks old were shifted from outside cold frames into a greenhouse with relatively high temperature. High night temperatures from germination to maturity inhibited flower production. Crimson clover flowered earlier as length of photoperiod increased. Long daylength imposed early in the life cycle of the plant produced smaller seed heads, fewer leaves, less branching, and greater height than did shorter photoperiods. A 30-minute break in the dark period was not effective in inducing flowering in crimson clover. 2. Defoliation

Rampton (1969) found that mowing crimson clover in the spring delayed flowering until favorable pollination conditions prevailed. Heavy defoliation late in the spring reduced head size and number of viable seeds per head and resulted in smaller seed with a higher percentage of hard seed (Knight and Hollowell, 1962; Rampton, 1969). Schmidt (1921) demonstrated the importance of seed size to rapid germination and growth. Excessive defoliation could cause weakened stands. C.

SEED

1, Germination The germination requirements of the seeds of many crop plants are critical in relation to moisture, aeration, light, and the interactions of these factors. Crimson clover has been considered an exception to most of these restrictions on germination, since the seeds of this winter annual crop produce successive volunteer stands through the summer whenever moisture is adequate to induce germination. As a rule, fresh crimson clover seed is of good viability, and failure to obtain a stand is not often caused by failure of the seed to germinate (Kephart, 1920). A germination of 90% in 48 hours is not uncommon (Smith, 1928). Toole and Hollowell (1939) reported that most seed of crimson clover will germinate when planted at any time during the summer. They found no significant difference in germination of crimson clover seed from 5 to 35OC. At 35"C, germination was slower than at 25OC and below. Fayemi (1957) found low seed viability in crimson clover seed at 6.7OC. In Alabama, Hoveland and Elkins ( 1965) obtained excellent germination of crimson clover at a constant temperature of 70°F, but under a temperature regime of 40°F for 8 hours and 70°F for 16 hours, germination of crimson clover was 42%. These results, which do not agree with those of Toole

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and Hollowell (1939) and Knight (1965), suggest that seeds with low viability or pathogens may have been involved. Vaughn (1961) found a close relationship between rate of swelling and viability. Dead seeds and seeds with low viability swell quickly. Since crimson clover seeds germinate quickly, the need for adequate soil moisture at time of seeding is critical (Stitt, 1944). Seeding either immediately preceding or soon after a heavy rain increases the chance of SUCcessful stand establishment (McKee, 1935a). 2 . Impermeable Seedcoat

Before 1938, most crimson clover was of the common type with low levels of hard seed. Seeds of common crimson clover germinate rapidly after planting. Often, there may be enough moisture for germination, but not sufficient to keep the seedlings growing. The result is that seedlings die, and the stand is lost, Hard-seeded crimson clover cultivars were developed to avoid excessive early germination and to assure self-reseeding stands in the fall (Bennett, 1959; Hollowell, 1946). Elrod (1960) and Knight et al. (1964) found that, once high levels of hard seed had been attained by genetic selection, hardseededness persisted in the environment of the South. In California, Williams and Elliott (1960) found that seed coat impermeability of crimson clover declined rapidly during summer months after seed maturation, while rose clover, Trifolium hirtum All., maintained high levels of impermeable seed. The hard-seed content of varieties may vary from 30 to 75%. Apparently, hard-seed content is affected by environmental conditions while the seed is maturing. James (1949) concluded that impermeability of the seed was not inherited, unless the possible heritable factors were masked by environmental effects. Crimson clover seeds are easily scarified (Hollowell and Knight, 1962). Seeds of reseeding varieties frequently are scarified during harvesting and processing. Combine-harvested seed may contain less than 5 % hard seed when planted. 3 . Dormancy

Embryo dormancy may be defined as failure of fully imbibed and viable seed to germinate (Morley, 1961). Highly dormant seeds may not germinate in soil at high temperature even when moisture is adequate. They will remain viable despite several cycles of wetting and drying. Dormancy is considered an important ecological adaptation serving to diminish seed losses in some species. Knight (1965) reported dormancy induced by high temperature in crimson clover inbred lines. Incorporation of high temperature dormancy and

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hard seed into the same variety should reduce the hazard of stand losses in the summer when moisture is adequate but temperature is unfavorable for stand survival. 4 . Longevity

Seed longevity in crimson clover is greatly affected by harvest and processing conditions, moisture in the seed at harvest and storage, and by storage conditions (Ching et al., 1959a,b; Helmer et al., 1962; Lim, 1963). High quality seed stored under favorable conditions will retain viability for an indefinite time, whereas seed stored under ordinary warehouse conditions should not be used after two years (Ching, 1961, 1972).

IV.

A.

Culture

ADAPTATION

Crimson clover does well in the cool, humid weather that occurs in most of the South in winter (Hollowell, 1947). In the northernmost part of the region where crimson clover is grown as a winter annual, it is important to seed the crop not later than late in August (Fergus et al., 1938). When planted later in such areas as Kentucky, southern Missouri, and southern Ohio, the plants may not become well enough established to survive the winter. It is also important in these northerly areas to plant the crop in fertile soil and to grow adapted varieties.

B.

SOILS

AND

SOIL FERTILITY

Crimson clover thrives on both sandy and clay soils and is tolerant of medium soil acidity (Hollowell and Knight, 1962; Donnelly and Cope, 1961). It grows best on well-drained, fertile soils. Low or wet soils that are subject to overflow or soils with p o x internal drainage are not suited for this clover. Crimson clover will not grow on the calcareous soils or high-lime soils of the Black Belt of Mississippi and Alabama because of iron deficiency (Rogers, 1947). Crimson clovcr will produce satkfactory yields of forage on soils of medium fertility. However, on most soils, it is necessary to apply fertilizers before seeding and to make annual applications after reseeding cultivars have been established. Phosphate and potash fertilizers are the most important (Kephart, 1920; Naftel, 1942). Fertilizers containing nitrogen are not needed if plants are inoculated with an effective strain of nitrogen fixing bacteria. Where crimson clover is grown with permanent-grass sods which have received heavy nitrogen applications, attention must be given to pH

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and potassium levels, particularly if hay crops are removed (Adams and Stelly, 1958; Adams and McCreery, 1959). Most of the soils on which crimson clover is grown are acid and need lime for satisfactory production (Moser, 1941; Naftel, 1942; Davis, 1949; Page and Paden, 1949; Stewart and Pearson, 1952; Donnelly and Cope, 1961). Although tolerant of more acidity than some other legumes, such as alfalfa, sweet clover, caley peas, and white clover, crimson responds to moderate lime applications on most soils having a pH of less than 5.7 (Fig. 3 ) . A soil test is the best method for determining the amount of lime needed. Generally, if the soil pH is less than 5.7, lime is needed and should be applied at the rate of about 1 ton per acre on sandy soils and 2 tons on heavy-textured soils (Adams, 1958). James and Bancroft (1951 ) used half-plants of crimson clover to demonstrate the need for calcium in the production of hard seed.

FIG. 3. Lime is needed on many soils for top crimson clover production. This photo, made May 7, 1959, in Tallassee County, Alabama, shows effect of lime. Area in the right background had not been limed since clover establishment in 1947. Area at left and in foreground received 2 tons of lime per acre in fall of 1958 (Donnelly and Cope, 1961).

It is commonly recognized that most legumes have a relatively high requirement for boron. In North Carolina and Alabama, the addition of borax gave increases of both hay and seed yields (Piland et al., 1944; Wear, 1957). Borax increased seed yield up to 529% over no borax on

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North Carolina soils. Response to borax depends on soil type (Hendricks, 1941; Davis, 1947-1948; Page and Paden, 1949; Wear, 1957). Experiments on sandy soils in Alabama showed large increases in seed yields from 10 pounds of borax. No response was obtained on two clay soils. Borax at 10 pounds per acre is commonly recommended for seed production, and this recommendation applies equally where reseeding is desired.

C. INOCULATION The importance of inoculation with effective Rhizobium was demonstrated in early work conducted at the Alabama Agricultural Experiment Station (Duggar, 1897, 1898, 1909, 1934). In these studies, hay yields were 0 and 761 pounds per acre on uninoculated soils and 4057 and 6100 pounds per acre on inoculated soils. Inoculum used in early experiments was imported from Germany. Later, soil was used from areas on which clover had been successfully grown. Scattering soil from a field where inoculated crimson clover has been grown is no longer recommended, because it may cause weed infestation and spread disease. Specific commercial Rhizobium cultures are available (Erdman, 1946; Burton and Allan, 1950). The nitrogen-fixing bacteria are dispersed in a carrier, usually peat soil. Inoculation is more effective if the seeds are moistened with a solution containing sugar, corn syrup, or molasses. The use of syrup or molasses sticks more of the culture to the seed and helps keep the bacteria alive in the soil for as long as 2-3 weeks (Erdman, 1959). While nitrogen-fixing bacteria are extensively distributed in agricultural soils, the effective strain may become diminished in soil where clover is not grown for several years. For this reason, proper seed inoculation is essential when planting crimson clover on new land or where clovers have not been recently grown (Donnelly and Cope, 1961). The small cost is repaid many times over in earlier and greater growth (Fig. 4 ) . D.

ESTABLISHMENT

Earliest growth of crimson clover is produced by planting annually on a firm but well-prepared seedbcd (Patterson et al., 1959; Donnelly and Cope, 1961; Hollowell, 1947). If the seedbed is loose, roots grow into air pockets between soil particles, dry out, and die. Best results with new plantings result when land is plowcd or disked 6 to 8 weeks before planting and fallowed (Donnelly and Copc, 1961). This controls weeds and conserves moisture for germinating the seed and maintaining the seedlings during fall droughts.

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FIG.4. Crimson clover must be properly inoculated for healthy, vigorous growth. Plot at right was inoculated, that at left uninoculated. Photo was made January 3, 1952, at the Alabama Experiment Station Plant Breeding Unit, Tallassee, Alabama (Donnelly and Cope, 1961).

Seed can be planted with a cultipacker seeder, grain drill or broadcast seeder. About one-fourth inch is the correct depth (Moore, 1943). Ten pounds of seed per acre is sufficient if seedbed conditions are favorable and percentage germination is high. However, if grazing is desired, 20 to 30 pounds of seed per acre will provide earlier forage and grazing (Knight, 1959, 1967). To obtain reseeding stands in bermudagrass or other warm-season grasses, close grazing or mowing late in summer is necessary (Hollowell, 1947; Knight, 1967; Hoveland et al., 1971). If stands are mowed with a sicklebar mower, heavy grass residues should be removed. Warm-season grasses offer serious competition to young clover seedlings for light, moisture, and plant nutrients. Earliness of grazing is affected by the amount of such competition. Light disking before frost is often beneficial in reducing grass competition and in getting an early stand. However, Knight (1967) did not find disking a Coastal bermudagrass sod to be beneficial, provided the summer grass residue was removed. Crimson clover can be successfully introduced into dense grass sods in the establishment year by sod seeding (Coats, 1957). This method may be advantageous in some farming systems. It would, however, be more expensive than surface seeding after close clipping or burning to remove the excess grass, since clipping is also recommended before sod seeding.

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E. COMPANION GRASSESAND CROP SEQUENCES Increased yields and a longer grazing season can be obtained by planting crimson clover in mixtures with adapted winter-annual grasses. Bloat is less common in cattle on crimson than on white clover. The incidence of bloat can be greatly reduced by planting grass with crimson clover (Donnelly and Cope, 1961). When companion crops, such as rye, vetch, ryegrass, and fall-sown grains are seeded with crimson clover, the clover usually is seeded at two-thirds the normal rate and the companion crop at one-third to one-half the normal rate (Hollowell, 1947). Annual ryegrass and rescuegrass seedlings develop at about the same rate as crimson clover. Rye grows more rapidly in the fall than wheat, oats, or the annual grasses. Therefore, mixtures of rye, ryegrass, and crimson clover provide the longest grazing season (Patterson et al., 1959; Donnelly and Cope, 1961). Results of grazing studies in Mississippi indicate that crimson clover makes a profitable combination with ryegrass, oats, or wheat for beef production (Blount and Ashley, 1952; Gill and Coats, 1952, 1955, 1956). In 1952, winter pastures of ryegrass and crimson clover at Mississippi’s Brown Loam Branch Station produced the heaviest yield of beef and returned the greatest profit (Gill and Coats, 1952). Crimson clover has been seeded with excellent results on established stands of bermudagrass, dallisgrass, johnsongrass, and bahiagrass (Hollowell and Knight, 1962). In the lower South, one of the most productive combinations which approaches all-year grazing, is crimson clover and Coastal bermudagrass (Stephens and Hollowell, 1942; Preston, 1949). This mixture requires a minimum expense for maintenance compared to annually seeded forage crops and has been used successfully through 20 years (Kight and Wellhausen, 1968). Adams and Stelly (1962) estimated that 60% of the acreage of Coastal bermudagrass in the Piedmont of Alabama, Georgia, and South Carolina is seeded to crimson clover (Fig. 5 ) . In Mississippi, total forage production was 47% higher from the sequence of reseeding crimson clover-Coastal bermudagrass than from pure stands of Coastal bermudagrass fertilized with 200 pounds nitrogen per acre (Knight, 1970). This clover-grass sequence extended the grazing season 8-1 2 weeks, provided higher quality forage, and increased total production with minimum competitive effects between the legume and grass species. A legume mixture that often gives excellent results is 5 pounds of red clover and 10 pounds of crimson clover per acre (Hollowell, 1947). The crimson clover is usually predominant in the winter and spring, while the red clover continues growing in the summer after crimson clover dies. Crimson clover has been successfully grown with sericea lespedeza and to a lesser degree with kudzu (Hollowell and Knight, 1962). In Alabama,

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FIG. 5. A good crop of crimson clover in Coastal bermudagrass. Crimson clover will provide good winter grazing, followed by a good yield of seed, and fits well into grazing sequences with other crops.

crimson clover and sericea provided more grazing over a 2-year period than any other combination of grasses and legumes (Stewart, 1948; Brackeen, 1948). This mixture provided grazing for 11 months of the year.

F. WEED CONTROL Crimson clover seed yields are frequently increased when weeds, including volunteer crop plants, are controlled. Seed quality is also improved by controlling weeds whose seed are difficult to remove from crimson clover seeds. Some weeds such as dock and sorrel (Rumex spp.) and wild onion ( A l lium spp.), whose seed are difficult to separate from crimson clover seed, cannot be selectively controlled in crimson clover. Thus, seed production should not be attempted in fields infested with these weeds (Anonymous, 1971). Winter-annual grasses, henbit (Lamium amplexicaule) , chickweed (Stellaria spp.), and volunteer small grains can be controlled by using 4-5 pounds per acre of isopropyl carbanilate (propham). Propham should be applied while the weeds are very young and small, but it should not be applied until the crimson clover has at least three leaves. In the Southern States, application of isopropyl m-chlorocarbanilate (chlorpropham) at 4 pounds per acre in granular form, when the crimson clover has at least four leaves, will control these same weeds. It, like propham, will not con-

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trol the weeds if they are much beyond the early stages of emergence when treated. In the Pacific Northwest, grasses arising from seed can be controlled in crimson clover seed fields by incorporating 3-4 pounds per acre of S-ethyl dipropylthiocarbamate (EPTC) in the soil before planting. Many broadleaf weeds, such as wild geranium (Geranium spp.), pepper-weeds (Lepidium spp. ), and plants of the genus Brassica (mustards, rape, turnips), can be controlled with [ (4-chloro-o-tolyl) oxylacetic acid (MCPA). MCPA should be applied at 0.10 to 0.13 pound per acre early in spring while both weeds and crimson clover are small. If treatment is delayed until the clover begins rapid upright growth, the weeds will not be controlled, and the crimson clover will be injured.

G.

DISEASES

Although crimson clover is attacked by several diseases, no one disease consistently causes great damage. The most widespread and serious disease is crown and stem rot, caused by Sclerotinia trifoliorum Eriks. This disease attacks during cool, wet weather (Wolf and 'Cromwell, 1919). Grazing during fall and winter destroys most of the initial infection and reduces subsequent spread of the disease (Knight and Hollowell, 1959; Knight, 1959). Crimson clover is highly susceptible to sooty blotch, Cymadothea trifolii Wolf; leaf and stem spot, Cercospora zebrina Pass.; and to viruses. Sooty blotch is a leaf-spot disease most in evidence at blooming. No great loss will occur if affected areas are mowed or grazed before severe leaf damage occurs.

H.

INSECTS

Several species of insects are destructive to crimson :lover in the seedling stage, but effective control measures are known for them (Donnelly and Cope, 1961) . The insects that normally cause the most injury in young clover are the fall armyworm, several cutworms, yellow-striped armyworm, the Hawaiian beet webworm, and several bean beetles. Two species of insects, the clover head weevil, Hypera meles (Fab.), and the lesser clover weevil, Hypera nigrirostris (Fab. ) , are responsible for seed losses and a reduction in the crimson clover acreage harvested for seed in the Southeast (Bass and Hays, 1961). The principal damage is caused by larvae feeding on the flowers, ovules, and growing seeds (Thomas and Parker, 1967; Tippens, 1958). After feeding, the larvae spin lacy cocoons attached to the clover head and pupate there until emergence

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as adults (Stanley et al., 1970). Individual egg, larva, and pupa development times vary from 8 to 13, 10 to 20, and 5 to 10 days, respectively (Thomas and Parker, 1967; Machado, 1964). The first reports of effective chemical control of H. meles came from Georgia, where applications of granular insecticides gave excellent control of the clover head weevil and increased seed yields 67 to 112% in 1957 and 1958, respectively (Beckham, 1956; Tippens, 1958). In Alabama, good control of seed weevils was reported when granular insecticides were applied. Best seed-yield increases resulted from application of insecticides at the prebloom stage of growth (Reed et al., 1962; Donnelly and Cope, 1961; Hays, 1964). When infestation by seed weevils is severe, reseeding varieties may fail to produce sufficient seed for volunteer stands the following fall. I.

SEEDPRODUCTION

One of the reasons why crimson clover is so important as a winter annual legume in the South is its capacity to produce an abundance of seed even under relatively adverse conditions ( Hollowell, 1951; Hollowell and Knight, 1962). The tripping of the florets is essential for pollination and seed setting. Placing colonies of honeybees in or near to blooming fields is highly recommended for maximum seed production (Amos, 1951 ; Knight and Green, 1957; Blake, 1958). Two colonies of bees per acre are recommended. If the clover is well fertilized, soil moisture is adequate, and cattle are removed early to allow good growth, three colonies per acre will prove profitable. If the clover is not to be harvested for seed but is expected to reseed itself in the fall, bees are still needed to produce enough seed for the volunteer crop. With good stands and pollination, the seed set may range from 1000 to 1200 pounds per acre (Hollowell and Knight, 1962). The average harvested seed yield is about 250 pounds per acre. Serious seed losses often occur in harvesting. Timeliness in harvesting is important, as the seed shatters readily when mature. When seed is harvested from standing plants, the crop must be fully mature for best results. A greater risk is taken when this method is used, since one heavy rain or windstorm may cause extensive shattering losses (Hollowell, 1947). If the clover is to be picked up from the swath or windrow, the crop usually is cut when about three-fourths of the seed pods have turned a golden brown (Fig. 6 ) . Shattering losses may be minimized by cutting when the plants are damp with dew. The less the seed crop is handled when dry, the less the seed loss from shattering. Regardless of the harvesting method, the seed should be rough cleaned and dried as

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FIG.6. A combine with pickup attachment threshing a crimson clover seed crop that dried in the swath.

quickly as possible to prevent heating and browning, which usually reduces germination (Donnelly and Cope, 196 1) . V.

Utilization

A.

PASTURE

Crimson clover has been used for years to extend the grazing season, increase total forage production, improve forage quality, and make better use of land resources. The value of crimson clover as a grazing crop was recognized early in its use in the United States (Voorhees, 1894; Duggar,

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1909; Grantham, 1911; Westgate, 1914). An expanding livestock economy in the South and the development of reseeding crimson clover cultivars caused a rapid increase in the use of crimson clover for grazing in the 1940’s and 1950’s (Lowery, 1939, 1943; Hendricks, 1941; Lowery and Harbor, 1945; Stewart and Boseck, 1947; LaMaster, 1950; Holt el al., 1951;Langford, 1957). Animals grazing on crimson clover seldom bloat (Henson and Hollowell, 1960). However, animals that are hungry should not be placed in a fast growing field of clover. Bloat is less likely to occur on a mixture of clover and grass or grain than on clover alone. This legume will provide good winter grazing and later a seed crop (Hollowell, 1951; Hollowell and Knight, 1962). This profitable combination fits well into grazing sequences with other crops such as bermudagrass and bahiagrass (Knight and Hollowell, 1962). During winter, carrying capacity is considerably less than during the spring months when growth is most rapid. Four to six weeks before flowering, livestock can be removed from the clover, permitting the clover to make seed. B.

HAY AND SILAGE

The quality of crimson clover hay is highest if the crop is cut for hay at the early-bloom stage ( Hollowell, 1947). Voorhees ( 1894) concluded that crimson clover hay was superior to red clover, and Emery and Kilgore (1894) found it to be highly digestible and suitable as a feed in association with concentrates. Crimson clover is not often cut for hay, since it reaches hay stage in the spring during periods of frequent rains. Crimson clover cures slowly because of its high moisture content and the wet weather during the season of the year when it is harvested. A good stand will yield from one to 2.5 tons of dry hay per acre, depending on growth conditions and intensity of grazing. Mixtures with small grains produce higher yields and are less likely to lodge. Crimson clover in pure stands or in mixtures may be made into silage by methods used for other legumes. Since frequent rains may occur during hay harvest, this method of feed preservation is less hazardous. C.

GREENMANURE

In Alabama, Duggar (1897) recognized the potential value of crimson clover as a soil-improving crop and considered it the most important plant for improvement of cotton soils. A good growth of green manure will produce as much corn as 60-90 pounds of commercial nitrogen (Cope, 1955).

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With the development of relatively inexpensive sources of mineral nitrogen, the use of winter legumes for soil improvement has declined. However, crimson clover remains an important crop for use in many rotations. In pecan, peach, tung, and other orchards (Bregger, 1951; Donnelly and Cope, 1961; Hollowell and Knight, 1962), it may be allowed to reseed and does not have to be incorporated to make the nitrogen available to the trees (Fig. 7 ) . This clover was regarded more for its ornamental value than as a forage crop before its value for agricultural purposes was appreciated (Kephart, 1920). In, recent years, it has been used extensively for roadside stabilization and beautification throughout the southeastern United States. Frequently, bermudagrass or bahiagrass is grown in succession with the clover and receives 100-200 pounds of N per acre from the clover residue (Erdman, 1959; Knight, 1970).

FIG. 7. Crimson clover is well adapted for use in orchards for grazing and green manure. Here CHIEF crimson clover is shown growing in a 1-year-old tung orchard.

D.

SEED

Production of good seed yields is another reason for the importance of crimson clover. It is an important seed crop in Oregon and in the South (Donnelly and Cope, 1961; Rampton, 1969). Seed may be mechanically harvested in three ways: ( 1 ) Combined direct from standing plants; (2) cut with a mower and left in the swath or windrow to dry, then picked up and threshed with the combine; and ( 3 ) cut with a mower and left in the swath or windrow to dry, then hauled to a stationary huller or thresher.

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Letting the crop dry in a swath or windrow permits earlier cutting, which reduces harvest shattering losses. Swathing or windrowing ,also reduces the risk of having seed shattered by strong winds or rain. Cutting and windrowing when the heads are damp and tough keeps shattering at a minimum. Because heads must be dry for direct combining, there is considerable shattering loss with this method of harvesting. Harvest when most of the hulls are light brown if the seed is stripped or cut with a mower. Wait until the hulls are dark brown for direct combining. Drying harvested seed usually is necessary in humid areas to lower moisture content to a safe level for storing. Drying may be done with hot-air driers, or seed may be thinly spread under shelter and frequently turned until dry enough to store. Remove trash and weed seed as soon as possible after harvest. Preharvest defoliation has not been very successful in humid areas. It is successful if the weather is dry at harvest time.

VI.

Genetics and Cytology

A. CYTOLOGY Crimson clover is a diploid annual with a generally accepted somatic chromosome complement of 2n = 14 (Britten, 1963; Favilli, 1952-1953; Hollowell and Knight, 1962; Pritchard, 1969; Wexelsen, 1928). Meiosis is regular, and the chromosomes pair as bivalents. None of the recent studies of the cytological behavior of crimson clover have agreed with Bleier ( 1925), who reported N = 8.

B. INHERITANCE OF CHARACTERS DeCillis ( 1914) reported success in selecting for various characteristics in crimson clover. The first efforts in crimson clover improvement in the United States were directed toward incorporating the hard-seed character into existing strains (Hollowell, 1946; Bennett, 1958, 1959; James, 1949; Rogers, 195 1 ) . This was successfully ' accomplished through the use of natural- and mass-selection techniques. James ( 1949) believed that the impermeability of crimson clover seed was not inherited, unless the possible heritable factors were masked by environmental factors. However, in Mississippi, efforts to isolate lines with a high percentage of hard seed were successful and indicated good heritability of this character (Bennett, 1958, 1959). Rogers (1951) also found selection for increasing hard seed percentages in crimson clover seed to be effective.

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Sandal (1955) described the inheritance of white flower color as a simply inherited recessive characteristic. He suggested the symbols Cr, cr for the alleles controlling flower color, the dominant gene being necessary for red flower color. Picard (1956) described the inheritance of several simply inherited mutant forms in crimson clover. He described variations between varieties and plants, but he did not report the inheritance of any of these characteristics. Inheritance of a male-sterile character was studied in the F,, F,, and F, by Knight (1969a). Sterility in this mutant was caused by the absence of anthers and was associated with multiple ovaries and absence of petals. Apparently, these characteristics are controlled by a single recessive gene pair with pleiotropic effects or closely linked genes. Inheritance of leaflet characteristics have also been studied in crimson clover (Picard, 1956, 1959; Knight, 1969b). Picard (1956) found albinism, absence of chlorophyll, and variations in flower colors. He suggested that a simply inherited two-unifoliolate-leaf character might be used as a genetic marker in seedling plants. Knight (1969a) determined that multifoliolate leaf, pubescent leaf, and petiolulate leaflet attachment were each determined by a simple recessive gene in the homozygous condition. In other studies, Knight and Lee (1971 ) found that a variegated flower color was controlled by two dominant genes; in the absence of either dominant gene, the flowers are white. A mutant sticky-leaf character was found to be controlled by a double recessive gene pair (Lee, 1969). Inheritance studies of crimson, deep pink, medium-pink, light-pink, lavender, and maroon flower colors indicated that crimson, deep- and medium-pink flower colors are under monogenic control (Sullivan, 1971; Sullivan et al., 1972). The remaining flower color mutants are under digenic control. Anthocyanins in color mutants of crimson clover were extracted and identified (Sullivan et al., 1972). All color mutants contained 3-glucoside and cyanidin 3-glucoside. The distinction between crimson and the varying pink forms was found to be caused by differences in concentration. Maroon flowers contained two additional pigments, cyanidin 3-sambubioside and an unidentified cyanadin 3-glucoside.

VII.

A.

Breeding

OBJECTIVES

Crimson clover breeding programs in the United States have been concerned with improvement and development of varieties to increase forage yields and reseeding ability. In addition to hard seed, breeding objectives

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KNIGHT AND E. A. HOLLOWELL

have involved seedling vigor, earlier fall growth, winterhardiness, resistance to seed shattering, and resistance to lodging. In spite of serious annual losses to insects and diseases, very little has been done to develop insectand disease-resistant varieties. B.

VARIABILITY

Crimson clover is less variable than most Trifolium species. Since this species is generally self-fertile, it is easy to inbreed and select for various characters within and among inbred lines. Upon inbreeding, wide differences are found for vigor and many plant characteristics. Vigor in some lines is reduced by inbreeding, until maintenance of the line is impractical. On the other hand, other plants lose very little vigor, and inbred lines can be maintained easily for a number of generations. Rogers (1951) suggested using these vigorous lines in a breeding and hybridization program.

C. SEEDSHATTERING Losses of crimson clover seed are severe when storms occur after the seed crop is ripe. In Mississippi, recurrent selection has been effective in obtaining genotypes with better seed retention and resistance to lodging.

D. SEEDLING VIGOR Seed size and seedling vigor are closely related in crimson clover. In 1962, a large-seeded crimson clover variety was released (Knight, 1963). In FRONTIER crimson clover, seedling vigor and early growth were associated with seed size, an indication that further improvement could be made for this characteristic by selecting large seed. At seven Alabama locations, the large-seeded FRONTIER variety exceeded the AUTAUGA variety by an average of 40% more dry forage in the fall and winter (Hoveland et al., 1964).

E. INBREEDING AND HYBRIDIZATION Crimson clover is easily inbred. Since the florets require tripping for pollination and seed set, the seedheads may be bagged in small cloth bags or the plants can be grown in an insect-free environment. Rolling the heads between the fingers effectively trips the florets. Seedheads should be rolled every few days as long as fresh florets are present on the head. Selection for general combining ability via the polycross method within

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and among selfed lines is effective in isolating superior lines for use in single and double-cross hybrids. Single- and double-cross hybrids can be made under saran-cloth bee cages or in isolated field crossing blocks. Lines chosen for insect or disease resistance could be effectively recombined by this method. Inbred lines selected for forage yield and combined in double-cross combinations have been equal to standard cultivars and in some cases superior in forage yield.

F. CULTIVARS The greatest differences between existing cultivars are time of maturity, percentage hard seed, and early fall growth. Before World War 11, all crimson clover was of the common type. More than half of the seed produced now is of the reseeding type. The term “reseeding” designates a type that produces good volunteer stands in the fall from seed shattered the previous spring. Fall volunteer stands are made possible by a hard seedcoat that delays germination from late spring, when the seed shatters, until fall. Common crimson clover is not a reseeding type. Five named varieties of the reseeding type are widely used. These are: DIXIE, AUBURN, AUTAUGA, CHIEF,and TALLADEGA. There are other reseeding strains less widely used. DIXIE,AUBURN, and AuTAUGA are early varieties-their seed matures about a week earlier than seed of CHIEF and TALLADEGA. They are also earlier than the common type. The early varieties make slightly more growth during the winter than the late varieties; the late varieties make more of their growth in the spring and can be grazed longer in the spring. DIXIEappears to be the most winter hardy crimson clover in the upper part of the South. A soft-seeded crimson clover variety named FRONTIER was released in 1962 by the Mississippi Agricultural Experiment Station in Cooperation with the Crops Research Division, USDA; likewise, a reseeding variety named TIBBEE was released in 1970 (Knight, 1963, 1972). FRONTIER and TIBBEE have the following characteristics : large seed size, superior seedling vigor, greater fall and winter growth, equal or superior forage and seed yields, and early maturity. The new varieties were derived from a plant introduction received from Italy in 1956 (PI-233,812). Under dry summer conditions such as occur in Oregon, shattered seed of common crimson behaves as the reseeding types. Volunteer stands from shattered seed occur with the advent of fall rains. Such seed is not of the reseeding type. The use of certified seed is the only way that consuming farmers can be assured of obtaining seed true to variety name as well as to avoid excessive numbers of noxious weed seeds.

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VIII.

Conclusions

The southeastern United States has the land and water resources for a thriving livestock economy. It is estimated that in Mississippi alone there are about 4,000,000 acres of improved permanent pasture. Of this total, only 1,000,000 acres has a legume growing in combination with grass. An abundance of high-quality forage with good seasonal distribution is the foundation for cattle profits. Economical production of this highquality forage is essential for the continued growth and success of the livestock industries. Labor and machinery costs involved in the production, handling, storage, and preservation of feed for livestock continually increase. Systems of year-round grazing that permit the animal to harvest most of the feed consumed should result in economical production of milk and beef. Through the years, reseeding crimson clover and Coastal bermudagrass has provided one of the most productive and economical systems. Generally, perennial grasses fertilized with heavy quantities of nitrogen produce more dry matter and total TDN/A than do pastures composed of legumes and grasses. However, the use of large quantities of nitrogen on grass pastures is questionable from the economic standpoint under many management systems. Yield alone does not necessarily make a practice economically efficient; but rather the amount of quality forage consumed and converted into beef and milk. There is universal acceptance of the fact that legume forage is highly digestible. This digestibility may range from 60 to 80% of digestible dry matter. Intake, by the animal, of legume or grass-legume mixtures is much greater than that of grass alone, even when the grass is fertilized heavily. Yields from crimson clover and grass mixtures usually compare favorably to grass alone fertilized with 100-200 pounds of nitrogen. In recent years, a renewed interest has developed in the utilization of annual clovers in pastures. Contributing to this has been an emphasis on use of idle acres, nitrate pollution, better-quality forage, and grazing systems for livestock. The economic advantage of clover-grass pastures has been demonstrated with both dairy and beef animals. Some of the less obvious, yet highly economic, benefits of clover in pastures involve animal health, milk flow, calf weaning weights, and conception rate. Economic analyses of grazing systems indicate that an increased emphasis will be placed in the future on the use of adapted clover varieties in grazing systems. Proper use and management of crimson clover in these systems should result in large economic gains to the livestock industry in the Southeast. This will require more widespread use of superior varieties already

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available, as well as others made available through future development. Economic gains would accrue to both beef and dairy farmers through an extended grazing season, increased forage production, increased forage quality, better utilization of land resources a stimulation of milk flow, higher calf weaning weights, and better calving percentages.

REFERENCES Adams, F. 1958. Ala., Agr. Exp. Sra., Bull. 301. Adams, W . E., and McCreery, R. A. 1959. Better Crops Plant Food 43(4). Adams, W. E., and Stelly, M. 1958. Agron. J. 50, 457459. Adams, W. E., and Stelly, M. 1962. J . Range Manage. 15, 84-87. Amos, J. M. 1951. Amer. Bee J. 91, 331-333. Anonymous. 1971. U.S., Dep. Agr., Leafl. 482. Ascherson, P., and Graebner, P. 1906-1910. Vol. 6, Part 2, p. 544. Englemann, Leipzig. Bass, M. H., and Hays, S. B. 1961. Ala., Agr. Exp. Sta., Highlights Agr. Res. 8, 1. Beaty, E. R., and Powell, J. D. 1969. J. Range Manage. 22, 36-39. Beckham, C. M. 1956. J . Econ. Entomol. 49, 542-544. Bennett, H. W. 1958. Miss. Farm Res. 21, 10. Bennett, H. W. 1959. Agron. J . 51, 15-16. Blake, G. H., Jr. 1958. 1. Econ. Entomol. 51, 523-527. Bleier, H. 1925. Jaltrb. Wiss.Bor. Pringslreini 64, 604-636. Blount, C. L., and Ashley, T. E. 1952. Miss. Farin Res. 15, 8. Brackeen, L. 0. 1948. Better Crops Plant Food 32, 17-18. Bregger, J. T. 1951. N.J. State Hort. Soc. N32,2408. Britten, E. J. 1963. Cytologia 28, 428-449. Buie, T. S. 1929. S. Car., Agr. Exp. Sta., Circ. 37. Burton, J . C., and Allan, 0. N. 1950. Soil Sci. Soc. Amer., Proc. 14, 191-195. Ching, T. M. 1961. Agron. J . 53, 6-8. Ching, T. M. 1972. Crop Sci. 12, 415-418. Ching, T. M., Parker, M. C., and Hill, D. D. 1959a. Agron. J. 51, 650-684. Ching, T. M., Taylor, H., and Jensen, L. A. 1959b. Proc. Assoc. Off. Seed Anal. 49, 167-1 72. Coats, R. E. 1957. Miss.,Agr. Exp. Sra., Bull. 554. Coombe, D. E. 1968. “Flora Europaea Organization,” Vol. 2. Cambridge Univ. Press, London and New York. Cope, J. T., Jr. 1955. AIa.# Agr. Exp. Sta., Higlrliglits Agr. Res. 2, 3. Crowder, L. V., Sell, 0. E., and Parker, E. M. 1955. Agvon. J . 47, 51-54. Davis, F. L. 1947-1948. Ala., Agr. Exp., Sra. Annu. Rep. 58/59. Davis, F. L. 1949. Agrorr. 1. 41, 368-374. DeCillis, E. 1914. Annu. Rep. Scuolo Sup. Agr. Portici [12] 2, 721-726. Donnelly, E. D., and Cope, J. T., Jr. 1961. Ala., Agr. Exp. Sta., Bull. 335. Duggar, J . F. 1897. Auburn Univ.(APZ), Agr. E x p . Sta., Bull. 87. Duggar, J . F. 1898. Auburn Univ. ( A P I ) ,Agr. Exp. Sta., Bull. 96. Duggar, J . F. 1909. Auburn Univ. ( A P I ) , Agr. E x p . Sta., Bull. 147.

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Duggar, J. F. 1934. J . Amer. SOC. Agron. 26, 919-923. Elrod, J. M. 1960. G a . , Agr. Exp. Sra., Mimeogr. Ser. [N. S.] 91. Emery, F. C., and Kilgore, B. W. 1894. N. Car., Agr. Exp. Sta., Bull. 97. Erdman, L. W. 1946. Soil Sci. SOC. Amer., Proc. 11, 255-259. Erdman, L. W. 1959. U S . , Dep. Agr., Farmers’ Bull. 2003. Favilli, R. 1952-1953. Univ. Pisa Inst. Agron. Gen. Colrivazioni Erbage, Exp. Rec. [N. S.] 6, 53-77. Fayemi, A. A. 1957. Agron. J . 49, 75-76. Fergus, E. N., Kenny, R., and Johnstone, W. C. 1938. Ky., Agr. Ex?. Circ. 318. Foury, A. 1950. “Les Cahiers de la Recherche Agronomique,” Vol. 3. Rabat, Morocco. Gill, J. B., and Coats, R. E. 1952. Miss. Farm Res. 15, 8. Gill, J. B., and Coats, R. E. 1955. Miss. Farm Res. 18, 7. Gill, J. B., and Coats, R. E. 1956. Miss. Farm Res. 19, 8. Grantham, A. E. 1911. Dela., Agr. Exp. Sra., Bull. 89. Hays, S . B. 1964. 1. Econ. Entomol. 58, 481-484. Helmer, J. C., Delouche, J. C., and Lienhard, M. 1962. Proc. Ass. Of. Seed Anal. 52, 154-161. Hendricks, H. E. 1941. Tenn., Agr. E x / . Spec. Circ. 146. Henson, P. R.,and Hollowell, E. A. 1960. US.,Dep. Agr., Farmers’ Bull. 2146. Hollowell, E. A. 1943-1947. Yearb. Agr. (US.Dep. A g r . ) pp. 427-432. Hollowell, E. A. 1946. US.,Dep. Agr. Mimeogr. BPIS & AE. Hollowell, E. A. 1947. U.S., Dep. Agr., Leap. 160. Hollowell, E. A. 1950. U.S., Dep. Agr., Mimeogr. BPIS & AE. Hollowell, E. A. 1951. In “Forages” (H. D. Hughes, M. E. Heath, and D. S. Metcalfe, eds.), 1st ed., pp. 206-214. Iowa State Coll. Press, Ames. Hollowell, E. A., and Knight, W. E. 1962. In “Forages” (H. D. Hughes, M. E. Health, and D. S. Metcalfe, eds.), 2nd ed., pp. 180-186. Iowa State Univ. Press, Ames. Holt, E. C., Potts, E. C., and Kapp, L. C. 1951. Tex., Agr. Exp. Sra., Progr. Rep. 1403, 1-5. Hoveland, C. S., and Elkins, D. M. 1965. Crop Sci. 5 , 244-246. Hoveland, C. S, Creel, J. M., and Webster, H. L. 1964. Ala., Agr. Exp. Sta., Highlights Agr. Res. 11. Hoveland, C. S., Carden, E. L., Buchanan, G. A., Evans, E. M., Anthony, W. B., Mayton, E. L., and Burgess, H. E. 1969. Ala., A g r . Exp. Sra., Bull. 396. Hoveland, C. S., Carden, E. L., Wilson, J. R., and Mott, P. A. 1971. A h . , Agr. Exp. Sta., Highlights Agr. Res. 18, 12. James, E. 1949. Agron. J . 41, 261-266. James, E., and Bancroft, T. A. 1951. Agron. J . 43, 96-98. Kephart, L. W. 1920. US.,Dep. Agr., Farmers’ Bull. 1142. Kight, T . G., and Wellhausen, H. W. 1968. Progr. Farmer No. 9, p. 20. Knight, W. E. 1959. Miss., Agr. Exp. Sta., Bull. 583. Knight, W. E. 1963. Crop Sci. 3, 460. Knight, W. E. 1965. Crop Sci. 5, 422-425. Knight, W. E. 1967. Agron. J. 59, 33-36. Knight, W. E. 1969a. Crop Sci. 9, 94-95. Knight, W. E. 1969b. Crop Sci. 9, 232-235. Knight, W. E. 1970. Agron. 1. 62, 773-775. Knight, W. E. 1971a. Miss. Farm Res. 34, 4. Knight, W. E. 1971b. Agron. J . 63, 418-420.

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Knight, W. E. 1972. Crop Sci. 12, 126. Knight, W. E., and Green, H. B. 1957. Miss. Farm Res. 20, 3. Knight, W. E., and Hollowell, E. A. 1958. Agron. 1. 50, 295-298. Knight, W. E., and Hollowell, E. A. 1959. Agron. I . 51, 73-76. Knight, W. E., and Hollowell, E. A. 1962. Crop Sci. 2, 124-127. Knight, W. E., and Lee, H. S. 1971. Agron. Abstr. 10. Knight, W. E., Donnelly, E. D., Elrod, J. M., and Hollowell, E. A. 1964. Crop Sci. 4, 190-193. Knight, W. E., Ahlrich, V. E., and Byrd, M. 1969. Crop Sci. 9, 393. LaMaster, J. P. 1950. S. Car., A g r . Exp. Sin., Bull. 380. Langford, W. R. 1957. Ala., A g r . Exp. Sta.. Higlrliglits Agr. Res. 4, 4. Lee, H. S. 1969. M. S. Thesis, Mississippi State University, Stale College, Mississippi. Lim, S. M. 1963. Thesis, Mississippi State University, State College, Mississippi. Lowery, J. C. 1939. Ala., Agr. Ext. Circ. 167. Lowery, J . C. 1943. Ala., Agr. Ext. Circ. 254. Lowery, J. C., and Harbor, A. R. 1945. A l a . , Agr. E x t . Circ. 312. Machado, W . C. 1964. M.S. Thesis, Louisiana State University, Baton Rouge. McKee, R. 1935a. I . A m e r . SOC.Agron. 27, 642-643. McKee, R. 1935b. U S . , Dep. Agr., Circ. 377. Moore, R. P. 1943. 1. A m e r . Soc Agron. 35, 370-381. Morley, F. H. W. 1951. Advan. Agron. 13,57-123. Moser, F. 1941. S. Car., Agr. Exp. Sta., Annir. Rep. p. 39. Naftel, J. A. 1942. 1. A m e r . Soc. Agron. 34, 975-985. Naftel, J. A. 1950. Better Crops Plant Food 34, 5. Page, N . R., and Paden, W. R. 1949.. Soil Sci. Soc. Amer., Proc. 14, 253-257. Patterson, R. M., Anthony, W. B., and Brown, W. L. 1959. Ala., A g r . E x p . Sta., Higlrliglits Agr. Res. 6, 3. Picard, J. 1956. Ann. Inst. Nut. Reck. Agron., Ser. B 6, 527-529. Picard, J . 1959. Ann. Inst. Nut. Rech. Agron., Ser. B 9, 319-331. Pieters, A. J., and Hollowell, E. A. 1937. Yearb. Agr. (U.S. Dep. A g r . ) pp. 1190-1214. Piland, J. R., Ireland, C . F., and Reisenauer, H. M. 1944. Soil Sci. 57, 75-84. Preston, J. B. 1949. Crops Soils 1, 32. Pritchard, A. J. 1969. Aust. I . Agr. Res. 20, 883-887. Rampton, H. H. 1969. Agron. J . 61, 92-95. Reed, J . K., Park, J, K., Hays, S. B., and Webb, B. K. 1962. S. Car., Agr. Exp. Sta., Circ. 134.

Rogers, T. H. 1947. J . A m e r . Soc. Agron. 39, 638-639. Rogers, T. H. 1951. Ph.D. Thesis, University of Minnesota, St. Paul. Sandal, P. C. 1955. Agron. J . 47, 147-148. Schmidt, D. 1921. N . I . , Agr. Exp. Sta. 42nd Annu. R e p . p. 3 3 3 . Smith, K. E. 1928. Proc. Ass. Off.Seed Anal. 19/20, 62-64. Stanley, R. L., Randolph, N. M., and Teetes, G. L. 1970. J . Econ. Entorno/. 63, 256-258. Stephens, J. S., and Hollowell, E. A. 1942. J . Arner. Soc. Agron. 34, 1057-1059. Stewart, F. 1948. Ala., A g r . E x p . Sta., Progr. Rep. Ser. 40. Stewart, F., and Boseck, J. 1947. Ala., Agr. E x p . Sta.. Progr. R e p . Ser. 9. Stewart, F., and Pearson, R. W. 1952. Agron. J . 44, 501-502. Stitt, R. E. 1944. J . Anzer. Soc. Agron. 36, 464-467. Sullivan, S. L. 1971. M.S. Thesis, Mississippi State University, State College, Mississippi.

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Sullivan, S. L., Baetcke, K. P., and Knight, W. E. 1972. Pkytochemisfry 11, 2525-2526. Thomas, J . G., and Parker, F. W. 1967. Ter., Agr. E r t . Ser., Entomol. Notes 8, 10. Tippens, H. H. 1958. J. Econ. Entornol. 51, 459-460. Toole, E. H., and Hollowell, E. A. 1939. 1. Amer. SOC. Agron. 31, 604-619. Vaughn, C. E. 1961. Miss., Agr. E r p . Sta., Inform.Sheet 313. von Gliemeroth, G. 1943. J. F. Landwirt. 89, 123-150. von Horn, A. 1936. Mitt. Landwirt. 51, 225-226. Voorhees, E. B. 1894. N.J., Agr. E r p . Sta., Bull. 100. Wear, J. I. 1957. Ala., Agr. Exp. Sta., Bull. 305. Westgate, J . M. 1913. U S . , Dep. Agr., Farmers’ Bull. 550. Westgate, J. M. 1914. U S . , Dep. Agr., Farmers’ Bull. 579. Westgate, J . M. 1924. U S . , Dep. Agr., Farmers’ Bull. 1411. Wexelsen, H . 1928. Univ. Calif. Agr. Sci. 2, 355-376. Williams, W. A., and Elliott, J. R. 1960. Ecology 41, 785-790. Williams, W. A., Love, R. M., and Berry, L. J. 1957. Calif., Agr. Exp. Sfa., Err. Ser. Circ. 458. Wolf, F. A., and Cromwell, R. 0. 1919. N . Car., Agr. Exp. Sta., Biill. 16. Zohary, M . 1970. “Flora of Turkey and the East Aegean Islands,” Vol. 3, p. 425. Edinburgh Univ. Press, Edinburgh.

ZERO-TILLAGE

. . .

K . Baeumer and W A P Bakermans Faculty of Agriculture. University of Goettingen. Goettingen. Federal Republic of Germany. and Institute far Biologicol a n d Chemical Research of Field Crops and Herbage. Wageningen. The Netherlands

I . Introduction: The Concept of Zero-Tillage . . . . . . . . . . . . . . . . . . . . . . . . A Historical Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Definition of Zero-Tillage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C . Motivation for Zero-Tillage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1 Comparison of Environmental Conditions in Tilled and Untilled Soils . . . A . Macroscopic Soil Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Soil Flora and Fauna . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C Soil Organic Matter . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D . Parameters of Soil Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E . Aeration and Soil Moisture . . . . . . . F. Soil Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . G . Soil Erosion . . . . . . . . H Soil Trafficability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I. Nutrient Concentration and Distribution ....................... I11. Effects of Zero-Tillage on Plant Growth .................. A . Germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Root Growth ...... ................ C . Nutrient Absor n ........................................ D. Crop Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ... E. Changes in Weed Populations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. Diseases and Pests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV . Crop Husbandry . . . .......................... A . Sowing Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Weed Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Pasture Renovation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Crop Yields and Cropping Systems . . ....................... V . Evaluation of Zero-Tillage in Farming Systems ..................... A . Applicability of Zero-Tillage in Humid, Temperate Climate Regions B. Applicability of Zero-Tillage to Dryland Farming . . . . . . . . . . . . . . . . VI . Conclusion . . . .............................................. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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78 78 78 79 80 80 81 82 84 87 91 92 92 93 95 95 96 97 99 101 102 103 103 104 106 108 109 114 114 118 119 120

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78 I.

Introduction: The Concept of Zero-Tillage

A.

HISTORICAL BACKGROUND

Moldboard ploughing or similar deep-tillage operations have for centuries been a feature of the more advanced systems of crop production. Nowadays, some farmers still consider it profitable to use the ever-increasing supply of more powerful tractors for ploughing deeper each year. Nonetheless, the concept of tillage requirements for crop production is changing rapidly. In 1927, Garber successfully ovcrsowed a legume into an unproductive grass sod without tillage using such simple techniques as close grazing or burning and heavy seed rates to manipulate the competition between the old sward and the surface sown forage species as well as the hooves of grazing animals to bring the seeds into close contact with the soil. This was an early demonstration of the essential features of zero-tillage, i.e., growing a crop with the least possible soil disturbance, which involves controlling unwanted vegetation by other than mechanical means. Realization of such a system became feasible in the 1950’s, when chemicals such as dalapon, amitrole, and atrazine, which can destroy the existing vegetation with relatively short or no residual effect on the crop to be established, were introduced. First used successfully in pasture renovation, the concept of zero-tillage received support as a consequence of the encouraging results obtained by mulch-farming practices in the United States where the till-plant system was developed for row crops in order to provide year-round protection of the soil from erosion and to minimize planting costs. This system can be regarded as a forerunner of zero-tillage which was initiated in the 1960’s and has since been used increasingly in the United States. For 1971, zerotillage production of maize, soybeans, sorghum, and cotton in the United States has been estimated at 438,600, 130,200, 22,900, and 2000 ha, respectively (D. M. Van Doren, personal communication, 1972). In Europe, the introduction of broad spectrum, nonresidual herbicides of the bipyridyl types opened new perspectives. Here, Great Britain takes the leading position with regard to zero-tilled acreage, which was doubled between 1970 and 1971. The census for zero-tillage production of fodder Brussicae, cereals and grassland in 1971 is recorded to be 19,600, 7500, and 4700 ha, respectively (J. T. Braunholtz, personal communication, 1972). B.

DEFINITION OF ZERO-TILLAGE

The term “conventional tillage” will be used here to designate the traditional tiIlage system, which typicaIIy begins with a primary deep tillage

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operation followed by some secondary tillage for seedbed preparation. Weed control after planting is effected by preemergence and/or postemergence cultivations and/or herbicide applications. The term “zero-tillage” is used to designate a tillage system in which mechanical soil manipulation is reduced to traffic and seedbed preparation only. It can be considered to be the most extreme form of minimum tillage, which, as a category of tillage systems, not only includes methods resulting in reduced tillage intensity but also the combined use of several implements in one operation, such as the plow-plant method. The term “direct-drilling” will be avoided in this review as it is used by horticulturists to mean sowing crops onto the final location instead of transplanting young plants grown as seedlings elsewhere. In zero-tillage studies, several tillage methods are usually compared with a standard conventional one. If in the following sections the term “zero tillage’’ is used, &hemost extreme form of zero-tillage examined has always been selected, if not otherwise stated.

C. MOTIVATION FOR ZERO-TILLAGE Soils are tilled to provide conditions suitable not only for optimum plant growth, but also for necessary field operations, e.g., planting and harvesting. But ncither the feasibility for, nor the advantage of, such a deep primary tillage operation is always given. An alternative to the conventional tillage system is most urgently needed where soils are subject to wind and water erosion, timing of tillage operations is too difficult, performance insufficient, and requirements of energy and labor too high. On slopes, bare, compactcd soils high in silt and fine sand content but low in organic matter content are exposed to soil erosion, especially when farmed continuously with a row cropping system. Only an improved soil structure such as is found under sod where organic matter is accumulated at the soil surface and aggregate stability is stimulated can reduce the risk of soil erosion. Very heavy, or shallow and stony soils are really marginal for arable farming undcr present economic conditions. Yet, as these occur in large areas in the world, methods must be developed to make arable crop production feasible under such conditions. The same question arises in the case of ameliorated, i.e., drained, peat soils. Repeated loosening and mixing of the top layer by tillage enhance the mineralization of organic matter; hence, the rapid loss of matter causes sinking of the soil surface so that the soil may soon become waterlogged again. Here too, zero-tillage may be preferable since it may involve a drastic reduction in the mineralization rate. Zero-tillage could also be of interest on medium- to fine-textured soils.

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Apart from reducing costs for tillage operations, zero-tillage may eventually alleviate some of the negative side effects of tillage and repeated heavy traffic on medium- to fine-textured soils. Tillage and traction, especially during a wet season and by the use of heavy implements, can result in formations of soil pans. When caused by deep cultivation, these pans are difficult to remove. It is thought that continued use of zero-tillage on arable land will ultimately result in a stable soil structure similar to that frequently found under a cover of permanent grass. This soil structure should provide the optimum conditions for both plant growth and the necessary traffic on the fields. Zero-tillage may be induced by the practical needs and aims of a farmer striving for more effective, less risky systems of crop production. Yet, as Kuipers (1970) pointed out, the possibility of growing field crops without tillage offers an excellent opportunity for tillage research to examine the simple but basic question whether soil tillage is really necessary and to what extent it is necessary under various edaphic, climatic, and economic conditions. Contrasting hypotheses as to whether weed control or soil tilth, as effected by tillage operations, are the predominant benefits of tillage, can now be tested.

II.

Comparison of Environmental Conditions in Tilled and Untilled Soils

A. MACROSCOPIC SOILSTRUCTURE In contrast to clean-tilled fields, a no-tilled site is covered always by some plant residue. On bare patches, some mosses, green algae or lichens may cover the zero-tilled soil. Especially under plant litter or a closed plant canopy, earthworms deposit their casts on top of the soil. Frequently, the earthworm burrows end underneath a “mitten.” This consists of little heaps composed of plant debris collected by earthworms as well as soil excreted by them. Compared to the rugged ground of a recently tilled field, the zero-tilled soil surface is relatively smooth and even. Minor height variations are caused by ruts and tilled strips, mole hills, vole burrows, and mice tracks. In general, undisturbed soil appears to be more dense and firm. More energy is needed to break up the soil into clods, especially in untilled soil with a higher clay content. Although naturally compacted soils are more homogeneous in structure than plowed soils, differently structured layers can be observed as well. The top layer, which is often no more than 5-15 mm thick, though it may be up to 50 mm thick, may have a crumbly and friable structure. This

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depends on the amount of mulch present, the activity of soil animals and the prevailing weather conditions. Where such a top layer of biologically stabilized crumb structure has been established, slaking of silt material and, consequently, formation of a dense crust are rarely observed on zero-tilled silty loams. The structure and size of deeper layers depend mainly on their soil texture and on the texture dependent reaction to changes in soil moisture and temperature. In 'hit soils, zero-tillage induces a platy structure (Bulfin, 1967). This type of frost structure is unstable in tilled soils owing to excessive water in the top layers during the thawing process; however, it normally remains visible throughout the year in zero-tilled silty loam soils. A polyhedric structure is typical for soils with a high clay content, low capillary water conductivity and distinct swelling and shrinking properties. Since swelling of the clay after remoistening will close every cleavage again if the soil has not been previously mechanically loosened, tilth induced by frost or drought may be a transient phenomenon in zero-tilled clay soils (Czeratzki, 1971).

B. SOIL FLORA AND FAUNA Changes in soil flora and fauna can be expected when zero-tillage practices are introduced. Suitable information is lacking, especially with regard to reactions of microorganisms to zero-tillage effects per se. Indirect evidence that zero-tillage changes microbial activity is derived from tests of cellulose decomposition under field conditions. On zero-tilled soils, higher decomposition rates than on plowed soils were observed by Herzog et al. (1969), whereas Bender and Adamczewski (1970) found the reverse. However, these results reflect more the prevailing soil conditions than possible changes in microbial populations. In two field experiments with continuous wheat in England (Corbett and Webb, 1970), the total number of nematodes was sometimes larger with zero-tillage, while migratory parasitic nematodes were usually less numerous on untilled soils. Small-sized species of nematodes seemed to be favored on naturally compacted soils; inadequate observations do not allow further conclusions. Although earthworms form the most conspicious group of soil-inhabiting animals, little information is available about the changes in weight and number of earthworms upon introduction of a no-tillage system. For sampling, all investigators used vermifuges, which do not allow complete recovery of existing worms; therefore, only relative values can be reported. In West Germany, Schwerdtle (1969) found on the average a 12-fold increase in number and a 16-fold increase in weight of earthworms collected

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on zero-tilled plots after three years’ cropping with corn. In England, Wilkinson (1967) reported less spectacular increases, e.g., on cereal stubble fields a mere 1.6-fold weight increase. On former leys and permanent pastures, he did not observe any difference in the weight of earthworm populations resulting from tillage treatments. On three sites of former permanent pastures in the Netherlands, we found about half as many earthworms on tilled as compared to untilled plots after seven years. More than in any changes in abundance of earthworm populations, the agronomist is interested in their activities which alter the ecological conditions of naturally compacted soils. On loamy sand in West Germany, Graff (1969) measured the rate of casting from September to May over a period of three years. On untilled, mulched plots, between 2 and 4.5 kg dry matter per m2, which is within the range of values encountered normally on old pastures (Evans and Guild, 1948), were deposited on the soil surface. Graff (1969) observed 20- to 25-fold increases in rate of casting on untilled plots as compared to turnplowed barley stubble. Normally, most earthworms deposit their castings in the soil, not on top of it. In compacted soils, however, most castings are deposited on the soil surface. Still, even on zero-tilled soils, considerable soil mixing is to be expected. Earthworm tunnels which open to the soil surface may influence the rate of water infiltration. Since small tunnels are difficult to distinguish from soil cracks, the number of earthworm “mittens” may serve as a first approximation. On untilled cereal stubble fields, we found an average of 55 mittens per m2 soil surface. One centimeter below the soil surface, an average of 68 tunnels (diameter 2-10 mm) was observed on no-tilled stubble as compared to 15 on plowed stubble (W. Ehlers, personal communication, 1972). Moles are predators of earthworms and increase in number when fields are left undisturbed for a prolonged period. In Switzerland, Vez (1969) counted 10 to 12 molehills per are on zero-tilled plots as compared to 1 to 2 on conventionally tilled plots. Similar differences can be observed in burrows of voles and mice; these have not yet been quantified.

C. SOILORGANIC MATTER With zero-tillage, plant residues remain on the soil surface. This is essential when soil erosion limits successful farming. Where erosion presents no problem, a mulch cover may be desirable to create a favorable soil tilth. The highest permissible level of mulch is determined by conditions governing the effective performance of drilling and weed control operations. In the Netherlands, 3000 to 4000 kg straw (dry matter) per hectare can remain on the ground only when it is chopped up into small pieces

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and evenly distributed. For dryland farming, an amount of 3500 kg straw per hectare at harvest is considered to provide adequate soil protection from erosion without presenting problems with seeding, weed control and soil fertility. Brown and Dickey (1970) determined losses of wheat straw buried in the soil, placed on the soil surface and exposed above the soil surface to simulate a standing stubble. At two locations in Montana, they found that the rate of dissipation increased with greater contact between soil and plant material and decreased when rising amounts of straw were applied. Lower mean annual temperature, though in combination with higher precipitation, retarded straw decompositibn. During the first 3 months of exposure, the weight of above-surface and on-surface straw increased by as much as 1 3 % due to an accumulation of soil particles inside the hollow straws. Some soil probably is moved by wind or raindrop splash and, near the ground, by the activities of soil-inhabiting animals. The experiment of Brown and Dickey was begun in May. After 18 months’ exposure, only 22 to 40% losses were measured on and above soil as compared to 93 to 98% buried in the soil. In the more humid climate of Germany, higher rates of wheat straw decomposition were observed, e.g., 40% during the period September through July (K. W. Becker, personal communication, 1972). The weight of adhering soil particles equaled the amount of straw remaining after 1 1 months’ exposures. These figures indicate that a slow surface accumulation of straw residue can occur if the above-mentioned process of incorporation into the soil is not effective. Plant residues with higher N content decompose more rapidly. Cornstalks applied to the surface of a cornfield in Iowa in May lost 50% of the initial weight after 20 weeks’ exposure (Parker, 1962). Sugar beet tops left on the ground in Western Europe are completely disintegrated by July. Hence, leafy and succulent plant material presents no problems in mulch management. In Fig. 1, some results of trials on former grassland and recently plowed soils concerning the distribution of organic matter in soil are summarized. No differences in organic matter concentration were found in regularly plowed soil layers. In undisturbed soils, the concentration was highest near the soil surface and declined steadily to subsoil values below those on conventionally tilled soils. The gradient of organic matter content was more pronounced on former grassland soils, where zero-tillage presumably preserved the original distribution of organic matter. No thorough investigation has yet been published as to whether zerotillage results in an accumulation of total soil organic matter. Available

84

K. B A E U M E R A N D W. A. P. B A K E R M A N S organic matter ( % . d r y s o i l ) 1

30i

2

3

4 5

arable l a n d (16)

6

7

N ( '/. )

8 9 1011

grassland

(22)

arable land

(16)

FIG.1. Average distribution of organic matter and N in tilled (-) and untilled (- - - ) soil. (From Bakermans and De Wit, 1970, grassland; Buhtz et al., 1970, arable land.)

data from long-term trials (Moschler et al., 1972; Buhtz el al., 1970) suggest that zero-tillage increases the total organic matter of the soil. Whether the observed differences in accumulated organic matter are caused by restricted decomposition andlor higher production of organic matter on zero-tilled soils is not yet known. As compared to a tilled chernozem soil in East Germany, concentrations of CO, in the atmosphere near the soil surface were lower on untilled soil (Buhtz, 1972). These observations suggest a reduced rate of mineralization in naturally compacted soils.

D. PARAMETERS OF SOIL STRUCTURE With zero-tillage, soils are loosened only locally and superficially; yet they have to bear the normal load of traffic in the field. Hence natural consolidation and mechanical compaction will cause a denser packing of zero-tilled topsoils. The average decrease in total porosity was found to vary between 0 and 6% (v/v) (Czeratzki and Ruhm, 1971; Herzog and Bosse, 1969; Vez and Vullioud, 1971a,b). A few exceptions were noted on heavy river clay rich in organic matter (Van Ouwerkerk and Boone, 1970), on two sites with silt loam-chernozem soil (Buhtz et al., 1970) and on silty clay (Bachthaler, 1971) where values of total porosity were lower on tilled than on zero-tilled plots, probably as a result of compaction caused by tillage operations. In general, the differences in total porosity were greatest in the soil layer which is loosened by plowing, but not compacted by seedbed preparation and cultivation ( 10-1 8 cm) . In deeper soil layers, the differences .tended to diminish. Near the soil surface, they varied with the effects of tillage operations, weather, and biological activities. Mean values of total pore space average over sampling dates, crops,

85

ZERO-TILLAGE

and locations, eliminate extreme values, which may be decisive for plant growth and farming operations in critical situations. The lowest sampling means of the porosity data published were found with values near 35 and 38% (v/v) on untilled plots on sandy soil (22-27 cm) and clay soil (15-20 cm), respectively (Czeratzki and Ruhm, 1971). The very high density of the soil layer 22-27 cm on sand merits special attention, as it is probably induced by mechanical compaction and perhaps by downward displacement of finer soil particles, which by turnplowing are redistributed to upper soil layers. This could be proved by particle size and pore size distribution analysis, but no information is yet available. The observed minimum values did not mark the final stage of soil density on zero-tilled soils. At subsequent dates, porosity increased again, especially on stable soils with medium to high clay content. The above-stated lower levels of pore space were reached within two to three years of zerotillage, after which time seasonal fluctuations of total porosity tended to be smaller as compared with conventionally tilled soils (Van Ouwerkerk and Boone, 1970). Similar results are shown in Fig. 2, which contains a time series of porosity measurements in the top 2-6 cm layer of arable silt loam soil derived from loess (Ehlers, 1973). Zero-tillage resulted in a smaller total porosity but also in reduced variability of- the sampling means; consetotal porosity

40

40 20 1s h

>

10

$ 5

- 0

10

5

medium pores

0

3

15 10

- 30rm

sma II pores 0.2 - 3.0p m

5

0 10 5

0 oats

-*

un ti lied

radish

rotabated

cultivated

tilled

FIG. 2. Changes of total pore space and pore size distribution with time at a depth of 2-6 cm on tilled and untilled silt loam soil. (From Ehlers, 1973.)

86

K. BAEUMER AND W. A. P. BAKERMANS

quently, homogeneity in time increased in naturally compacted soils. The remaining fluctuations of total porosity presumably result from the combined effect of seasonal changes in climate and soil cover on the activities of soil flora and fauna. The example in Fig. 2 shows further that changes in total porosity were accompanied by concomitant changes in other pore size fractions. It can be concluded, therefore, that mechanical loosening effects mainly the fraction of large pores and that dense parts of the soil remain more or less unchanged. As compared to the fraction of large pores, the other pore size fractions fluctuated to a smaller extent.

5

Y

30 ..

20

10

0

p o r e space

('I-vlv)

60

10

20

40

30

10

;

20

0

30 1

pore size

A

-F

3

P

N I W

w

W

0

I

I

w

0)

o

O

"

W

m o

o z

F

3

=

z A

-F

3

W

R

W

I

I

W

O I

w

m

0

0

:! 0--.

-Fn 3

FIG. 3. Changes of total pore space and pore size distribution with depth on tilled (right panel) and untilled (left panel) silt loam soil. (From W. Ehlers, personal communication, 1972.)

Figure 3 shows the vertical pore size distribution of a silt loam soil (W. Ehlers, personal communication, 1972). Although in this case the total porosity and the fraction of large pores did not differ much between zerotilled and conventionally tilled soils, the pattern of porosity reveals an important difference: on undisturbed soil, the relative space occupied by each pore size fraction varied less than on the ploughed soil, where the layers at 0 to 15 cm and 25 to 30 cm were compacted as compared to the layer at 15 to 20 cm. The compaction at 25-30 cm is presumably caused by pressure and smearing actions during plowing. It resulted not only in an absolute reduction in large and medium pores-based on volume as well also in a relative increase in small and very small as on weight-but pores-based on volume only, as discussed by Ehlers (1973). Untilled soil, though generally denser, may also exhibit more structural homogeneity in space as compared to conventionally tilled soils. A relatively higher amount of smaller pores, but greater homogeneity in time as well as in space are thus the dominant changes in porosity when

ZERO-TILLAGE

87

a soil remains untilled for a long period. Another feature may be connected with the continuity of pores. Since earthworm tunnels can be regarded as primarily continuous pores, an estimate of the relative pore space occupied by them may serve as a first approximation. Figure 4 shows that the space occupied by large pores with presumably uninterrupted connections to the atmosphere is more than doubled near the soil surface and in the top 20 cm of zero-tilled soil as compared to plowed soil (W. Ehlers, personal communication, 1972) . p o r e space (% v/v)

o

0.2

0.4

0.6

ae

1.0

FIG. 4. Pore space occupied by rainworm tunnels on tilled (O---O) and untilled (0-0) silt loam soil (From W. Ehlers, personal communications, 1972.)

701 ao

Other composite parameters of soil structure are resistance to penetration and shear stress, which are highly dependent on texture, soil moisture, and porosity. In general, larger resistance to a cone-shaped probe forced into the soil was observed on zero-tilled soil (Buhtz et al., 1970). On sand soil, J. M. Houben (personal communication, 1972) found no rooting when penetrometer resistance exceeded 40 kg/cm2. In one case, we observed that continuous zero-tillage on sandy soil produced a comparable compaction in layers between 5 and 30 cm.

E.

AERATION AND SOILMOISTURE

Soil aeration depends on porosity and water content. Hence when a soil is water saturated to field capacity (soil moisture tension: 0.1 bar A p F 2), the extent of the remaining pore space filled with air (air capacity) may be critical for the maintenance of soil aeration. A minimum volume of 10% is thought to be necessary for adequate gas exchange between the soil air and the free atmosphere. Though zero-tillage generally causes a decrease of large, mostly air filled pores (diameter > 30 pm) and thus reduced aeration, air capacity at p F

88

K. BAEUMER AND W. A. P. BAKERMANS

2 was observed only on medium- to heavy-textured soil to be below 10% (v/v) (Van Ouwerkerk and Boone, 1970; Czeratzki and Ruhm, 1971; W. Ehlers, personal communication, 1972). Impeded aeration, if caused by zero-tillage, may provide a serious objection to the application of this system on heavy soil in humid regions. With regard to this point, an evaluation of large, continuous pores, such as earthworm tunnels, would be of interest. The observed relative increase in the amount of medium to small pores caused by zero-tillage has consequences for the water-holding capacity of the soil. Plowing up grassland results in the redistribution of organic matter ( Fig. 1 ) ; zero-tilled sod retains its original accumulation of organic matter near the soil surface. Water-holding capacity is related to organic matter content, especially on sandy soils; this was confirmed by Van Ouwerkerk and Boone (1970), who found that water content at p F 2 changed more in conjunction with organic matter content than with soil porosity. Hence, in the top 6 cm of the zero-tilled soil, a higher water content at p F 2 was found than in the plowed soil, whereas the reverse was true in the layer at 11-1 6 cm. Thus, beginning with a permanent pasture, changes in soil behavior caused by different tillage systems cannot be ascribed solely to differences in porosity. On arable land, the situation is less complicated since waterholding capacity generally increases with increasing pore space of an equivalent diameter <30 pm. On zero-tilled soils, therefore, a relatively larger part of the pore space ( % v/v) was found to be water filled, though this is of no consequence for the amount of available water, i.e., the difference in moisture content in % (w/w) at p F 4.2 and p F 2.0 (Van Ouwerkerk and Boone, 1970; W. Ehlers, personal communication, 1972). Information about the energy associated with soil water is essential for understanding its movement in soil and its availability for plant growth. W. Ehlers (personal communications, 1972) investigated changes in gravimetric water content and matric potential in time and down the profile of a silt loam derived from loess. Differences between tilled and untilled soils are shown for four situations (Fig. 5, a-d). These are characterized by beginning and advanced stages of either depletion (4-8 and 6-7, respectively) or recharge of soil moisture (6-10 and 6-21, respectively). Most remarkable is the observation that soil water tensions were effected by the tillage system down to a soil depth of 220 cm. This demonstrates the consequences of changing the structure of one soil layer only for the moisture regime of a whole profile. Differences in soil water content between tilled and untilled soils were relatively small and inconsistent compared to differences in soil water tension and hydraulic potential. Zerotilled soil with a similar water content generally had a lower soil water

89

ZERO-TILLAGE matric potential

JI

hydrauiic potential

(cm water column)

-400 -200

0

I""""

Q+

-...

100

200

9

water content

(cm water column)

*200

9 6 - 21 -1971 i P

t

FIG.5 . Matric potential, hydraulic potential, and water content of tilled (O---O) and untilled (0-0) silt loam soil during phases of depletion (a, b ) and recharge of soil moisture (c, d ) . Arrows indicate situations where gradients of hydraulic potential are zero. (From W. Ehlers, personal communication, 1972.)

tension, which indicates a smaller resistance to water uptake by plant roots and a higher conductivity of soil water. The largest differences between tilled and untilled soils were observed during the rewetting phase (Fig. 5 , c, d ) . The rain water infiltrated rapidly into the plowed layer, but slowly into the subsoil of the tilled plots. Thus, soil water tensions were reduced to near zero in the upper soil layer, but continued almost unchanged at greater depth. Yet, in the untilled soil, the soil water tensions remained at a higher level near the soil surface and decreased rapidly in the subsoil.

90

K. BAEUMER AND W. A. P. BAKERMANS

This behavior indicates a lower resistance of the zero-tilled soil to infiltration, which may be typical for light to medium loam soils, where earthworms or other soil animals construct a continuous set of large pores connecting the soil surface with the subsoil. Decaying roots which remain undisturbed in place could provide ready avenues for water infiltration into the soil profile as well (Barley, 1954). Mulch physically absorbs raindrop impact energy. Thus, slaking and sealing of the soil surface is prevented or at least retarded. Therefore, zero-tillage generally reduces surface runoff. On silt loams with an 8-10% slope planted with row crops, reduction ranged from one-half to one-sixth of the amount observed on clean tilled land (Harrold et al., 1967; Shanholtz and Lillard, 1969; Jones et al., 1969). On a silt loam in Ohio, Triplett et al. (1968) found an increase of both the infiltration rate and total infiltration with increasing soil cover by cornstalks, the zero-tillage normal residue treatment resulting in higher values than the conventional tillage treatment. Partition of the mulch effect due to physical protection and structural stability of the soil showed that in this case the accumulation of soil stability was more effective than physical protection of the soil surface. The purely protective effect of residue cover may influence the rate of soil water evaporation too. During the initial constant rate of evaporation, when rates depend solely on the saturated hydraulic conductivity of the soil and the evaporative demand of the atmosphere, Bond and Willis ( 1969) observed decreased evaporation with increasing residue rates. During the following stage of falling rates of evaporation, when the soil surface also dried underneath a mulch cover, no differences in evaporation rate between bare and mulched soil were found. Most of the evaporation losses in row cropped soil should occur before the closing plant canopy reduces the incident radiation and thereby evaporation at the soil surface. Hence differential gains in soil moisture content by means of zero-tillage as induced by mulch protection are to be expected mainly during the early growth stages of row crops, when evaporation rates of the more or less saturated soil are high. Generally, zero-tillage resulted in higher mean volumetric moisture content in the upper 30-60 cm soil layer than conventional tillage on soils situated in the subhumid regions of North America on gently sloped silt loams planted with row crops (Harrold et al., 1967; Amemiya, 1968; Blevins et al., 1971; Jones et al., 1969). The greatest differences in total available water always occurred early in the growing season (Shanholtz and Lillard, 1969; Van Doren and Triplett, 1969). Zero-tillage methods could be expected to increase water conservation in dry-farming regions. As compared to conventional stubble mulch fallow,

ZERO-TILLAGE

91

complete chemical fallow resulted in lower moisture conservation at one location in the semiarid Great Plains (Black and Power, 1965), whereas water storage gains were observed at two other locations (Smika and Wicks, 1968; Army et al., 1961). These contradictory results could perhaps be explained in part by the differential reduction of evaporation by a mulch cover during constant and falling rate drying phases. After prolonged falling rate drying, the cumulative evaporation from a mulched or bare soil was nearly equalized (Bond and Willis, 1969). Greater soil water storage may be attained with chemical fallow only under the following conditions: first, when cumulative evaporation during drying intervals is less with an undisturbed upright standing stubble than with a residue cover knocked down by subtillage; second, when more frequent rains are prevalent, since mulches are of little value for water conservation during extended dry periods. F.

SOIL TEMPERATURE

Soil temperature depends on the thermal conductivity and volumetric heat capacity of a soil, and on the amount of heat that enters or leaves the soil surface. Hence the amount of soil cover and the water and air content of the various soil layers are decisive factors for the temperature regime of soil. Van Duin (1956), who used the results of a theoretical investigation, showed that loosening the upper soil layer by mechanical means should increase the diurnal temperature variation near the surface of a clean-tilled soil, but decrease the amplitude in the deeper, undisturbed layers. Thus, the loosened zone acts as an insulating layer. During phases of rising soil temperature, a tilled soil should be warmer near the surface but cooler in the subsoil than in undisturbed soil. The reverse is true during periods of falling temperature. Since the effect of a mulch cover is similar to that of a loosened soil layer, differences in soil temperature between conventionally tilled and zero-tilled soil will become larger with increasing amounts of cover. During the growing season, untilled or merely mulched soil were observed to be cooler than clean tilled soil (Van Wijk et al., 1959; Parker and Larson, 1962; Shanholtz and Lillard, 1969). At a depth of 10 cm, the average difference in maximum soil temperature ranged from l o to 3 O C , which was greater than differences in minimum temperature, which were less than 1OC. During cool periods in May, Moody et al. (1963) observed higher soil temperatures on mulched soil, confirming the postulated reversal of differences during periods of falling temperatures (Van Duin, 1956). Similar

92

K. BAEUMER AND W. A. P. BAKERMANS

effects were found by Kohnke and Werkhoven (1963). In winter, the mulched silt loam was warmer by either 5O or 1OC. At a depth of 5 cm, the frequency of freezing and thawing was 3.6 times greater in clean-tilled soil than in straw-covered soil. Due to the kind and amount of mulch used, most of the reported differences are probably larger than those usually encounterd with zero-tillage systems. Nonetheless, they indicate temperature effects that may limit the applicability of zero-tillage. On compacted, heavy textured soils, a lower frequency of freezing and thawing may not result in the necessary friable tilth and soil porosity. The slower warming up in spring may seriously retard the emergence of field crops with high demands on germination temperature.

G. SOILEROSION Soil particles may be detached from land surfaces by the action of either water or wind. Accumulation of organic matter near the surface of untilled soil may cause significantly higher stability of soil aggregates (Tomlinson, 1968). This, as well as the absorption of energy by impact of falling raindrops and the impedance to water flow by surface trash, can increase infiltration rates, reduce runoff and hence soil losses due to water erosion. Harrold (1972) reports that zero-tillage of corn on a silt loam with a 9 % slope reduced soil losses to 2 tons per hectare between 1964 and 1970, as compared to 20.5 tons per hectare with conventional tillage. Wind erosion may become a serious problem on soils with surface textures of fine sand, loamy fine sand, or fine sandy loam, especially when cropped intensively with row crops. Schmidt and Kroetz (1969) reported that zero-tillage with residues removed resulted in slightly lower soil losses than plowing with the normal amount of residues. Zero-tillage with normal residue reduced soil losses by wind erosion to one-sixth of those of the plowed treatment. During one severe windstorm, 321 tons per hectare of soil were lost from a till-planted cornfield as compared to only 5 tons per hectare from a zero-tilled field (Schmidt and Triplett, 1967).

H. SOILTRAFFICABILITY Adequate traction of agricultural machinery cannot be attained when soils are either too loose or too wet. Although no quantitative data are available at present, it has been repeatedly observed that zero-tilled soil is accessible to heavy machinery earlier after the last rain and longer during wet seasons than tilled soil (Baeumer and Pape, 1972). This may result in a greater number of days suitable for farming operations in the field.

93

ZERO-TILLAGE

In such operations, the effect of the vehicle on the soil is as important as the traction capacity developed. Untimely traffic may cause severe soil compaction and hence excessive erosion, poor aeration, increased mechanical impedance, which can curtail the growth of field crops. Whether such negative effects are reduced on zero-tilled soils when similar traffic loads are compared on tilled and untilled soils has not yet been investigated. Observations generally show that zero-tilled soils are less rutted than plowed soils if driven on in wet conditions.

I.

NUTRIENT CONCENTRATION AND DISTRIBUTION

Since lime and organic matter are applied on the surface, the concentration of nutrients in the top layer should be higher in zero-tilled than in conventionally tilled soils. The reverse should be true in deeper soil layers. In agreement with this picture, the content of available P and K near the soil surface was higher on untilled than on tilled soil, whereas in deeper layers the reverse has been observed (Moschler et al., 1969, 1972; Shear and Moschler, 1969; Kahnt, 1971; Triplett and Van Doren, 1969). Figure 6 shows that P and K are accumulated in the upper layer of the untilled soil whereas the Mg content is lower in the top layer and higher in lower layers. During the experimental period of series a (Fig. 6 ) , no Mg was added since this element is subject to leaching, the depletion of the top layer is to be expected. The same holds for Ca. This situation is reflected in a generally lower pH for untilled top soils (Buhtz et al., 1970).

p2 0 5 a

5

(rng1100g)

K20

(rng1100g)

Mg '(rng/loog)

10

v

5(5 20 u

0

30

FIG. 6. Average distribution of P, K, and Mg in tilled ( - - - ) and untilled (-) soil of grassland ( a ) and arable origin ( b ) . (From Bakermans and De Wit, 1970; Buhtz et d.,1970.)

94

K. BAEUMER AND W. A. P. BAKERMANS

Although no reliable and thoroughly investigated set of data is available at present, the observed changes in nutrient content per unit soil weight suggest that zero-tillage generally results in an increase of available P and K (Kahnt, 1971; Triplett and Van Doren, 1969; Moschler et al., 1972). Differential accumulation of organic matter implies changes in concentration and distribution of total N (Fig. 1). Differential increase in N content (Kahnt, 1971; Buhtz, 1972), greater C/N ratios (Tomlinson, 1968), and a relative increase of the nonhydrolyzable N fraction near the surface (H. Fleige, personal communication, 1972) suggest changes with rates of N mineralization and hence in the content of available N. Different NO, and NH, concentrations can be caused not only by direct relationships between soil properties and processes such as mineralization, leaching, and volatilization, but also by differential N uptake of plants. Buhtz (1972), Debruck (1971), Herzog et al. (1969), and Buhtz et al. (1970) measured soluble N (NO, or NO, NH,) in tilled and untilled soils cropped with cereals or sugar beets. Generally, lower concentrations of available N were observed on untilled soils. In a few cases, higher N concentrations were noted on zero-tilled soils. This took place mainly after peaks of soluble N concentrations had occurred on plowed land (During ef ul., 1963; Herzog et al., 1969), indicating a time lag in availability of N on zero-tilled soils. Similar results were obtained by Arnott and Clement (1966), who found more mineralized N on ploughed than on sprayed grassland kept free of plant growth, but no significant differences in mineralization rates

+

NO3-N (pprn) 0

50

100

150

200

250

300

350

FIG.7. Nitrate nitrogen distribution with depth in tilled (0-0) and untilled (O---O)Maury soil cropped with corn on July 23, 1971. (From Blevins et al., 1972.)

ZERO-TILLAGE

95

during 19 subsequent weeks of sampling. Thus, not only a reduction but also a time lag in N mobilization appear to be common features of zerotilled soil. The time lag may be due to temperature differences between mulched and bare soil. Nitrification can be retarded to a considerable extent very early in the season when temperature depression on mulched soils is greatest (Parker and Larson, 1962). The higher water content in the surface of untilled soil may influence the downward displacement of soluble N. As Fig. 7 shows, soil depth measurements of NO,-N indicate lower quantities of nitrates remaining in the upper soil layers under zero-tillage. These results of Blevins et al. (1972) suggest that more leaching of nitrate occurs on zero-tilled soils. Whether this and/or greater volatilization of N compounds due to restricted aeration is an important cause for reduced concentration of soluble N on zerotilled soils has yet to be investigated.

Ill.

Effects of Zero-Tillage on Plant Growth

As shown, zero-tillage involves higher water content in the top soil layer, reduced soil aeration, stronger mechanical resistance to root penetration, smaller soil temperature amplitudes and a different pattern of nutrient distribution in the soil profile. All these changes may be relevant to plant growth. A. GERMINATION Due to climatic conditions or technical requirements, the soil surface is usually dry at the time of seeding. Therefore, broadcast seeds may germinate slowly, if at all, and may become an easy prey for grain feeding animals. In order to minimize the risks of drying out and being eaten by animals, seeds have to be brought into close contact with moist soil and covered by some soil, even with zero-tillage methods aiming at the least possible soil disturbance. Mean seedling establishment by zero-tillage methods is reported to be about 20% less than by conventional methods (Rhixon, 1969). This figure reflects primarily the technical difficulties of sowing at the proper depth of soil which is always covered by trash and is sometimes too hard to allow sufficient penetration with a drill or too sticky to close the sowing slots. Yet, where improved sowing techniques comply with the requirements considered to be normal in conventional systems, the advantages and disadvantages of zero-tillage methods can be evaluated with regard to seedling establishment.

96

K. BAEUMER A N D W. A. P. B A K E R M A N S

On light to medium-textured soils with short, standing stubble and a friable soil surface, a higher number of emerged plants was observed with zero-tillage than with conventional tillage (Buhtz et al., 1970; Debruck, 1971 ) . This happened to be the case more often under conditions in which a lack of available soil moisture restricted seedling emergence on tilled soils. Straliik (1968) observed more rapid water absorption by seeds on untilled soil. Therefore, higher rates of seedling emergence can be expected with zero-tillage than with conventional tillage during warm and dry periods. The reverse may be true when the soil is so wet and cold that loosening it for seedbed preparation results not only in better aeration, but also in higher soil temperatures. A difference of 1-2OC between tilled and untilled soil may be decisive for germination and subsequent growth if minimum temperature requirements are not fulfilled, as can be observed with maize grown in mulched soils in a temperate climate (Willis et al., 1957). There are additional effects of zero-tillage which can negatively effect germination and emergence. Residues of nonselective herbicides can still be concentrated enough at sowing time to retard or prevent emergence of zero-tilled plants (Adams et al., 1970). Thick mulches were observed to smother emerging seedlings (Bakermans and De Wit, 1970), probably by shading and/or transmitting herbicides such as paraquat. Though these herbicides must be applied before emergence and should be either inactivated or positionally ineffective, they may be partly absorbed by plant residues and hence still be effective when they come into contact with seeds and seedlings (Taylor et al., 1966; Schwerdtle, 1971). Plant residues may contain phytotoxic substances (Boerner, 1960). Aqueous extracts of corn, sorghum, and cereal straw were toxic for wheat seedlings in laboratory tests even after several weeks’ exposure of the straw to field conditions (Guenzi et al., 1967). Microbial decomposition of wheat straw can result in the development of phytotoxic substances, such as patulin (Norstadt and McCalla, 1968). Whether soluble plant substances and/or microbially transformed compounds can be leached from mulch material into the seedbed at such concentrations that germination and emergence of seedlings can be impeded under field conditions in zerotilled soil is not yet known. B.

ROOT GROWTH

As measured by root density or weight, the amount of roots observed at different growth stages and soil layers tended to be lower on zero-tilled soil (Newbould et al., 1970; Cannel and Ellis, 1972). This difference in root mass was accompanied be shallower rooting in undisturbed soil, espe-

ZERO-TILLAGE

97

cially during early vegetative growth phases. The extension rate of seminal root axes was slower, yet lateral branching started earlier in zero-tilled soil, thus leading to the production of a dense but shallow seminal root system on undisturbed soil. No differences were found between the effects of tillage treatments on the length and frequency of adventitious roots of wheat (J. R. Finney and B. A. G. Knight, personal communication, 1972). Therefore, the final root weight and pattern of soil depth distribution at the ripening stage may be similar on tilled and untilled soil (Baeumer et al., 1971). However, on sandy soil in the Netherlands, shallow rooting persisted until harvest, probably owing to mechanical impedance of the soil to root penetration. Sometimes, the restricted axial growth of roots was compensated for by greater radial growth and, hence, by a larger diameter of the seminal root axes of barley (Yueruer, 1972) or greater weight per unit root length of corn (Barber, 1971). Thesc results probably indicate the effect of increased mechanical resistance of zero-tilled soil to root penetration. A shallow but intense root system reflects not only increased mechanical impedance, but also the different pattern of water and nutrient concentration in tilled and untilled soil. No information is yet available about the function, i.e., the rate of activity in nutrient absorption and water uptake of roots in differently structured root environments such as tilled and untilled soil. Only such information-in combination with data on root size and distribution-could provide the explanations for the observed response of shoot growth to changed soil structure. C.

NUTRIENT ABSORPTION

So far, measurements of nutrient content in leaves or other parts of plants have been used to detect differences in nutrient absorption of crops grown on tilled and untilled land. Since the amount of dry matter produced and the stage of maturity may differ, nutrient content data have to be interpreted with care; total uptake of nutrients by the crop in question may be a more relevant figure. P, K, Mg, and Ca contents at various stages have been reported for corn (Moody et al., 1963; Shear, 1968; Triplett and Van Doren, 1969), cereals (Kahnt, 1969), and fodder kale (During et al., 1963). In most cases, the P and K content of plants grown on untilled or mulched soil was higher or equal to the contents observed on conventionally tilled soil. Singh et al. (1966), studying uptake of "P-labeled superphosphate by corn, observed a higher uptake of surface-applied P especially during the early growth phases, as compared to the uptake from P fertilizer mixed with the soil by rototilling. Whether this higher uptake is caused by

98

K. BAEUMER AND W. A. P. BAKERMANS

changed P availability due to a different concentration and position of the applied P compound in zero-tilled soil is not yet known. Final uptake of P and K by the harvested oats was not significantly different (Ehlers et al., 1973). It may be concluded that the concentration and distribution of surface applied P and K do not seriously restrict plant growth on zero-tilled soil. Rather, different results can be expected with N, which, in its available form, is more subject to temporarily changing soil conditions. Analysis of plant tissue samples from untilled or mulched soil showed generally higher N content of corn (Moody et al., 1963; Shear, 1968), cereals (Arnott and Clement, 1966; Kahnt, 1969), and fodder kale (During et al., 1963), as compared to samples from plowed soils. This increase in N content contradicts the observations on the distribution and concentration of soluble N in undisturbed soil. It can be partly explained if increased N content is accompanied by reduced plant growth, which may result in increased N content of less mature plant tissue.

f5 L

N uptake

z 0 Total dry matter produced (100 kglha)

FIG.8. Diachronic changes of N content, dry matter produced, and N uptake of wheat forage grown on tilled and untilled silt loam soil. (From G . Pape and H. Fleige, personal communication, 1972.)

Our results, presented in Fig. 8, indicate, however, that, independently from dry matter production, the N content of forage grown on zero-tilled soil may be higher as compared to plowed treatments. The differences between tillage treatments diminished during later stages of growth. Finally, at harvest, the lower grain yield and the lower N content of grains resulted in lower total N uptake on zero-tilled soil, as shown for this (1971; Table I, winter wheat) and other cases (Debruck, 1971). This time pattern of N uptake appears to be typical for mulched soil. Parker (1962) compared

99

ZERO-TILLAGE

TABLE I Total N Uptake by Cereals Grown on Tilled and Untilled SoiP~b a. Winter wheat, 1971 Nitrogen applied (kg/ha) Tillage Conventionally tilled Zero-tilled LSD0.05: 5.7

0

50

100

150

Mean

,50.0*

74.5 70.5

103.3 87.5

197.2 113.3

88.8 78.8

44.1

b. Winter barley, 1972 Nitrogen applied (kg/ha) Tillage Conventionally tilled Zero-tilled 1,SDo.o~:6.5

0

80

120

160

Mean

30.7 41.8

72.5 79.2

95.2 93.3

105.2 100.5

75.9 77.2

Silt loam, West Germany.

* Uptake values are expressed as kilograms per hectare. the effects of buried and mulched corn residues on the N content of corn. During the first 35 days after planting, he found a higher N content, during later stages a lower N content of plants grown on mulched soil. These results do not suggest that N absorption by crops is generally more restricted on zero-tilled soil. This opinion can be supported by findings such as those presented in Tablc I, which show that barley grown in 1972 with N fertilization took up more N on untilled soil than on tilled soil. The causes for this result and the different time pattern in N uptake are not yet known. D.

CROP

GROWTH

Tillage induced changes in soil environment are effective only in combination with numerous other factors such as weather, weed growth or diseases and pests. Hence tillage effects can be expected to be highly inconsistent if evaluated over a wide range of ecological conditions (cf. Fig. 12). Disregarding cases in which lower plant density or less complete weed control in one or the other tillage system does not allow the comparison of growth rates, there are situations in which early growth of zero-tilled crops is either enhanced or retarded by soil conditions.

100

K. B A E U M E R A N D W. A. P. B A K E R M A N S

In the corn growing region of North America, faster growth of sod-sown maize seedlings, as judged by plant height, was observed by Moody et al. (1961), Shanholtz and Lillard (1969), and Jones et al. (1968). This was explained by an increase in available water and the favorable root zone environment provided by the mulch and soil structure of undisturbed soil. Van Doren and Triplett (1969) analyzed the mechanism of this growth response and concluded that it was directly or indirectly caused by improved soil moisture regime, especially during the first half of the growing season. With increased available moisture, they observed an increased leaf area production, which in turn resulted in yield increases if a water shortage during later stages did not restrict carbohydrate synthesis. More vigorous growth requires additional water withdrawal from soil; b

a

.

.

15 21

.

29

35

49

64

4-22

5-15

days from planting

6-2

6-23 7-12 sampling date

FIG.9. ( a ) Growth of maize in Iowa on mulched (0-0) and plowed ( O - - - O ) soil. ( b ) winter wheat in Germany on tilled ( O - - - O )and untilled (0-0) soil. (From Parker, 1962; G . Pape and H. Fleige, personal communication, 1972.) Final Yield of Grain (Dry Matter) (a) Corn (hu/ncre)

(b) Wheat (tons/ha)

N applied

Mulched

Plowed

TJntilled

Tilled

0 120 Ib/acre 150 kg/ha

120 124

126 130

2.2

3.1

-

-

-

-

3.8

4.5

ZERO-TILLAGE

101

this was calculated by Shanholtz and Lillard (1969). The water use efficiency of maize crops grown on zero-tilled and conventionally tilled soil was 81% and 57%, respectively. Despite the greater water extraction, visible wilting of maize and sugar beets was delayed for hours or days, which indicates an enhanced depletion of soil water on undisturbed soil. In other cases, an early season depression of maize growth was observed on mulched soil (Moody et d.,1963), as shown in Fig. 9a. Similar effects were observed with zero-tilled cereals (Fig. 9b, Bosse and Herzog, 1969). Where N fertilizer had been applied, the difference in dry matter production eventually disappeared. As shown by the N content in Fig. 8 and similar results of Parker (1962), the retardation of early growth cannot be primarily a consequence of reduced N availability in mulched or zero-tilled soil, though the time lag of N mobilization, sometimes observed on undisturbed soil, may take part in this effect. Burrows and Larson ( 1962) and Moody et al. (1963) found lower soil temperatures under mulch to be the causative factor in retarding early growth of corn. Where soil temperatures are high enough to answer the requirements for optimum growth, as shown by Van Wijk et al. (1959), the depression of soil temperature by zero-tillage methods should be without noticeable effects on the early growth of corn. Whether the depressed early growth of zero-tilled cereals is caused by lowered soil temperatures has not been yet investigated. E.

CHANCES I N WEEDPOPULATIONS

Leaving an arable soil undisturbed prevents deeply buried but viable weed seeds from germinating. This results in diminishing rates of emerging annual weeds if the replenishment of the weed seed population is curtailed by preventing seed shedding of weeds as accomplished with effective weed control (Roberts and Dawkins, 1967). Debruck (1971) and Schwerdtle (1971) verified this effect, which is shown in Fig. 10. Incomplete herbicidal control resulted in increased annual weed growth, especially of gramineous annual weeds. The observed reduction of annual weed may be caused, at least for some species, by less favorable conditions for germination and/or by destructive effects of herbicides applied on viable, yet dormant weed seeds. Paraquat, for instance, drastically reduced the viability of grass seeds (Evans, 1961; Schwerdtle, 1971). Deep plowing and cultivation serve to keep many perennial species at least in check; with zero-tillage, some of these weeds remain almost undisturbed. Therefore, large populations of perennial weeds can build up in untilled soil, if either adequate control measures are neglected or available herbicides are ineffective or perhaps not applicable.

102

K. BAEUMER AND W. A. P. BAKERMANS

zero-tillage

-

persistent weeds

I

looE +-.-.-.d 1

2

3

year

FIG.10. Changes in weed population with time on continuously tilled (O---O) and untilled soil. (From Debruck, 1971.)

In addition, on old sods, some species of well established and adapted grassland vegetation may be able to resist most control measures feasible in a zero-tillage system (Hood, 1965). Peters (1972) compiled a list of the most problematic weed species in reduced tillage in the United States. Quite often it can be observed that zero-tillage methods result in higher amounts of volunteer plants from previous crops, especially where cereals, maize, or sorghum are grown continuously. Although yields may not be lowered seriously, the value of the crop is depreciated at least by lack of purity.

F. DISEASESAND PESTS Takeall (Ophiobolus graminis) and eyespot (Cercosporella herpotrichoides) are soil-borne fungi which cause serious diseases, especially of wheat, when cereals are grown continuously in the same field. It has been frequently observed that cereal crops were less severely attacked by these pathogens on zero-tilled soil than on plowed soil (Hood, 1965; Schwerdtle, 1971). Brooks and Dawson (1968) found a reduced rate of spread for Ophiobolus on untilled soil, especially when soil temperatures began to rise and plant growth became rapid. The occurrence of pests is also influenced by zero-tillage. In North America, several species of the corn rootworm endanger the production of maize. Musick and Collins (1971) found in Ohio that the number of eggs oviposited by the Northern corn rootworm (Diabrotica longicornis) increased with the amount of ground cover; hence, there were more eggs in zero-tilled soil. Since root damage was significantly lower for zero-tilled corn plants, it was suggested that zero-tillage impeded survival of eggs or larvae. Insect populations in old grassland are often very large and may

ZERO-TILLAGE

103

pose problems for sod-seeded crops. Therefore, it is necessary to protect seeds and seedlings with suitable insecticides. A soil cover of crop residues attracts and protects animals which can especially damage the emerging seedlings. Slugs, mice, voles, hares, and birds were observed to feed preferentially on zero-tilled crops. Some of the reported damage, of course, may have been caused by unsatisfactory sowing methods. In dryland farming, some rodents may increase to such an extent that zero-tillage methods are rendered impracticable if control methods are inadequate or too expensive.

IV.

Crop Husbandry

Zero-tillage is still passing through its first stage of trial and error; a vast and reliable body of knowledge about the applicability of methods and implements, such as that gained in conventional systems, has not yet been accumulated. A.

SOWINGMETHODS

It appears to be rather difficult to insert seeds into the soil at the proper depth or at equidistant intervals where drilling performance is hampered by a layer of surface trash and where seed bed preparation is to be reduced to the least possible soil disturbance. In contrast to traditional tillage, in which the process of sowing requires several separate manipulations, often with a time lapse between each, zero-tillage machinery should adequately accomplish three tasks in one operation: it should open the soil for seed insertion, place the seed properly, and sufficiently cover the seed. Available equipment for opening the soil falls into two categories: “direct drought” and “power operated.” Working area assumed to be equal, power operated implements such as rotavators and powered harrows generally cause greater soil disturbance than “direct draught” implements such as flat sweeps, rolling or moldboard coulters, and tines. Seeds and fertilizers are inserted into the soil with hollow chisels or tines, fluted spear point openers, or double-disk seeders. When employed with a front disk, this device is known as a triple-disk seeder. Seeding furrows or slots are closed by devices such as covering chains, dividing knives or concave disks. Under dry conditions, seed-firming press wheels (which press seeds into the soil before any soil covers the seed), and press wheels (which press from the soil surface, so that seeds are covered by a compacted layer of soil) may help to close the furrows and improve the soil water supply to the seeds.

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K. BAEUMER AND W. A. P. BAKERMANS

Equipment usage has been described and tested by Stickler and Fairbanks (1965) and Taylor et al. (1969). Insufficient establishment of stands was caused mainly by failure to control sowing depths and to provide enough cover. When surface covering trash has to be cut by rolling coulters, difficulties may be encountered with fresh straw, which sometimes is too tough to be cut sufficiently. Sowing methods, by means of which either a strip or the total soil surface is cleared of existing vegetation or remaining plant residues and loosened thoroughly, as by rotavating or listing, are intended to minimize the risk of establishing an adequate stand. If sowing depth and covering are left uncontrolled, no great improvement can be expected. Although problems encountered with a living sod or a thick mulch layer are solved more easily by rotavating or listing, the specific advantages of zero-tillage soil structure may be lost. Thus, such methods are useful only for row crops and in renovating pastures. B.

WEED CONTROL

With zero-tillage, consistently satisfactory performance of herbicides is imperative as cultivation cannot be used to destroy vegetation that escapes the herbicide. As compared to conventional tillage, herbicide functions are extended. Before sowing, the vegetation initially present must be completely destroyed. This task calls for broad spectrum, nonselective herbicides with relatively short residual effects, e.g., paraquat, dalapon, or amitrole. During germination and subsequent growth of zero-tilled crops, potential weed competition has to be sufficiently suppressed. Here, highly selective and persistent herbicides are needed, herbicides which are not injurious to the crops grown, e.g., atrazine or simazine. At present, there is no herbicide available which possesses the qualities that would meet both demands equally well. Hence, without a panacea in sight, complicated systems of weed control must be developed if zero-tillage is to be used continuously. The first element is the herbicide system. Split application of one or several herbicides in combination is one method to increase the effectiveness of an herbicide system in some zero-tillage situations. Thus, at the transition from a sod crop, either old grassland or a cover crop to a zerotilled crop, a combination of translocated herbicides, applied as soil and/or foliage treatment, can be used as a first step to kill gramineous and broadleaved perennials. In a prolonged fallow, e.g., in humid areas during the winter, more persistent herbicides can be applied to kill perennial weeds. The timing of these treatments is determined by the time when the existent vegetation can be controlled and by the cropping program. If a susceptible

ZERO-TILLAGE

105

crop is to follow, the application has to be timed in accordance with the persistence of the herbicide at different locations. The determining factors are the dose needed to kill existent vegetation, soil moisture and temperature, frequency and amount of precipitation, which all influence the rate of inactivation or percolation of the herbicide used. If the amount of mulch present is not relevant to the success of zerotillage, doses of most herbicides can be kept low when the existent vegetation is reduced by mechanical means, e.g., by shredding, grazing, or cutting for conservation. On the other hand, foliage treatment with translocated herbicides, e.g., dalapon or “hormone” weed killers requires lush vegetation with a large leaf area in order to be effective. As a second step before sowing, a quick-acting but nonpersisting herbicide, such as paraquat or diquat, can be used to destroy the still living unwanted vegetation. During the third stage, the growing crop is treated with chemicals which selectively control all weeds escaping from previous herbicide treatments. Starting from a stubble situation, the system of split herbicide applications begins at stage 2, i.e., paraquat application followed by a selective weed killer, which is tolerated by the following crop. The second element of weed control in long-term zero-tillage systems consists of the proper choice of suitable main and catch crops as well as a sophisticated use of cropping sequences. Crops with slow seedling growth or a prolonged ripening phase can be grown only if protected by persistent and highly selective herbicide treatments. Otherwise, fast-growing and therefore weed-suppressing crops, which do not slacken in competitive power during later growth stages, are to be preferred. If water conservation during fallow periods is not an essential part of a cropping system, green manure or mulch crops should be grown whenever possible. The competitive power of such fast growing crops must be strengthened by using high seed rates and liberal amounts of fertilizers. As a third element of weed control, the effectiveness with which normal husbandry operations are performed is even more important in zero-tillage than in conventional tillage. Irregular stands resulting from imperfect sowing methods, malnutrition of crops, which may cause either poor growth or severe lodging, lack of plant protection against pests and diseases, and ineffective timing and dosing of herbicide applications, often encourage weed growth. Extra efforts are necessary in zero-tillage systems with regard to early identification and prevention of a beginning invasion of rhizomatous perennial weeds, especially from field borders. Herbicide systems have been developed and tested for zero-tillage situations by Triplett (1966, maize), Bakermans and De Wit (1970, cereals and other crops in mixed farming), Phillips ( 1972, wheat-fallow-wheat

106

K. BAEUMER AND W. A. P. BAKERMANS

rotation), Wicks (1972, maize), Kincade (1972, soybeans), Kirby (1972, grain sorghum), and Peters (1972, maize and sorghum). In zero-tillage, problems are posed mainly by gramineous weeds. In continuous no tillage maize cropping in North America, crabgrass (Digitaria sanguinalis, Digitaria ischaemum ) and fall panicum (Panicum dichotorniflorurn) may become prevalent. Peters (1972) proposed to solve this problem with split applications of herbicides, especially of residual selective herbicides. It has yet to be proved whether such a measure suffices to stabilize the system. Changes of the cropping system which would allow the use of different herbicide-crop combinations for weed control would probably be more effective. D. Tiedau (personal communication, 1972) found that a sequence which completely controlled quackgrass or couchgrass (Agropyron repens) was horseradish (Raphanus sativus) sown in autumn into the cereal stubble followed by maize in the spring. Both crops are fairly competitive in relation to couchgrass, radish owing to its fast growth during early stages and maize after it closes its leaf canopy. They allow the repeated application of relatively small, yet still effective doses of herbicides, e.g., for the green manure crop the sequence dalapon (preemergence)-paraquat (preemergence)-dalapon (postemergence), and for maize paraquat (preemergence)-atrazine (postemergence) . The combined effects of competitive crops and suitable herbicides applied at times when the weeds involved are most susceptible have to be used in a system of small steps in order to solve the problems with perennial weeds under continuous zero-tillage. C.

PASTURERENOVATION

Since it is feasible to destroy or temporarily suppress the existing vegetation of unproductive grassland with herbicides and to establish herbage stands with sod seeding equipment, the concept of zero-tillage has been adapted for pasture renovation over a wide range of situations. It is a promising alternative to conventional methods, in which topographic, climatic, and edaphic conditions do not allow the use of the plow or other deep tillage implements (Charles, 1962). Renovation methods differ according to whether a complete or partial replacement of the existing vegetation is intended. For complete renewal, herbicides and sowing methods have to be applied, as described for the transition of old grassland to arable land. Some regrowth of weeds and indigenous species which, in a renovated sward, is difficult to control with herbicides alone, seems to be inevitable (Allen, 1968). Hence, success in reseeding a permanent pasture will finally depend on the subsequent management of the newly established sward.

ZERO-TILLAGE

107

Whenever possible, the use of a two-stage system of renovation may be more effective. The first step is to grow a zero-tilled crop like maize (Moschler et al., 1969), wheat (Van Keuren and Triplet, 1972), or Brassica fodder crops (Toosey, 1971). Thus the combined effect of selective herbicides and the competition of the cover crop can be used. Then, the herbage species are sown without tillage either into this crop or, after harvest and repeated herbicide application, following the arable crop. Where persistent weed grasses like Agropyron repens or Deschampsia caespitosa dominate the old sward, zero-tillage methods may fail to eradicate these unwanted species. In such cases, where conventional tillage can be applied, Hoogerkamp (1970) found that thoroughly rotavating the upper soil layer was indispensable before reseeding. Nonetheless, zero-tillage in its most extreme form appears to be an effective means of renovation where less complete control of the existing vegetation is tolerated or intended. This is the case with resowing rangeland under dry or mediterranean conditions. Evans et al. (1967), Everson et al. (1969), and Kay and Owen (1970) reported successfully reseeding some wheatgrass species (Agropyron ssp.) on abandoned crop and range land in the western United States with sod-seeding methods. Here, the advantages of sod-seeding under dryland conditions on steep and rocky sites can be fully exploited. Thus, a firm seed bed and the protective cover of old litter enhance seedling establishment and prevent soil erosion. The possibility of sowing soils which are too wet for conventional tillage leaves the option of seeding or not seeding in case of a late opening rain. Band seeding has the added advantage of preserving a growing sod for reliable erosion protection on more than half the area. This system has been successfully employed in introducing more productive herbage species into permanent pastures. The old sward is partially suppressed by spraying the herbicide in narrow bands and/or by strip-tilling the sod. Taylor et a/. (1969) and Van Keuren and Triplett (1972) reported satisfactory establishment of legumes or grasses in unproductive grass sods in the humid eastern United States. Growing arable crops in live grass sods to increase total production through the use of periods when grasses are less vigorous may be considered a dubious practice. Yet, coastal bermudagrass (Cynodon dactylon) and maize (Beale and Langdale, 1964) or rye (Welch et al., 1967) have been grown simultaneously using zero-tillage methods with satisfactory results in the southeastern United States. This is possible because this summer perennial remains dormant during a period in which crops adapted to temperate climates still grow vigorously. Of course, some reduction in yield of either complement of this system may be inevitable.

108

K. BAEUMER AND W. A. P. BAKERMANS

D. FERTILIZATION In zero-tillage, all fertilizers are broadcasted except when row crops are grown and fertilizers are applied in a band near the seed. Therefore, P and K were found to be concentrated near the surface of untilled soil. Comparing various application methods, Triplett and Van Doren ( 1969) and Moschler et al. (1972) observed that surface application of P and K did not limit the growth of maize even on sites quite low in available nutrients (Triplett et al., 1972). Here, at low rates of nutrient application, band placement was more efficient. Under the more humid conditions that prevail in Western Europe, P and K near the soil surface are generally readily available (Ehlers et al., 1973). Thus, P-K fertilization seems to offer no special problems with zero-tillage. b

a

c

e . 2 0

N

2

-

60. 50

1961 1967

-

- _ _ _ - - - - - ---_ _ _ ~

D-

-2

. 0 x.

N

0

v

40 -

52 .

44

-

30 1970

.-C

c

30 -

28

-

0)

201

0

100

200 kg N l h a

300

201

0

50

100

150

kg N l h a

FIG. 11. Response of maize (a) and winter wheat (b) to N fertilization on tilled soil. (From Triplett and Van Doren, 1969; Blevins et a!., 1972; G. Pape and H. Fleige, personal communication, 1972.)

(O---O)and untilled (0-0)

More attention has been paid to N fertilization (Triplett and Van Doren, 1969; Debruck, 1971; Blevins et al., 1972). Figure 1 1 shows the typical yield response to N fertilization for maize in the United States and for cereals in Western Europe. In general, field crops grown on untilled soil need and can stand higher doses of N fertilization. This is especially the case when zero-tillage methods are applied on old arable soil. It is not yet known whether this higher demand for N fertilization is a transient phenomenon only. A few observations indicate that after some years of continuous zero-tillage (cf. Table I, winter barley), especially on old grass-

ZERO-TILLAGE

109

land (Bakermans and De Wit, 1970), cereal crops may not exhibit differential N demands on tilled and untilled soil. Triplett and Van Doren ( 1969), in an experiment involving 6 years of continuous maize cropping, found that the lime deficit increased markedly at high rates of N application, particularly in the top 5 cm of the untilled treatment. This result and some observations of Shear and Moschler (1969) demonstrate the need for more frequent liming with zero-tillage methods. E.

CROPYIELDSAND CROPPING SYSTEMS

Differences in crop yield caused by tillage methods reflect the overall performance of the systems examined. Factors contributing to yield depressions, such as lower stand or less complete weed control, may be inherent to one or the other tillage system. Nonetheless, some failures observed with zero-tillage may be due only to lack of experience and the inadequate techniques employed. Therefore, if possible, data are cited only from experiments whose results are not hampered by these shortcomings.

1. Row Crops Zero-tillage research and practice in the United States centers around corn production. Recently, other row crops, such as soybeans, sorghum, and cotton, have been included. Maize is grown in rotation with the above-mentioned row crops, with small grains and sod crops, such as tall fescue, orchardgrass, clovers, alfalfa and lespedeza, or in a system of continuous corn cropping. Gross average maize grain yields were compiled by Van Doren and Triplett (1969) and are listed in Table 11. Zero-tillage planted maize which followed sod crops on silt loam soils produced substantially greater yields as compared with the spring-plowed conventional systems. The highest corn yields were observed where the largest amounts of mulch occurred (Van Doren, 1965; Moschler et al., 1967). Corn yields were equal for both tillage systems-first, on clay loam to clays following a sod crop; second, on silt loam soils following a row crop-whereas zero-tillage plant following a row crop on clay loam to clays produced lower corn yields than the fall-plowed conventional tillage system. This apparent interaction between soil type and previous crop is relevant for the applicability of either tillage system. In Northwestern Europe, maize is grown mainly for ensilage. Zero-tillage methods have been used only experimentally but with the same success as in the United States.

110

K. BAEUMER AND W. A. P. BAKERMANS

TABLE I1 Corn Grain Yield as a Function of Previous Crops, Soil Types, and Tillage Systems" Grain yield (kg/ha)

State

Ohio Ohio Ohio

Ohio Virginia

Soil surface texture

Clay loam to clayb Clay loam to clayb Silt loam" Silt loam" Silt loamd

Number of Previous location crop years

Row Sod Row

Sod Sod

18 13 24 16 15

Conventional tillage Zero-tillage

6550 6610 5890 6560 5170

5890 6360 5890 7400 6180

Data from Van Doren and Triplett (1969).

* Hoytville and Toledo series.

Wooster, Crosby, Canfield, and Ravenna series primarily. Greendale, Groseclose, and Lodi series primarily.

Soybeans are often grown in short rotations with corn, cotton, small grains or a sod crop. Experimentation with tillage methods in soybean production is rather limited. In Ohio, zero-tilled and spring-planted soybeans produced slightly less than conventionally planted stands at 4 locations, whereas at one location higher yields were observed during a period of 6 or 3 years, respectively (D. M. Van Doren, G. B. Triplett, and J. H. Henry, personal communication, 1972; D. M. VanqDoren and G. B. Triplett, personal communication, 1972). On heavy clay soils in Mississippi, stubble planting of soybeans resulted in substantial yield increases as compared to plowing in the fall and repeated disking in the spring (Kincade, 1972). In states south of Ohio, a system of double cropping, i.e., planting soybeans immediately following small grain harvest, is widely used. After 3 years of experimentation in Ohio, zero-tillage planting produced yields superior or equivalent to those produced by plowing in four trials out of five (Triplett et al., 1972). The most pronounced yield differences occurred in years with the least rainfall. Similar observations were made by Lewis (1972) in North Carolina. In the southern half of the Great Plains, where corn production is hazardous because of drought and heat, grain sorghum is grown extensively in rotation with small grains and, if necessary, with fallow-e.g., wheat-sorghum-fallow. In an 8-year study of this type of rotation in Kan-

ZERO-TILLAGE

111

sas, Phillips (1969, 1972) obtained equal or slightly higher grain yields of Sorghum bicolor with zero-tillage as compared to conventional methods. Under the influence of the herbicide treatments used, the invasion of the untilled plots by grasses, e.g., Cenchrus incertus, has developed into an unsolved problem. Stickler and Fairbanks (1965) concluded from a study of continuous sorghum cropping that zero-tillage appears to be less promising for grain sorghum than for corn. Proper control of volunteer sorghum could be obtained only with fall tillage. Zero-tillage production of cotton is practiced in the southern United States, but information about results is rather sparse. Lewis (1972) reported an equal lint yield of cotton produced by conventional and zerotillage methods. He obtained similar results with peanuts. To sum up the available information, it appears that the experience gained will allow an evaluation of no-tillage in corn production only. Much more experimentation is needed to more fully develop and evaluate suitable zero-tillage production of other row crops.

2 . Cereal Crops

In Europe, experimentation with zero-tillage centers around the production of small grains. Cereal crops are usually grown by rotating spring and autumn sown cereals with an occasional “break” consisting of root crops, forage or oil crops. Cropping systems with continuous wheat or barley have been employed increasingly during the last decade. In such systems, fallow periods between cereal crops are used for growing short-lived green manure crops in order to maintain a high level of soil productivity. Figure 12 summarizes the results of experiments on winter wheat and spring barley or oats, respectively. In trials with winter wheat, reductions and increases in yield caused by zero-tillage methods occurred with about equal frequency, whereas with spring sown barley or oats, 56% of the reported results are favorable to conventional tillage methods. No explanation can be given for the higher frequency of failures in growing spring barley with zero-tillage methods. The reasons for the observed yield differences cannot be traced in every single case, but are attributable to a number of factors. Disparity in plant population, especially in the early experiments, differences in weed infestation and in incidence of diseases and pests are the main causes. Nonetheless, similar and even higher yields can be obtained with zero-tillage methods than with conventional tillage.

112

K. BAEUMER AND W. A. P. BAKERMANS

V a D.

-

? m

1

3

5

7

(0)

-

D

$ 7 . + I

1 (b)

3

5

FIG. 12. Yield response of ( a ) wheat (@), ( b ) spring barley ( 0 ) and oats ( A ) t o tillage methods. (Compiled data from Cannel and Ellis, 1972; Debruck, 1971; Bachthaler, 1971; G. Pape and H. Fleige, personal communication, 1972; J. R. Finney and B. A. G . Knight, personal communication, 1972.)

7

untilled, grain yield ( f / h a )

3. Root Crops Since more soil disturbance occurs in planting and harvesting sugar beets or potatoes than with other crops, application of zero-tillage methods in root crop production must be regarded as a dubious practice. Similar to the experiences with maize, sugar beet yields indicate an interaction between soil type and tillage method (Baeumer and Pape, 1972). On clay loams to clay zero-tilled sugar beets yielded up to 20% less than conventionally tilled beets; on medium textured soils prone to slaking and crusting, e.g., silt loams, equal or higher yields were obtained; and on light sandy soils, which are subject to wind erosion, the only possible method to grow sugar beets was zero-tillage. Generally, the number of fanged or forked beet roots increased when deep plowing was omitted. Yet, as zero-tillage improved the trafficability

ZERO-TILLAGE

113

of soil, harvesting operations appeared to be more efficient during wet periods. When the availability of N on a zero-tilled loam was reduced, the quality of the sugar beets improved consistently over an investigation period of 4 years (Baeumer and Pape, 1972). Zero-tillage methods have been tried in potato production. With adequate N fertilization, an equal total yield of potatoes was obtained on light sandy soil (Bakermans and Dc Wit, 1970) and on heavy marine silt soil in the Netherlands. Yet, zero-tillage reduced the marketable yield.

4 . Fodder Crops Short-lived forage crops are usually grown as catch crops or in systems of double cropping. Hence, zero-tillage is likely to increase yields in situations in which deep and clean tillage would consume valuable growing time, induce unwanted loss of soil moisture and, as a result, would delay germination. The firm soil surface left by this method is less liable to be poached. Therefore, these crops can be successfully grazed even during prolonged spells of wet weather. On a commercial scale in Great Britain, zero-tillage of fodder crops thus far has been confined to sowing Brassica root and green forage crops into grassland or cereal stubble (Toosey, 1971). Here, as elsewhere in northwestern Europe, turnips, rapes, kales, and Italian ryegrass are usually the only source of fresh succulent feed available during the late winter months or early in the spring. Given high doses of N fertilizers, no-tilled fodder kale produced equal or even higher yields than conventionally tilled crops (During et al., 1963; Hood, 1965). Winter cereals are widely grown for forage in the southeastern United States and in South Australia. In analogy to the results obtained with cereal grain crops, zero-tillage methods should be expected to be equally successful. Yet, in the United States, the common practice is still to sow fodder or cover crops by conventional methods. Favorable results for sod seeding winter cereals in Australia are reported by Wheeler and Campbell (1969). Robinson (1963) reviewed similarly good results obtained in the United States and evaluated the usefulness of this system in relation to rainfall distribution.

5 . Other Crops Besides the crops reviewed here, various other crops have been experimentally grown with zero-tillage methods. It must suffice to report some results obtained with oil seed rape, which is mainly grown in northwestern Europe. Vez and Vullioud (1971b) reported equal and higher seed yields in three out of four experiments on heavy soil in Switzerland, whereas

114

K. BAEUMER AND W. A. P . BAKERMANS

Bakermans and De Wit (1970) obtained mainly reduced yields with zerotillage in 6 experiments conducted in the Netherlands.

V.

Evaluation of Zero-Tillage in Farming Systems

In selecting tillage practices, the individual farmer considers factors such as the net return achieved by a tillage system, its feasibility with regard to time and labor required per hectare, climate, soil, cropping system, weeds, pests, and other factors which might limit the choice of a tillage system. The general public may be interested in this choice as far as changes in environmental quality are concerned. Economic evaluation of zero-tillage has been mainly confined to the comparison of machinery and labor working rates in contrasting tillage systems (Kincade, 1972). The number of tractor hours needed for growing cereals in England was reduced to 18% and 8% of the time consumed by conventional tillage on light and heavy soils, respectively, by zero-tillage (Wybrew, 1968). Yet, this reduction of costs may be counterbalanced by increased expenses for weed and pest control as indicated by the results of an investigation into the economics of zero-tillage production of maize in the United States cornbelt (Doster, 1972). Hence, as far as present :osts of herbicides and other inputs are concerned, only increased crop yields, greater ease in timing of planting, harvesting, and other farming operations, the possibility of introducing a more profitable cropping system or reducing such hazards as soil erosion would induce a farmer to adopt zero-tillage methods.

A.

APPLICABILITY OF ZERO-TILLAGE I N HUMID,TEMPERATE CLIMATE REGIONS

At present, maize appears to be the crop best adapted to zero-tillage methods. This is true not only from the standpoint of possible yield increases, but also to the fact that herbicide systems that provide season long weed control for maize production are available. As demonstrated by the data presented in Table 11, the factors soil, climate, and cropping system interact strongly with tillage practices. A more detailed analysis is available from Ohio (Fig. 13; Triplett et al., 1968, 1970; Van Doren, 1971 >,where, on sloping, structurally unstable soils with silt loam surface textures, not only the ever present erosion hazard but also runoff and unproductive evaporation depress corn yield. In this situation, a sod crop improves water infiltration and resistance to soil ero-

115

ZERO-TILLAGE

sion. Hence, preservation of this soil structure with zero-tillage resulted in highest grain yield observed (cf. Fig. 13, treatment 1 ) . Soil conditions resulting from .a previous row crop generally reduce the ability of these soils to transform precipitation and soil moisture into grain yield, even with a good ground cover present. In this situation, loosening the soil with minimum tillage and interrow cultivation resulted in higher corn yields than those obtained by zero-tillage (cf. Fig. 13, treatment 6 as compared to 7 ) . Removing any soil cover left by a row crop resulted in the lowest yield, even with zero-tillage (Fig. 13, treatment 10). All these effects of mulch cover and tillage intensity did not influence the yield when sufficient water was made available by irrigation.

5

previous

tillage operat ions

f e crop

plant

1

2

3

d i s k -.-D

.............. D

wdisk,etc

-.D

plant r:..

plant

5

6

7

good,-^ disk

.:.”

....... ......o ...................

.....

D

................ ...

“%disk, etc

D

......D 7001

plant

D

plant

6619 5983 5601 5155 4519

FIG. 13. Yield response of maize (mean grain yield, 1958-1965) to tillage systems on “crusting” soil in Ohio. (From Van Doren, 1971.)

From these results it can be concluded that the response mechanism for soil stirring is presumably similar to that for soil cover and that on crusting, sloped soils in Ohio, the intensity of tillage must be increased as surface cover and structural stability of these soils decreases. Yet, the decision whether to employ some secondary tillage is influenced by the fact that overall secondary tillage can lead to as great as 10-fold increases in soil loss. Hence, zero-tillage may be advisable despite reduced yields in some situations. The data presented in Fig. 13 concern the immediate crop response to a cropping-tillage treatment; long-term effects of rotation-tillage systems, however, are of equal importance. As shown in Table 111, yields of corn grown without tillage were greater for each rotation examined than with conventional tillage for crusting, sloping silt loams in Ohio. From the foregoing discussion, this could not be expected for zero-tillage in combination with row crop rotations. Triplett et al. (1970) speculated that perhaps

116

K. B A E U M E R A N D W. A. P. B A K E R M A N S

after several years without plowing, a stable structure that would not require high levels of mulch for maintaining satisfactory infiltration rates would develop at the soil surface. The same authors investigated long-term tillage effects on level, structural stable soils with clay loam to clay surface textures. Due to the high clay content, cracks which rapidly absorb water during summer rains form upon drying. Therefore, runoff and soil erosion is reduced to a minimum. On these soils, the timing of tillage operations is most difficult and tillage costs are highest; hence, the farmers' need to employ zero-tillage is greatest. Yet, from a standpoint of immediate yield responses, as shown by the maize data in Table 11, fall plowing appears to be indispensable on these soils. Again, this conclusion is modified by long term rotation-tillage effects (cf. Table 111). On poorly drained, noncrusting, heavy soils in Ohio, corn TARLI.: 111 Long-Term Itotation-Tillage Effects 011 IXffcrent Soil Types: Corn Yields (kg/ha) Expressed as No-Tillage Minus Conventional Tillage" Well drained silt loam soil

Corn, oats, meadow Corn, soybeans Continuous corn LSDO.06

+G93 +a93 +756 630

Poorly drained silty clay loam to clay soil

-63

- 189 -819

567

Data from Triplett et d. (1970), average for fifth through seventh years whenever weed control and stands were equal on all treatments at a given location. Two locations for each soil.

yields were essentially equal for both tillage systems in the corn-oatsmeadow and corn-soybean rotations. With continuous corn, however, the yield declined with zero-tillage. The reason for this is not readily apparent since, in contrast to the Ohio results, Moschler et al. (1972) observed the highest yield increase (39 % ) by zero-tillage on the least productive soil examined, a poorly drained clay loam in Virginia cropped with continuous corn. In this 5-year trial, maize was planted onto a cover crop of rye, which might have been indispensable to the favorable results obtained with zero-tillage. The above-quoted results of long-term trials indicate that, in an almost weed-free environment, zero-tillage can be sustained for several years with-

ZERO-TILLAGE

117

out encountering a yield reduction. This was confirmed in a 6-year comparison between conventional, zero-tillage and alternate corn production in Virginia by Shear and Moschler (1969). Plowing a loam soil cropped with a rye mulch and continuous corn every second year resulted in a significantly lower yield than the continuous application of zero-tillage and an essentially equal yield as compared to the continuous use of conventional tillage methods. To sum up, maize can be successfully grown without tillage where rotation with sod or cover crops is possible and profitable on structurally unstable soil which is exposed to wind and water erosion or on which increased water infiltration increases the yield and, with some limitations, on structurally stable clay soil. The marked interaction between tillage, soil type, and cropping system noted above underlines the need for more information about system responses under various ecological conditions. This applies equally to other row crops, for which zero-tillage probably would enhance the adoption of double cropping systems. Small grains and forage crops appear to be the second group of crops well adapted to zero-tillage practices. It has been proved, especially by experimentation in Europe, that cereals and some fodder crops can be grown successfully without any tillage on soil which iies in the textural range from light to medium, if only one essential requirement is fulfilled: satisfactory weed control, especially of persistent grass weeds. This appears to be most difficult in rotations in which cereals are grown continuously and where possible fallow periods are too short for growing competitive “break” crops, which allow herbicide treatments to kill all noxious weeds selectively. Due to increzsing infestations of untilled plots by gramineous weeds, several long-term trials with extensive cereal cropping have had to be terminated. Unless new herbicides or herbicide cropping systems prove to be more effective the application of zero-tillage as a continuous system appears to be restricted to rotations in which a cereal crop alternates with maize, a Brassica crop or a ley which is killed by a suitable herbicide and leaves a weed-free environment for the following cereal crop. Since such rotations are feasible only in connection with animal production, the application of zero-tillage methods can be envisaged mainly with some systems of “mixed” farming. Here too, it must remain an opportunist’s technique for the present time. Thc same holds for “pure” arable farming, in which drilling green manure crops or winter cereals may be developed to the main area for application of zero-tillage methods. Nonetheless, the experience gained with zero-tillage has promoted the development of minimal tillage techniques aimed at circumventing the problem of weed infestation and maintaining the advantages of zero-tillage effects.

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Thus, zero-tillage does not have the wide application first envisaged. This is especially disappointing for those who have to farm very heavy soil. Here it would be profitable to omit moldboard plowing and to use zero-tillage methods. So far, most such attempts have failed, especially when the heavy soil was waterlogged during spells of rainy weather. As the need to apply zero-tillage is greatest in such situations, research must be continued to find the causes and develop remedies. Only little information is available about the suitability of zero-tillage methods for farming other marginal soil. H. Kuntze and R. Bartels (personal communication, 1972) reported increased cereal yields on peat soil with continuous zero-tillage application over a period of 4 years. Bachthaler (1971 ) obtained a higher yield of winter wheat, but slightly lower yields of spring barley and oats on loamy clay soil with a stone content of 22-26%. To sum up, the possibility of growing cereal and fodder crops with zero-tillage with reasonable success has been shown repeatedly. Where wind and water erosion or other conditions restrict arable farming, continuous zero-tillage may offer a solution. Yet, with intensive farming, due to the higher risks and costs of complete weed control with chemicals only, continuous zero-tillage cannot be regarded as an alternative to conventional methods at present. If needed, zero-tillage may be the last resort when proper sowing cannot be achieved by conventional means. Finally, where soil conditions and requirements of a crop allow the application of zero-tillage, it will certainly be an economically attractive choice. B.

APPLICABILITY OF ZERO-TILLAGE TO DRYLAND FARMING

Since in dryland farming tillage expenses make up a far greater percentage of total farming expenses than in humid regions, it would be economically attractive to use zero-tillage methods if the yields obtained are similar to those with stubble mulch farming or the still widely used black fallow by plowing. Whereas Stibbe and Ariel (1970) observed reduced yields on Grumusol clay soil in Israel, the same yields were produced by zero-tillage and conventional dryland tillage methods on light- to mediumtextured soil in the United States. With continuous zero-tillage, weed control still presents problems. Phillips ( 1972), experimenting with tillage systems in a wheat-sorghum-fallow rotation in Kansas, concluded that the zero-tillage concept was not sufficiently consistent and that herbicides should be supplemented with some tillage. Controlling a volunteer crop may be difficult when a system of continuous sorghum is used (Unger and Wiese, 1972). Hence, further research on the applicability of zero-tillage in dryland farming is needed.

ZERO-TILLAGE

VI.

119

Conclusion

Zero-tillage refers to tillage systems in which soil disturbance is reduced to sowing operations and traffic only and where weed control must be achieved by chemical means. It has been demonstrated to be of practical value in maize production on sloping, structurally unstable soil, in double cropping systems with cereal and forage crops, and in pasture renovation. More than any other tillage system, zero-tillage maintains crop residues on the soil surface; hence it protects the ground against wind and water erosion. Therefore, zero-tillage acreage will probably increase where erossion hazards limit arable farming. In other situations, further adoption of zero-tillage depends on potential production benefits with this new system which would exceed those with conventional tillage. Except for the abovementioned cases, those benefits could not be shown to occur in all cases at the present time. The problem of how to eradicate persistent weeds with continuous application of zero-tillage has yet to be solved. At present, incomplete weed control is the main obstacle to further adoption of zero-tillage. If this system is to be widely used in humid areas, substantial improvements must be made in the development of more effective herbicides and/or croppingherbicide systems. In order to predict the range for zero-tillage application, much more information is needed on interactions between soil type and climate on the one hand and cropping and tillage systems on the other. Erosion losses and, hence, pollution are minimized by zero-tillage. This fact alone justifies continued study of this system. A clean tilled field is certainly pleasing to the eye, but such a tillage objective has to be questioned with regard to the essentials of crop production and to maintaining environmental quality. Thus, the feasibility of zero-tillage can be an incentive for changing farming practices toward better management in relation to the environment. As part of applied research, there is a need to investigate the practical aspects of zero-tillage. Furthermore, this system appears to be an excellent tool for basic research in the field of agronomy. As demonstrated by the approach of the research group at the Ohio Agricultural Research and Development Center, realistic tillage requirements can be established in a weed-free environment. The results obtained indicate that in some cases the important factor in tillage is not exclusively weed control, but improvement of the soil structure. Compared to the conclusions drawn by McCalla and Army in 1961 about the state of knowledge on stubble mulch farming and the need for further information about the effects of such a system so close to zero-til-

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lage, the increase in practical experience and experimental results gained since is obvious. Yet, as shown by our review, only little has been gained in understanding plant production systems influenced by tillage methods. It has to be questioned whether the effort to obtain ever more pertinent data with extended and refined research will lead to substantial improvement in understanding systems such as zero-tillage. Clearly, a synthesis is required; it may eventually be attained with a more fundamental rather than empirical approach. It is hoped that system modeling will be a means of predicting tillage effects and that, in order to achieve this goal, zero-tillage research will function as an abundant source of information. ACKNOWLEDGMENT The authors are indebted to many colleagues who kindly supplied information and unpublished experimental results. Thanks are due to Mr. B. Fodiman for correcting the grammar and style of this manuscript. REFERENCES Adams, W. E., Pallas, J. E., and Dawson, R. N. 1970. Agron. 1. 62, 646-649. Allen, G. P. 1968. Proc. Brit. Weed Contr. Conf.,9th, 1968 pp. 1231-1237. Amemiya, M. 1968. Agron. J . 60, 534-537. Army, T. J., Wiese, A. F., and Hanks, R. J. 1961. Soil Sci. SOC. Amer., Proc. 25, 410-413. Arnott, R. A., and Clement, C. R. 1966. Weed Res. 6, 142-157. Bachthaler, G. 1971. Landwirt. Forsch. 26, 245-263. Baeumer, K., and Pape, G. 1972. Zucker 25, 71 1-718. Baeumer, K., Ehlers, W., and Pape, G. 1971. Landwirt. Forsch. 26, 264-272. Bakermans, W. A. P., and De Wit, C. T. 1970. Neth. J. Agr. Sci. 18. 225-246. Barber, S. A. 1971. Agron. 1. 63, 724-726. Barley, K. P. 1954. Soil Sci. 78, 205-210. Beale, 0. W., and Langdale, G. W. 1964. J. Soil Water Conserv. 19, 238-240. Bender, J., and Adamczewski, K. 1970. Pol. J . Soil Sci. 3, 59-64. Black, A. L., and Power, J. F. 1965. Soil Sci. SOC.Amer., Proc. 29, 465-468. Blevins, R. L., Cook, D., Phillips, S. H., and Phillips, R. E. 1971. Agron. 1. 63, 593-596. Blevins, R. L., Thomas, G. W., and Phillips, R. E. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 140-145. Boerner, H. 1960. Bot. Rev. 26, 393-424. Bond, J. J., and Willis, W. 0. 1969. Soil Sci. SOC. Amer., Proc. 33, 445-448. Bosse, O., and Herzog, R. 1969. AIbrecIit-Tlraer-Arclr. 13, 1141-1 159. Brooks, D. H., and Dawson, M. G. 1968. Ann. Appl. Biol. 61, 57-64. Brown, W. L., and Dickey, D. D. 1970. Soil Sci. SOC. Amer., Proc. 34, 118-121. Buhtz, E. 1972. Arch. Acker- Pflanzenbau Bodenk. 16, 381-390. Buhtz, E., Bosse, O., Herzog, R., and Waldschmidt, U. 1970. Albreclrr-Thaer-Arch. 14, 795-812. Bulfin, M. 1967. Ir. J . Agr. Res. 6, 189-201.

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Burrows, W.C., and Larson, W. E. 1962. Agron. J . 54, 19-23. Cannel, R. Q., and Ellis, F. B. 1972. Agr. Res. Counc. Letcornbe Lab. Annu. Rep. pp. 43-49. Charles, A. H. 1962. Herb. Abstr. 32, 175-181. Corbett, D. C. M., and Webb, R. M. 1970. Ann. Appl. Biol. 65, 327-335. Czeratzki, W. 1971. Landbauforsch. Voelkenrode 21, 1-12. Czeratzki, W., and Ruhm, E. 1971. Landwirt. Forsch. 26, 281-289. Debruck, J. 1971. Londwirt. Forsch. 26, 230-244. Doster, D H. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 41-54. During, C., Robinson, G. S., and Cross, M. W. 1963. N . Z. 1. Agr. Res. 6, 293-302. Ehlers, W. 1973. Z. Pflanzenernaehr. Bodenk. (in press).. Ehlers, W., Pape, G., and Boehm, W., 1973. Z. Pflanzenernaehr. Bodenk. 133, 24-36. Evans, A. C., and Guild, W. J. 1948. Ann. Appl. Biol. 35, 485-493. Evans, R. A. 1961. Weed Sci. 9, 216-223. Evans, R. A., Eckert, R. E., and Kay, B. L. 1967. Weed Sci. 15, 50-55. Everson, A. C., Hyder, D. U., Gardner, W. R., and Bement, R. E. 1969. Weed Sci. 17, 548-551. Garber, L. F. 1927. J. Amer. Soc. Agron. 19, 994-1006. Graff, 0. 1969. Pedobiologia 9, 120-127. Guenzi, W. D., McCalla, T. M., and Norstadt, F. A. 1967. Agron. J . 59, 163-165. Harrold, L. L. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 21-28. Harrold, L. L., Triplett, G. B., and Youker, R. E. 1967. J . Soil Water Conserv. 22, 98-100. Herzog, R.,and Bosse, 0. 1969. Albrecht-Thaer-Arch. 13, 739-763. Herzog, R., Bosse, O., and Igel, H. 1969. Albrecht-Thaer-Arch. 13, 1061-1069. Hood, A. E. M. 1965. Outlook Agr. 4, 286-294. Hoogerkamp, M. 1970. Neth. 1. Agr. Res. 18, 315-320. Jones, J. N., Moody, J. E., Shear, G. M., Moschler, W. W., and Lillard, J. H. 1968. Agron. J . 60, 17-20. Jones, J. N., Moody, J. E., and Lillard, J. H . 1969. Agron. J . 61, 719-721. Kahnt, G. 1969. Z. Acker- Pflanzenbau 129, 277-295. Kahnt, G. 1971. Landwirf. Forsch. 26, 273-280. Kay, B. L., and Owen, R. E. 1970. Weed Sci. 18,238-244. Kincade, R. T. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 113-123. Kirby, B. W. 1972. Proc. No-Tillage Syst. Symp. 1972 pp. 124-125. Kohnke, H., and Werkhoven, C. H. 1963. Soil Sci. SOC.Amer., Proc. 27, 13-17. Kuipers, H. 1970. Neth. J . Agr. Sci. 18, 219-224. Lewis, W. M. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 146-152. McCalla, T. M., and Army, T. J. 1961. Advan. Agron. 13, 125-196. Moody, J. E., Shear, G. M., and Jones, J. N. 1961. Soil Sci. SOC. Amer., Proc. 25, 516-517. Moody, J. E., Jones, J. N., and Lillard, J. H. 1963. Soil Sci. SOC. Amer., Proc. 27, 700-703. Moschler, W. W., Shear, G. M., Hallock, D. L., Sears, R. D., and Jones, G. D. 1967. Argon. 1. 59, 547-551. Moschler, W. W., Jones, G. D., and Shear, G. M. 1969. Agron. J. 61,475-476. Moschler, W. W., Shear, G. M., Martens, D. C., Jones, G. D., and Wilmouth, R. R. 1972. Agron. 1. 62, 646-649. Musick, G. J., and Collins, D. L. 1971. Ohio Rep. 56, 88-91.

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Newbould, P., Ellis, F. B., Barnes, B. T., and Howse, K. R. 1970. Agr. Res. Counc. Letcombe Lab. Annu. Rep. pp. 40-43. Norstadt, F. A., and McCalla, T. M. 1968. Soil Sci. SOC.Amer., Proc. 32, 241-245. Parker, D. T. 1962. Soil Sci. SOC.Amer., Proc. 26,559-562. Parker, D. T., and Larson, W. E. 1962. Soil Sci. SOC.Amer., Proc. 26, 238-242. Peters, R. A. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 132-139. Phillips, W. M. 1969. Weed Sci. 17, 451-454. Phillips, W. M. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 100-102. Rhixon, L. 1969. Colloq. Cult. Sans Laboure, 1969 pp. 89-122. Roberts, H. A., and Dawkins, P. A. 1967. Weed Res. 7, 290-301. Robinson, R. 1963. Agron. 1. 55, 306-307. Schmidt, B. L., and Kroetz, M. E. 1969. Proc. N . Cent. Reg. Workshop Wind Erosion, 1969 pp. 66-72. Schmidt, B. L., and Triplett, G. B. 1967. Ohio Rep. 52, 35-37. Schwerdtle, F. 1969. Z. Pflanzenkr. (Pflanzenpathol.1 Pflarrzenschutz 76, 635-641. Schwerdtle, F. 1971. KTBL-Ber. Landtech. p. 149. Shanholtz, V. O., and Lillard, J. H. 1969. J. Soil Water Conserv. 24, 186-189. Shear, G. M. 1968. Outlook Agr. 5, 247-251. Shear, G. M., and Moschler, W. W. 1969. Agron. J . 61, 524-527. Singh, T. A., Thomas, G. W., Moschler, W. W., and Martens, D. C. 1966. Agron. J . 58, 147-148. Smika, D. E., and Wicks, G. A. 1968. Soil Sci. SOC. Amer., Proc. 32, 591-595. Stibbe, E., and Ariel, D. 1970. Neth. J. Agr. Sci. 18, 293-307. Stickler, F. C., and Fairbanks, G. E., 1965. Agron. J . 57, 497-500. StrahBk, A. 1968. Outlook Agr. 6, 241-246. Taylor, T. H., England, J. M., Powell, R. W., Freeman, J. F., Kline, C. K., and Templeton, W. C. 1966. Proc. Brit. Weed Contr. Conf. 7th, 1966 Vol. 2, 792-803. Taylor, T. H., Smith, E. M., and Templeton, W. C. 1969. Agron. J . 61, 761-764. Tomlinson, T. E. 1968. “Research Curricular.” Agr. Div., I.C.I., London. Toosey, R. D., 1971. ADAS Quart. Rev. 3, 121-133. Triplett, G. B. 1966. Agron. I . 58, 157-159. Triplett, G. B., and Van Doren, D. M. 1969. Agron. J . 61, 637-639. Triplett, G. B., Van Doren, D. M., and Schmidt, B. L. 1968. Agron. J. 60, 236-239. Triplett, G. B., Van Doren, D. M., and Johnson, W. H. 1970. Trans. A S A E (Amer. Soc. Agr. Eng.) 13, 765-767. Triplett, G. B., Osmond, C. A., and Sutton, P. 1972. Ohio Rep. 57, 39-41. Unger, P. W., and Wiese, A. F. 1972. Proc. No-Tillage Syst. Symp., 1972 pp. 103-107. Van Doren, D. M. 1965. Soil Sci. SOC.Amer., Proc. 29, 595-597. Van Doren, D. M. 1971. Proc. Hybrid Corn Ind. Res. Conf.,22nd, 1971 pp. 37-44. Van Doren, D. M., and Triplett, G. B. 1969. Ohio, Agr. Res. Develop. Cent., Res. Circ. 169. Van Duin, R. H. A. 1956. Versl. Landbouwk. Onderz. 62, 7. Van Keuren, R. W., and Triplett, G. B. 1972. Proc. No-Tillage Sysi. Symp., 1972 pp. 69-79. Van Ouwerkerk, C., and Boone, F. R. 1970. Neih. J . Agr. Sci. 18, 247-261. Van Wijk, W. R., Larson, W. E., and Burrows, W. C. 1959. Soil Sci. SOC. Amer., Proc. 23, 428-434. Vez, A. 1969. Rev. Suisse Agr. 1, 5-12.

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THE GENETIC CONTROL OF FLOWERING AND GROWTH IN SORGHUM J. R. Quinby Pioneer Hi-Bred Company, Plainview, Texas

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Genetics of Flowering . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . .. . . . . . . .. 111. The Floral Stimulus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Physiology of Flowering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Genetics and Physiology of Cell Elongation . . . . . . . . . . . .. . . . . . . . . . A. Genetics of Height . . . . . . . . . . . . . . ................. B. Physiology of Cell Elongation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Height Genes and Leaf Size . . . . . . . . . . . .. . . ...,.. . . . ... ... D. Height and Peduncle Length . . .. . . . . . . .. . , . . . . . . . . . . . . .. . E. Height and Maturity Genes and Panicle Size . . . . . . . . . . . . . . . . . F. Types of Internode Distribution . . . . . . . . .. . . . . . . . .. . . . . . . . . . . VI. Influence of Photoperiod, Temperature, and Leaf Area on Flowering . . A. Photoperiod . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Leaf Area . .. . . . . . . . . . . . . . . ....................... VII. Influence of Maturity Genotype on PI owth and Adaptation . . . . A. Influence on Plant Growth . . . . . . . . , . . . . . , . . . . . . . . .. . . . . . B. Adaptation to Climate . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . VIII. Morphological Effects of Hybrid Vigor in Sorghum . . . . . . . . . . . . A. Panicle Size, Number of Seeds per Head, and Grain and ............ . . . . . . . . . .. . . . . . . . . . . . . . . . Stover Yield B. Leaf Blade Size ..............................

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............... ............... ............... ............... G. Size of Root System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

H. Seed Size and Test Weight per Bushel . . . . . . . . . . . . . . . . . . . . . . . I. Seed Size and Grain Filling Period . . . . . . . . . . . .......... J. Protein Content of Seed . . . . , . . . . . . . . . . . , . . . . . . . . . . .

K. Summary of Morphological Effects of Hybrid Vigor . . . . Genetic Control of Hybrid Vigor A. Effect of Heterozygosity at Maturity Loci B. Effect of Heterozygosity at 0 C. Discussion of Effects of Heterozygosity . . . . . . . . . X. Sorghum Genotypes as Experime A. The MILO Maturity Genotypes ................ B. Maturity Genotypes Recessive a r Maturity . . . . . . . ...... ....... . C. Pairs of Varieties that Differ at

126 127 129 129 132 136 132 132 133 135 135 136 136 137 138 140 140 140 141 141 142 143 143 143 144 144 145 145

IX.

125

151 152 152

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J. R. QUINBY

D. Temperate and Tropical Pairs of Varieties . . . . . . . . . . . . . . . . . . . E. Height Genotypes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . XI. Summary and Discussion of Genetic Control of Growth in Sorghum . XII. Implications to Plant Breeding ................................. A. Sorghum Breeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Plant Breeding in General . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . XIII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I.

152 153 154 156 156 159 160

Introduction

Plant hormones have been known since 1928, and the literature concerning the influence of hormones on plant growth and development has become voluminous (Leopold, 1964). Nevertheless, no mechanism of genetic control over growth that involves hormones has been recognized and reported. A dogma in the physiology of flowering is that the floral stimulus is hormonal and that a vegetative growing point differentiates into a floral bud whenever the floral hormone, that is produced in the leaves, reaches the proper level at the growing point. Because the different maturity genotypes of sorghum initiate floral buds at different times, there is reason to assume that the maturity genes, in some way, control hormone levels, Fifty years ago, Kiesselbach (1922) measured pith cells of parents and hybrids of Zea mays L. and concluded that hybrid vigor resulted largely from more rapid cell division in the apical meristem. Other data from corn cited by Patanothai and Atkins (1971) and recent data from sorghum seem to indicate the validity of that conclusion (Quinby, 1970; Patanothai and Atkins, 197 1 ) . If a greater rate of cell division is the basis of hybrid vigor, an understanding of the genetics and physiology of hybrid vigor should contribute to an understanding of the genetic control of plant growth . The inheritance of time of floral initiation and duration of growth in sorghum, Sorghum bicolor L. Moench, has been known since 1945 (Quinby and Karper, 1945; Quinby, 1966). More recently, Lane (1963) studied the influence of light on flowering in sorghum and Miller et al. (1968a) observed sorghum in monthly plantings throughout the year in Puerto Rico. Based on the information from these studies and on some knowledge of the genetic control of flowering in sorghum, it is now possible to formulate some hypotheses concerning the physiology of flowering in sorghum. Until now, genetics has contributed little to an understanding of the physiology of flowering and of growth. It is the purpose of this chapter to present a working hypothesis to explain the genetic control of flowering and growth which can be subjected to experimentation. It is hoped

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127

that the presentation of this model will stimulate an interest in the genetics and physiology of growth and result in work that will prove or disprove the hypothesis.

II.

Genetics of Flowering

Four gene loci that control time of floral initiation and duration of growth have been recognized in sorghum (Quinby and Karper, 1945; Quinby, 1966). The four gene loci segregate independently. Although no additional gene loci have been found, a number of recessive alleles at locus 1 (mal) and locus 3 (ma,)have been recognized. The assignment of dominance to late maturity was made because F, plants of certain MILO crosses were late to flower, but the lateness was due to gene interaction or epistasis rather than to dominance or recessiveness at one or more loci (Table I ) (Quinby, 1967). The maturity genes control leaf number because no leaves are laid down in the meristem after a floral bud is initiated. Maturity genes also control plant size, irrespective of growth rate, because the longer a plant grows the larger it becomes. In the past, it seemed reasonable to attribute only the initiation of the floral bud to the maturity genes (Quinby, 1967). It has become apparent that the maturity genes influence rate of growth as well as time of floral initiation because comparable leaves of plants of different durations of growth differ in size (Quinby, 1972). Additional functions must now be assigned to the maturity genes. The continuous variation of maturity in sorghum is thought to exist because of alleles, both dominant and recessive, at the four maturity loci and not to modifiers at other loci. The allelic situation has been discussed previously (Quinby, 1967, 1 9 7 2 ~ ) .Most tropical varieties are dominant at all four maturity loci and one reason for this conclusion is that a recessive at any locus causes temperate zone adaptation. Several single-gene recessive, temperate varieties have been identified (Quinby, 1967). Most of the 3000 temperate varieties in the world are recessive at locus 1 and are dominant at the other three. Because mutations to temperate zone adaptation must have occurred at many times in the past, recessive alleles at locus 1 must be numerous. Only one recessive allele is known at locus 2 and only one at locus 4, and recessive allelic series are not known at those loci. Five recessive alleles are known at locus 3, and three of the five occurred in the United States since sorghum was introduced about a century ago. More than 100 tropical varieties have now been converted to temperate zone adaptation by substituting recessive ma, for dominant Ma,. Because

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TABLE I Assumed Hormone Level and Duration from Time of Planting t o Floral Initiation and Flowering of Maturity Genotypes of MILO” Days t o Homoxygous maturity genotype and hormone 1evelh.c

Floral initiation

Flowering

1OOM

49

85

90M

49

78

80M

40

72

60M

39

68

SM80

36

66

SM60

31

64

SM90

29

62

SMlOO

29

60

44M

21

51

S8M

20

48

Strain

Data from a June 1, 1972, planting at Plainview, Texas.

“A” indicates high, and “a” low, auxin level. “G” indicates Iiigh, and “g” low, gibberellin level.

most tropical varieties are dominant at all four maturity loci, the converted varieties must be of the genotype malMazMa,Ma, with the recessive at the first locus the same in each. (Here, and henceforth in this chapter, a single gene symbol per locus will be used to indicate homozygosity) . Nevertheless, the converted varieties vary in flowering from 60 to 85 days (Quinby, 1 9 7 2 ~ ) Apparently, . early-maturing tropical varieties are converted into early-maturing temperate varieties and late-maturing tropical varieties into late-maturing temperate varieties. Because of the diversity in time of flowering among the converted varieties, the dominants at maturity loci 2, 3, and 4 must differ among varieties. Dominant Mal from lOOM M I L O causes later flowering in segregating populations than dominant Mal from Hegari. Furthermore, according to Haupt (1969), Wellensick (1965) found evidence in Pisum sutivum L. to indicate allelic series

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129

in late-, intermediate-, and early-flowering varieties of that species. Because dominant and recessive allelic series exist, it is not only the dominant or recessive condition at each locus that is important in determining time of floral initiation in sorghum; but, also, which allele is present at each locus. Ill.

The Floral Stimulus

The identity of the floral stimulus is the subject of much discussion in the literature. The literature has been reviewed many times and recently by Salisbury (1963), Lang (1965), and Evans (1969). Hamner (1940), using data from soybeans (Glacine max (L) Merrill), concluded that flower induction is governed by processes in the light, processes in the dark, and processes from an interaction between the two. Chailakhian (1961) suggested that the floral stimulus consists of two components and that the long-day component is gibberellin. The short-day component has not been identified but is probably auxin. Auxin is known to be involved in the flowering process; is used to initiate floral buds uniformly in the production of pineapples (Clark and Kerns, 1942) ; and interactions between auxin and gibberellin are well known (Leopold, 1964). The interaction of auxin and gibberellin in differentiation and growth of tissues has been discussed by Evans (1969). Some of the reasons for the failure to recognize auxin as a part of the floral stimulus are discussed in Section XI. In the rest of this chapter, auxin will be assumed to be the short-day component even though proof is lacking. There is reason to think that a vegetative bud changes into a floral bud whenever the floral stimulus reaches the proper level at the growing point. Assuming that a combination of auxin and gibberellin is the flowering stimulus, differences in time of floral initiation between maturity genotypes shown in Table I could be interpreted to mean that the floral stimulus accumulates at the growing point at different rates in different genotypes. This should indicate that auxin and gibberellin are being synthesized in the leaves at different rates in different genotypes and that there must be some genetic mechanism to control the rate of synthesis of the two hormones. Dominant and recessive alleles at the maturity gene loci and gene interaction appear to exercise this control. IV.

Physiology of Flowering

Phytochrome appears to be a regulatory agent in the growth of all seed plants (Hendricks and Borthwick, 1963) and is both a pigment and an enzyme. Phytochrome exists in a far-red absorbing form (Pis,,) and a red

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absorbing form (Paso) Because the sunlight that reaches the earth through the atmosphere contains both red and far-red wavelengths, plants growing in sunlight contain both forms of phytochrome in about equal amounts. During the night, and after conversion of P730 to P660, most of the phytochrome is in the P 6 6 0 form. P,,, was considered by Hendricks and Borthwick (1963) to inhibit flowering in short-day plants but to promote flowering in long-day plants. Phytochrome is generally considered to be involved, in some way, in controlling the reactions that lead to flowering. Some understanding of the genetics of flowering in sorghum has prompted some surmises regarding the role phytochrome plays in controlling time of floral initiation. Borthwick and Cathey (1962) have pointed out three possibilities to explain the long time that phytochrome must be in the P 7 3 0 form to prevent flowering of some varieties of Chrysanthemum. They concluded that different varieties might ( 1 ) contain different absolute amounts of phytochrome; (2) have different rates of conversion of PTs0to P660; or (3) have different levels of PTs0that would inhibit flowering. Differences in sensitivity to inhibition by phytochrome is a fourth possibility and is akin to the third possibility that different levels of P,30 might inhibit flowering. The MILO maturity genotypes of sorghum have contributed greatly to an understanding of the genetics of flowering in sorghum. Their origin appears in Section X, A. Lane (1963) determined that the MILO maturity genotypes do not differ in phytochrome content or rate of conversion of P,,, ,to Po60 in darkness. It seems logical, therefore, to assume that dominant and recessive maturity alleles cause differences in sensitivity to inhibition by phytochrome. Assuming that the floral stimulus consists of auxin and gibberellin, P 7 3 0 appears to inhibit the synthesis of auxin during daylight and P660 to inhibit synthesis of gibberellin during the night. Because of these inhibitions, auxin is synthesized largely during the night and gibberellin largely during daylight. P,,, converts to P 6 6 0 in darkness and, after the conversion to P660, synthesis of auxin is not inhibited for the rest of the night. P 6 6 0 appears to inhibit the synthesis of gibberellin during the night; and, if this is true, P660 is not inactive as argued by Hendricks (1960); but is inhibitory to flowering as suggested by Takimoto (1969). Alleles at loci 1 and 2 appear to cause differences in sensitivity to inhibition by PTs0,and alleles at loci 3 and 4 to cause differences in sensitivity in inhibition by P,,,. It is likely that recessive alleles at loci 1 and 2 allow the synthesis of some auxin during the day to supplement that produced during the night despite the presence of PTs0during the day. Likewise recessive alleles at loci 3 and 4 probably allow the synthesis of more gibberellin during the day than dominant alleles. a

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The assumed effects of dominant and recessive alleles on duration from planting to floral initiation and to flowering and on hormone levels are shown in Table I. Dominant alleles result in low levels of auxin and gibberellin and recessive alleles in higher levels of the two hormones. 100M, that is dominant at all four loci, is assumed to synthesize small amounts of both hormones because of sensitivity to inhibition by Ps30and by P G G o . 80M is recessive at ma2, is assumed to synthesize more auxin than 100M, and flowered earlier. SM80 (rnalma2)is assumed to synthesize more auxin than either 80M or 100M and flowered earlier than either. However, SMlOO (malMaz) is assumed to synthesize less auxin than SM80 but flowered earlier indicating that too much auxin, as well as too little delays floral initiation. This is not an isolated case because Early Kalo (malMa,) flowers earlier than Kalo (malmar) (Quinby, 1967) and KMH-1 (Malma2)flowers earlier than KMH-2 (rnalrna,) (Quinby, 1 9 7 2 ~ )SM90 . (ma1Ma2)flowered earlier than 60M (Malmaz) and this is assumed to indicate that recessive ma, and recessive ma, result in different amounts of auxin. All ten maturity genotypes of MILO are dominant at Ma,. Recessive mu3 is assumed to result in more gibberellin than dominant Ma, and all recessive ma3 genotypes are earlier to flower than the dominant Mas counterparts. 38M and 44M differ from the other eight maturity genotypes of Milo in being recessive ma,R. Presumably, these two genotypes synthesize more gibberellin than the others. Both 38M and 44M in addition to being early to flower, have long narrow leaves, slender stems, and long internodes. Even the first four embryonic leaves are long and narrow and these two genotypes can be recognized in the seeding stage. The early flowering of 44M and 38M appears to be caused by a high rate of synthesis of gibberellin during the day that results from a low level of sensitivity to inhibition by P,;co.44M and 38M initiate floral buds before SM60, and the presence of recessive ma3 appears to result in too little gibberellin for earliest floral initiation when the level of auxin is at the level resulting from either Ma,ma, or ma,mu,. But when recessive masR is present, the higher level of gibberellin that is synthesized matches the high level of auxin; and early floral initiation results. Unlike auxin, high levels of gibberellin appear not to delay flowering. It is apparent that the maturity genes, by controlling hormone levels, control plant growth until a floral bud initiates and begins rapid growth. It is not apparent when the maturity genes cease to function, but it is obvious that a second genetic control of growth begins to function as soon as the developing inflorescence becomes large enough to synthesize appreciable amounts of auxin. The genes that begin to function then have been recognized as height genes.

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V.

Genetics and Physiology of Cell Elongation

A.

GENETICSOF HEIGHT

Dwarfing genes have been useful in sorghum because they favor me-. chanical harvesting and reduce lodging. Four, nonlinked, brachytic dwarfing genes are known (Quinby and Karper, 1954). Tallness is partially dominant to shortness. Five height classes have been recognized. The tall or zero-dwarf class may grow to be as tall as 3 or 4 m and 4-dwarf plants may be as short as 1 m. Plants of the same height genotype may differ in height by as much as 10 to 50 cm, and these differences are thought to be due to allelic series at the four height loci (Quinby and Schertz, 1970). A dwarfing gene may reduce height by as much as 50 cm or more but the reduction is less if there are dwarfing genes at other height loci. Differences between the height of 3-dwarf and 4-dwarf genotypes may be as little as 10 or 15 cm. The first maturity gene ma, is linked to the second height locus dw, but crossovers occur (Quinby and Karper, 1945). All height genotypes occur in all maturity genotypes and it is assumed that the height genes and maturity genes are at different loci. However, each dwarfing gene might be linked to one of the maturity genes, but the possible linkage between them has not yet been established.

B. PHYSIOLOGY OF CELL ELONGATION The usual sites of hormone production in vascular plants are meristems and enlarging tissues (Leopold, 1964). It is reasonable to assume, therefore, that the developing inflorescence and expanding leaves synthesize auxin and that the exposed leaves also synthesize gibberellin. The presence of a floral, rather than a vegetative, bud has profound effects. Soon after a floral bud is initiated, the grand period of growth begins, internode elongation accelerates, tillering is suppressed, and the inflorescence begins rapid growth. It seems likely that the maturity genes continue to control synthesis of auxin and gibberellin in the leaves as long as they are growing. A leaf blade is almost fully expanded by the time the ligule can be seen due to the elongation of the internode below the node of leaf sheath attachment. After all the leaves are fully grown and exposed a few days before the head is in the boot, the leaves appear to no longer be the major site of hormone synthesis. The expanding inflorescence then becomes the major site of hormone synthesis and the height genes appear to be in control of hormone synthesis. The reduction of cell elongation in the internodes of short-statured

GENETIC CONTROL OF FLOWERING AND GROWTH IN SORGHUM

133

plants probably results from inhibition to cell elongation due to an excess of auxin and too little gibberellin. During the period from floral initiation until emergence from the boot, the developing panicle is protected from sunlight and the phytochrome in the panicle should be in the Pfjo0form. If this is true, the developing panicle, in the absence of Pi,,, should synthesize auxin during the day as well as during the night, the amount depending on the height genotype. However, developing panicles of all genotypes should synthesize little or no gibberellin because of inhibition by P,,,. The upper, expanding leaves, however, should synthesize both auxin and gibberellin. The height genes are assumcd to control levels of auxin and gibberellin, and it is reasonable to assume that inhibition by PTs0and P,,, is the mechanism involved. The hormone levels that are assumed to result from dominant and recessive alleles at the four height loci are shown in Table 11. Alleles at height gene loci 1 and 2 are assumed to control levels of auxin and alleles at loci 3 and 4 to control levels of gibberellin. Four dominant genes for height result in a low level of auxin and a high level of gibberellin. For this reason, even though both maturity and height genes control hormone levels, different functions must be assigned to the height genes at loci 3 and 4 as compared to the maturity genes at loci 3 and 4. Apparently, dominants Mu, and Ma, result in a low level of gibberellin and dominants Dw3 and Dw, in a high level of gibberellin. Schertz et al. (1971) concluded that the dw, height locus in sorghum may regulate the expressed level of peroxidase activity. There is no agreement about the function of peroxidase in plants at present but peroxidase is generally thought to be involved in interactions with gibberellin or auxin. How peroxidase may be involved in the control of plant growth is not apparent. Several brachytic dwarfing genes exist in Zea mays L. and applications of gibberellin in microgram amounts to plants of five of them result in plants of tall height (Phinney, 1961). The probable explanation of this response to gibberellin application in corn is that short plants contain too much auxin for normal cell elongation unless some gibberellin is added. This is the same response recognized in the early floral initiation in sorghum that results from the presence of recessive and greater synthesis of gibberellin. Presumably, any sorghum genotype that is high in auxin content or is low in gibberellin content would grow taller if gibberellin were applied at the proper time and at appropriate concentrations.

C. HEIGHTGENESAND LEAFSIZE Schertz (1973) has compared leaves of a doubled haploid of 4-dwarf SA403 with leaves of a 3-dwarf obtained from a tall mutation of the same

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TABLE I1 Assumed Hormone Level and Height Genotype of Certain Sorghum Cultivars” Homozygous height genotype and hormone level

Cultivar

Zero-dwarf or tall None identified One-dwarf TALLWHITE SOONER MILO DwiDwnDwadwr a a G g STANDARD BROOMCORN DwlDwzdwaDw4 a a g G None identified DwldwzDwaD~r a A G G None identified ~w~Dw~Dw~Dw~ A a G G Two-dwarf TEXAS BLACKHULL KAFIR Dw1Dwzdwadwr a a g g HEGARI DwidwzDwsdwc a A G g DWARFYELLOW MILO dw1Dw2Dwadwa A a G g ACME BROOMCORN DwldwzdwsDwr a A g G JAPANESE DWARF BROONCORN ~w~Dw~~w~DwI A a g G None identified dwidwaDwsDwc A A G G Three-dwarf None identified COMBINEK A F I R - ~ O 60M

MILO

None identified Four-dwarf SA40S

“A” indicates high, and “a” low, auxin level. “G” indicates high, and “g” low, gibberellin level.

a

strain. His results, and those of others cited in his paper, indicate that the taller plants had longer leaf blades and longer leaf sheaths than the shorter plants. The gene involved in all these studies was dw,.

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135

Quinby (1961) compared leaves of 1- and 2-dwarf MILO plants and leaves of 2- and 3-dwarf MILO plants. In these cases, the comparisons were between the effects of recessive dw, and dominant Dwl, and between recessive dw, and dominant D w p . Leaf sizes of the different height genotypes were not significantly different. In view of the fact that the dw, is involved in the synthesis of gibberellin and dw, and dw, with the synthesis of auxin, it might be expected that recessive dw, might have a different effect on leaf size than recessive dw, and dw,. Recessive dw, results in less gibberellin than dominant Dw,, but recessives dw, and dw, result in more auxin than dominants Dwl and Dw2.

D. HEIGHTAND PEDUNCLE LENGTH Plants of 4-dwarf and 3-dwarf height appear to have peduncles as long as taller genotypes. The published information on the subject of peduncle length is inconsistent as reported by Schertz (1973), but it is apparent that the shorter genotypes sometimes have longer peduncles than taller genotypes and that there is not a consistent relationship between tall plants and long peduncles. The long peduncle lengths of plants with short internodes could result from the fact that peduncle elongation occurs after the panicle is no longer synthesizing large amounts of auxin, but could, also, result from the production of gibberellin in the still-enlarging panicle during daylight after the panicle had emerged from the boot. Furthermore, any auxin that might be produced in the upper leaves would not inhibit cell elongation in the peduncle because auxin is reported to move in plants in polar fashion (Leopold, 1964). Conversely, gibberellin produced in the leaves could promote cell elongation in the peduncle because the movement of gibberellin in the plant may be either up or down.

E. HEIGHTAND MATURITY GENESAND

PANICLE

SIZE

The published information on the relationship of plant height and panicle length is inconsistent (Schertz, 1973). Panicle weight (head weight less grain weight) of SM60 ( malma,ma3Ma,) was found to be greater than that of SM80 (ma,ma,Ma,Ma,) (Quinby, 1972aj, and the inference is that a higher level of gibberellin in SM60 caused greater growth of the panicle in SM60. The heads of SMlOO (rna,Ma,Ma,Ma,) and SM80 (malma~Mu,Ma,)are noticeably more compact than heads of SM60 (malma,ma3Ma,) and SM90 (ma,Ma,ma,Ma,). The inference is that lower levels of gibberellin in SMlOO and SM80 cause less elongation of the rachis and rachilla in these two genotypes.

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J. R. QUINBY

F. TYPESOF INTERNODE DISTRIBUTION Three types of internode distribution, associated with early, medium, and late maturity, were recognized in sorghum in India (Ayyangar et al., 1938), and were called ever-increasing, unimodal, and bimodal. These three types of internode distribution occur in sorghum from June plantings at Chillicothe, Texas (Quinby and Karper, 1945), and Ryer MILO (Malma2ma2RMa4) is ever-increasing, 60M (Mama2ma,Ma,) is unimodal, and lOOM MILO (Ma,Ma,Ma,Ma,) is bimodal. In the ever-increasing type, the internodes are longer from the ground upward. In the unimodal type, internode eight, near the base of the culm, is shorter than the internodes above and below it. In the bimodal type, an internode near the base and another near the top of the culm are shorter than internodes above and below them. A graph presented by Ayyanger et al. (1938) shows that ever-increasing plants have long peduncles. The physiological reason for the short internodes in unimodal and bimodal plants is not obvious. However, early flowering plants that must have high gibberellin content in comparison to auxin content to allow early floral initiation are ever-increasing in internode distribution. The inference is that ever-increasing internode distribution is associated with high gibberellin content and that the short internodes that appear in unimodal and bimodal plants are, in some way, associated with temporary high auxin content. The short internode near the base elongates about the time a floral bud is initiated and the short internode near the top, at the time the panicle is large and still growing. A little later, the panicle begins to emerge from the boot, or upper leaf sheath, and the elongation of the upper internodes and peduncle is probably being influenced by the gibberellin being produced by the panicle that has emerged into the sunlight. VI.

Influence of Photoperiod, Temperature, and l e a f Area on Flowering

A.

PHOTOPERIOD

Miller et al. (1968a) grew 22 tropical and temperate varieties from the world collection in monthly plantings throughout the year in Puerto Rico. Part of their data was presented in different form by Quinby ( 1 9 7 2 ~ ) . These data are the basis of the discussion that follows. PI276769 is a late-maturing variety from Ethiopia that is planted there in the spring and is harvested in January. This variety did not flower in Puerto Rico until November when planted in any month from January to August. Apparently, floral initiation took place in October when the nights were about 12.2 hours long. PI291 227, a rabi (winter-growing)

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variety from India, flowered in October in Puerto Rico when planted in any month from March to August, Apparently, floral initiation took place when the nights were about 11.8 hours long. TEXASBLACKHULL KAFIR is a temperate variety that was grown extensively in the southern Great Plains fifty years ago. This variety was not delayed greatly in flowering in any planting, even when the nights were shorter than 11 hours. Presumably, plants of PI276769 are so sensitive to inhibition by P7,, that they produce little or no auxin during the day, and nights as long as 12.2 hours are needed for plants to synthesize sufficient auxin to allow floral initiation. PI291227 apparently has a critical dark period about 0.4 hour shorter than PI276769. Presumably, PI291 227 is slightly less sensitive to inhibition by Piy,,, and plants of this variety produced enough auxin during the day, to supplement that produced during the night, to substitute for the amount of auxin that could be produced in 24 minutes of divkness during the period of floral induction. Presumably, plants of the temperate variety TEXAS BLACKHULL KAFIR are so insensitive to inhibition by P;,,, that they produce enough auxin during the day, to supplement that produced during the night, to allow floral initiation regardless of the length of the night. Miller et al. (1968a) divided the varieties they grew into five classes depending on the day lengths required to delay floral initiation. The data show that tropical varieties of different maturities have different critical dark periods and that tropical varieties need longer nights to allow floral initiation than temperate varieties. Temperate varieties, many of which will flower in continuous light, have no critical dark periods but differ in the length of night that will delay floral initiation. All this information leads to the conclusion that the photoperiodic effect is apparent only if the nights are too short to allow the synthesis of sufficient auxin to allow early floral initiation.

B.

TEMPERATURE

Some information on the influence of temperature on the physiology of flowering has accumulated, but how temperature affects time of floral initiation is still not obvious. Lower temperatures have been observed to hasten flowering in some varieties but to delay it in others (Quinby, 1967). Hesketh et al. (1969) and Downes (1972) found that different temperatures caused a change in leaf numbers in a phytotron. Caddel and Weibel (1971) found that the effect of night temperature on photoperiodic response depended upon the day temperature as well as on the variety and that day temperatures were more important in determining length of panicle development than in the time needed to reach floral initiation. Quinby et al. (1973) found that alleles at all four maturity loci caused

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differences in response to temperature and that no two varieties responded to differences in temperature in the same way. Also, varieties produced more leaves at either high or low temperatures than at intermediate temperatures. If the mechanism of control of hormone levels that has been assumed is correct, gibberellin would be synthesized largely during daylight and auxin largely during darkness. Presumably, temperatures during the day would affect synthesis of gibberellin more than synthesis of auxin. Conversely, night temperatures would affect synthesis of auxin more than synthesis of gibberellin. That some varieties are hastened in floral initiation by cool night temperatures while others are delayed could result from the fact that some varieties, because of genotype, need more (or less) auxin and some, more gibberellin for early floral initiation. If this is true, the temperature effect could be the influence of temperature on the rate of chemical reaction and nothing else. However, nothing is understood about the nature of sensitivity to inhibition by phytochrome, and temperature might have an influence on sensitivity. Hendricks and Borthwick ( 1963) have reported that the reversion of PT3,, to P,,, in darkness is hastened by increase of temperature. As mentioned in Section VI, A, a difference in critical dark period of 24 minutes can cause a difference of a month in time of flowering. For this reason, an increase in temperature could influence time of floral initiation by lengthening the period of time during darkness when phytochrome is in the P660 rather than in the P730form. The fact that sorghum plants continued to initiate leaves at temperatures too high or too low to allow early floral initiation seems to indicate that homone levels that allow cell division are not as precise as the levels that allow floral initiation (Quinby et al., 1973). The data of Miller et al. (1968a), as presented by Quinby (1972c), show that both tropical and temperate varieties initiate floral buds at slightly different lengths of night in the different monthly plantings. It is presumed that these differences are caused by the differences in temperature that occurred from month to month. The influence of temperature apparently varies enough from variety to variety to cause parents that will flower together in one planting to flower several days apart in another planting even though the nights differ in length by only a few minutes during the periods of induction.

C . LEAFAREA The 60M, 80M, 90M, and lOOM maturity genotypes initiate floral buds later than four earlier flowering genotypes of MILO in the short nights of

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the summer in Texas and have more leaves at time of floral initiation (Quinby, 1972). Genotype 60M initiated a floral bud two days later than the four earlier genotypes and had nine leaves fully exposed, rather than eight, at the time. Leaf nine of 60M was almost twice as large as leaves eight of the earlier flowering genotypes. The total exposed leaf area of 60M at time of floral initiation was almost twice that of the earlier genotypes. Genotype 80M had a leaf area more than four times greater than that of SM100, SM90, SM60, and SM80; and 90M and lOOM had leaf areas almost 15 times as great as these four genotypes at time of floral initiation. The different leaf areas of the various maturity genotypes could indicate that the leaves of the later-maturing genotypes, that are sensitive to inhibition by phytochrome, produced less of the floral stimulus per unit area; and thus needed larger leaf areas to synthesize sufficient amounts of the floral stimulus to induce floral initiation. Quinby (1967) considered sorghum to have a disadvantage as an experimental subject because of the 8 or 10 long nights needed to induce floral initiation. This conclusion was based on the finding of Keulemans (1959), who reported that the juvenile stage in sorghum is 3 weeks and that 10 to 14 long nights were needed to induce floral initiation. Lane (1963), working with four MILO maturity genotypes, found that 12 consecutive 14-hour nights were needed to induce floral initiation if the longnight treatment began when the plants were 7 days old. Caddel and Weibel (1972) found that five long nights were sufficient to induce floral initiation after plants of three sorghum cultivars were 15 days of age. It is realized now that the longer periods of induction assumed by Keulemans and Lane included several days when the small plants did not have leaf areas large enough to synthesize appreciable floral stimulus. Presumably, genotypes that are early flowering and relatively insensitive to inhibition by phytochrome need smaller leaf areas to synthesize sufficient floral stimulus to induce floral initiation than more sensitive genotypes. If this is true, a genotype relatively insensitive to inhibition by phytochrome would begin synthesis of hormones earliei and at a more rapid rate than more sensitive genotypes. The result would be differences in time of floral initiation like those shown in Table I. Plants of a homozygous variety growing in a row may begin to flower over a period as long as 10 or 12 days (Quinby, 1967; Miller et al., 1968b). These extreme differences in time of flowering of plants of the same maturity genotype are probably caused by differences in leaf area among plants. Plants that emerge a day early or are favorably located are larger and intiate floral buds earlier than others. Plants that are disadvantaged are smaller and may lay down two or three more leaves before floral initiation than the larger plants in the row. The assumption is that the

J. R. QUINBY

140

disadvantaged plants need more exposed leaves to have sufficient leaf area to synthesize enough of the floral stimulus to allow initiation. The literature, that has been reviewed by Salisbury (1963), indicates that plants must reach a certain age or a certain size before their leaves will be sensitive to the environment that promotes the production of the floral stimulus. But, if maturity genes of sorghum control hormone levels, it would not be necessary to assume a juvenile or “ripeness to flower” stage because, in young plants, small leaf area rather than insensitivity to inductive environments would inhibit floral initiation. VII.

Influence of Maturity Genotype on Plant Growth and Adaptation

A. INFLUENCE ON PLANTGROWTH If the floral stimulus consists of auxin and gibberellin, and the maturity genes control levels of the two hormones, it would be inconceivable that the maturity genes would not affect rate of growth and development during the vegetative period prior to floral initiation. Evans (1969) has reviewed the literature on the multiple effects of the photoperodic stimulus and has listed flower development, sex expression, .growth rate, cambial activity, leaf shape, dormancy, senescence, and tuberization as being some of the many plant responses to day-length control. In sorghum, data have been interpreted to mean that a hormone level that causes early floral initiation inhibits growth of the meristem and leaves (Quinby, 1972). Likewise, a hormone level that delays floral initiation promotes growth of the meristem and leaves. This difference in response to hormone level between organs might be expected. Thimann (1937) found that different organs of a plant have different optimun concentrations of auxin that promote growth.

B.

ADAPTATION TO CLIMATE

Nitsch (1963) surmised that climatic conditions cause changes in the balance of endogenous growth factors, and suggested that neither photosynthesis nor mineral nutrition is crucial in the control of the course of plant development. He recognized that a regulatory system played a key role and that the reception of the climatic stimulus could involve phytochrome. Alleles at maturity gene loci control auxin and gibberellin levels and the synthesis of the two hormones is influenced by both photoperiod and temperature is discussed in Section VI. For that reason, adaptation, or lack of it, appears to depend on maturity genotype.

GENETIC CONTROL OF FLOWERING AND GROWTH IN SORGHUM

VIII.

141

Morphological Effects of Hybrid Vigor in Sorghum

If yield of grain and stover is the measure of performance, hybrid vigor necessarily must show in differences in morphology between parents and hybrids. Differences in morphology between the two might indicate what kinds of genes are involved in hybrid vigor. An interpretation of the sorghum literature that might indicate where hybrid vigor is and is not influencing plant growth and development follows.

A.

NUMBEROF SEEDS PER HEAD,AND GRAINAND STOVERYIELD

PANICLE SIZE,

Data presented by Quinby (1970) show that the weight of the panicle (head less grain) is greater in hybrids than in parents even though the panicles of hybrids develop in less time. Liang (1967) found that panicles of hybrids were larger (length x width) than those of the larger parent. Patanothai and Atkins ( 1971) have presented graphs that show that the weight of the fruiting body of hybrids, before kernel development, was greater than that of parents. It appears that panicles of hybrids grow to be larger than those of parents, and in less time. Increased grain yield is one universally recognized manifestation of hybrid vigor (Stephens and Quinby, 1952; Argikar and Chavan, 1957; Quinby et al., 1958; Arnon and Blum, 1962; Quinby, 1963; Niehaus and Pickett, 1966; Kambal and Webster, 1966; Chiang and Smith, 1967; Beil and Atkins, 1967; Liang, 1967; Kirby and Atkins, 1968; Nagur and Murthy, 1970; Patanothai and Atkins, 1971). A greater number of seeds per plant has been recognized as a most important component that contributes to greater grain yield of hybrids (Argikar and Chavan, 1957; Arnon and Blum, 1962; Quinby, 1963; Kambal and Webster, 1966; Beil and Atkins, 1967; Kirby and Atkins, 1968; Ali-Khan and Weibel, 1969; Blum, 1970); but Patanothai and Atkins (1971 ) have presented data that show that hybrids do not always have more seeds per plant than one parent. Quinby (1963) found that RS610, a widely grown hybrid, produced 82% more grain than the average of its parents but produced only 31% more stover. Graphs presented by Patanothai and Atkins (1971) show much greater differences between hybrids and parents in head weight than in stover weight. These differences in grain and stover production, due to hybrid vigor, are probably explained by the fact that growth is exponential and that the limit of stover production is determined in the first onethird of the life cycle and the limit of grain production in the second onethird of the life cycle.

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J. R. QUINBY

B. LEAFBLADESIZE Leaf blades of hybrids are larger than comparable leaf blades of parents, from the first embryonic leaf upward until maximum leaf size is reached in hybrids (Quinby, 1970). Above that point, leaf blades of hybrids are sometimes smaller than those of parents and, because some hybrids have fewer leaves than parents, the largest leaf blade on a hybrid may be smaller than the largest leaf blade of a parent. The smaller upper leaves of hybrids has the following logical explanation. Leaves of grasses are larger from the ground upward until a maximum is reached; above which the leaf blades become progressively smaller. Borrill (1959) attributed the smaller upper leaves of grasses to the onset of floral initiation in the shoot apex and to less cell extension in the upper leaves. Data presented by Quinby (1970) can be interpreted to mean that the inhibiting influence of the developing terminal inflorescence on size of the meristem from which the upper leaves originate is greater in hybrids than in patients. The largest leaf of the hybrids, in his study, was the fourth or fifth from the top and, of the parents, the third from the top. The upper leaves of hybrids may not only be smaller but the inhibiting influence appears earlier in hybrids. Argikar and Chavan (1957), Quinby (1963), and Liang (1967) measured either the third or fourth leaf blade from the top of the plant and found that these leaf blades of hybrids were larger than those of parents. The data mentioned in the previous paragraph show that comparisons between either third or fourth leaves from the top of parents and hybrids are not exactly valid, but it is apparent that leaves of hybrids are larger than comparable leaves of parents except for the two or three upper leaves whose growth is inhibited by the developing inflorescence. Because of the smaller upper leaves of hybrids, some hybrids have smaller leaf blade areas during the period of grain development than parents (Quinby, 1970). Stickler and Pauli (1961a) reported that all leaves of a sorghum plant that were alive during the period of seed development contributed to grain yield. Nevertheless, in a second paper, Stickler and Pauli (1961b) presented data that showed that leaf sheaths contributed to grain yield if the leaf blades had been removed but contributed nothing if the leaf blades were intact. In view of the fact that sorghum has photosynthetic areas, other than the leaves, such as the developing seeds, glumes, peduncle, etc., and because sorghum plants make little use of leaf sheaths in photosynthesis, it appears that the photosynthetic areas of either parent or hybrid sorghum plants are adequate. Apparently, greater leaf blade area of hybrids is not a major cause of greater grain yield.

GENETIC CONTROL OF FLOWERING AND GROWTH IN SORGHUM

C.

143

PLANTHEIGHT

Quinby and Karper (1954) reported that some sorghum varieties are taller or shorter than expected in view of their height genotypes and attributed the tallness or shortness to a modifying complex. It is realized now that allelic series at the four known height gene loci could also account for the unexpected tallness or shortness. Most presented grown hybrids are 3-dwarfs and are recessive at the same three loci, but there is considerable difference in height among them just as there is among parents. Grain hybrids are usually taller than the average of their parents (Quinby e t a ! . , 1958; Arnon and Blum, 1962; Quinby, 1963; Kambal and Webster, 1966; Liang, 1967; Kirby and Atkins, 1968; Patanothai and Atkins, 1971) as are forage hybrids (Chavda and Drolsom, 1970); and tall height has been reported to be a manifestation of hybrid vigor. Plant height is made up of the length of the internodes that make up the stem, the length of the peduncle, and the length of the head. Kambal and Webster (1966) reported the length of each component, and all were longer in hybrids. The length of the stem depends on the amount of cell elongation as well as on number of internodes, and hybrid vigor appears to increase cell elongation.

D. TILLERING The amount of tillering in sorghum, as in other species, is determined by the effectiveness of apical dominance. The inhibiting influence of apical dominance on axillary bud development is known to be hormonal. The amount of tillering varies in both parents and hybrids and much or little tillering is not unique to either. Karper and Quinby (1937), Quinby and Karper (1946), and Quinby (1963) concluded that greater tillering is a manifestation of hybrid vigor in sorghum. However, Kambal and Webster (1966) and Beil and Atkins (1967) found little difference in amount of tillering between parents and hybrids, and Chiang and Smith (1967) found that, on the average, hybrids had fewer tillers than parents. The data do not show conclusively that greater tillering is a manifestation of hybrid vigor.

E.

LEAF A N D INTERNODE NUMBER

Argikar and Chavan (1957) found no consistent difference and Niehaus and Pickett (1966), and Liang (1967), and Quinby and Liang (1969) found little difference between parents and hybrids in leaf number. Apparently, hybrid vigor does not increase leaf number.

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J . R. QUINBY

F. EARLYFLOWERING A sorghum plant continues to produce leaves in the meristem until a floral bud is initiated, and the production of an additional leaf delays flowering by about 3 days (Sieglinger, 1936). Quinby (1967), without showing leaf numbers, presented data that show that hybrids flowered, on the average, 3 or 4 days earlier than the average of parents. Liang (1967), and Quinby and Liang (1969) presented data that show that, on the averaage, parents and hybrids had the same leaf number but that hybrids flowered earlier. than parents. The shorter period from planting to flowering in hybrids was shown by Quinby and Liang (1969) to be made up of a 1.2-day shorter period from planting to floral initiation and a 2.6-day shorter period of panicle development. Niehaus and Pickett (1966) and Chiang and Smith (1967) have reported late flowering rather than early flowering to be a heterotic effect in sorghum but their diallel studies included parents that produced late hybrids due to complementary action of maturity genes. Early flowering of hybrids is usually not caused by lower leaf number; but lower leaf number would cause earliness if it occurred. Early flowering of hybrids is caused by more rapid development of the meristem prior to floral initiation and by more rapid development of the panicle. A difference in rate of growth in favor of hybrids is probably involved in early flowering because the meristems of hybrids become larger than those of parents in a shorter time; and earliness could result without hybrids having fewer leaves than parents. G . SIZE

OF

ROOT SYSTEM

Measurements of root growth of a sorghum hybrid and its two parents were made by McClure and Harvey (1962) using radiophosphorus. A difference in root growth in favor of the hybrid did not exist until after heading. At the time of heading, the roots of parents occupied more soil volume than those of the hybrid. A week later at time of flowering and at maturity, the hybrid root system was more extensive than that of parents because only the hybrid continued to expand its root system after heading. The lesser root growth of hybrids during early stages of growth when above ground parts were growing rapidly might be expected because auxin concentrations that promote stem growth are known to suppress root growth (Thimann, 1937). The reason for the cessation of root growth after heading in parents and the continuation of root growth after heading in hybrids is not obvious and is not apparent in the literature.

GENETIC CONTROL OF FLOWERING AND GROWTH IN SORGHUM

H.

SEED SIZE

AND

TESTWEIGHT

PER

145

BUSHEL

Seeds produced by sorghum hybrids are frequently heavier than the average seed weight of parents (Niehaus and Pickett, 1966; Kambal and Webster, 1966; Chiang and Smith, 1967) but Beil and Atkins (1967) and Kirby and Atkins (1968) found seeds of parents of hybrids not to differ significantly in seed weight. Liang (1967) found that seeds of some hybrids were not significantly heavier than those of the heavier parents but seed of hybrids were significantly above mid-parental values. Whenever mean values of parents and hybrids were presented (Argikar and Chavan, 1957; Quinby, 1963; Liang, 1967), the data show that seeds of hybrids were usually between those of parents in weight but that seeds of hybrids were sometimes lighter and sometimes heavier than those of parents. It is apparent that larger seed size is not a consistent difference between parents and hybrids. Quinby et al. (1958) found that hybrids produced seeds whose average test weight per bushel was 0.6 pound above the average of the heavier parents. Kambal and Webster (1966) found that, on the average, hybrids produced grain that was slightly higher in test weight per bushel than parents. However, 10 hybrids were below the lowest parent in test weight, and 53 hybrids were below the mid-parental value in test weight. Apparently, hybrids do not consistently have seeds of greater test weight than parents. The influence of hybrid vigor on test weight per bushel is in doubt.

I.

SEEDSIZE AND GRAINFILLINGPERIOD

The length of the grain filling period of parents and hybrids was determined by Quinby (1972b), and he cited some earlier reports. He found that final kernel weights of male parents were above those of hybrids but that differences in age of kernels when parents and hybrids reached maximum kernel weight were not significantly different. Hybrid vigor appeared not to lengthen the period of starch accumulation in the endosperm. J.

PROTEINCONTENTOF SEED

Arnon and Blum (1962) determined the protein content of the seeds of the variety MARTIN and several hybrids and, although their results were not consistent, reported that seeds of hybrids usually had a lower protein content than the seeds of MARTIN. Kambal and Webster (1966) and Liang (1967) found that seeds of hybrids were lower in protein content than the average of parents. Collins and Pickett (1972), in a diallel study involving four female, eight male, and the 48 hybrids made from them, found

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J. R. QUINBY

that only four hybrids contained a higher percentage of protein than parents and no hybrid was superior to either parent in percentage of lysine. Apparently, hybrids usually have seeds that contain slightly less protein, on a percentage basis, than parents and it is obvious that hybrid vigor does not increase percent protein in sorghum seed.

K.

SUMMARY OF

MORPHOLOGICAL EFFECTS OF HYBRID VIGOR

Hybrids produce more grain and stover than parents. Hybrid plants become taller and hybrid panicles larger than those of parents in less time. Early flowering of hybrids is caused by a shorter period of growth prior to floral initiation and a shorter period of panicle development rather than by a difference in leaf number between parents and hybrids. Root growth prior to heading is greater in parents than in hybrids but the above ground growth of hybrids is greater. The fact that hybrid vigor shows more in grain than in stover yield is attributed to the fact that hybrids grow faster than parents and because growth is exponential. Processes that do not involve rate of cell division, like the deposition of starch or the accumulation of protein in the endosperm, show little effect due to hybrid vigor. Hybrid vigor appeared not to lengthen the period of starch accumulation in the endosperm. All the information on plant morphology of parents and hybrids seems to indicate that any character that is affected by rate of growth will be different in parents and hybrids. It seems logical to assume that hormone levels in parents and hybrids must be different.

IX.

Genetic Control of Hybrid Vigor in Sorghum

Gregor Mendel (1 865) observed hybrid vigor in an F, hybrid of tall and dwarf peas and called the phenomenon luxuriance. Fifty years ago, geneticists working with Zea mays L. could not reconcile the stimulation of hybrid vigor with genetic principles and, for that reason, assumed that heterozygosity could not account for hybrid vigor. More important to this discussion, they also assumed that the reduced growth of inbreds was due to small deficiencies in metabolism and that recessive alleles at numerous gene loci were involved. The possibility that plant hormones, rather than metabolic deficiencies, might be responsible for differences in plant growth has largely been ignored by plant breeders; and this is true in spite of the fact that varieties of self-pollinated crops such as sorghum are not adversely affected by inbreeding. This lack of interest in the hormonal control of plant growth

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147

has been due to the fact that no mechanism to control hormone levels had been recognized. If such a mechanism has now been recognized, there is reason to revise some of the theories that are the basis of practices in plant breeding. The theory that varieties of self-pollinated crops such as sorghum are burdened with numerous, small metabolic deficiencies is now untenable. Hageman et al. (1967) has postulated that hybrids are superior to parents in having better balanced metabolic systems. They suggested that the fundamental metabolic systems involved in growth and yield needed to be recognized and, particularly, the optimum levels of activity of each enzyme. The idea that the genetic control over growth is hormonal is probably not in conflict with their concept and they have recognized that “a single enzyme, hormone, vitamin, or growth factor could be solely responsible for the enhanced growth of a hybrid.” Nevertheless, they have stated that “the complexities of metabolism preclude a single factor from being the universal underlying cause of hybrid vigor.”

A. EFFECT OF HETEROZYGOSITY AT MATURITY LOCI Data in Table I11 (Quinby and Karper, 1946) show that plants heterozygous at locus 1 when locus 2 is homozygous recessive were later to flower than either homozygous genotype. But when locus 2 was homozygous dominant, the genotype heterozygous at locus 1 was earlier to flower than the later homozygous genotype. The heterozygous genotype Malmalma2ma, was much later to flower than either homozygous genotype and produced a much greater yield of heads. However, the difference in duration of growth between genotypes was great and the influence of duration of growth and of hybrid vigor cannot be separated. However, the heterozygous genotype Ma,maIMa,Ma, was only 3 days earlier to flower than the homozygous genotype MalMalMa,Ma, but produced a yield of heads 60% greater due largely to more heads per plant. Heterozygous genotypes for maturity were different from homozygous genotypes in both maturity and yield of heads and heterozygosity was important largely because of interaction among genes at different loci rather than between alleles within a heterozygous locus. Differences, due to gene interaction, between pairs of hybrids that differ only in being homozygous or heterozygous at one locus are shown in Table IV. These data were presented previously (Quinby and Karper, 1948), but, at that time, the maturity genotypes of most of the parents were not known. Now that the maturity genotypes are known, it is possible to draw conclusions regarding the genetic cause of hybrid vigor that could not be drawn in 1948.

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J. R. QUINBY

TABLE 111 Effect of Heterozygosity at the ma1 Locus on Days to Flower and Yield of Heads ‘ , b

Class

Genotype

Days to flower

Head weight per plant (g)

Planted Sune 20, 1944 Homozygous (SM60) Difference Heterozygous Difference Homozygous (60M)

ma,malma?ma~maamaa Ma4Mac

51 32** 13** 70

94 55** 149 19** 130

50 43** 93 3* 96

91 149** 240 90 * 150

83

Ma1 Malmazmazrnaama3Ma4 Mac Planted June 9, 1942

Homozygous (SM90) Difference Heterozygous Difference Homozygous (9OM)

malmalMa~Ma~ma3maaMa,Ma4 M a l m a lMazMazma3maaM a rM a 4 Ma1MalMa?Mazma3maaM a 4 M a 4

Data from Quinby and Kaper (1946). Plant populations were grown at Chillicothe, Texas.

It is assumed that the paired varieties listed in Table IV differ only in the genes controlling maturity. Many plant breeders or geneticists, including Schuler (1954), are skeptical that two varieties could differ only at one or two gene loci. Such skepticism is difficult to allay because the skepticism originates in the misconception that so-called quantitative characters are, necessarily, complex in inheritance. Part of the data from the 1948 paper are presented again in Table IV with the yield figures converted to grams. Only the data from pairs of hybrids that differ in one allele are presented. Quinby (1967) has presented evidence that multiple allelic series exist at the maturity loci; but, because the information has no bearing on the point under discussion, the multiple allelic designations are not shown. Heterozygous Masmas in the HEGARI x TEXAS MILO hybrid as compared to homozygous recessive ma3ma3in the EARLY HEGARI X TEXAS MILO hybrid resulted in little difference in days to flower but in a large difference in grain yield. The same was true in the HEGARI x SOONER MILO and EARLY HEGARI X SOONER MILO hybrids. Heterozygous Masmas as compared to homozygous dominant Ma,Ma, in TEXAS BLACKHULL KAFIR x EARLY HEGARI and TEXAS BLACKHULL KAFIR x HEGARI pair of hybrids resulted in earlier flowering and greater grain yield. TEXAS

TABLE IV Maturity Genotype, Days to Flower, and Grain Yield of Parents and Hybridso.b

Variety or hybrid

Days to flower

Genotype

Grain yield per plant (g)

% ' Higher

SOONER MILO T E X A S MILO

EARLYHEGARI HEGARI EARLYKALO KALO

HEGARI x

TEXAS MILO

EARLYHEGARI X HEG.AR1

x

TEXAS M I L O

n

S O O N E R MILO

EARLYHEGAHI

x SOONER

TEXAS BL.ACKHT-LL TEXAS BLACKHULL

KAFIR

TEXAS BLACKHULL TEXASB L A C K H U L L

KAFIR

KAFIR

KAFIR

MILO

x E A R L Y IIEGARI x HEGARI x KALO x E A R L Y K.4LO

E 3lalma1-lla2Ma?Ma3ma~M a4ma4 .Ifa ~ r n a ~ M a 2a2Ma3Ma3&1 M a4ma4

m a ~ m a ~ M a ~ m a da& f a ~a& M

a4

malma1M a2Ma2Af aaMa3Ma4Ma4

Data from Quinby and Karper (1948).

* Plant populations were grown at Chillicothe, Texas, in 1941. Significantly greater than yield of other member of pair at 0.01 level.

98 104

l?4c 94

3?

57 56

130c 96

37

1

z

3 CL

P W

150

J. R. QUINBY

BLACKHULL KAFIR x KALO and TEXAS BLACKHULL KAFIR x EARLY KALO hybrids are similar in maturity to the commercial hybrids in general use. Heterozygous Mu2mu,, in the former hybrid as compared to homozygous Mu2Mu2 in the latter caused a 37% increase in grain yield even though the days to flower of the two hybrids differed by only one day.

B.

EFFECTOF HETEROZYGOSITY AT O N E HEIGHT LOCUS

Graham and Lessman (1968) presented data at the 1968 meeting of the Crop Science Society that showed hybrid vigor due to heterozygosity at the dw, height locus in sorghum. This hybrid vigor was not the point of their presentation and the abstract contains no reference to the yield of the plants heterozygous for height. The 2-dwarf parent used in their crosses was TEXAS MILO and the 3-dwarf parent was CALIFORNIA 38 MILO. Both parents are Mulma2mu3Ma4for maturity but CALIFORNIA 38 MILO is recessive dw, whereas TEXAS MILO is dominant Dw,,for height. Because both are MILO varieties, they are in similar genetic backgrounds. The pertinent data are shown in Table V. Plants heterozygous Dwz dw? produced more grain than plants of either homozygous parent. TABLE V Effect of Heterozygosity at the diup Height Locus I N MII.Oa*h

Entry %dwarf X %dwarf, FI 2-dwarf X 3-dwarf, FI %-dwarfparent (dwIDw2!hJ3d21)4) 3-dwarf parent (dw~dwzDiuaDwa)

Gtain yield per plant (9) 241c 238" 228 197

Data from Graham and Lessman (1968). Plant populations were grown at Lafayette, Indiana, in 1963 and 1965. Significantly above either parent at 0.01 level. a

C. DISCUSSION OF EFFECTS OF HETEROZGOSITY The information presented leads to the conclusion that heterozygosity at one height or one maturity locus, due to interaction between loci or epistasis, results in greater grain yield; and this is true regardless of the dominant or recessive condition at the homozygous locus.

GENETIC CONTROL OF FLOWERING AND GROWTH I N SORGHUM

151

Assuming that maturity genes control hormone levels, it appears that heterozygous genotypes, due to gene interaction, produce levels of auxin and gibberellin that are different from the levels produced by homozygous genotypes. Some heterozygous combinations apparently produce levels of hormones more favorable to growth than any homozygous combination, but some heterozygous combinations would produce hormone levels more favorable than others. Quinby (1963) presented data from two high- and one low-yielding hybrid. Patanothai and Atkins ( 1971 ) presented growth curves from two hybrids showing medium and high heterosis, but a growth curve for the low heterosis hybrid was not shown because that hybrid was not significantly superior, in the characters measured, to midparental values.

X.

Sorgnum Genotypes as Experimental Subjects

Sorghum hybrids came into use in 1957 after a female parent was produced using cytoplasmic male-sterility (Stephens and Holland, 1954). Prior to that time, farmers grew true-breeding varieties. Plant breeders, for about 40 years, worked at producing improved varieties. Because farmers saved mutations and plant breeders were interested in genetics, the sorghum species now includes a number of varieties or genotypes that are useful experimental subjects. If the hypotheses presented here are taken seriously, they will need to be confirmed or refuted. Strains will be identified in this section that are in similar genetic backgrounds, but differ at only one or two loci that affect growth. Physiologists working on the flowering process have, for the most part, neglected to use varieties, and have thus been working without a check. A.

THEMILOMATURITYGENOTYPES

A tropical sorghum variety reached the United States in 1879 and was called “MILLO MAIZE” (Karper and Quinby, 1947). In spite of its tall height and late maturity, farmers grew the variety and by 1910 had selected earlier maturities and short statures from the original variety. All the varieties that originated in this way are MILOS and differ from one another only in maturity, height, or pericarp color. It was determined about 30 years ago that four mutations at maturity loci, two mutations at height loci, one mutation for pericarp color, and one mutation for Periconia rootrot resistance had been preserved (Quinby, 1967). In the process of studying the genetics of duration of growth, eight maturity genotypes were produced by selection from a cross between two va-

152

J . R. QUINBY

rieties of the genotypes Malmarrna3Ma, and malMa2Ma3Ma4.A linkage between height and maturity was broken and the resulting eight genotypes are all in the same genetic background and are recessive at three height loci. When the eight genotypes are grown in long nights, they flower at about the same time (Miller et al., 1968a); but in the short nights of temperate zones in the summer, they flower at different times as shown in Table I. Subsequently, a second mutation at the third maturity locus was found in a 3-dwarf MILO variety (Quinby and Karper, 1961) and named RYER MILO. The new variety was identified for maturity as being Malma2ma,RMa, and was given the designation of 4 4 M . 38M was then obtained as a segregation product out of a cross between 44M and SM60. The list of MILO maturity genotypes now includes the ten strains shown in Table I. B.

MATURITY GENOTYPES RECESSIVE AT LOCUS FOURFOR MATURITY

The only recessive known at locus 4 was identified in HEGARI. Because all the MILO maturity genotypes are dominant at locus 4, 4-recessive maturity genotypes in pure MILO could not be obtained. But several useful maturity genotypes using recesives from BLACKHULL KAFIR, MILO, and HEGARI have been produced. These genotypes are KMH-1 (Ma,ma,ma,ma, ), KMH-2 ( ma,mu,ma3ma,), MH-3 ( mulma2nza:,Rma4). C. PAIRSOF VARIETIES THAT DIFFER AT ONE MATURITY Locus Fourteen pairs of genotypes that differ at only one maturity locus exist .among the MILO maturity genotypes shown in Table I. In addition, KALO and EARLY KALO differ at locus 2; and HEGARI and EARLY HEGARI at lOCUS 3. The origins of KALO and EARLY KALO and of HEGARI and EARLY HEGARI have been presented previously (Quinby, 1967). Maturity loci 1 and 2 have been assumed here to control the synthesis of auxin and loci 3 and 4, the synthesis of gibberellin. These pairs of genotypes might be used to verify or refute these assumptions.

D. TEMPERATE AND TROPICAL PAIRSOF

VARIETIES

In an effort to make tropical germplasm readily available to plant breeders of sorghum in temperate zones, more than 100 tropical varieties have now been converted to temperate zone adaptation. Most tropical varieties are dominant at all four maturity loci and the conversion to temperate

GENETIC CONTROL OF FLOWERING AND GROWTH I N SORGHUM

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adaptation can be accomplished by substituting a recessive maturity allele for a dominant one. The process is to cross a short, temperate variety to the desirable tropical variety, to select short and early plants from the segregating population, and to backcross to the original tropical variety. The backcrossing is continued for four or five backcrosses or until the temperate, short-statured strain looks like the original tropical variety, except for being short, when grown in the winter in Puerto Rico or Jamaica. The Texas Agricultural Experiment Station and the U.S. Department of Agriculture have distributed 62 converted lines and have several hundred more in some stage of conversion. The Pioneer Hi-Bred Company also has numerous converted varieties. When selections are mzide from the segregating population of the last backcrosses, it is possible to select lines that are either dominant or recessive at the first maturity locus. The two lines will look alike in the tropics in the winter but will differ in time of flowering in temperate zones by 20 or 30 days. If any physiologist is interested in this kind of material, it would be possible, with a little advance notice, to obtain a number of temperate and tropical pairs of varieties. There are now converted varieties from low elevations in Nigeria and from extremely high elevations in Ethiopia, where lowland varieties will grow but not shed pollen. There are also varieties that are grown in the summer in India and others that are grown in the winter. These varieties should be ideal subject for certain studies of temperature effects.

E. HEIGHT GENOTYPES Three height genotypes exist in MILO, all of which are of the maturity genotype malMa2MaJMa4,The first is recessive at dw,; the second, at dwl and dw,; and the third at dwl, dwL, and dw,. In addition, a number of pairs of isogenic strains exist. The first member of each pair is a 3-dwarf of the genotype dw,Dw,dw,dw,. The second member of each pair arose as a tall mutation at locus 3 and has the genotype dw1Dw2Dw3dw4. Early HEGARI and HEGARI are both DwldwLDw3dw4for height but the former is unstable for height while the later is stable and produces no tall mutations. Early HEGARI is Ma,Ma,ma3ma, for maturity while HEGARI is MalMa2Majrna,.There is a possibility that recessive maj is, in some way, associated with the unstable condition at height locus dw, in EARLY HEGARI. Even though this might be due to an influence within a linkage group, the linkage can be broken because KARPER (1953) distributed HI-HEGARI, a forage hybrid of HEGARI maturity, that was selected from a cross between HEGARI and a tall-mutant strain from EARLY HEGARI. Because of the instability, presumably at dwr, 2-dwarf and 1-dwarf height genotypes exist in EARLY HEGARI.

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XI.

Summary and Discussion of Genetic Control of Growth in Sorghum

If the control of growth is as simple as suggested in this chapter, there is reason to wonder why the genetic control has been unrecognized for so long. One may wonder, also, why the identity of the flowering stimulus has remained so elusive. The inhibitory effect of high as well as low levels of auxin might explain the failure to hasten floral initiation with many species of plants. using applications of auxin to short-day plants growing in long days. These failures have caused physiologists to conclude that endogenous auxins do not play a central role in the process that leads to floral initiation. The fact that applications of gibberellin to many long-day plants growing in short days hastens floral initiation could indicate that an excess of auxin exists in such plants. In such a case, additional auxin would not be expected to hasten floral initiation. Short-day plants such as Xanthium, will initiate floral buds following exposure to one long night and must need only a little auxin to allow floral initiation. Such plants under short-night treatment should not contain too much auxin; nevertheless, they do not respond to applications of auxin. Perhaps the auxin level that promotes floral initiation in such plants is so low that applications of auxin result in auxin levels high enough to inhibit rather than promote floral initiation. The inhibition of both high and low levels of auxin could explain why the floral stimulus was not recognized long ago. For 50 years plant breeders have been taught that inbred lines are burdened with numerous cryptic, recessive, deleterious genes. Assuming that such deleterious genes prevent normal growth, how could the control of growth be simple genetically? The notion about the complexity of the genetic control of plant growth spawned the development of the disciplines of population and quantitative genetics. The interest in population genetics diverted attention away from the obvious fact that a few genes such as the maturity genes of sorghum have profound effects on duration of growth and plant size. Sorghum has many advantages as an experimental species. In the first place, it is self-pollinated and inbred lines are vigorous. Only a few varieties were introduced to the United States about a century ago, and the two most important ones were tropical varieties. The varieties were too late and too tall to satisfy farmers who promptly selected shorter and earlier maturing types that suited them better. As a result, a number of dwarf and early varieties in similar genetic backgrounds originated. In the 1930’s it seemed desirable to make a shorter SOONER MILO and the tall EARLY MILO was crossed to DWARF YELLOW MILO. When F, rows of this cross were grown, it became apparent that a linkage between tall

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height and early maturity existed and that the inheritance of duration of growth was relatively simple. Ultimately, the inheritance of maturity in MILO was determined and three genes were recognized (Quinby and Karper, 1945) . The different maturity genotypes appeared to be the same size if grown in 14-hours nights under which treatment they flowered at about the same time. It was assumed, therefore, that the maturity genes, in some way, controlled synthesis of a floral hormone that had no influence except on time of floral initiation. At long last, an effort was made to see whether the maturity genes of MILO might influence growth rates when the maturity genotypes were grown in short nights and the genotypes had different times of floral initiation and durations of growth. Contrary to expectation, maturity genes were found to influence growth rates (Quinby, 1972a). This disclosure led me to the conclusion that the floral stimulus was probably a combination of common hormones, and prompted the thinking that led to the hypotheses presented in the previous pages and summarized in the following paragraphs. The genetic control of flowering in sorghum appears to be genetically simple because only four gene loci have been recognized. The continuous variation in flowering is thought to result from allelic series at the four loci and because of complementary action between gene loci. The floral stimulus appears to consist of auxin and gibberellin, and an interaction between the two hormones produces the stimulus that changes a vegetative bud into a fruiting bud. Auxin is produced largely during darkness, and gibberellin during daylight. Temperate varieties, because of less inhibition by phytochrome, produce more auxin than tropical varieties during daylight. Early-flowering temperate varieties produce more auxin and more gibberellin during daylight than late ones. The PT3"form of phytochrome appears to inhibit synthesis of auxin during daylight, and the PGGO form to inhibit the synthesis of gibberellin during darkness. Both forms of phytochrome are present in plants during the day. Alleles at loci 1 and 2 are assumed to cause differences in sensitivity to inhibition by P,,",and alleles at loci 3 and 4 to cause differences in sensitivity to inhibition by P,,,. Dominant alleles at the maturity loci cause sensitivity and recessive alleles less sensitivity to ,inhibition by phytochrome. As a result, recessives at loci 1 and 2 allow the synthesis of some auxin during daylight to supplement that produced in darkness. Recessives at loci 3 and 4 allow the synthesis of more gibberellin during daylight. The maturity genes appear, through differences in sensitivity to inhibition, to regulate levels of auxin and gibberellin that, in turn, control time of floral initiation and growth. High, as well as low, levels of auxin inhibit floral initiation. Low levels

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of gibberellin inhibit floral initiation, but there is no indication that high levels of gibberellin are inhibitory. The four height genes constitute a second genetic mechanism of control over plant growth. The tallest genotype is high in gibberellin content but low in auxin content. The shortest genotype is high in auxin content and low in gibberellin content. The height genes, like the maturity genes, control levels of auxin and gibberellin through differences in sensitivity to inhibition by P,,, and Pee,. Genes dw, and dw, are assumed to be involved in the synthesis of auxin and genes dw, and dw,, in the synthesis of gibberellin. The influence of levels of auxin and gibberellin is recognizable not only in time of floral initiation and height but in leaf size, peduncle length, panicle size, and internode distribution. Photoperiod, temperature, and leaf area all influence the rate of synthesis of auxin and gibberellin. The preoccupation of physiologists with temperature and photoperiod has tended to divert attention away from the genetic mechanism of control of plant growth. Hybrid vigor seems to result from the fact that'plants heterozygous at maturity or height loci synthesize amounts of auxin and gibberellin that differ from the amounts synthesized by homozygous plants. Some heterozygous genotypes are better than others and some are little better than homozygous genotypes. The hypotheses presented here seem to be logical in the light of the information presented. However, there are numerous bits of information that do not fit properly into the picture. For instance, the reason for the late flowering that results from heterozygosity at locus 1 when locus 2 is homozygous recessive (Table 111) is obscure. Long nights eliminate the late flowering induced by the heterozygous condition at locus 1 (Quinby and Karper, 1945; Miller et al., 1968b). Heterozygosity at loci 2, 3, and 4 has not been observed to cause late flowering (Quinby, 1967), and the gene interaction involving heterozygosity at locus 1 appears to be unique. The late flowering that results from heterozygosity at locus 1, when locus 2 is homozygous recessive, calls attention to the fact that many details of the physiology of flowering in sorghum are not understood.

XII.

Implications to Plant Breeding

A.

SORGHUM BREEDING

The evidence from sorghum indicates that the genetic control of floral initiation and of plant growth during the vegetative period is simple as far as number of genes is concerned. The continuous variation that exists

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appears to be due to allelic series at the four maturity loci. The simple genetic control over growth may explain the inability of sorghum breeders in the United States to increase yield of varieties. Sorghum breeders shortened duration of growth and stature and made sorghum more suitable to be harvested mechanically, but did not increase yielding capacity until cytoplasmic male-sterility was found and hybrid vigor could be used. The evidence presented here emphasizes that a breeder cannot change maturity genotype without changing hormone levels that, in turn, influence growth rate and adaptation. The corollary of this is that a breeder will not change yield without changing maturity genotype. The problem of finding maximum hybrid vigor in the sorghum species for any particular environment apparently depends on choosing strains to cross at the inception of a breeding program that, between them, contain the most favorable complimentary maturity alleles for that environment. The hybrid vigor that occurs in sorghum hybrids at present must result from differences in complementary action between recessive alleles or between dominant alleles. For instance, REDLAN and CAPROCK are the female and male parents of a vigorous hybrid. They have similar but not identical parentages (Quinby, 1967) and both are ma,Ma,Ma,Ma, in maturity genotype. Because of their parentages, the recessive at the first locus in REDLAN and CAPROCK are likely to be a little different because the two KAFIR parents used in Oklahoma and in Texas to produce REDLAN and CAPROCK differ by about 3 days in time of flowering. The dominants at loci 2 and 3 in both REDLAN and CAPROCK must have come from the KAFIR parents and might be identical but could be slightly different. The dominants at the fourth locus in REDLAN and CAPROCK probably came from UFIR and MILO, respectively, and are probably different. But all the differences must be in complementary action between recessive alleles or between dominant alleles. Hybrids made with female parents of the genotypes ma,mazma3ma4or Malma,manma, crossed to male parents of the genotype ma,Ma,Ma,Ma, have not yet been evaluated and it remains to be seen whether heterozygosity due to dominants and recessives is more effective in producing hybrid vigor than heterozygosity due to two recessive or two dominant alleles. But it appears that an opportunity to produce parents to make higher yielding hybrids still exists because hybrids heterozygous at some of the four maturity local have not yet been evaluated. In addition, numerous dominant alleles not previously available in temperate zones are now available in the temperate varieties recently converted from tropical adaptation. Duration of growth is an important part of adaptation and one plant breeding problem in sorghum is to identify parents that produce vigorous

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hybrids in each of a number of different maturities. Because of the association of high yield with long duration of growth reported by Quinby and Karper (1945) and Dalton (1967), farmers are inclined to grow hybrids that are as late to flower as temperature conditions permit. Under irrigation in temperate zones, the length of the favorable growing season sets the limit on suitable durations of growth; but, on dryland, the amount of soil moisture may set the limit. Double cropping makes short duration of growth necessary in many areas. There is evidence in the data presented by Quinby (1972a) to indicate that a hormone level that allows early floral initiation and flowering inhibits vegetative growth. This association may account for the difficulty of finding extreme hybrid vigor in hybrids of extremely early maturity. It is not yet apparent to what extent local adaptation exists. RS610 is adapted from the Gulf Coast of Texas to South Dakota, a span of 20 degrees in latitude, and is grown in Israel, South Africa, the Argentine, and Australia. CSHl, one of the first hybrids put into production in India, is adapted in the kharif season between latitudes 9 and 32 degrees (Rachie, 1970). A REDBINE X HEGARI-derivative hybrid that is Ma,ma, at the first maturity locus is a late, dual-purpose hybrid in the United States but a mid-season grain hybrid at lower latitude in Rhodesia and Venezuela. It appears that vigorous hybrids have wide adaptation to differences in latitude or elevation. Nevertheless, different hybrids must be grown in North Dakota and Texas and, in India, different varieties, if not hybrids, are grown in the kharif and rabi seasons. Differences in resistance or susceptibility to diseases or insects is also important in determining adaptation. The first two hybrids put into production in India were named CSHl and CSH2. Both have CK60A as the female parent. IS84 is the male parent of CSHl and IS3691 the male parent of CSH2. IS84 is a yellow endosperm FETERITA derivative and is recessive at the first maturity locus. IS3691 is a yellow endosperm HEGARI derivative and is dominant at the first maturity locus. IS84, IS3691, and CK60A all originated in the breeding program at the Texas Agricultural Experiment Station at Lubbock, Texas. CK60A is dominant at the second maturity locus, and CSH2 might be considered to be a tropical hybrid. CSHl might be considered to be a temperate hybrid because it is homozygous recessive at the first locus and might be suitable to grow in the temperate zone in the United States except that it is a 2-dwarf and too tall. Actually, CSHl is probably adapted from 9 to 40 degrees north latitude. A tropical grain hybrid of 2-dwarf height like CSH2 is suitable to be used as a late-maturing forage hybrid in the temperate zones. Experience has shown that the most suitable hybrid for the area of the Coastal Plains in Texas is not the most suitable hybrid on the High Plains

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of Texas largely because maturities of hybrids are different in the two areas because of a two-month difference in planting date. In addition, the two areas differ in elevation by as much as 1500 meters. It is apparent that there is some local adaptation; but, at the same time, some hybrids are suitable in both the tropical and temperate zones and from sea level to as high as 1500 meters. The Texas Agricultural Experiment Station and the U.S. Department of Agriculture have been converting tropical varieties to temperate zone adaptation and shortening them in stature in an effort to make tropical germplasm available for use in the temperate zones. All these converted tropicals might well be evaluated as parents of tropical hybrids as soon as a female parent of the genotype Ma,ma,ma,ma, is available. Such hybrids could be produced in the temperate zone and only a testing program in the tropics would be needed to recognize the superior hybrids. It seems logical to think that a converted variety from a high elevation in Ethiopia might be the male parent of a suitable hybrid for high elevations in Ethiopia or a converted variety from a lower elevation in Nigeria, a parent for a suitable hybrid for Nigeria. After being recognized, such hybrids could then be produced in the tropics in the suitable season, or in one of the temperate zones. At the time the program of converting tropical varieties to temperate zone adaptation was begun, it seemed logical to convert varieties from most of the seventy groups that were thought, at the time, to constitute the species. The idea was to make a diversity of germplasm available in the temperate zones even though some of the varieties appeared not to be agronomically suitable. Now that the conversion of the first group of varieties has been accomplished, it seems that the objective might well be changed. It is apparent that the alleles at the maturity gene loci are important in determining yield, and it seems logical now to convert the best of the tropical varieties without regard to the botanical group to which they belong. Since there are so many good tropical varieties in existence, it might be well to observe the F, plants of each cross in the winter season in the tropics. It might then be well to continue to convert only those tropical varieties that produce vigorous F, plants.

B.

PLANTBREEDING IN GENERAL

Doggett (1970) has presented an excellent review of the theories that are the basis of theories of population improvement and recurrent selection and has suggested how suitable sorghum populations might be established. Gardner (1973) has concluded that increases in yield from population improvement in sorghum as high as 6 % per year are theoretically possible.

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If the genetic control of plant growth is hormonal and is as genetically simple as it appears to be, recurrent selection programs to increase yield alone appear to be unnecessary because allelic series, rather than modifiers, account for the continuous variation. Also, the use of composites to allow population improvement should be reevaluated because the assumed deleterious linkages do not exist if the modifiers do not exist. So-called “variation” has come to be much sought after in many plant breeding programs, and x-irradiation or some other method of producing cryptic mutations have been resorted to in some instances. But, if the coiltrol of growth is hormonal and is genetically simple, the variation sought after would be ineffective because mutations of structural genes probably would result only in abnormalities. Finding extreme hybrid vigor in hexaploid, as compared to diploid or tetraploid, species could be difficult. In a diploid species with differences at 2 loci, 4 homozygous and 5 heterozygous genotypes would be possible. In a tetraploid species with differences at 4 loci, 16 homozygous and 65 heterozygous genotypes would be possible. In a hexaploid species with differences at 6 loci, 64 homozygous and 665 heterozygous genotypes would be possible. The problem of finding the superior heterozygous genotype among 665 rather than 65 or 5 would be greater; and, of more importance, some of the 64 homozygous genotypes would be made up of combinations that would be vigorous, due to epistasis, without being heterozygous. REFER ENcEs Ali-Khan, S . T., and Weibel, D. E. 1969. Can. J. Plant Sci. 49, 217-218. Argikar, G. R., and Chavan, V. M. 1957. Indian 1. Genet. Plant Breed. 17, 65-72. Arnon, I., and Blurn, A. 1962. Isr. .I. Agr. Res. 12, 35-103. Ayyangar, G. N. R., Rao, V. P., and Reddy, T. V. 1938. Proc. Indian Acad. Sci. 7, 161-176. Beil, G . M., and Atkins, R. E. 1967. Crop Sci. I, 225-228. Borrill, M. 1959. Ann. Bor. ( L o n d o n ) [N.S.] 23, 217-227. Borthwick, H.A., and Cathey, H. M. 1962. Bot. C a z . (Chicago) 123, 155-162. Blurn, A. 1970. Crop. Sci. 10, 28-31. Caddel, J . L., and Weibel, D. E. 1971. Agron. .l. 63, 799-803. Caddel, J. L., and Weibel, D. E. 1972. Agron. J . 64,473-476. Chailakhian, M. Kh. 1961. In “Plant Growth Regulation” (R. M. Klein, e d . ) , pp. 531-542. Iowa State Univ. Press, Ames. Chavda, D. H., and Drolsom, P. N. 1970. Indian J. Agr. Sci. 40, 967-973. Chiang, M. S., and Smith, J . D. 1967. Can. J . Genet. Cytol. 9, 44-51. Clark, H. E., and Kerns, K. R. 1942. Science 95, 5 3 6 5 3 7 . Collins, F. C., and Pickett, R. C. 1972. Crop Sci. 12, 5-6. Dalton, L. G . 1967. Crop Sci. 7, 271. Doggett, H. 1970. “Sorghum.” Longmans, Green, New York. Downes, R. W. 1972. A N S J. ~ .Agr. Res. 23, 585-594.

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Evans, L. T. 1969. In “The Induction of Flowering” (L. T. Evans, ed.), pp. 457-480. Cornell Univ. Press, Ithaca, New York. Gardner, C. 0. 1973. In “Sorghum in the Seventies” (N. Ganga Pradada Rao and L. R. House, eds.), pp. 180-196. Oxford-IHB Private Limited, New DelhiBombay, India. Graham, D., Jr., and Lessman, L. J. 1968. Agron. Abstr. p. 8. Hageman, R. H., Leng, E. R., and Dudley, J. W. 1967. Advan. Agron. 19, 45-86. Hamner, K. C. 1940. Bot. G a z . (Chicago) 101, 658-687. Haupt, W. 1969. In “The Induction of Flowering” (L. T. Evans, ed.), pp. 393-408. Cornell Univ. Press, Ithaca, New York. Hendricks, S. B. 1960. Cold Spring Harbor Symp. errant. Biol. 25, 245. Hendricks, S. B., and Borthwick, H. A. 1963. I n “Environmental Control of Plant Growth” (L. T. Evans, ed.), pp. 223-263. Academic Press, New York. Hesketh, J. D., Chase, S. S., and Nanda, K. K. 1969. Crop Sci. 9, 460-463. Kambal, A. E., and Webster, 0. J. 1966. Crop Sci. 6, 513-515. Karper, R. E. 1953. Agron. J. 45, 322-323. Karper, R. E., and Quinby, J. R. 1937. J . Hered. 28, 82-91. Karper, R. E., and Quinby, J. R. 1946. J . Amer. SOC. Agron. 38, 441-453. Karper, R. E., and Quinby, J. R. 1941. J. A m e r . SOC. Agron. 39, 937-938. Keulemans, N. C. 1959. Thesis, Agricultural University at Wageningen, Wageningen, The Netherlands. Kiesselbach, T. A. 1922. Nebr., Agr. Exp. Sta., Res. Bull. 20. Kirby, J . S., and Atkins, R. E. 1968. Crop Sci. 8 , 335-339. Lane, H. C. 1963. Crop Sci. 3, 496499. Lang, A. 1965. I n “Handbuch der Pflanzenphysiologie” (W. Ruhland, ed.), Vol. 15, lpp. 1380-1536. Springer-Verlag, Berlin and New York. Leopold, A. C. 1964. “Plant Growth and Development.” McGraw-Hill, New York. Liang, G. H. 1967. Can. J. Genet. Cytol. 9, 269-276. McClure, I. W., and Harvey, C. 1962. Agron. .I. 54, 457-459. Mendel, G. 1865. “Verhandlungen naturforschender Verein in Brunn, Abhandlungen” (translation by the Royal Horticultural Society of London) [published in “Principles of Genetics” (E. W., Sinnott, L. C. Dunn, and T. Dobzhandsky, eds.), 5th ed., McGraw-Hill, New York,1958]. Miller, F. R., Barnes, D. K., and Cruzado, H. J. 1968a. Crop Sci. 8 , 499-502. Miller, F. R., Quinby, J. R., and Cruzado, H. J. 1968b. Crop Sci. 8 , 675-677. Nagur, T., and Murthy, K. N. 1970. Indian 1. Genet. Plant Breed. 30, 26-35. Niehaus, N. H., and Pickett, R. C. 1966. Crop Sci. 6, 33-36. Nitsch, J . P. 1963. In “Environmental Control of Plant Growth” (L. T. Evans, ed.), pp. 175-193. Academic Press, New York. Patanothai, A., and Atkins, R. E. 1971. Crop Sci. 11, 839-843. Phinney, B. 0. 1961. In “Plant Growth Regulation” ( R . M. Klein, ed.), pp. 489-501. Iowa State Univ. Press, Ames. Quinby, J. R. 1961. Nat. Acad. Sci. Nat. Res. Corrnc., P u b / . 891, 183-205. Quinby, J. R. 1963. C r o p Sci. 3, 288-291. Quinby, J. R. 1966. Crop. Sci. 6, 516-518. Quinby, J. R. 1967. Advan. Agron. 19, 267-305. Quinby, J. R. 1970. C r o p Sci. 10, 251-254. Quinby, J. R. 1972a. C r o p Sci. 12, 490-492.

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Quinby, J. R. 1972b. Crop Sci. 12, 690-691. Quinby, J. R. 1972~.In “Sorghum in the Seventies” (N. Ganga Prasada Rao and L. R. House, eds.), pp. 161-172. Oxford-IHB Private Limited, New DelhiBombay, India. Quinby, J. R., and Karper, R. E. 1945. J. Amer. SOC. Agron. 37, 916-936. Quinby, J. R., and Karper, R. E. 1946. Amer. J. Bot. 33, 716-721. Quinby, J. R., and Karper, R. E. 1948. J. Amer. SOC. Agron. 40, 225-259. Quinby, J. R., and Karper, R. E. 1954. Agron. J. 46, 211-216. Quinby, J. R., and Karper, R. E. 1961. Crop Sci. 1, 8-10. Quinby, J. R., and Liang, G. H. 1969. Can. J. Genet. Cytol. 11, 275-280. Quinby, J. R., and Schertz, K. F. 1970. In “Sorghum Production and Utilization” (J. S. Wall and W. M. Ross, eds.), pp. 73-117. Avi, Westport, Connecticut. Quinby, J. R., Kramer, N. W., Stephens, J. C., Lahr, K. A., and Karper, R. E. 1958. Tex. Agr. Exp. Sta., Bull. 912. Quinby, J. R., Hesketh, J. D., and Voigt, R. L. 1973. Crop Sci. 13, 243-246. Rachie, K. 0. 1970. In “Sorghum Production and Utilization” (J. S. Wall and W. M. Ross, eds.), pp. 328-381. Avi, Westport, Connecticut. Salisbury, F. B. 1963. “The Flowering Process.” Macmillan, New York. Schertz, K. F. 1970. Crop Sci. 10, 531-534. Schertz, K. F. 1973. Crop Sci. 13, 324-326. Schertz, K. F., Sumpter, N. A., Sarkissian, I. V.,.and Hart, G. E. 1971. J. Hered. 62, 235-238. Schuler, J. F. 1954. Genetics 39, 908-922. Sieglinger, J. B. 1936. J. Amer. SOC.Agron. 28, 636-642. Stephens, J. C., and Holland, R. F. 1954. Agron. J . 46, 20-23. Stephens, J. C., and Quinby, J. R. 1952. Agron. J. 44, 231-233. Stickler, F. C., and Pauli, A. W. 1961a. Agron. J. 53, 99-102. Stickler, F. C., and Pauli, A. W. 1961b. Agron. J. 53, 352-353. Takimoto, A. 1969. In “The Induction of Flowering” (L. T. Evans, ed.), pp. 90-1 15. Cornell Univ. Press, Ithaca, New York. Thimann, K. V. 1937. Amer. J. Bot. 24, 407-412. Wellensick, S. J. 1965. Rep. Meet. FAO, U N , IAEA p. 393.

ION ABSORPTION BY PLANT ROOTS' T. K. Hodges Department of Botany and Plant Pathology, Purdue University, Lafayette, Indiana

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Overview of Nutrient Absorption by Roots 111. Energy-Dependent and Active Ion Transport

.................... ........................ ........................

A. Terminology . . . . . . ............................ B. Active Transport of S .............................. IV. Kinetics and Selectivity of Ion Absorption . . . V. Energetics of Ion Transport . . . . . . . . . . . . . . . . VI. Proposed Model for Ion Absorption by Roots . . . . .

............................... .................

I.

163 164 167 167 169

201

Introduction

Sustained growth of higher plants requires light, carbon dioxide, water, and mineral ions. One of the most fundamental problems of plant growth is how inorganic ions enter root cells and then move through the root and up to the shoot. It is well known that green leaves convert light energy into chemical energy (NADPH and ATP) by photosynthesis and provide the roots with an energy supply in the form of reduced carbon compounds. Probably the most vital function of the root is the utilization of this energy in procuring essential inorganic ions. Although roots have other important functions, such as anchorage, providing a pathway for water and nutrient transfer to the shoot, metabolism for their own growth, synthesis of growth regulators, their unique ability to extract and concentrate inorganic ions selectively ranks as one of their most important functions. During the last-50 years much effort has been devoted to elucidating nutrient absorption and transport in roots, and although progress has been considerable, much still remains to be learned. In this article I shall restrict the discussion to ion absorption by cells (mainly root cells) and not consider long distance transport from cell to 'Paper No. 5090 of the Journal Series of the Purdue University Agricultural Experiment Station, Lafayette, Indiana. 163

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cell or organ to organ. As it seems relevant to our understanding of ion absorption by roots, I will also consider ion transport in other tissue, such as storage roots, leaves, algae, and in organelles, such as mitochondria and chloroplasts. My emphasis on ion absorption by cells, including the flux of ions across both the plasma membrane and tonoplast, is based not only on the primacy of these processes, but also on very exciting studies involving relatively new techniques and methods of analysis being used for investigating these phenomena. Only selected works are considered here, and for additional coverage the reader is referred to the recent books or reviews by Briggs et al. (1961), Sutcliffe (1962), Jennings (1963), Hope (1971), Gauch (1972), MacRobbie ( 1970, 1971 ), Epstein ( 1972a, 1973), Higinbotham ( 1973) and to the Annual Reviews of Plant Physiology, where various aspects of ion transport are considered annually.

II.

Overview of Nutrient Absorption by Roots

Most studies concerning the mechanism( s ) of nutrient absorption have been conducted with excised roots (Hoagland and Broyer, 1936; Epstein, 1973). Excised roots usually function for several hours, at least with regard to ion absorption, as if they had never been removed from the shoot (Hoagland and Broyer, 1936; Jackson and Stief, 1965). Hoagland and Broyer (1936) were the first to show the value of using excised roots that were low in salt content for studying nutrient absorption. Such roots accumulate salts in a short time and one can easily measure the increase in ion content either chemically or by using the radioisotope of a specific element. When low-salt, excised roots are placed into a warm (room temperature) salt solution such as KCl, they absorb both the cation and anion rapidly during the first 10-30 minutes, and this is followed by a gradually decreasing rate of absorption, which continues for several hours. In such experiments it is advisable to include Ca?+ in the experimental solution since this ion is essential for maintaining the functional and structural integrity of plant membranes (Epstein, 1961; Marinos, 1962; Foote and Hanson, 1964). The initial phase of absorption is readily reversible; i.e., an absorbed radioisotope washes out of the roots if they are transferred to water or a salt solution that does not contain the radioisotope. The phase of rapid absorption is little affected by temperature, anaerobiosis or metabolic inhibitors, indicating that it is a physical rather than a metabolically linked absorption (Butler, 1953; Briggs and Robertson, 1957). The portion or volume of the root into which ions enter rapidly and rever-

ION ABSORPTION BY PLANT ROOTS

165

sibly is referred to as the apparent free space (AFS) (Hope and Stevens, 1952). It often represents 15-25% of the root volume (Butler, 1953; Epstein, 1955; Briggs and Robertson, 1957). The AFS is thought to consist of the interconnected cell wall system (apoplast) up to the Casparian strip of the endodermis. Thus, after a short time, the cortical cells and the epidermal cells are bathed in a solution that is virtually identical to the external solution. The phase of slow ion absorption continues for several hours at a continually diminishing rate until eventually no apparent absorption occurs. This steady-state condition is referred to as salt saturation, and the tissue is now in a high-salt state as contrasted to the low-salt state at the beginning of the experiment. Before salt saturation, ion influx greatly exceeds ion efflux; efflux may be almost nonexistent in low salt roots (Johansen et al., 1970; Epstein, 1972a). At the salt-saturated state, ion influx continues but at a diminished rate (Pitman, 1969; Neirinckx and Bange, 1971; Cram and Laties, 1971), and the influx is balanced by an equal rate of ion efflux (Pierce and Higinbotham, 1970; Cram and Laties, 1971). Several features about the slow absorption phase are important. First, it requires energy. If metabolism is impaired by lowering the temperature, by imposing anaerobic conditions, or by adding a variety of metabolic poisons, ion absorption ceases. Under these conditions, the ion concentration in the tissue may not even equal that in the external solution, indicating that concentration-dependent diffusion is restricted. The reason for this is that highly charged electrolytes cannot readily enter (or solubilize in) the hydrophobic lipid of the cell membrane. Permeability coefficients for inorganic ion entry into plant cells are in the order of cm/sec (Scott et al., 1968; Pierce and Higinbotham, 1970; Cram and Laties, 1971), which is very low compared to the 10-*-10-' values commonly found for nonelectrolytes (Collander, 1959). Another characteristic that illustrates the energy dependency of ion absorption is that when metabolism is allowed to proceed the internal concentrations of both cations and anions become greater than the external concentration. This phenomenon is frequently expressed as the concentration or accumulation ratio, i.e., c , , l d e / ~ o , , t , , d , = . Accumulation ratios of 10 to 100 are common, and some values are as high as 10,000 (MacDonald et al., 1960). Although an accumulation ratio significantly greater than 1 indicates energy expenditure was required to concentrate the ion, it does not necessarily mean that the ion being studied was actively transported; active transport being defined as the movement of an ion against an electrochemical potential gradient (Ussing, 1949). Root cells maintain an electrical potential difference across the cell membrane, and this gives rise to the distinction between

166

T. K. HODGES

energy-dependent transport and active transport, which will be discussed in Section 111. Studies in which both the electrical and concentration gradients have been evaluated indicate that anions are actively transported across the plasma membrane into the cytoplasm (Higinbotham et al., 1967; Pierce and Higinbotham, 1970). Cations, with the possible exception of K , enter cells passively, i.e., down the electrochemical gradient, and they then appear to be actively transported back across the plasma membrane from the cytoplasm to the external solution (Higinbotham et al., 1967). Transport of K+ at the plasma membrane appears to be active inward in certain instances and active outward in other situations (Etherton, 1963, 1967; Scott et al., 1968; Pierce and Higinbotham, 1970). At the tonoplast only K', Na+, and C1- have been investigated and the results, though needing confirmation, suggest that K+and Na+ are actively pumped into the vacuole while C1- may be passively distributed (Pierce and Higinbotham, 1970) or actively transported (Cram, 1968a). Another important characteristic of energy-dependent transport of ions into roots is that as the external ion concentration is increased, the rate of absorption increases in a biphasic manner. This apparent saturation of the transport system at high external ion concentrations gave rise to the ion-carrier concept (Osterhout, 1935; van den Honert, 1937). The ion-carrier complex has been considered to be analogous to a substrate-enzyme complex (Epstein and Hagen, 1952), and Michaelis-Menten kinetic analysis have been employed extensively to describe ion absorption data (Fried and Broeshart, 1967; Epstein, 1973). It is now apparent, however, that the kinetics of ion transport into root cells is very complex and that Michaelis-Menten kinetics do not accurately describe the phenomena (Epstein, 1966; Nissen, 1971; Leonard and Hodges, 1973). However, influx kinetics can be adequately described by assuming a single carrier consisting of several ion-binding sites which interact. This concept is based on a model proposed by Koshland (1970) to account for enzyme kinetics that deviate from Michaelis-Menten kinetics. Energy-dependent transport is also selective. That is, the ion composition of plant extracts is totally different from the composition of the external solution (Collander, 1941, 1959). Calcium ions play an important role in regulating the selectivity of ion transport (Jacobson et al., 1950; Epstein, 1961). Furthermore, the selectivity of transport is different at low and high external ion concentrations (Rains and Epstein, 1967a,b). It is proposed here that the basis for selective ion transport in plants is the electrical field strengths (Eisenman, 1 962; Diamond and Wright, 1969) of the carrier binding sites, and the concentration-regulated speci-

ION ABSORPTION BY PLANT ROOTS

167

ficity is due to interactions of the binding sites, which change their field strengths. The actual energy source for ion absorption by roots has its origin in aerobic respiration. Anaerobiosis (Hoagland and Broyer, 1936) and specific respiratory poisons (Ordin and Jacobson, 1955) inhibit ion absorption. Considerable evidence indicates that ATP drives cation transport across plant cell membranes (Higinbotham, 1959; MacRobbie, 1970; Fisher et al., 1970), and some evidence suggests that anion transport is driven by some other product or aspect of aerobic respiration (Atkinson and Polya, 1968; Cram, 1969a; Raven, 1969). ATP-driven cation transport at the plasma membrane appears to be mediated by an ATPase enzyme (Fisher et al., 1970; Hodges et al., 1972), and it is proposed here that anion influx is brought about by an exchange reaction mediated by an anion carrier. The internal anion driving the anion carrier could be OH- that is generated by the ATPase and/or HC0,- that is generated by aerobic respiration.

Ill.

Energy-Dependent and Active Ion Transport

A.

TERMINOLOGY

The terms energy-dependent and active transport are sometimes used synonomously although they are quite different. Energy-dependent transport is broader and pertains to any transport that depends directly or indirectly on metabolism. Transport of this type generally results in accumulation ratios ( c , / c , ) significantly greater than 1. Active transport, on the other hand, is defined as the movement of an ion against its electrochemical potential (Ussing, 1949; Dainty, 1962). Other definitions or treatments of active transport have been proposed (Kedem, 1961); however, they have not been employed for studies of ion transport in higher plants. The basis for the difference between energy-dependent and active transport is that an electrical potential difference exists across membranes of actively metabolizing cells. Charged solutes such as inorganic ions move passively in response to this electrical field as well as to the concentration (activity) gradients. The early studies of Lund (1928), Blinks (1935), Osterhout (1935), and others (see Rosene and Lund, 1953) as well as more recent studies (see Dainty, 1962; MacRobbie, 1971; Higinbotham, 1973) have clearly established that the cytoplasm is electrically negative with respect to the external solution bathing the cells. The basis for this membrane potential will be discussed subsequently, but its maintenance depends on energy; the electrical potential difference falls when the cells

168

T. K. HODGES

are killed. Because the electrical potential is negative inside relative to outside, cations are drawn in and anions are repelled. Thus, cations may exist in cells at much higher concentrations than outside, but when the concentration (activity) and electrical gradients (both are physical driving forces) are both taken into account, the ion may possess the same electrochemical potential on both sides of the membrane. In this situation, an ion can exist at a higher concentration inside than outside due to the electrical driving force, and this would be called an energy-dependent transport since energy is necessary for maintaining the electrical potential. But, transport per se would be passive since only physical driving forces acted on the ion. In this situation, energy expenditure would be indirect. Active transport is a special type of energy-dependent transport. Since active transport is defined as the movement of an ion against its electrochemical gradient, this type of transport is an “uphill” process, and it must be directly coupled to an energy releasing reaction. Carriers, permeases, translocases, transporters, and porters are terms used to describe substances which reside in membranes and aid the solute in moving across the membrane, presumably through an association or binding. In this discussion the term carrier is used since it is most common in the literature on transport in plants. The two main characteristics of carrier-mediated transport are saturating kinetics and specificity. Active transport, as defined above, exhibits these characteristics and is therefore believed to be carrier mediated. Passive transport that is energy-dependent also frequently exhibits saturation kinetics and specificity and is therefore also thought to involve carriers. Such transport is frequently termed facilitated diffusion.Still another type of carrier-mediated, but passive, transport phenomenon is exchangediffusion. In this type of transport, a carrier can only traverse the membrane when complexed with a specific ion. For example, when a radioactive ion is moved across the membrane from outside to inside by this type of carrier and then released, the carrier will not return until it binds a similar ion. There is a small chance the carrier will recombine with the labeled ion; thus the return trip is likely to be with a similar, but nonradioactive ion. Thus, exchange-diffusion results in a bidirectional transport, and no net transport occurs. In summary, the term energy-dependent transport accurately describes all transport that depends on metabolism, and it frequently leads to accumulation ratios significantly greater than 1, but the transport itself may be either active (i.e., against the electrochemical gradient) or passive (down the electrochemical gradient). Both types of transport may be carriermediated. Facilitated diffusion and exchange-diff usion are merely descriptive terms for carrier-mediated passive transport.

ION ABSORPTION BY PLANT ROOTS

B.

169

ACTIVETRANSPORT OF SPECIFIC IONS

From the previous discussion, it is apparent that information about the electrical potential difference across cell membranes is necessary in order to determine whether a specific ion is actively transported. Numerous reports describe experimental techniques for measuring membrane potentials of plant cells, and the problems encountered in these studies have been clearly discussed by Dainty (1962). In the most common technique a Ag/AgCl microelectrode with a salt bridge ( 3 N KC1) is inserted into the cytoplasm or vacuole and connected through an electrometer to a similar electrode placed in the ambient solution. The major problems in these studies are that electrodes frequently break due to the impervious nature of the plant cell wall, and it is difficult to know the cellular location of the electrode tip. In addition, protoplasm plugs the salt bridge, membranes reseal over the tip of the electrode, junction potentials occur at the electrode tip, etc. The problems notwithstanding, reliable data are now available about membrane potentials for several species of algae (MacRobbie, 1970) and for a few higher plants (Higinbotham, 1973). The electrical potential difference across the plasma membrane is in the range of -60 mV to -200 mV (cytoplasmic phase negative) and the electrical potential difference across the tonoplast is relatively small, being only 0 to -20 mV with the cytoplasm being negative relative to the vacuole. Two types of analysis have been used with plant tissue for determining whether ions are actively transported. One of these employs the Nernst equation which relates ion activity (concentration) difference across cell membranes to the electrical potential difference across the cell membrane under equilibrium conditions. The other analysis used is the flux-ratio comparison which was developed independently by Ussing (1949) and Teorell (1949). In this analysis the ratio of the actual measured flux rates (influx/efflux) of a particular ion is compared to the ratio of the predicted passive flux rates (influx/efflux) . Both the Nernst and flux-ratio analysis predict the passive distribution of ions. If the actual ion concentrations or flux rates differ significantly from that predicted on the basis of the physical driving forces, this is interpreted as proof that the ion under consideration is actively transported.

1. Nernst Equation Analysis The Nernst equation is based on equilibrium conditions (see Dainty, 1962; Higinbotham, 1973), and for any ion ( j ) that is passively distributed across a semi-permeable membrane the electrochemical potential ( p ) of the ion is the same on the two sides of the membrane i.e., p j 0 = pi',

170

T. K. HODGES

where o and i refer to an outside solution and an inside solution, respectively (as an example, the plasma membrane separating the outside solution, 0, from the cytoplasmic solution, i ) . The electrochemical potential of an ion consists of two major components-the chemical potential ( R T In a ) and the electrical potential ( z F E ) where R is the gas constant, T is the absolute temperature, a is the activity of the ion,* z is the valence of the ion, F is the Faraday, and E is the electrical potential. Thus, ii, = z,FE RT In a, and since the electrochemical potential of a passively distributed ion is the same on both sides of the membrane at equilibrium, it follows that z,FEjo RT In aj0 = z,FE,' RT In a j l . Then E,' - E , O = AE = R T / z , F In al0/a,', which is the Nernst equation. For our considerations, we will only be concerned with monovalent ions and if we assume a temperature of 2OoC and convert to the common logarithm and also substitute concentration ( c ) for activity ( a ) , the Nernst equation simplifies to AE = 2 5 8 log c,o/cli. The Nernst equation, in this application, simply indicates the equilibrium relationship between an electrical potential difference across a membrane and the concentration or accumulation ratio, i.e., cjl/c,O, for an ion which is passively distributed across the membrane. For example, an electrical potential difference ( A E ) , at 20°C, of -58 mV would result in an equilibrium concentration ratio of 10 for cations and 0.1 for anions. A AE of -1 16 mV, which is close to that found for higher plants (Etherton and Higinbotham, 1960; Higinbotham et al., 1964), would yield an equilibrium concentration ratio of 100 for cations and 0.01 for anions. If the latter situation were, in fact, found to be true in an experiment, i.e., a AE of -116 mV, external cation and anion concentrations of say 1 mM and internal cation and anion concentrations of 100 mM and 0.01 mM, respectively, one would have to conclude that both the cation and anion were passively distributed. The cation transport would be described as an energy-dependent transport because the accumulation ratio was greater than 1 and this was made possible by energy expenditure in maintaining the electrical potential difference across the membrane. Although anion transport is also energy-dependent, this would not be recognized as such if only the internal and external anion concentrations were known. When major deviations occur between the actual internal concentrations and those that are predicted based on the AE, and quasi-equilibrium conditions exist, this is considered proof that the ion is actively transported. In the above example where the AE was - 116 mV, if the cation was maintained at a concentration exceeding 100 mM, this would indicate that the

+

+

+

* In practice, concentrations are frequently substituted for the activities, but direct estimates of activities, using ion selective microelectrodes, have been used (Coster, 1966; Vorobiev, 1967; Etherton, 1968).

ION ABSORPTION BY PLANT ROOTS

171

ion was being actively pumped into the cell. If, on the other hand, the cation was maintained at a concentration less than 100 mM, this would indicate the ion was actively transported out of the cell. Similarly, internal anion concentrations in excess of 0.01 mM would indicate an inward directed active transport, whereas concentrations less than 0.01 mM would indicate an active extrusion. The Nernst equation has been used commonly for evaluating ion fluxes in algae (MacRobbie, 1970) but only rarely for higher plants. The most thorough studies using this approach with higher plants is that of Etherton and Higinbotham (1960) and Higinbotham et al. (1964, 1967). They have reported that the interior of cells of oats, peas, and corn is electrically negative by 80 to 115 mV relative to an external solution of 0.1 mM KCl (Etherton and Higinbotham, 1960). Most of this electrical potential difference is across the plasma membrane; only a small electrical potential difference across the tonoplast seems to be a general feature of plant cells (MacRobbie, 1970). Subsequent studies using roots and coleoptiles of oats, and roots and stems of peas, indicated that all anions (i.e., C1-, NO,-, H,PO,-, and SO,") were actively transported into the cells of these tissues (Higinbotham et al., 1964, 1967). Although the cations (Na+, Ca2+,Mg ,+) entered the cells by an energy-dependent process (i.e., accumulation ratios were in excess of 1) , they appeared to be actively secreted. In other words, the internal concentrations of these cations were less than they should have been based on the passive driving forces. However, because of the low permeability coefficients of the divalent cations they are probably excluded rather than actively secreted (Higinbotham et al., 1967). Potassium appeared to be close to electrochemical equilibrium, and therefore passively distributed, when the external salt concentration was low, but actively extruded from the cells, like the other cations, when the external salt concentration was high. Based on other studies using the Nernst equation, there seems to be no conflict with the conclusion that anions are actively absorbed by higher plant cells (Dunlop and Bowling, 1971; Gerson and Poole, 1972); however, there is some uncertainty with regard to the nature of cation transport. For example, in red beet tissue (Poole, 1966) and in corn roots (Dunlop and Bowling, 1971) K' i6 actively transported inward. Both K+ and Na' have been reported to be actively absorbed by sunflower roots (Bowling and Ansari, 1971, 1972). In the pitcher of the pitcher plant (Nepenthes henryana), Na+ was actively transported into the cells (Nemctk et al., 1966), but K+ appeared to be passively distributed. Thus, using the Nernst equation, it is not clear whether cations are actively pumped or passively distributed across the membranes of higher plant cells.

172

T. K. HODGES

One of the major difficulties in using the Nernst equation for evaluating ion transport is that this equation is based on an equilibrium condition, and this does not exist in actively metabolizing cells. For this reason, the flux-ratio equation, which does not require equilibrium conditions, has also been used for evaluating the driving forces acting on ions.

2 . Flux-Ratio Analysis The flux-ratio, or Ussing-Teorell, equation for passive ion transport was developed independently by Ussing ( 1949) and Teorell (1949). The equation is as follows: Jin ~-

c,

Jout cJLe x p ( z , F E / R T )

Where I,,,and Jollt represent radioactive tracer influx and efflux, respectively, across a particular membrane, c,” and c,’ are the concentrations of ion j on the two sides of the membrane, and the other terms were identified in the previous section. By measuring E , c j 0 , and c I 1one can which is the ratio of the rates of ion influx calculate a value for J,I1/J~,,lt and efflux which would occur passively, i.e., in response to the existing concentration and electrical driving forces. This passive flux-ratio can then be compared to the actual flux-ratio of the ion in question, and if the ion is in fact moving passively the calculated and measured flux-ratios will be identical. If they are different, this indicates that an additional driving force is acting on the ion, and this is taken as evidence that the ion is actively transported, and depending on whether the measured J l n / J o r l t ratio is greater or smaller than the calculated J,,I/Jo,ltratio, the direction of active transport can be ascertained. It is difficult, however, to obtain the necessary information to make the flux-ratio test. One needs to know the rates of influx and efflux of a specific ion across both the plasma membrane and tonoplast as well as the concentrations of the ion in the external solution, cytoplasm, and vacuole. As difficult as it seems though, great strides have been made in the last 10 years in determining these values. MacRobbie and Dainty (1958a,b) and Diamond and Solomon (1959) were the first to use what is called a “compartmental analysis” technique for estimating these various parameters in plant cells. Since the estimation of the various fluxes across the two membranes and the concentrations of the ion in the cytoplasm and vacuole is crucial to the flux-ratio test, the basis of the compartmental analysis will be considered first. a . Compartmental Analysis. When certain assumptions are made (MacRobbie, 1971), one can estimate specific ion fluxes at the plasma mem-

ION ABSORPTION BY PLANT ROOTS

173

brane and tonoplast by evaluating the kinetics of movement of a radioactive ion into and out of a tissue. The assumptions in this analysis have been discussed by Cereijido and Rotunno (1970), and the most important ones are (1 ) that the cells consist of compartments whose fluxes are in series rather than in parallel, i.e., vacuole + cytoplasm e cell wall F? outside solution as opposed to say vacuoleeoutside solution and cytoplasm e outside solution, ( 2 ) that the vacuole compartment is much larger than the cytoplasmic compartment, and ( 3 ) that the tissue is in a steady-state with respect to ion content, i.e., the chemical ion content of the tissue does not change during the course of “loading” and “unloading” the tissue with the radioisotope. MacRobbie ( 1971) has provided a most valuable assessment of these assumptions and the method in general, and the reader should consult this review for a critical evaluation. Also, the papers by Cram (1968a) and Pallaghy and Scott (1969) provide a most lucid derivation of the equations involved in calculating the various flux rates and ion contents of various compartments. Experimentally, plant tissue in a steady-state condition3 is exposed to a nutrient solution containing radioisotope for a given time (generally several hours) and then transferred to a solution containing an identical nutrient solution, except for the radioisotope, for an additional period of time (again for several hours). Entry of isotope into the tissue is monitored during the “loading” period, and its exit from the tissue is monitored during the “unloading” period. The nutrient solution must be replaced frequently during the “unloading” period in order to minimize reabsorption of the radioisotope. The loss of radioisotope from the tissue appears to be best described as a series of first-order reactions (Cereijido and Rotunno, 1970), which can be resolved by plotting the efflux data logarithmically as a function of time-as in Fig. 1A [first-order reactions yield a straight line when the loss of reactant (ion in this case) is plotted logarithmically as a function of time, i.e., log A = (--k/2.303)t A , with the slope equal to --k/2.303 and the intercept, A,,, being the initial amount of reactant]. The radioisotope loss from tissue is initially rapid but develops with time into a slow, linear rate of loss. This loss is interpreted as the loss from a specific cell compartment, and by extrapolating this line to t = 0, one has an estimate of the amount of radioisotope in this cell compartment at the beginning of the “unloading” period. Depending on the “loading” time, the

+

‘ A net accumulation of ion occurs in low salt roots, thus a steady-state does not exist and such roots are not amenable to the compartmental analysis. The negligible efflux under these conditions (Epstein, 1973) must be attributed t o the low ion content of the roots.

174

T. K. HODGES

amount of radioisotope in this compartment can represent as much as 90% of the total radioisotope in the tissue, and it is argued that the only cell compartment likely to contain this much of the label is the vacuole (Pitman, 1963; Cram, 1968a; MacRobbie, 1971). From the slope of the linear component one can calculate the first-order rate constant (slope = - k / 2 . 3 0 3 ) from which one can then determine the

~

A

h\

\ LOSS

from vccuoIes

Loss trom cytoplasm

Time (mid

--L

‘

FIG. 1. Logarithm of the efflux of radioactive ions from roots as a function of time. ( A ) The linear portion of the curve is interpreted as the loss of ions from cell vacuoles. Extrapolation of this slope to time zero gives the amount of radioactivity in the vacuoles at the beginning of efflux. I , is the radioactivity in vacuoles at time zero divided by the specific radioactivity of the “loading” solution, So. (B) Same as in plot A, but with the radioactive content of the vacuoles subtracted. Linear component is interpreted as the loss of radioactivity from the cytoplasm. I , is the radioactivity at time zero divided by the specific radioactivity of the “loading” solution, So.

half-time (t,,2 = 0.693/k) for radiois.otope loss from the vacuoles. For higher plants the reported half-times for ion efflux from vacuoles ranges from about 50 to 2000 hours (Pitman, 1963; Pierce and Higinbotham, 1970), depending on the tissue employed, the ion, and the experimental conditions. The most common values, however, range from about 50 to 100 hours. So, for most plants, under steady-state conditions, replacement of half the ions in the vacuoles would require 2-4 days. For complete turn-

ION ABSORPTION BY PLANT ROOTS

175

over or replacement of ions in vacuoles, it would take in excess of 10-20 days (about 98 % loss occurs in 5 half-times) , a period considerably longer than most ion absorption experiments. The amount of radioisotope remaining in the vacuoles at any time can be directly determined from the extrapolated line (Fig. l A ) , and if these values are subtracted from the total radioactivity in the tissue at the various times, one obtains the loss of radioactivity from the other parts of the cell. When these values are plotted logarithmically as a function of time (Fig. l B ) , an initial rapid loss of radioisotope from the tissue develops into another linear component. This first-order component is believed to represent the loss from the second largest cell compartment, the cytoplasm (MacRobbie and Dainty, 1958a; Pitman, 1963; Etherton, 1967; Cram, 1968a; Pierce and Higinbotham, 1970). The rate constant for ion loss from the cytoplasm is determined from the slope and then the half-time for radioisotope loss from the cytoplasm can be calculated. Half-times for ion losses from cytoplasm of higher plant cells vary from about 8 to 250 minutes, depending on the tissue, the ion, and the experimental conditions (Pierce and Higinbotham, 1970). The most common cytoplasmic half-times are between 10 and 40 minutes. Thus, for most situations, 98% of the ions in the cytoplasm would turnover in 50 to 200 minutes. Accordingly, absorption periods of these durations would result in the specific radioactivity of the cytoplasm being similar to that of the external solution. By continuing to subtract the slow component of radioisotope loss from that in the tissue it is possible to distinguish the loss of radioisotope from 2 additional compartments. Macklon and Higinbotham ( 1970) have suggested these compartments correspond to cell walls and a surface film. The half-times for isotope loss from cell walls and the surface film is only a few minutes. The apparent ion content of the cytoplasm can be estimated directly from the radioisotope data if the loading time exceeds 5 times the cytoplasmic half-time (i.e., cpm at intercept of second plot divided by the external specific radioactivity-referred to as I,. below). The ion content of the cytoplasm in micromoles/gram is readily converted to concentration by assuming 1 g of tissue equal 1 ml (or an appropriate correction factor can be applied for the water content of the tissue) and dividing by the volume of the cytoplasm. The ion content of vacuoles (QV) can be estimated by determining the total ion content of the tissue by chemical methods and subtracting the ion content of the cell walls and cytoplasm that is estimated from the radioactivity data (again the loading time should be in excess of 5 times the cytoplasmic half-time for this to be a reliable estimate). The ion content of vacuoles can be converted to concentration by knowing the volume of the cell occupied by the vacuole.

176

T. K. HODGES

The various flux rates (Cram, 1968a; Pallaghy and Scott; 1969; Pierce and Higinbotham, 1970; MacRobbie, 1971) can then be determined from the following equations: *Jo+c

= kclc

Jc+o

= kclc

Jc,v

=

Jo+c

1, +t”* +

kv&v

4-J v - o

-

Jc+o

where J is the flux rate, o is the outer phase, c is cytoplasm, v is the vacuole, k, and k , are the efflux rate constants for cytoplasm and vacuole, respectively, and they are obtained from the slope of the “unloading” curves, I , and I , are the apparent radioisotope contents based on the t = o intercepts from the cytoplasmic and vacuole efflux curves divided by the external specific activity, t , , is the absorption or “loading” time and Q, is the vacuole content of ion as described above. The compartmental analysis is obviously of great interest since it provides estimates of ion fluxes across separate membranes and ion contents of different cell compartments which heretofore had not been made. However, it is still not clear whether this analysis is valid for higher plant cells. Both Pitman (1963) and Cram (1968a) have obtained evidence in support of the series model for higher plant cells; however, MacRobbie ( 1969, 1971) has found that the series model does not accurately describe ion fluxes in Nitella cells. In Nitella, the transfer of C1- to vacuoles occurs more rapidly than predicted by the series model. Pallaghy et al. (1970) and Neirinckx and Bange (1971 ) have also reported that ion influx in corn and barley roots, respectively, is not consistent with the series model. It has also been found that the “unloading” curves for excised roots have an anomalous shape at low external concentrations which does not occur for roots of intact plants (Pallaghy et al., 1970; Weigl, 1971). This anomaly may represent the transfer of ions into the xylem and out into the external solution through the cut ends of the roots; Pitman (1971) estimates that this type of ion transfer may account for as much as 75% of the radioisotope in the wash-out solutions. Although various discrepancies and problems have arisen in the compartmental analysis, it represents the only procedure at the present time for even qualitatively estimating ion fluxes at both the plasma membrane and tonoplast and the concentrations of ions in the cytoplasm and vacuole of higher plant cells. 6. Experimental Flux-Ratio Comparisons. Several attempts have been made to test for passive or active ion transport in higher plant cells using

177

ION ABSORPTION BY PLANT ROOTS

the flux-ratio equation in association with the flux rates, and ion concentrations that are estimated using the compartmental analysis procedure (Pitman, 1963; Pitman and Saddler, 1967; Etherton, 1967; Cram, 1968a; Scott et al., 1968; Poole 1969; Pallaghy and Scott, 1969; Macklon and Higinbotham, 1970; Pierce and Higinbotham, 1970). Although the actual conclusions based on this test must be made with reservations due to the TABLE I A. Ion Fluxes across the Plasma Membrane of Oat Coleoptilesn,*

K+

Na+

c1-

.TO*

JC-0

12 4.6 5.2

0.75 1.8 1 .a

Q" 10 10 10

Measured ratio: QC

1 R5 19 R9

Jo+JJc-m

12 2.6 4.6

Calculated ratio: Jo+c/Jc-

4.5 68.0 0.0016

B. Ion Fluxes across the Tonoplast of Oat Coleoptilesamb

K+ Na+ Cl-

JH"

J v --re

QC

Qv

10 9.9

5.1 0,083 5.9

185 12 89

155 ?1 . s

9.9

89

Measured ratio

Calculated ratio

Jc+v/Jv+c

Jc+v/Jv+c

3.1 35.0 1.9

1.1 0.5 1.3

Adapted from Pierce and Higinbotham (1970). X 10lO/g/secand Q values are millimolar. The calculated = c,O/c,' exp ( z , F E / R T ) ] flux ratios were based on the Ussing-Teorell equation [Jln/Jout using measured E values of - 110 mV across the plasma membrane and 0 mV across the tonoplast, and activity coefficients of 0.81 for all ions in the outside solution and 0.77-for all ions in the cytoplasm and vacuole. Qc and Q, were calculated assuming that the cytoplasm and vacuole represented 3.5 and R9% of the cell volunie. a

* Units for flux rates are moles

uncertainty of the compartmental analysis, it does provide a tentative appraisal of the driving forces involved in transport. For higher plant cells, the most complete analysis to date using this approach was made by Pierce and Higinbotham (1970) for K+, Na+, and C1- transport in oat coleoptiles. Some of their data are summarized in Table I. At the plasma membrane, the calculated passive flux-ratio for C1- was 0.0016 and the measured flux-ratio was 4.6. From this it would certainly appear that C1- is actively pumped inward across the plasma membrane of the oat coleoptile cells. Cram (1968a) obtained similar results with

178

T. K. HODGES

carrot tissue. The passive flux-ratio for Na+ at the plasma membrane of the coleoptile cells (Table IA) was estimated to be 68 and the measured value only 2.6 indicating an active efflux of this ion. Active Na+ efflux at the plasma membrane has also been reported for pea roots (Etherton, 1967), barley roots (Pitman and Saddler, 1967), and broadbean roots (Scott et al., 1968). Conclusions about Kt transport at the plasma membrane are variable. In the oat coleoptile, K appears to be actively pumped inward (Table IA, Pierce and Higinbotham, 1970). A similar conclusion was reached for barley roots (Pitman and Saddler, 1967) and for pea epicotyl cells (Macklon and Higinbotham, 1970). However, Scott et al. (1968) concluded that only nonvacuolated cells of barley roots transported K+ inward at the plasma membrane; Kt was passively distributed in the mature vacuolated cells. Etherton (1967) also found K+ to be passively distributed across the plasma membrane of pea roots. In contrast to these results, Poole (1969) found a low flux-ratio for K+ at the plasma membrane of beet cells, and he suggested that 'an active K+ extrusion or possibly a K+ exchange-diffusion phenomenon was involved. At the tonoplast of the oat coleoptile cells, active transport of both K+ and Na+ into vacuoles appeared to occur (Table IB). Chloride was passively distributed. In carrots, however, chloride appears to be actively pumped across the tonoplast into vacuoles (Cram, 1968a, 1969a). Although the number of investigations concerning active and passive ion transport in cells of higher plants are limited, some generalizations, based on both the Nernst equation and flux-ratio analysis, appear to be valid. Chloride, and anions in general, are actively transpgrted inward across the plasma membrane. Cations, for the most part, enter cells by an energy-dependent process, but the movement is down the electrochemical gradient. Under certain situations the cations also appear to be actively transported across the plasma membrane but the direction of transport is variable; sometimes it is into the cell and other times it is out of the cell. In most cases, Na+ seems to be actively secreted. Observations on tonoplast ion fluxes are very limited, but it seems that active transport may also occur at this membrane. Additional investigations of the individual ion fluxes across both the plasma membrane and tonoplast and tests for passive or active transport are urgently needed and a complete picture of ion transport will not be possible until such studies have been conducted. 3 . Origin of the Electrical Potential Difference The electrical potential difference across biological membranes has generally been considered to be only a diffusion potential (Dainty, 1962); however, recent studies indicate that this may not be so (Higinbotham,

ION ABSORPTION BY PLANT ROOTS

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1973). A diffusion potential results from different mobilities of cations and anions which gives rise to a very slight charge separation and thus an electrical potential. Because of active ion transport across cell membranes, large concentration differences on the two sides of the membrane develop, and concentration-dependent diffusion occurs. Thus, diffusion of the various cations and anions at different rates across the membrane gives rise to a diffusion potential. An equation was developed by Goldman (1943) which has been used to assess whether the electrical potential difference across cell membranes is, in fact, a diffusion potential (Higinbotham, 1970). The Goldman voltage equation is as follows: ItT E=-In

F

+ +

+ PcJCli] + other ions + Pc~[Clo]+ other ions

P,[K,] P,,[Nao] P K ( K ~ ] P~.[Nail

where P is the passive permeability coefficient for the various ions, and the bracketed ions represent concentrations of the ions on the two sides of the membrane. This equation assumes that the electrical potential gradient within the membrane is linear and that ions move independently of each other (Dainty, 1962). If the membrane potential calculated with the Goldman equation equals the measured membrane potential, it is then concluded that the observed potential is due to a diffusion potential. If a significant deviation occurs, it is then concluded that a part of the membrane potential is due to some other phenomenon (Higinbotham, 1970). There is increasing evidence that the membrane potentials of cells in general are greater than that predicted by the Goldman equation (Slayman, 1970; Thomas, 1972). The evidence for this in higher plants is limited, but the reports by Pierce and Higinbotham (1970) and Higinbotham et al. (1970) certainly indicate that this is true for the oat coleoptile. In this tissue, the measured electrical potential difference was -1 10 mV and the diffusion potential, estimated with the Goldman equation, was only -37 mV. It was also shown that cyanide and DNP caused a rapid decrease in the membrane potential. In the presence of 1 mM cyanide the measured electrical potential was -42 mV, which is nearly the same as the predicted diffusion potential. Thus, the membrane potential in the oat coleoptile seems to consist of both a diffusion potential and a metabolic-driven potential which can be eliminated almost immediately by respiratory inhibitors. A similar situation appears to exist for various algae, fungi, and bacteria (Slayman, 1970). The metabolic component that contributes to membrane potentials is generally believed to be due to ion pumps that carry a net charge (ie., electrogenic pumps) across the membrane. An electrogenic HCOs- influx pump has been suggested for Chara australis (Hope, 1965); however, Spanswick (1970) has obtained evidence which indicates that this may

T. K. HODGES

180

not be true. Evidence has also been presented that indicates that an electrogenic C1- influx pump exists in Nitella cluvata (Barr, 1965) and Acetabularia mediterrunea (Saddler, 1970). Kitasato ( 1968) has also postulated that Nitella possesses an electrogenic H+ extrusion pump and Pitman (1970) has also concluded that barley roots have an electrogenic H' efflux pump. Additional evidence concerning electrogenic ion pumps has been summarized by Higinbotham (1973), and it seems that such pumps contribute directly to the membrane potential of plant cells. Thus, the electrical potential difference across cell membranes is thought to be due to both a diffusion potential and a potential generated by the operation of the ion pumps. IV.

Kinetics and Selectivity of Ion Absorption

Absorption rates of inorganic ions by roots increase as the external ion concentration increases until an apparent saturation occurs. This saturation, along with the selective nature of ion absorption (Hoagland and Davis, 1929; Collander, 1941) served as the basis for the ion-carrier concept (Osterhaut, 1935; van den Honert, 1937). In 1952, this concept was extended by Epstein and Hagen (1952) when they employed the Michaelis-Menten enzyme kinetic analysis to quantitatively describe ion absorption by barley roots. In the ensuing 20 years, much effort has been devoted to utilizing this analysis, and the various findings have recently been discussed in detail by Epstein (1972a, 1973). I will summarize only the salient points and then consider some relatively new concepts that strongly suggest that only a single cation carrier and a single anion carrier could adequately account for the kinetics, as well as the selectivity, of ion transport into roots. It was recognized very early that absorption of ions could not be described by a simple Michaelis-Menten treatment because ion absorption, over large concentration ranges, did not saturate (Epstein and Hagen, 1952; Leggett and Epstein, 1956). Lineweaver and Burk (1934) and Eadie (1942), Hofstee (1952) plots of ion absorption data resulted in curved lines rather than a single straight line as predicted by MichaelisMenten kinetics (Hagen and Hopkins, 1955; Leggett and Epstein, 1956; Fried and Shapiro, 196 1) . These results were interpreted as indicating that two mechanisms or two sets of carrier sites existed for the transport of a single ion; one carrier having a high affinity for ions and being functional when the external concentration was low and a second carrier, having a low affinity for ions and being functional at higher external concentrations (Fried and Noggle, 1958; Epstein, 1966). Epstein and associates (see Epstein, 1972a, 1973) have shown that absorption in the low concentration

ION ABSORPTION BY PLANT ROOTS

181

range (0-1 mM) does saturate and can be adequately described by Michaelis-Menten kinetics (for barley roots the K,,, for K+ is about 0.01 mM and V,,,.,,is about 10 pmoles per gram fresh weight per hour), and they have referred to this as mechanism I (see Fig. 2 ) . But in the high concentration range (1-50 mM), a true saturation does not occur and the absorption isotherm is not smooth, but “bumpy” or heterogeneous (Elzam et al., 1964; Epstein and Rains, 1965; Epstein, 1966; see Fig. 2). Epstein refers to absorption in this range as mechanism 11.

Ion Concentration (mM)

FIG. 2. Diagrammatic representation of the velocity of ion influx into roots as a function of the external ion concentration.

The most thorough characterization of the kinetics of ion absorption has been for K+, Na+, and C1- in barley roots (Epstein, 1972a, 1973). Mechanism I is highly specific for K+ and C1-, providing Ca2+is present in the absorption solution (Jacobson et al., 1950; Epstein, 1961). Other monovalent cations and anions, except for Rb+ and Br-, respectively, have little effect on K+ and C1- absorption. This specificity is lost in the absence of Ca2+and ions and like Na+ or H+ will interfere with K+ absorption. K+ absorption by mechanism I is virtually unaffected by the counter anion; K+ absorption rates are the same in the presence of the rapidly absorbed C1- ions or the slowly absorbed SO,’- ion (Epstein et al., 1963). Mechanism I1 is quite different. It is more specific for Na’ than K+, and Ca2+ inhibits the absorption of these ions (Rains and Epstein, 1967a,b). The nature of the anion was also shown to be important in the high concentra-

182

T. K. HODGES

tion range; K+ or Na’ absorption from K,SO, or Na,S04 is much less than from KC1 or NaCI. The kinetics and selectivity of K+ and Na+ transport in roots of several other species is similar to that found for barley roots; however, some differences do exist (Fried and Broeshart, 1967; Gauch, 1972; Epstein, 1972a, 1973). The complexity of ion absorption kinetics and the various ion interactions in roots are not easily interpreted, and they have led to considerable debate (Laties, 1969; Epstein, 1973). Bacteria have been suggested to be responsible for absorption at low concentrations (Barber, 1966), but this seems to have been ruled out using roots grown and handled aseptically (Epstein, 1968, 1972b). Absorption in the high concentration range has been suggested to be a concentration-dependent diffusion phenomena (see Laties, 1969). However, at least for C1-, transport over the entire concentration range (up to 60 mM) is against the electrochemical gradient (Gerson and Poole, 1972) and therefore active. Also, metabolic inhibitors impair transport at both low and high external ion concentrations (Toni and Laties, 1966a; Rains and Epstein, 1967a; Ordin and Jacobson, 1955). Torii and Laties (1966a) and Luttge and Laties (1966, 1967) concluded that mechanism I is located at the plasma membrane and mechanism I1 is located at the tonoplast. Welch and Epstein (1968, 1969), on the other hand, concluded that mechanism I and I1 were located at the plasma membrane. Recently Nissen ( 1971) has suggested that a single mechanism, rather than two, is responsible for the transport of sulfate into barley roots and leaves, and that this mechanism resides in the plasma membrane. He suggested that the carrier undergoes phase transformations, and changes in K,,, and V,,la., at certain critical external concentrations. From these various interpretations, it is apparent that the kinetics of ion transport are complex and that controversy exists. However, if one considers the kinetic studies along with the evidence concerning which ions are actively transported (see Section 111), three observations seem to be particularly important. First, all anions are actively pumped inward across the plasma membrane and some cations, like Na+, seem to be actively extruded across the plasma membrane (Higinbotham et al., 1967). Second, all the cations and all the anions exhibit influx kinetics that are of the pseudo-saturation type. This results in the kinetic constants, K , and V,,,,, continually increasing as the external ion concentration increases, and in certain cases both cations and anions exhibit the “bumps” in the absorption isotherm (Hagen and Hopkins, 1955; Hagen et al., 1957; Fried and Noggle, 1958; Fried et al., 1961; Noggle and Fried, 1960; Hodges and Vaadia, 1964; Bange and Meijer, 1966; Weigl, 1967, 1970; Penth and Weigl, 1969; Nissen, 1971; Leonard and Hodges, 1973) [also see reviews by Laties (1969) and Epstein (1973) for their compre-

ION ABSORPTION BY PLANT ROOTS

183

hensive studies]. Thus, active inward anion transport appears to involve carriers (two or more?) and cation entry also appears to involve carriers (two or more?), but the cation transport is supposedly passive. Furthermore, since some studies show cations to be actively extruded, this presumably means that cation efflux is carrier mediated. This, of course, implicates a rather bewildering array of different carriers. The third important observation is that the selectivity of transport changes as the external ion concentration increases (Epstein, 1966, 1973). All these experimental observations, complex as they seem, can be readily accounted for by a single ion carrier. The basis for this view is the similarity between ion transport kinetics and cooperativity kinetics of single enzymes (Monod et al., 1963; Koshland, 1970). Kinetics of single enzymes are basically of 3 types (Koshland, 1970). One is the standard Michaelis-Menten kinetics which exhibit a true saturation when velocity is plotted as a function of substrate concentration (i.e., v vs S) . A second is positive cooperativity kinetics which yields a sigmoidal or S-shaped curve in the v vs S plot. The third is negative cooperativity kinetics which shows a pseudo-saturation curve in the v vs S plot. A fourth type of kinetics yields a “bumpy” isotherm in the v vs S plot, but this is believed to be primarily due to negative cooperativity with a minor component of positive cooperativity kinetics (Levitski and Koshland, 1969). A model to account for these various types of kinetics has been proposed by Koshland (1970). The model assumes a multisubunit enzyme with each subunit possessing identical binding sites for a particular ligand (e.g., substrate, activator, or inhibitor). Ligand binding to the first subunit, however, induces a conformational change (Gerhart and Pardee, 1962; Koshland, 1969) which alters or distorts the other subunits sufficiently to change the kinetic characteristics of their binding sites; with negative cooperativity the K,, increases, and with positive cooperativity the K , decreases. Thus, with negative cooperativity, binding of the first ligand makes it more difficult for the second, binding of the second makes it more difficult for the third, etc. So, with increasing ligand concentration the velocity of the reaction approaches a maximum rate or saturation more slowly than a reaction where no subunit interaction occurs, i.e., one possessing Michaelis-Menten kinetics. Because of the decreasing affinity of the subunits as the ligand concentration increases, Lineweaver-Burk plots of negative cooperativity kinetics are always concave downward curves rather than straight lines, and similarly Eadie, Hofstee plots yield curves instead of the straight lines typical of a Michaelis-Menten reaction (Koshland, 1970). The kinetics of ion transport are virtually identical to the kinetics described as negative cooperativity for single enzymes (Koshland, 1970).

T. K. HODGES

184

Lineweaver-Burk and Eadie, Hofstee plots of absorption data always yield curves when a large concentration range is examined (see all the references cited previously that show the pseudo-saturation kinetics and also see Fig. 3 ) . Thus, as the external ion concentration increases, the K , and V,,, for ion transport continually increases. Additionally, it has been found that the Hill coefficient (Hill, 1910) for 4*K+transport into oat roots is 0.56 (Leonard and Hodges, 1973), which is characteristic of negative cooperativity kinetics (Koshland, 1970). Thus, it would seem that the seemingly

I

I

I

I

FIG. 3. Eadie, Hofstee plot of “K’ influx into oat roots. (From Leonard and Hodges, 1973.)

complex kinetics of ion transport could be accounted for by a single carrier consisting of several identical subunits. In keeping with the Koshland (1970) model, ion binding to the first subunit would induce a conformational change, and this would distort the other subunits such that their affinity for ions would decrease. This would bring about the increasing Km’s as the ion concentration is increased. Overall, the negative cooperativity model accounts for ion transport kinetics, but due to the “bumps” in the absorption isotherms, an additional component of positive cooperativity could also be involved. This model for explaining ion transport kinetics is quite similar to the phase transformation model of Nissen (1971), however, the present model provides an explanation for the changing kinetic patterns which occur.

ION ABSORPTION BY PLANT ROOTS

185

A single carrier having binding sites with varying affinities for ions could also account for the selectivity of ion transport. For example, it has been shown that the specificity of alkali ion binding to anionic groups of glass electrodes is determined by the electric field strength of the negative site (Eisenman, 1961, 1962), and this has been shown to be valid for all kinds of anionic groups on many types of substances including resins, clays, artificial membranes, and numerous biological systems (Diamond and Wright, 1969). Eisenman showed that for the 5 alkali cations, only eleven selectivity sequences (out of a possible 120 permutations) occur as the binding site field strength changes from a low to a high value. These sequences are as follows: I I1 I11 IV V VI VII VIII IX X XI

> Na+ > Li+ > Na+ > Li+ Rhf > K+ > Cs+ > Na+ > 12 K+ > Rb+ > Cs+ > Na+ > Li+ K+ > Rh+ > Na+ > CY+> Li+ K+ > Na+ > Rb+ > Cs+ > Li+ Na+ > K+ > Rhf > Cs+ > Li+ Na+ > K+ > Rb+ > Li+ > Cs+ Na+ > K+ > Li+ > Rb+ > Cs+ Na+ > Li+ > K+ > RIP > Cs+ Li+ > Na+ > K+ > Rb+ > Cs+ Cs+ > Rb+ > K+ Rbf > Cs+ > K+

Sequence I is in the order of increasing apparent hydrated size and Sequence XI is in the order of increasing nonhydrated size. In each of the intermediate sequences, one pair of cations shifts positions. The basis for these selectivity patterns is the relative free energy differences between ion: site and ion :water electrostatic interactions. Thus, the cation preferred by a specific negative site will be that cation which experiences the greatest decrease in free energy when its nearest neighbor becomes the negative site rather than water. When the negative site has a very strong electric field strength, the free energy differences between ion :site and ion: water interactions is such that the cation with the smallest ionic radius will be preferred and thus the selectivity pattern will be that shown in Sequence XI. But, if the negative site has a weak electric field strength the free energy differences between ion:site and ion:watcr interactions is such that the largest nonhydrated cation, which has the lowest free energy of hydration, will be preferred and the order of selectivity will be that shown in Sequence I. Thus, when the electric field strength of the negative site is very weak, Sequence I is preferred, and as the electric field strength of the negative site increases, the order of specificity of ion binding progressively shifts until at very high electric field strengths, Sequence XI is the order of preference. Eisenman also showed that the selectivity for H+ relative to the

186

T. K. HODGES

alkali ions is also dependent on the field strength of the binding site. At high field strengths, H+ is preferred over the alkali ions and at low field strengths, the alkali ions are preferred over H+. The basis for selective ion transport by plants is almost sure to reside in the electric field strength of the ion binding sites and in shifts in the electrical strength of the sites. For example, in barley roots, the preference for K+ over Na+ at low external concentrations and the reverse at high external concentrations (Epstein, 1961; Rains and Epstein, 1967a,b) indicates that the field strength of the binding site increases as the external ion concentration increases. A change in the field strength of the binding sites could be brought about by conformational changes in carrier subunits as described previously. The shift from a low to a high field strength, with sequential ion binding, would also bring about a continually increasing preference for Ht by the binding sites. This could account for the continually decreasing affinity, or increase in apparent K,, for the alkali cations as the external concentration increases. There are numerous reports for the selectivity of ion absorption by plants where two or three of the alkali cations have been considered (Collander, 1941; Fried and Broeshart, 1967), but very few where all five of the alkali cations have been studied. Steward and Mott (1970) reported an order of alkali cation preference by carrot cells that corresponds to Sequence VI. In a very thorough study, Jacobson et al. (1960) determined the effect of both pH and Ca2+on the absorption of the alkali ions by barley roots. In the presence of Ca2+and at pH 7 the preferred sequence was Kt > Rb+ > Na’ > Cst > Lit (i.e., Sequence V ) . As the pH decreased to 3, in the presence of Ca2+,a shift occurred such that the preferred sequence was Rb+ > K > Cs’ > Nat > Li+ (i.e., Sequence 111). It was not possible to determine from their figures whether Sequence IV occurred. This effect of H+ on changing the selectivity pattern of transport is analogous to the effect of Ht on the selectivity pattern of alkali ion binding to glass electrodes (see Diamond and Wright, 1969). The effect of increasing the proton concentration is to reduce the “effective” negative charge strength of the binding site. The effect of Ca2+on the selectivity is complex because of its association with various negative charges, but it too appeared to alter the “effective” field strength of the transport sites since selectivity was shifted from the higher to the lower sequences in barley roots (Jacobson et al., 1960). The CaZt-induced specificity for Kt over Nat at low external concentrations (Epstein, 1973) would also be consistent with this interpretation. An alteration in the “effective” field strength by Ca2+might also be the basis for the anomalous effect of Ca2+on Kt absorption in barley and wheat roots (Hiatt, 1970a,b) as well as the promotive effect of CaZt on K+ transport under some conditions (Viets, 1944; Overstreet et al.,

ION ABSORPTION BY PLANT ROOTS

187

1952; Kahn and Hanson, 1957; Epstein, 196 1 ), and its inhibition in others (Handley et al., 1965; Elzam and Hodges, 1967). Eisenman ( 1965) has further shown that halide specificity by fixed positive charges is also governed by the relative free energy differences between ion:site and ion: water interactions. Of the 24 possible selectivity sequences, only seven occur commonly. Diamond and Wright (1969) have cited some deviations from the main seven orders and discuss why these sometimes occur. The normal seven are as follows: I

I1

I11 IV V VI

VII

I- > Br- > CIBr- > I- > C1Br- > CI- > ICI- > Rr- > IC1- > Br- > FCI- > F- > Br-

F- > CI- > Rr-

> F> F> F>P > I> I> J-

A site with a very strong electric field would prefer the ion having the smallest nonhydrated radius, F-, and Sequence VII would be the order of specificity. A very low field strength site would prefer the most nonhydrated ion, I-, and Sequence I would be preferred. In roots, C1- is generally absorbed at about the same rate as Br- (Epstein, 1953; Boszormenyi and Cseh, 1961, 1964) or slightly faster (Elzam and Epstein, 1965) and both are absorbed more rapidly than either F(Venkateswarlu et al., 1965) or I- (Boszormenyi and Cseh, 1964). Probably one of the sequences from I1 to V correctly describes the normal selectivity pattern for halide absorption by roots. Whether the ion concentration, pH or Ca+affect the selectivity sequence is unknown. The concept of a single cation carrier and a single anion carrier is supported by observations that the total cation or total anion absorption is generally constant from salt solutions that vary in the proportions of the cations or anions (Bear and Prince, 1945; Jacobson et al., 1960; Jackson and Stief, 1965; Hiatt, 1968, 1969, 1970a,b; Pitman et al., 1968). The clearest example of this is for K and Na' absorpion by barley roots (Jackson and Stief, 1965). They found the combined rates of K' and Na' transport were constant even though the individual rates of K+ and Na+ transport were different. These experiments were conducted in the absence of Ca2+.However, Hiatt ( 1970a,b) obtained virtually the same results when Ca2+was present. A single carrier for cation influx would not account for the active efflux of cations, such as sodium (see Section 111), unless the carrier functions in an exchange manner. There is evidence that cation influx is in exchange for H i in low salt roots (Jackson and Adams, 1963; Jacobson et al., 1950; Pitman, 1969) and that a Kt/Kt exchange becomes more prominent as

188

T. K. HODGES

salt saturation is approached (Pitman, 1969; ,also see Poole, 1969). Active sodium efflux might be accomplished by a general cation carrier if exchange is involved and if the carrier has a high affinity for Na+ when the site(s) faces the cytoplasm. All that would be needed to accomplish an active Na+ efflux would be for the carrier site, when facing the cytoplasm, to have a sufficiently high electric field strength that Na+ is preferred over the other cytoplasmic ions. Jeschke (1970) and Pitman and Saddler (1967) have presented evidence that a K+ influx-Na+ efflux does occur in barley roots. This type of exchange, however, is not as specific as it PlOIlnO

MambrOM Li < Csc No< Rb c K Hiqh Ccncentration Li c Csc Rb.r K c Na

I

I CATION CARRIER H+. No'

,TF

OH-, HCO;

ANION CARRIER

FI < I c Br < CI

FIG.4. A model depicting a single cation exchange carrier and a single anion exchange carrier in the plasma membrane of root cells.

is for the active K+/Na+ exchange reaction of mammalian cells (Skou, 1965). This is also evident from the failure of ouabain to inhibit ion fluxes in plants (Hodges, 1966; Cram, 1968b). Cram (1968b) did observe a slight inhibition of Na+ efflux by ouabain, but there was no evidence that the Na+ efflux was tightly coupled to K influx. Thus, energy-dependent cation exchange does occur, but it is not highly specific. It is suggested, however, that it could have sufficient specificity to account for the active Na+efflux at the plasma membrane. A model depicting a single cation carrier and a single anion carrier is shown in Fig. 4. Both carriers are considered to carry out an energy-dependent exchange of external for internal ions. The approximate order of specificity for the alkali cations at low and high external concentrations is shown. Also, the apparent order of halide specificity by the anion carrier is shown. As discussed above, there is evidence for energy-dependent ca-

ION ABSORPTION BY PLANT ROOTS

189

tion exchange. However, evidence for energy-dependent anion exchange is limited. A suggestion of the latter comes from studies that show changes in organic acid levels in the cell when the absorption rates of cations and anions are different (Ulrich, 1941; Jacobson and Ordin, 1954; Hiatt and Hendricks, 1967; Hiatt, 1967a,b). Thus, when inorganic anion absorption exceeds inorganic cation absorption, an anion/HCO,- exchange is a strong possibility. Also, as will be discussed in Section VI, a HC0,- influx coupled to a OH- efflux on the anion carrier is suggested when cation absorption exceeds anion absorption. Finally, the exchange-diffusion of C1- reported by Cram (1968a) and Cram and Laties (1971) might represent a manifestation of the anion exchange carrier. One of the strongest arguments against a single carrier for cations is the shift in preference for Na+ and K+ as a function of aging in stem tissue (Rains, 1969; Rains and Floyd, 1970) and in red beet tissue (Poole, 1791a,b). At low external concentrations freshly cut bean stem slices transport Na+ much more rapidly than K+, but after aging 20 hours in CaS04, K+ is transported more rapidly than Na'. A similar specificity occurs at high concentrations, but it is not as pronounced. Rains (1 969) and Rains and Floyd (1970) interpret these changes in transport specificity as evidence for the development of a K' carrier that is independent of the Na+ carrier. A similar phenomenon occurs in the beet tissue (Poole, 1971a,b). K+ transport is more rapid than Na+ transport in slices aged for 1 day, whereas Na' transport is more rapid than K+ in slices aged for 6 to 7 days. Poole also interprets these data as indicating two separate carriers. In both tissues, however, an altered specificity of the same carrier could conceivably account for the results. Many metabolic changes occur during the washing (aging) period, and alterations in the membrane lipids or proteins could alter the molecular environment of the carrier to such an extent that the charge density or field strength of the binding sites would undoubtedly be altered. Because such a change would alter ion selectivity, one carrier could probably account for the results. The model of ion transport proposed here (Fig. 4 ) represents the combination of two widely different concepts, the negative cooperativity concept of Koshland (1970) and the selectivity concept of Eisenman (1961, 1962). Together they account for most, if not all, of the kinetic and selectivity aspects of ion transport in plants.

V.

Energetics of Ion Transport

Aerobic conditions are essential for nutrient absorption by roots. This has been shown by the pioneering investigations of Steward (1932),

190

T. K. HODGES

Lundegirdh (1934), and Hoagland and Broyer (1936). These studies were followed by demonstrations of parallels between aerobic respiration and nutrient absorption (Lundegdrdh and Burstrom, 1933; Ulrich, 1941; Vlamis and Davis, 1944; Robertson and Turner, 1945; Robertson and Wilkins, 1948). Finally, the finding that respiratory poisons. such as cyanide, azide, and carbon monoxide inhibited ion absorption clearly established the requirement of aerobic respiration for nutrient absorption by plant roots (Ordin and Jacobson, 1955). The precise manner in which aerobic respiration is coupled to ion transport is still uncertain, but many significant observations and interpretations have been made. The first detailed interpretation of the link or couple between respiration and ion transport was presented by Lundegdrdh and Burstrom (1933). Lundegdrdh’s concept has been discussed at length (Lundegirdh, 1939, 1945, 1955), and only the major features will be consided here. In essence, he postulated that during the oxidation of reduced compounds, electrons were transferred through a chain of cytochromes and associated with this electron flow was a reversed flow of anions along the cytochrome chain. Cations were considered to enter cells passively in order to maintain electrical neutrality. Lundegirdh’s concept met with disfavor when it was realized that the cytochrome chain was localized in mitochondria and not in the plasma membrane. The concept was also inconsistent with the finding that the phosphorylation uncoupler, 2,4-dinitrophenol (DNP), which eliminates the formation of ATP but does not inhibit electron transfer through the cytochrome chain, is a powerful inhibitor of ion absorption (Robertson et al., 1951 ) . The latter finding was taken as evidence that ATP was the intermediary link between aerobic respiration and ion transport. This view was further supported by subsequent findings that arsenate (Ordin and Jacobson, 1955; Higinbotham, 1959; Weigl, 1963, 1964) and oligomycin (Hodges, 1966; Jacoby, 1966; Bledsoe et al., 1969), which interfere with ATP formation, were also potent inhibitors of ion absorption. Thus, it would appear that ATP is the actual energy source for ion transport; however, some observations indicate that this may not always be so. Evidence discounting ATP as the source of energy for ion transport has come from tissues other than roots with the exception of storage root tissue. With aged root tissue of carrots (Atkinson et al., 1966) and beets (Polya and Atkinson, 1969), various inhibitors such as a nitrogen atmosphere, uncouplers and ethionine (an ATP-trapping agent) did not affect ion absorption and the levels of ATP in the tissue in parallel. Thus, the corelation that one would expect if ATP were the energy source did not exist, and these authors concluded that electron transfer reactions, rather than ATP, were involved in ion absorption. This interpretation assumes

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that there are no cellular pools or compartments of ATP, i.e., all the ATP in the cell is considered to be available for transport. This may not be so, and one must question whether total tissue levels of ATP would be expected to show correlations with ion transport rates. However, Cram (1969a) has also shown that C1- influx across the plasma membrane of carrot cells is not inhibited by either carbonyl cyanide rn-chlorophenyl hydrazone (CCCP) or oligomycin but is inhibited by anaerobiosis. In comparing these results to those of Atkinson et al. (1966) concerning ATP levels in the tissue, Cram also concluded that active C1- influx at the plasma membrane was more closely linked to redox reactions than to ATP per se. At the tonoplast, CCCP, oligomycin and anaerobiosis all inhibited C1- influx from cytoplasm to vacuole which would appear to implicate ATP. However, a longer time was required for oligomycin to inhibit C1influx than to bring about a decrease in tissue levels of ATP (Atkinson el al., 1966), and Cram suggested that a high energy intermediate (presumably of mitochondria1 respiration) rather than ATP was the likely energy source for C1- transport at the tonoplast. Light stimulates ion transport in green tissue (leaves and algae). Presumably the energy for ion absorption is derived from some aspect of photosynthesis (in addition to respiration). In these systems there have been claims that ATP is the energy source for ion transport (mostly for cation transport) (Rains, 1968; Nobel, 1969, 1970) as well as claims that electron transfer reactions are more closely linked to ion transport (mostly for anion transport) (MacRobbie, 1965, 1966; Raven, 1967, 1969; Nobel, 1969). In segments of corn leaf tissue, Rains (1967, 1968) showed that the light-stimulated K+ transport was not inhibited by 3- ( 3,4-dichlorophenyl) -1 ,I-dimethylurea (DCMU) . This indicated that photosystem 11, which is inhibited by DCMU, was not necessary for K+ transport. This result, along with the effect of other inhibitors, led Rains to conclude that ATP produced by cyclic photophosphorylation (photosystem I) provided the energy for K+ transport. In pea leaf tissue, Nobel (1969) showed that light stimulated both K+ and C1- absorption. Bicarbonate ions markedly enhanced the light-driven K+ absorption and this was thought to be due primarily to the absorption of HC0,- (although this was not measured) down a gradient which resulted from light-stimulated CO, fixation; K+ presumably entered passively as an electrical balance for the negatively charged HC0,-. Absorption of K+ was inhibited by the phosphorylation uncoupler, p-trifluoromethoxy carbonyl cyanide phenylhydrazone (tri-F1CCP). Nobel suggested this could be due to a diminished supply of ATP and a consequent curtailment of CO, fixation which would in turn diminish the gradient for HC0,- and thus the driving force for K+ entry. This interpretation could also account for the results obtained with corn leaves by

192

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Rains (1968). Chloride transport in pea leaves was little affected by the uncoupler tri-F1-CCP, indicating that ATP was not the energy source for C1- transport. DCMU did inhibit C1- absorption, and it was concluded that C1- transport was somehow closely coupled to the noncyclic electron transfer reactions. Thus, with regard to light-driven ion transport in leaf tissue, K+ transport appears to depend on ATP, either directly or indirectly, whereas C1- transport may be more closely linked to the photosynthetic electron transfer reactions. The energetics of ion transport in several algae have been carefully reviewed by MacRobbie (19,70), and I will only summarize the main points. In the two species studied most thoroughly (Nitella translucens and Hydrodictyon africanurn), ATP seems to be the energy source for cation transport but not for anion transport (MacRobbie, 1965, 1966; Raven, 1967, 1968, 1969). In both organisms, K and C1- are actively pumped across the plasma membrane and Na+ is actively extruded. The active fluxes of all 3 ions are stimulated by light, and K+ influx is coupled to Na+ eflux. The Kt- Na+ exchange in the algal cells is inhibited by ouabain which also inhibits the active K+ - Na-bexchange in animal cells (Skou, 1965). Also, this exchange is inhibited by uncouplers (DNP, CCCP) and phosphorylation inhibitors (phlorizin and Dio 9). All these results implicate ATP in K+ influx and Na+ efflux. Influx of C1-, on the other hand, was less sensitive to the uncouplers and phosphorylation inhibitors than either Kt influx or CO, fixation. Additionally, the blocking of photosystem I1 with DCMU inhibited C1- influx. Finally, it was shown in experiments with red and far-red light (Raven, 1967) that cation transport could be driven solely by photosystem I but C1- transport required both photosystems I and 11. From these results it was concluded (see MacRobbie, 1970) that C1- influx required something other than ATP; i.e., it was either coupled directly to electron transfer reactions or was dependent on some reduced product. From the foregoing discussions, it seems justifiable to conclude that ATP serves as the energy source for cation transport, but in certain tissues, especially those having a photosynthetic capability, a separate energy source is used for anion transport. In roots, there is no evidence that cation and anion transport require different energy sources. On the basis of the arsenate and oligomycin inhibition of both cation and anion transport, the energy source would appear to be ATP; however, the contrasting results with the fleshy tissues of beet and carrot indicate that a separate or alternative energy source may be involved. Additional evidence that ATP is the energy source for ion transport in roots is provided by the finding that the plasma membrane and tonoplast

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of root cells have ATPase activity. This has been shown histochemically by Poux (1967) and Hall (1969, 1971a) and we (Hodges et al., 1972; Hodges and Leonard, 1973) have shown that isolated plasma membranes of oat roots possess an ion-stimulated ATPase. The association of this enzyme with the plasma membrane is especially interesting since it could represents the mechanism of energy coupling between ATP and ion transport. It is well documented that a plasma membrane-bound ATPase participates in the coupled transport of Na+ and K+ in animal cells (Skou, 1965). In roots of cereals we have obtained considerable evidence that the ATPase mentioned above is involved in ion absorption. It was first shown that crude preparations of membranes, i.e., differential centrifugation fractions, contained ATPase activity that required Mg", but was further stimulated by a variety of monovalent salts, such as KCl, NaCl, K,SO, (Fisher and Hodges, 1969). Activation of the ATPase by monovalent salts depends on Mg"; in the absence of Mg2+,the monovalent salts are ineffective. Mn2+will substitute for the Mg" requirement, but other divalent cations are less effective (Leonard and Hodges, 1973). Fisher et al. (1970) have shown that the component of the ATPase activated by K+ or Rb+ is highly correlated with K+ or Rb+ absorption in roots of 4 plznt species (Fig. 5 ) . These results suggest that the ATPase is involved in ion absorption. In subsequent studies it was found that the ATPase that is stimulated by monovalent ions is associated with the plasma membranes of oat root cells (Hodges et al., 1972; Hodges and Leonard, 1973; Leonard et al., 1973). The ATPase is very specific; other nucleoside triphosphates are hydrolyzed at less than 5 % of the rate of ATP. In experiments using the purified plasma membranes (Leonard and Hodges, 1973), the ATPase was found to be primarily activated by cations with a selectivity preference at 50 mM salt concentrations of K+ > Rb+ > Na+ > Cs+ > Li+ (Sequence V in the Eisenman selectivity scheme). Preliminary studies indicate this to be the order of specificity for transport at 50 mM concentrations in oat roots (Fisher, 1969; H. Sze and T. K. Hodges, unpublished). Organic cations (tris, choline, and tetramethyl ammonium ions) are also capable of activating the ATPase, but they were less effective than the inorganic cations (Leonard and Hodges, 1973). Ratner and Jacoby (1973) have recently reported that organic cations are as effective as the inorganic cations in activating ATPases. This result was probably due, however, to their use of crude membrane preparations which are known to contain several different membrane-bound ATPases (Hodges and Leonard, 1973; Leonard et al., 1973). In addition, the pH of their ATPase assays was 8.2, but the pH optimum for K' stimulation of the plasma membrane ATPase is 6.5 (Leon-

T. K. HODGES

194

ard and Hodges, 1973). Whether the organic cation activation of the plasma membrane ATPase (Leonard and Hodges,, 1973) is related to organic cation absorption is unknown. The kinetics of the plasma membrane ATPase have been determined for ATP, Mg2+,and K+ (Leonard and Hodges, 1973). ATP and Mg2+activation of the ATPase exhibited typical Michaelis-Menten kinetics, and the K , values were 0.38 and 0.84 mM, respectively. K+ activation of the 33

0

7

Rb* or K' CONCENTRATION (mM)

FIG. 5 . Upper: Influx of K+ (oats) or Rb' (barley, wheat, corn) into roots as a function of the external concentration of K+ or Rb'. Lower: K+ or Rb+-stimulated ATPase activity of membrane fractions obtained from roots of the various species as a function of K' or Rb' concentration A-A, barley; 0-0, oats; X-X, wheat; 0-0, maize. (From Fisher and Hodges, 1969.)

ATPase was not typical of Michaelis-Menten kinetics since a saturation did not occur for K+ concentrations from 0.01 to 100 mM (see Fig. 6). Instead, the K, for K+ continually increased as the K concentration increased, and, as discussed in Section IV, these kinetics are described as negative cooperativity (Koshland, 1970). The different Km's for K+ do not appear to result from several ATPases having different affinities for K+ since the affinities for both Mg2+and ATP did not vary; the latter might be expected if different enzymes were involved. The similarity in the kinetics of K+ activation of the plasma membrane ATPase of oat roots and

195

ION ABSORPTION BY PLANT ROOTS

K+ absorption by oat roots is apparent when one compares Figs. 3 and 6. In view of the negative cooperativity kinetics for K+ activation of the ATPase, the enzyme should consist of interacting subunits according to the Koshland model. We have not determined whether this is the case, but it is interesting that the ATPase of mitochondria consists of at least 11 subunits (MacLennan, 1970) and the ATPase of chloroplasts have been shown to consist of five subunits (Nelson et al., 1973).

I

0

I

10

I

I

20

30

I

40

50

Velocity KCI (mM)

FIG. 6. Eadie, Hofstee plot of the K+-stimulatedATPase activity of plasma membranes obtained from oat roots. (From Leonard and Hodges, 1973.)

In the last 10 years there have been several other reports of ATPase activity in cell free homogenates of plant tissue (Brown and Altschul, 1964; Brown et al., 1965; Dodds and Ellis, 1966; Gruener and Neumann, 1967; Neumann and Gruener, 1967; Atkinson and Polya, 1967; Hall and Butt, 1969; Hansson and Kylin, 1969; Horowitz and Waisel, 1970; Kylin and Gee, 1970; Sexton and Sutcliffe, 1969; Hall, 1971b; Leonard and Hanson, 1972; Ratner and Jacoby, 1973). Of these reports, only the ones by Leonard and Hanson (1972), Hansson and Kylin (1969), and Kylin and Gee (1970) seem to illustrate a potential role of the ATPase in transport, whereas the paper by Ratner and Jacoby (1973) claims that the

196

T. K. HODGES

enzyme is not involved in absorption. Leonard and Hanson (-1972) found that the K+-stimulated ATPase of a membrane fraction of corn roots increased as a result of washing (aging) the roots and that this correlated with an increased capacity for ion absorption. However, the increased ATPase activity caused by washing was not as great as the increased ion absorption rates, so it is not clear whether the two phenomena were related. Hansson and Kylin (1969) and Kylin and Gee (1970) report that the ATPase activity of membrane fractions of sugar beet and mangrove is stimulated more by combinations of Nat and K+ than by either ion alone. This is an interesting finding because it is similar to that reported for animal cells (Skou, 1965); however, it is not clear whether the plant enzyme studied by Kylin and associates is involved in transport. It should be pointed out here that there are at least 5 membrane-associated ATPases in oat root cells (Hodges and Leonard, 1973; Leonard et al., 1973), and presumably this would be true for the beet and mangrove cells. Thus, the possibility exists that the Na+ Kt stimulated ATPase activity found in Kylin's studies was due to two different membrane-bound ATPases. With the ATPase of the purified plasma membrane fraction of oat roots, various combinations of K+ and Na+ were not significantly better than either ion separately (Leonard and Hodges, 1973). It may also be relevant that oats are glycophytes whereas both the sugar beet and mangrove are halophytes, and Horowitz and Waisel ( 1 970) have obtained evidence that the Na+ stimulated ATPase activity of membrane fractions from these two groups of plants is somewhat different. The disparity between organic cation stimulation of ATPase activity and cation absorption by roots led Ratner and Jacoby (1973) to question the role of an ATPase in ion absorption. However, the basis for this view is questionable since their studies involved the use of impure membrane preparations, and an assay pH that may have discriminated against the plasma membrane ATPase. Although reservations have been expressed (Ratner and Jacoby, 1973), the evidence that an ATPase functions in ion absorption by roots can be summarized as follows: (1 ) a high correlation exists betwen K+ or Rb+ absorption and the K+ or Rb+ stimulated ATPase activity in roots of 4 plant species (Fisher and Hodges, 1969; Fisher et al., 1970). ( 2 ) The ATPase is cation-activated, and it is specific for ATP (Hodges et al., 1972; Leonard and Hodges, 1973). ( 3 ) The ATPase is on the plasma membrane (Hodges et al., 1972). (4) The kinetics of K+ activation of the plasma membrane ATPase is virtually identical to the kinetics of K+ absorption by oat roots (Leonard and Hodges, 1973). Taken together, these results strongly support the concept that ATP provides the energy for transport and that the plasma membrane ATPase is responsible for the energy coupling involved in ion transport.

+

ION ABSORPTION BY PLANT ROOTS

197

The mechanism of energy transfer, via an ATPase, to ion transport has been most thoroughly studied in mitochondria (Vasington and Murphy, 1962; Hanson and Hodges, 1967; Moore, 1971) and chloroplasts (Packer et al., 1970; Dilley, 1971). In these organelles, it has been shown that either ATP or the electron transfer reactions can provide the energy for ion transport (Hodges and Hanson, 1965; Elzam and Hodges, 1968; Packer et al., 1970). With either energy source a common high energy intermediate state is produced which is very closely coupled to ion transport. The formation of the high energy state can be depicted as follows: Uncouplers

Electron transport P hospho ry lat ion inhibitors

Electron transport inhibitors Ion transport

Ion transport driven by electron transport reactions is inhibited by substances such as antimycin A or cyanide, but not by phosphorylation inhibitors, such as oligomycin or phlorizin. When AT? is the driving force for transport, the phosphorylation inhibitors a-e effective in blocking ion transport but the electron transport inhibitors are ineffective. Uncouplers such as DNP or CCCP inhibit ion transport when either electron transport or ATP is the energy source, and this is generally believed to be due to the hydrolysis or dissipation of the intermediate high energy state. The high energy intermediate state is believed by some to be a proton gradient across the membrane (Mitchell, 1961, 1966; Robertson, 1960, 1968), a specific compound having a high free energy of hydrolysis (Slater, 1953; Chance and Williams, 1955), a specific conformational state of the membrane or proteins within the membrane (Dilley, 1971; Green et al., 1968), or a combination of these alternatives (Hanson et al., 1972). Presently, it is uncertain which of these concepts is correct (Slater, 1971); however, the proton gradient has received the most support with respect to how it might function in driving ion transport (Mitchell, 1966, 1968; Robertson, 1968; Chappell and Haarhoff, 1967). The formation of a proton gradient across a membrane by the action of an ATPase has been discussed by Mitchell ( 1961, 1966, 1968). In essence, the 2 sides of the membrane are thought to be sufficiently different that the components of water (H+ and OH- or 2H+ and 0 2 - ) involved in the hydrolysis of ATP are believed to approach the ATPase

T. K. HODGES

198

from different sides of the membrane (Mitchell, 1961). In its simplest form, this leaves a H+ on one side of the membrane and an OH- on the other. Depending on the reactive elements of H,O, the magnitude of the pH gradient generated by ATP hydrolysis might be different, e.g., Mitchell's ATPase I and I1 (1966, 1968). The main feature, however, is that a pH and charge gradient is created across the membrane, and, if the membrane is impermeable to H+ and OH-, this gradient represents a form of energy which can be coupled to endergonic processes. Mitchell (1366, 1968) suggests that the transport of K+,Ca2+,phosphate, organic acids, ADP, and ATP could be coupled to either H+ or OH- fluxes across the membrane with the mediation of carriers (or porters in his terminology). Chappell and Haarhoff (1967) have obtained evidence for these exchange reactions in mitochondria. The plasma membrane ATPase could conceivably be coupled to ion transport in a manner similar to that observed for ATPase-linked ion transport in the organelles. As mentioned previously, the exact nature of the high energy intermediate state resulting from ATP hydrolysis is uncertain, but the proton gradient concept of Mitchell (1968) can most readily account for a variety of associated ion fluxes. Accordingly, it is proposed in the next section that the monovalent c'ation-activated ATPase of the plasma membrane gives rise to a pH and charge gradient across the plasma membrane which serves to drive anion fluxes across the membrane.

VI.

Proposed Model for Ion Absorption by Roots

In an attempt to reconcile the various observations discussed here, a model is proposed (Fig. 7) that could account for both cation and anion absorption by root cells. This model consists of two main features: (1) A cation-activated A TPase in the plasma membrane. This ATPase brings about the exchange of cations across the membrane, and it generates a charge and pH gradient across the membrane. ( 2 ) An anion carrier that brings about the exchange of anions across the plasma membrane. The internal anions can be either OH- resulting from the pH gradient established by the ATPase or HC0,- ions resulting from aerobic respiration. The ATPase is activated by monovalent cations, and the kinetics of this activation are consistent with the concept that the enzyme consists of subunits which interact (Leonard and Hodges, 1973). Cation activation of the enzyme involves the exchange of an alkali cation for H+ which brings about a conformational change of the cation-subunit complex (Koshland, 1970). This conformational change could move the cation from the outside surface of the membrane to the inside surface of the membrane where it

ION ABSORPTION BY PLANT ROOTS

199

would, in time, exchange for cytoplasmic H'. The initial conformational change of the cation-subunit complex alters or distorts the other subunits of the ATPase such that their electrical field strength is increased (Eisenman, 1962). An increased field strength would increase the affinity of the subunit for H , thus decreasing the overall affinity for the alkali cations. As a consequence of the higher field strength of the binding sites, the preference for the alkali ions is shifted. This accounts for the observed change in selecOutside

Plasma Membrane

Cytoplasm

No, K *

FIG. 7. A hypothetical model depicting how inorganic cations and anions are transported across the plasma membrane into root cells. See text for explanation.

tivity of ion transport as the external concentration is increased (see Section IV) . The ATPase can also give rise to a pH and charge gradient across the membrane (Mitchell, 1961) which represents an intermediate conservation of the energy originally present in ATP. Since a charge separation occurs, the ATPase contributes directly to the electrical potential and is therefore electrogenic. Inhibition of the ATPase by shutting off the supply of ATP or by direct inhibition would cause the electrical potential to fall abruptIy. This accounts for the view that H+ is actively secreted by roots (Pitman, 1970), and for the evidence that ion transport is electrogenic (see Section II,3).

200

T. K. HODGES

The anion carrier exchanges internal OH- for external anions, and this collapses the pH gradient. Thus, inward anion transport uses the energy which was temporarily conserved in the pH gradient. According to the model, the ATPase is directly responsible for cation transport and indirectly responsible for anion transport. However, the anion carrier depends on an internal anion such as OH- or HC0,- and is not necessarily dependent on ATP. Any intracellular reaction that generates excess OH- or HC0,- could drive the anion carrier. For example, the light-driven C1- transporr in green tissue or cells may be a Cl-/OHexchange with the OH- being generated by the chloroplast redox reactions. This possibility is supported by studies which show a light stimulated HC0,-/OH- exchange in green algae (Smith, 1970; Raven, 1970; Lucas and Smith, 1973). In roots, anion/HCO,- and HC0,-/OH- exchanges are probable. This is based on the increase or decrease in organic acids which accompany excess cation or excess anion uptake (Ulrich, 1941; Jacobson and Ordin, 1954; Hurd, 1958; Hurd and Sutcliffe, 1957; Torii and Laties, 1966b; Hiatt, 1967a,b; Pitman, 1970; Zioni et al., 1971). For example, when cation absorption exceeds anion absorption a HC0,-/OH- exchange is likely. When anion absorption exceeds cation absorption an anion/ HC0,- exchange is likely. In the latter situation, the HC0,- would be generated by breakdown of organic acids, and thus anion entry would not be driven by ATP. Direct evidence for this has not been obtained, but one would predict that uncouplers of phosphorylation should have less effect on anion transport than on cation transport. This is true for photosynthetic tissue (see Section V ) , but similar comparisons have not been made with roots. The important point here is that cation transport depends on ATP and the plasma membrane ATPase. But, the anion carrier, and thus anion influx, is driven by internal anions, which can be generated by the action of the ATPase, breakdown of organic acids or, in the case of green tissue, by OH- ions produced by chloroplasts. The relationship between ion fluxes and membrane electrical potentials also deserves further comment. Na+ appears to be actively secreted at the plasma membrane, and K+ is generally close to electrochemical equilibrium (see Section 111). In this model, ATP hydrolysis, via the ATPase, contributes directly to the membrane potential. Since cations activate the ATPase, one would expect to find a close relationship between the electrical potential difference generated by the ATPase and cation transport, and this generally is what is observed for K+, but not for Na+. The basis for active Na+ efflux could reside in the ion binding sites on the ATPase having a high electric field strength following the ion-induced conformational change. A site having a high field strength prefers either H+ or Na+ over K+ (see section IV). Whether a K+/Na+exchange on the binding site at

ION ABSORPTION BY PLANT ROOTS

20 1

the cytoplasmic side of the membrane would induce the carrier to return to its original conformation is unknown, but if this occurred, it could account for Na+ being actively transported back across the membrane. This might also be the basis for the plant ATPase being slightly stimulated by combinations of Na' and K (Hansson and Kylin, 1969; Kylin and Gee, 1970). This model is admittedly speculative, but it is based on the characteristics of ion absorption by a variety of plant organs, tissues, and organelles. In addition, it combines the concepts of negative cooperativity kinetics (Koshland, 1970), the thermodynamic basis for selective ion binding by charged sites (Eisenman, 1962; Diamond and Wright, 1969), an ATPase generated proton gradient (Mitchell, 1961, 1966), and an anion exchange carrier (Mitchell, 1968). Thus, the model represents the integration of several different concepts with a variety of experimental observations. It is, however, a hypothetical model, and many of its features need to be critically evaluated.

VII.

'

Summary

Major advances are being made toward elucidating the mechanism of nutrient absorption by roots. Some of these are as follows: 1. It is now possible to estimate the concentrations of ions in the cytoplasm and vacuoles of root cells. The bidirectional fluxes of ions across both the plasma membrane and tonoplast can be determined. A knowledge of these parameters is permitting the electrophysiologist to evaluate the driving forces responsible for ion movements into and out of root cells. 2. Kinetics of ion absorption by roots is similar to the kinetics of enzyme catalyzed reactions. This is providing insight into the nature of ion carriers. It is suggested here that an ion carrier consists of several subunits, and it is the interaction of these subunits that is responsible for the observed decrease in ion affinities as the external ion concentration is increased. 3. The selectivity of ion absorption by roots is similar to the selectivity of ion binding to glass electrodes. The basis for the latter is the electrical field strength of the binding sites. It is suggested here that variations in the field strength of binding sites on the carriers are responsible for the selectivity of ion absorption by roots. The field strength of the binding sites may be governed by the interaction of carrier subunits, as well as by the molecular environment of the ion carrier, e.g., the lipid and protein composition of the membrane. 4. Aerobic respiration provides the energy for ion absorption by roots.

202

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ATP appears to be the primary energy source for absorption, and an ATPase in the plasma membrane may represent the energy transducing agent between ATP and transport. The possibility of the ATPase being a cation carrier is considered. The possibility of anion absorption being coupled to HC0,- and/or OH- efflux, via an anion exchange-carrier, is suggested. 5 . The plasma membrane of root cells has only recently been isolated. This should facilitate the isolation and identification of ion carriers. In this paper I have primarily concentrated on reconciling the mechanism of ion transport. Hopefully, the ideas and concepts that have emerged will lead to a better understanding of fertilizer usage by crops, the effects of moisture or temperature stresses on nutrient absorption, the unique ability of certain plants to thrive in saline areas, and plant growth in general. ACKNOWLEDGMENTS

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LODGING IN WHEAT, BARLEY, AND OATS: THE PHENOMENON, ITS CAUSES, AND PREVENTIVE MEASURES Moshe J. Pinthus The Hebrew University of Jerusalem, Faculty of Agriculture, Rehovot, Israel

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

........................... ........ A. Stem Lodging and Root Lodging . . . . . . . . . . . . . . . .................... B. Mechanical Aspects of Lodging . . . . . . C. Recovery from Lodging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

11. Description and Causes

111.

IV.

V.

VI.

VII.

...

D. Lodging Caused by Foot-Rot or Root-Rot Diseases . . . . . . . . . . . . . . E. Lodging of Insect-Attacked Culms . . . . . . . . . . . . . . . . . . . . . . . . . . Effects of Lodging on Crop Development and Yield . ......................... A. Methods of Investigation . . B. Effects on Grain Yield . .:. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .................... C. Effects on Grain Quality . . . . . . . D. Effects on Culm Development and Tillering . . . . . . . . . . . . . . . . E. Physiological Effects of Lodging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. Impact of Lodging on Grain Harvest . . . . . . . . . . . . . . . . . . . . . . . . G. Incidence of Diseases in Lodging Crops . . . . . . . . Plant Characters Associated with Lodg A. Culm Characters .................................. B. Root and Crown Characters . . . . . . . ................. .................................. C. Mechanical Prope D. Other Characters . . . . . . . . . . . . . Environmental and Agronomic Factor A. Light and Temperature . . . . . . . . B. Nitrogen Supply . . . . . . . . . . . . . C. Phosphorus, Potassium, and Trace Elements . . . . . . . . . . . . . . . . . . D. Moisture Supply and Soil Aeration . . . . . . . . . . . . . . . . . . . . . . . . . . E. Crop Rotation and Tillage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. Synergistic Effects . . . . . . . . . . ............. Prevention of Lodging . . . . . . . . . . . ............. ....................... A. Cultural Practices . . . . . . . . . . . . B. Application of 2-Chloroethyl T r C. Application of Herbicides and Other Che Breeding for Lodging Resistance . . . . . . . . . . . . . . . . ............ A. Evaluation of Lodging Resistance . . . . . . B. Inheritance of Lodging Resistance and Associated Characters . . . . . . C. Achievements and Prospects of Breeding . . . . . . . . . . . . . . . . . . 209

210 21 1 21 1 213 216 216 217 217 217 220 221 222 222 223

224 226 228

235 236 236 237 238 238 246

210 VIII.

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Increased Exploitation of Yield-Promoting Factors Due to the Prevention of Lodging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256

I.

Introduction

Lodging was long ago recognized to be a severe malady of small grains in most parts of the world. Previous rather comprehensive reviews of this subject were published by Dorofeev and Ponomarev (1970) and by Kohli and Mukherjee ( 1966), Lodging may damage grain yield directly by interfering with dry matter accumulation, and reduce the yield indirectly owing to the difficulties that it imposes on harvest. Lodging may also adversely affect grain quality (Section 111). The severity of lodging and the extent of the losses resulting from it depend on the crop’s environment (see Section V) and on the growth stage at which lodging occurs (Section 111, B, 1) . Generally speaking, favorable growing conditions, promoting crop development and grain yield, will evoke lodging and increase its severity. Consequently, lodging should be regarded as an “abundance disease” which restricts the exploitation of otherwise yield-promoting factors. The conjunction of lodging with rather high yields may result in a serious underestimate of its economic importance. However, the extensive experimentation during the last decade with the lodging-inhibiting chemical 2-chloroethyl trimethylammonium chloride (CCC) indicates that the losses due to lodging may often amount to up to 30% of the grain yield. Considering also other estimates on the frequency and severity of lodging (Ansiaux, 1969; Moore, 1949; Paleev, 1953), it may be concluded that in regions where high grain yields are obtained, the damage due to lodging is at least as great as that due to cryptogamic diseases and insect pests. The past decade should be credited with two outstanding achievements in the control of lodging: The release of short-strawed varieties and the introduction of CCC (Sections VII and VI, B, respectively). However, neither the new varieties nor the application of CCC has eliminated the problem of lodging but has rather concentrated it into a narrower range of conditions and transferred it to a higher level of yields. Another aspect of lodging is its occurrence in eyespot-infested fields (Section 11, D) . The severity of this problem has grown recently in different parts of the world, following intensification of wheat production and its increased part in the crop rotation (Manning, 1967; Mielke, 1970).

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21 1

Complete losses of crops were reported by Witchalls (1970) from southern New Zealand. The dependence of lodging on a great number of environmental factors as well as on numerous plant characters warrants a detailed examination of the phenomenon and its control. This is attempted in the present review. II.

Description and Causes

Lodging is the state of permanent displacement of the stems from their upright position. It is induced by external forces exerted by wind, rain, or hail. It may culminate in the plants being laid flat on the ground, and sometimes involve breakage of the stems. Although bending at the base of the peduncle has also been considered as lodging (Patterson et al., 1957), cereal culms generally lean over at their bases. The culms may remain straight throughout their length or become curved in various forms (Grafius and Brown, 1954). Lodging is often not distributed uniformly throughout an affected field but may be scattered over certain sections or spots. The degree of lodging, i.e., the degree at which the culms lean from the perpendicular, may also vary at different places within the field. The prevalence, together with the degree, determine the severity of lodging. A.

STEM LODGING AND ROOTLODGING

Stem lodging follows bending or breaking of the lower culm internodes, whereas root lodging refers to straight and intact culms leaning from the crown, involving a certain disturbance of the root system. Stem lodging may be caused by hail or by previous damage of the culms by insects or by foot rot, but its occurrence is induced mainly by storm. Stem lodging is restricted to plants that are held tightly by a dry and hard upper soil layer. In moist soil the roots and crowns will yield to the torque created by the wind, and root lodging will develop. In this case cracks parallel to the planting rows, on the side opposite to lodging, can sometimes be observed after the soil has dried again (Fig. 1). Experiments in wind tunnels (Bauer, 1964; Udagawa and Oda, 1967) indicate that in order to cause stem lodging high wind velocities (15-30 m/sec) , which correspond to strong wind or gale, are necessary. Moreover, even under such conditions, as long as the intact culms are moist and turgid, they will rarely break. Consequently, lodging due to fracture of the culms is to be expected only of senescent plants after ripeness (Grafius et al., 1955).

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If the upper soil layer is softened by rain or irrigation, the anchorage of the plants is weakened, and even a light breeze may exert a sufficient torque to induce lodging (Udagawa and Oda, 1967). Rain or sprinkler irrigation may promote lodging also by wetting the plants and thus adding

FIG.1. Soil-crack following root lodging of wheat.

to their weight, which in turn increases the torque. Sprinkler irrigationinduced lodging in nascent stage is illustrated in Fig. 2. The decrease in lodging resistance due to wetting of the upper soil layer can be demonstrated by means of a chain hooked to the head of a plant grown in dry soil. When the soil around the plant is watered, a gradual drop in the number of chain links supported by the culm can be observed. In our own (unpublished) experiments, this drop amounted to about half the initial value before watering.

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It is concluded that root lodging is the predominant type of lodging occurring during the crucial growth stages (Section 111, B, 1 ) and that rain and irrigation, which moisten the soil and thus loosen the anchorage of the plants, are its main causal agents.

B. MECHANICAL ASPECTSOF LODGING The cereal plant is anchored in the ground by its root system, its crown, and by the lower portions (5-30 mm) of the first elongating internodes

FIG. 2. Lodging of sprinkler-irrigated wheat in nascent state (Tirat Zevi, Israel, 1965).

of its culms (main shoot and tillers) which are embedded in the soil. Provided that their anchorage and culms are undamaged, plants are able to support their own weight as long as they are not affected by external forces. However, the plant is subjected to wind, rain, and hail, which exert forces ( p ) operating perpendicularly to the culms, thus inducing a torque which causes bending. Once a culm has been drawn out of its vertical position, the weight of the shoot to which it belongs operates as a force ( f ) which will increase the torque. Moreover, this force will grow as bending proceeds. The external factors which evoke p , especially wind, act predominantly on the head of the plant. Therefore, the torque will affect the whole culm

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and increase gradually from the top down to the basal portion, near the ground, where the lever attains its greatest value. Consequently, the properties of the basal region of the culm are decisive for bending. Since the nodes are too rigid to enable bending, this will occur in the internodes, which will permit more bending the longer they are. The total torque ( T ) will be

where 1, and I , are the levers of the forces p and f, respectively; 1, may be assumed to equal the height of the erect plant up to the center of the head; I , is related to the center of gravity of the shoot which will be located near, below or above the base of the head. The exact location changes somewhat according to the development of the plant. During the period of intensive filling of the grain, after stem elongation has been completed, the center of gravity will move upward, whereas during the later stages of ripening, when the kernels are drying, it will move downward. Average percentages of total shoot weight at the dead-ripe stage were reported by Hancock and Smith (1963) as 42.1, 47.5, and 43.6 for regular wheat, barley, and oat heads, respectively. In short-straw varieties these percentages will, of course, be higher. It follows that the length of either lever, 1, or 12, is rather similar to that of the culms. Therefore, the crucial effect of plant height on the torque T is obvious. The torque T is resisted by the anchorage of the culm in the soil and by the bending-resistance moment of its aboveground internodes. The interrelationship of soil, underground plant parts, and aboveground parts, and their individual and combined responses to external forces, constitute a complex system. The mechanical aspects of this complete system have, apparently, not yet been investigated. However, as far as stem lodging is concerned, the mechanical analysis may be restricted to the response to external forces of undamaged culms which are anchored in the soil firmly enough not to permit wind or rain to cause any shift of their underground parts. Such culms may be considered as similar to cylindrical rods which are fastened at one end and will be treated accordingly hereafter, following some principles of statics (Timoshenko, 1940). The highest bending-resistance moment of the culm should be regarded as the straw strength, which is, unfortunately, often confused with lodging resistance. The extent of bending increases with the torque T . However, up to a certain limit it is reversible, and the plant will resume its upright position as soon as the forces which have induced the bending moment cease to operate. Beyond this limit bending cannot be restored and lodging occurs.

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The property of the plant to return to its original position after bending, conforms with the definition of elasticity. In the region of bending, stresses (S) originate. These stresses evoke deformations, the summation of which is expressed by the removal of the lower part of the culm from the vertical, as well as by the lowering of the head. At the peak of reversible bending, the stresses at each point reach the elastic limit. Up to the elastic limit the deformation increases proportionally to the stress. Beyond the elastic limit the yield point is reached and from this point the deformation may increase greatly for very little increase in stress. The magnitude of the elastic limit of the straw of a certain crop will affect the percentage of lodging plants ( = prevalence of lodging), whereas the degree of lodging will depend on the yield point. Stresses smaller than the elastic limit may affect lodging only indirectly, through their effects on culm displacement which affects the force f . Straw strength may be estimated by the torque which will cause stresses of the same magnitude as the elastic limit of the straw. It is dependent on the value of the elastic limit as well as on the rate of increase of the stresses with the torque T . The relation between torque and stress for a cylindrical rod is

T

=

S(&Z/d)

where I is the moment of inertia depending on the shape of the cross section of the rod and d is its diameter. For a solid cylinder I = ( a d 4 / 6 4 ) , whereas for a hollow cylinder with inner diameter d,, I = [a(d4- d,')1/641. Consequently, increased values of culm diameter, culm-wall thickness, and elastic limit may all promote straw strength. The deformation evoked by S will be inversely proportional to E, which is Young's modulus of elasticity for the material of the rod. Consequently, the deformation originating from the torque T will be inversely proportional to the product ZE. This product is called the flexural rigidity of the rod, which should correspond to straw stiffness of cereal plants. The latter term has, unfortunately, sometimes been confused with straw strength and even with lodging resistance. It should be emphasized that culms may be stiff and nevertheless weak because of a low elastic limit. Moreover, high straw stiffness may contribute to straw strength only to the extent that it results from a high moment of inertia ( I ) rather than from a high modulus (El. Very stiff straw, in which no deformations may occur, will transfer the torque which operates on it to the underground plant parts and may thus promote root lodging, if soil conditions are appropriate. On the other hand, reduced stiffness will increase the swing movements of the culm, which may be induced by a light breeze. This, presumably, may promote root

216

MOSHE J. PINTHUS

lodging due to the effects of these movements on the adhesion of the roots to the soil. The analysis of lodging according to the concepts and laws of elasticity has been attempted by Hashimoto (1963), Hozyo (1969), Oda et al. (1966), and Ustum and Hungerbuhler (1968).

c.

RECOVERY FROM LODGING

Cereal culms which have not yet completed their internode elongation may recover from lodging. The upper internodes of lodged culms may resume their erect growth after an upward bending at one or at several of the lower nodes. This bending is induced through geotropic stimulus (Percival, 1921 ) and is performed through elongation of node cells and sheath cells on that side of the node which is turned to the ground (Dudinskii, 1970). The regained upward growth of young internodes, which had only started to elongate when lodging occurred, may be attributed to the activity of their basal intercalary meristem (Dudinskii and Mikolenko, 1970). Recovered lodging can sometimes contribute to the prevention of later lodging, due to its height-reducing effect. Furthermore, in certain cases, adventitious roots develop at the lowest bent node and this strengthens the anchorage of the plant. D.

LODGING CAUSED BY FOOT-ROTOR ROOT-ROTDISEASES

Root rots and foot rots weaken the anchorage of plants and affect the lower stem internodes, thus promoting lodging. The lodging of infested plants is characterized by the culms leaning or lying in disorder, whereas the stem or root lodging discussed above occur in a uniform direction throughout the field. The main root-rot disease which may induce lodging of cereals is “takeall,” caused by Ophiobolus graminis, which has been investigated extensively by Nilsson (1 969). However, the most serious and widespread diseas.e resulting in lodging is the “eyespot” foot rot caused by Cercosporella herpotrichoides. On plants infested with this fungus, brown elliptical lesions develop on the sheaths of the lower leaves and on the lower culm internodes. The fungus may penetrate deeply into the culms, and the lesions may eventually girdle them near ground level. Eyespot is found on all three cereals under consideration, but wheat is the most severely affected one, and the relation between lodging of this crop and eyespot has been investigated extensively (Bauer, 1963; Bock-

LODGING IN WHEAT, BARLEY, AND OATS

217

mann, 1964; Glynne, 1963; Gregory, 1959; Manning, 1967; Mielke, 1970). Eyespot infection results from infested stubble of a previous crop and therefore its occurrence increases with the frequency of these cereals in the crop rotation. The spread of the disease and its severity are promoted under conditions of high humidity and a temperature range of 5-1OoC (Mielke, 1970). Cool and damp weather during the period of stem elongation is favorable for the disease and therefore it is most frequent on winter wheat in northwestern Europe. In the United States, eyespot has become a serious disease of semidwarf wheat grown at high fertility level because of its adaptation to the microclimate prevailing within the dense canopy of such wheat (Briggle and Vogel, 1968). The effects of most cultural practices as well as those of various culm characters on the incidence of eyespot, are similar to their effects on lodging. Moreover, infection by eyespot is often increased by the conditions prevailing in a lodged crop. Therefore, in many cases it is difficult to decide whether the correlation between eyespot and lodging should be attributed to the effect of eyespot on lodging, the effect of lodging on eyespot, or the effect of a certain plant character or environmental factor influencing both maladies similarly. E.

LODGING O F INSECT-ATTACKED

CULMS

Insect-induced lodging rarely affects great areas of a field but it occurs frequently to individual culms distributed throughout the field. It concerns wheat primarily and is caused mainly by the Hessian fly (Mayetida destructor Say) and by sawflies (Cephus cinctus Nort. and C . pygmaeus L.). The maggots of the Hessian fly girdle the culms at their bases by scratching the leaf sheaths and internodes, whereas the larvae of the sawfly bore within the stem. The occurrence of these insects has been restricted considerably due to adequate cultural practices and the use of resistant varieties (Dahms, 1967). Ill.

Effects of lodging on Crop Development and Yield

A.

METHODSOF

INVESTIGATION

The effects of lodging on the crop are confounded with the effects on the crop of the factors causing lodging. No completely satisfactory method has been found to distinguish between these effects and to isolate the effects of lodging. The main methods which have been applied are outlined below. In spite of the shortcomings of each one of them, the results obtained

218

MOSHE J. PINTHUS

through them in many experiments fall into line with each other and enable rather definite conclusions to be reached with regard to certain effects. 1 . Comparison between Samples from Lodged and from Standing Areas within the Same Plot

This method has been used in early work (e.g., Welton and Morris, 1931) as well as in more recent studies (Das et al., 1966; Miladinovic, 1959; Mulder, 1954; Syme, 1968). It is based on the assumption that the variations in lodging within the plots have not been caused by factors that may per se affect the crop characters under investigation. In most cases such an assumption will not be justified. 2 . Comparison of Lodging Plants in Untreated Plots with Erect Plants in CCC-Treated Plots A vast number of field experiments with 2-chloroethyl trimethylammonium chloride (CCC) on cereals, primarily wheat, have been conducted throughout the world since 1961 and up to the present day. The reports on these experiments provide much information on various plant characters, particularly grain yield, from lodged and from standing plots. However, many plant characters, including grain yield, are affected by CCC also in the absence of lodging (Humphries, 196Sa). Moreover, strong CCC x environment interaction effects should also be considered. Some characters, e.g., those determining baking quality of wheat grain, are hardly affected by CCC (Humphries, 1968a) and their response to lodging can be ascertained by the method under consideration. This method also enables us to deduce the effects of lodging on characters for which reliable estimates on their response to CCC, in the absence of lodgig, are available, e.g., elongation of culm internodes. Moreover, considering information on the effect of CCC on the grain yield of wheat, in the absence of lodging (Humphries, 1968b; Lowe and Carter, 1972; Pinthus and Rudich, 1967; Primost, 1968; Schultz, 1971; Sturm and Jung, 1964; Zadontsev et al., 1969), it can be assumed that this effect will in most cases be slight or account for an increase of up to 15%. Consequently, differences in grain yield beyond this limit, between standing treated plots and lodging untreated plots, can be attributed to the effect of lodging on grain yield. 3. Artificially Prevented Lodging

Within a crop which is liable to lodge, the plants in some plots are supported to prevent lodging. This method has been applied by Mulder

LODGING I N WHEAT, BARLEY, AND OATS

219

(1954) and by Zadontsev et al. (1969). Theoretically, this is the most sound method. However, its restriction to rather small plots reduces its practical usefulness. 4 . Artifically Induced Lodging

In order to be effective this method should be accompanied by supporting the plants in control plots in order to prevent their lodging. Harrington and Waywell ( 1950) induced lodging by exposing plots individually to a strong controlled wind produced by an airplane propeller. A movable chamber in which field plots can be subjected artificially to various rainfall and wind intensities was constructed and applied by LekeS and ZeniSEeva (1962) to induce lodging. A mobilc wind tunnel for the same purpose was described by Udagawa and Oda (1967). Lodging induced by these techniques is most similar to that occurring in nature, but their application is too cumbersome. Spraying plants after anthesis with heteroauxin was used to induce lodging by Petinov and Urmantsev (1964). This technique will most probably cause effects on plant characters in addition to lodging. Lodging was accomplished by Laude and Pauli (1956) through bending and pinching the culms between the fingers. The results obtained by this technique, which involves mechanical injury, can pertain only to stem lodging following breakage of the culms. Sisler and Olson ( 195 1 ) induced lodging by pushing the plants down with a long board following irrigation of the plot. This was done gently and with care to avoid damaging the culms or the roots. Consequently, lodging accomplished by this technique resembles root lodging. The most frequently applied technique was devised by Sisler and Olson ( 195 1 ) and used by them to induce lodging in barley. It was subsequently applied with this crop by Day (1957) and by Day and Dickson (1958), with oats by Norden and Frey (1958) and Pendleton (1954), and with wheat by Jankovid (1966a) and Weibel and Pendleton (1964). In this technique the plants are allowed to grow up through a wire netting which is installed for each plot 30-60 cm above the ground. Lodging is obtained by moving the wires of the respective plots horizontally; in the control plots it is prevented by the support of the intact wire. The obvious advantages to this technique are the possibilities of inducing lodging at different degrees from the perpendicular and at various growth stages, as well as its maintaining the erect position of the control plants. The disadvantages are some damage to the plants, which can hardly be avoided, and the difficulty of applying this technique to large field plots.

MOSHE J. PINTHUS

220

B.

EFFECTSON GRAINYIELD

1 . Degree of Lodging and Growth Stage at Which I t Occurs

The effect of lodging on grain yield is dependent on its severity and on the time of its occurrence. Early lodging, during the period of intensive stem elongation, may hardly affect grain yield because of the rapid recovery, which will restore the upright growth of the plant prior to heading. Culm breakage at this stage, to which should be ascribed the yield reduction from lodging in Laude and Pauli's (1956) experiment, is not to be expected under natural field conditions. Lodging close to maturity cannot affect grain yield directly but may cause losses due to its interference with harvest. Heading and early grain debelopment are obviously the most crucial stages. Artificially induced lodging at heading reduced grain yield by 27-40%, whereas the yield reduction due to lodging at about the softdough stage surpassed 24% only at one location (Table I ) . TABLE I Reduction of Grain Yield Due to Artificially Induced 90' Lodging at Two Growth Stages Lodging induced at:

Crop

Location

Winter wheat Winter wheat

Kansas Illinois

Spring barley Fall-sown barley Oats Oats

Manitoba Arizona Iowa Illinois

Heading

15-20 Days after heading

Reference

(%I

(%I

Laude and Pauli (1956) Weibel and Pendleton (1964) Sisler and Olsoii (1951) Day (1957) Norden and Frey (1958) Pendleton (1954)

27 31

22 20

34 40 36 37

24

39 23

17

In other experiments reported by Sisler and Olson (1951) and in those of Jancovid ( 19866a), lodging at heading reduced grain yield by 65 % , perhaps because in these experiments plants were forced to remain flat on the ground. Artificially induced lodging at 45" caused one-fourth to onehalf the reduction of that at 90" (Day, 1957; Norden and Frey, 1958; Pendleton, 1954; Sisler and Olson, 1951) .

LODGING IN

WHEAT, BARLEY,

AND OATS

22 1

Comparison of the yields in lodged plots with those of supported plants, in experiments in the Netherlands (Mulder, 1954) showed that reductions of 4-33%, 4-22%, and 0-31 % for spring wheat, barley, and oats, respectively, were obtained, depending on the severity and time of occurrence of lodging. As mentioned above, experiments with CCC may also supply information on the effect of lodging on the grain yield of wheat. In these experiments, which were conducted primarily in Europe, the greatest increase in grain yield from treated plots was 82% (Humphries, 1968a). However, an estimated increase of up to 40% would be more realistic. The effect of the growth stage at which lodging occurs may also be deduced from some of the CCC experiments. This is illustrated by some of our own (unpublished) results from an experiment with F.A. 8193 wheat at two locations in Israel, where severe lodging was effectively controlled by CCC. The grain yield at one location, where lodging started 3 days after heading, was 3130 kg/ha in control plots and 4400 kg/ha in CCC-treated plots; at another location, where lodging started 20 days after heading, the yield both in treated and in control plots was 4500 kg/ha. 2. E#ect on Grain-Yield Components

The above cited reports on artificially induced lodging, as well as Mulder’s experiments, indicate that lodging at heading affects both the number of kernels per head and the individual kernel weight. Lodging that occurs later affects primarily kernel weight. The increase in wheat yield from plots in which lodging had been prevented by the application of CCC, was associated in many cases with an increase in the number of kernels per spike, whereas kernel weight was only rarely, and then slightly, affected (Humphries, 1968a; Lowe and Carter, 1972; Martin, 1968). c.

EFFECTSON GRAINQUALITY

Lodging may cause shriveling of the grain and reduce its test weight (bushel or hectoliter weight). In most of the experiments in which lodging was artificially induced or prevented, a similar reduction in test weight was found amounting to about 8 % for wheat and barley and 15% for oats. In these experiments as well as in others (Gately, 1968; Hirano et al., 1970; Miladinovic, 1959), the N (or protein) content of the grains from lodged plots exceeded that from standing plots by 3-20%. Lodging may reduce milling quality of wheat (Hirano et al., 1970) whereas its effect on baking quality seems to be negligible and may sometimes even be advantageous (Miladinovic, 1959). Lodging, however, ad-

222

MOSHE J. PINTHUS

versely affects the malting quality of barley (Coenradie and Wilten, 1961; Day and Dickson, 1958). Sprouting in the heads has also been found to occur more frequently in lodged than in standing crops (Kivi, 1961 ) .

D. EFFECTS ON

CULM

DEVELOPMENT AND TILLERING

The elongation of the two upper culm-internodes, which is not completed until 5-10 days after heading, can be affected by lodging which occurs up to this period. Thus, although CCC reduces internode elongation, the two upper culm internodes of erect treated plants have often been found to be longer than those from lodged untreated plants (see, e.g., Pinthus and Halevy, 1965). Since these internodes comprise about twothirds of the total culm length, any interference with their development may affect straw yield considerably. Straw yield was indeed as much as 25 and 21% lower for lodged wheat and oat plants, respectively, than for supported plants (Mulder, 1954). Lodging may sometimes promote the development of late tillers, presumably because of the reduction in the competition for minerals and carbohydrates by the lodging culms. However, these tillers rarely attain normal growth. E.

PHYSIOLOGICAL EFFECTSOF LODGING

The most obvious effect of lodging on the plant’s physiological processes is its interference with carbohydrate assimilation (Mulder, 1954). This results from a large part of the foliage and other photosynthesizing parts being shaded by plants which are leaning or lying on top of them. The heads of low-lying plants in a lodging crop may sometimes be completely empty, whereas those of the plants lying on top develop normal grain. The reduced carbohydrate assimilation will, of course, affect primarily their accumulation in the grains, but, depending on the time of lodging, may affect any process or plant part demanding carbohydrates during that time. The protein in cereal grain originates primarily from nitrogen which has accumulated in the foliage prior to heading. Therefore, its absolute amount in the kernels is hardly affected by lodging, which occurs at heading or thereafter. Consequently, the percentage of N, or protein, in the grain of lodged plants may rise due to the decrease in carbohydrate accumulation. Lodging which involves culm breakage will also interfere with the translocation of carbohydrates and of minerals (Hashimoto, 1959; Pauli and Laude, 1959). In this case the absolute content of N and other minerals in the grain may also be reduced if lodging occurs during heading or early grain development.

LODGING I N

F.

IMPACT

OF

WHEAT, BARLEY,

AND OATS

223

LODGING ON GRAINHARVEST

Very few data are available on the quantitative effects of lodging on combine harvesting. Considering the report of Baumgartner ( 1969), it may be concluded that, in a lodged crop, harvest capacity can be reduced by up to 25% and the loss of unthreshed heads may be doubled. The moisture content of lodged grain will be higher than of unlodged grain, which also interferes with the harvest and may increase the expenses for grain drying by 30%.

G.

INCIDENCE OF

DISEASESI N LODGING CROPS

Some environmental factors and several plant characters which promote lodging also improve the growing conditions for rots and leaf diseases. Moreover, these diseases are often favored by the microclimate prevailing within a lodged crop. These facts have been recognized by various workers (e.g., Bauer, 1963; Mulder, 1954; Weibel and Pendleton, 1964), but no relevant data seem to be available. The eyespot disease, which itself may cause lodging, seems to be enhanced by the conditions within a lodged crop. Its reduction due to the application of CCC can be attributed partly to the control of lodging by this chemical (Bockmann, 1968).

IV.

Plant Characters Associated with lodging

Culm length and the shape of the head affect the magnitude of the lodging-inducing torque whereas the plant’s resistance to the torque is dependent on various other characters. The information on the association of these characters with lodging is derived predominantly from the study of varieties or lines differing in lodging resistance. In evaluating this information, which is often contradictory, the following points should be considered: First, the reliability of the assessment of lodging resistance, considering the strong variety x environment interaction effects on lodging (Section VII, A, 1 ). Moreover, in certain cases lodging assessments have been based on mechanical properties rather than on direct field observations. Second, varietal differences in lodging are accompanied by differences in many other characters which may or may not be correlated with each other. Partial correlation and path-coefficient analyses can be useful in this respect. Third, interaction effects of variety x different characters on lodging cast much doubt on the relevance of studies performed on a small number of varieties. Similarly, the association with characters which are

MOSHE J. PINTHUS

224

strongly affected by variety x environment interaction effects must be based on extensive tests of these characters. Finally, a high correlation between a certain plant character and lodging does not necessarily imply a causal relationship. This reservation also holds for the information obtained through comparison of lodged and erect plants in the same plot. A.

CULMCHARACTERS 1 . Length

Culm length, which comprises the lever of the lodging-inducing torque, is obviously associated with lodging. Nevertheless, in many of the investigations in which no dwarf or semidwarf varieties were included, no marked correlation between these traits was ascertained (Baier, 1965; Rodger, 1956; Zimina, 1968). This may be ascribed to the occurrence of lodging prior to complete culm elongation as well as to culm length X maturity interaction effects. An early, short-strawed variety close to maturity will be taller and more prone to lodging than a late, long-strawed variety, which at that time has attained only the late boot or heading stage. With regard to lodging at heading, the length of the three or four lowest internodes is of greater effect than that of the two uppermost internodes, which, although comprising about two-thirds of the final culm length, have not yet completed their elongation at this stage. 2 . Basal Internodes From the mechanics of lodging it is apparent that the properties of the basal culm internodes should affect lodging resistance. Some durum and rivet wheats have solid stems, and this character has also been bred into certain common wheat varieties in order to achieve sawfly-resistance (Dahms, 1967). However, in most wheat varieties, as well as in barley and oats, the internodes are hollow. Therefore, their flexural rigidity is greatly dependent on both diameter and wall thickness (Section 11, B ) . Varietal differences in lodging resistance were indeed found to be significantly positively associated with the diameter and wall thickness of the basal internodes-primarily the second one-in many studies (Hamilton, 1941; Hansel, 1957; Jellum, 1962; Mukherjee et al., 1967; Multamaki, 1962; Oda et al., 1966; Sechier, 1961). In other studies, marked positive correlations were established between these characters and culm bending or breakage (Bhamonchant and Patterson, 1964; Hancock and Smith, 1963; Norden and Frey, 1959). The coefficients for the correlations which were found between these culm characters and lodging, bending or breakage, rarely exceeded the value of 0.7.

LODGING IN WHEAT, BARLEY, AND OATS

225

The association between lodging and the diameter and wall thickness of the basal internodes is also evident from comparisons between lodged and erect plants of the same variety in the same plot (Das et al., 1966; Mulder, 1954). The diameter of the basal internodes was found to be closely correlated with the number of coronal roots (Hamilton, 1951; Hansel, 1957). Its association with lodging resistance may therefore be attributed in part to the relation between lodging and root development. The length of the basal internodes has been rather closely correlated with lodging of barley (Baier, 1965). Moreover, increased internode elongation, due to cell elongation rather than cell division, is usually accompanied by reduction in diameter and wall thickness. Consequently, the length :diameter ratio has been found to be distinctly correlated ( r = 0.71-0.78) with lodging (Baier, 1965). Culm density, i.e., dry weight per unit length of culm measured at the base of the plant, is, of course, dependent on the diameter and wall thickness. It was found by Atkins (1938) to be closely correlated with breaking strength of wheat. Its correlation with lodging resistance in the field, though significant, was rather low ( r = 0.4-0.6). Obviously, this character may affect mainly stem lodging rather than root lodging. 3 . Anatomical Structure The anatomic structure, as well as the chemical compostion, should affect the modulus of elasticity of the straw ( E ) and through it, the flexural rigidity of the culm. The relationship between lodging and culm anatomy, and in particular that of the basal internodes, of all cereal crops, has been investigated extensively. Results of early work have been summarized by Esteves (1952) and Ramaswamy (1963). More recent studies have been carried out primarily in eastern Europe (e.g., MiliEa et al., 1966 NBtr, 1964; Strutsovskaya, 1968). Significant differences between extremely lodging-resistant and susceptible varieties have been found in most studies. However, consistent relationships, relcvant to a complete array of varieties differing in lodging resistance, have not been ascertained. The most marked and significant anatomical feature related to lodging resistance was a great number of vascular bundles. The results regarding the width of the sclerenchyma layer are contradictory. This may be due to differences in the quantity of assimilating parenchyma embedded in this layer, which was found to be negatively correlated with lodging resistance (Skucifiska, 1965). The above mentioned relationships between anatomical features and lodging resistance may be partly ascribed to the effect of lignification on culm rigidity. A significant positive relationship between lodging resistance and the proportion of the

226

MOSHE J. PINTHUS

lignified tissues in the cross section of the basal internodes was found by Multamaki (1962) for oats and for barley. The changes in lignification throughout the growing period (Heyland, 1956) presumably contribute to the inconsistent relationships between lodging and culm anatomy.

4 . Chemical Composition Early work attributed culm rigidity to a high content of silicia, but later investigations disproved this hypothesis (Heyland, 1959; Ramaswamy, 1963). Cellulose and lignin contents in the basal internodes have been found to be associated with lodging resistance in certain cases. However, the results are inconsistent and sometimes even contradictory (Heyland, 1959; Ramaswamy, 1963). Spahr (1960) found that in barley a high cellulose content in the lower two-thirds of the culm was associated with lodging resistance. Recently, Galkovskaya and Baltaga (1970) reported on a high content of cellulose, hemicellulose, and lignin in the culms of lodgingresistant winter wheat strains. The cellulose:lignin ratio in the lower part of the culm was foynd to be associated with lodging in wheat (Heyland, 1959) and barley (Skopik, 1969). B. ROOTAND

CROWN CHARACTERS

The qualities of the root system affect the anchorage of the plant in the soil and therefore are of major importance in determining resistance to root lodging. The association of various root and crown characters with lodging of the different cereal crops has generally been accepted (Troughton, 1962). Many studies indicate the relationship between lodging resistance and a vigorous root system in the upper soil layer (Hamilton, 1951; Hurd, 1964; Maas, 1970; Percival, 192 1 ; Pinthus, 1967a; Sechler, 196 1 ) . Visual daerences between the root systems of extremely lodging-resistant and lodging-susceptiblevarieties are obvious (Fig. 3). Numerical ratings according to the visual appearance have been used for the assessment of root development (Hamilton, 1951; Maas, 1970; Pinthus, 1967a). Through such assessments, as well as determinations of root volume (Sechler, 196 1 ) , relationships were established between root development and lodging resistance for varieties differing greatly in these respects. The dry weight of the roots seems to be a rather poor parameter of the development of the root system of cereals because it does not represent its extension and its surface area. Moreover, its determination is subject to great experimental errors (Troughton, 1962). A relationship between

LODGING IN WHEAT, BARLEY, AND OATS

227

FIG.3. The root systems of a lodging-resistant wheat variety (SELKIRK) and a susceptible variety (CCC 10).

228

MOSHE J. PINTHUS

this character and lodging was found in certain studies (Strutsovskaya, 1968), but not in others (Spahr, 1960). Significant correlations, ranging from 0.4 to 0.9, have been found between lodging resistance and the number of coronal roots per plant or per tiller (Bauer, 1964; Hansel, 1957; Harrington and Waywell, 1950; Multamaki, 1962). A positive relationship between these characters has also been found by Sechler (1 961 ) . However, the number of coronal roots per plant is strongly affected by environmental factors whereas varietal differences within the same species and maturity class are rather slight (Pinthus, 1969). Positive relationships between lodging resistance and coronal root diameter were found for the different‘species when a limited number of varieties differing greatly in lodging resistance were compared (Dorofeev, 1959; Sechler, 196 1 ; Wag, 1970). The roots of lodging-resistant varieties of barley had greater tensile strength, as indicated by a higher breaking point, than susceptible varieties (Spahr, 1960). Sechler (1961) found a close association between the length of the root crown and lodging resistance in oats. Anatomical root characters were also investigated: Dorofeev ( 1959), examining one lodging-resistant and one susceptible variety each of durum, turgidurn, aestivum, and compactum wheat, found thicker cell walls and a larger diameter of the sclerenchymatic layer in the lodgingresistant varieties. A consistent and rather high correlation (0.8) was established in wheat between lodging resistance and the spread of the coronal roots, expressed as the angle from the perpendicular at which these roots penetrate the ground (Pinthus, 1967a). This relationship seems to be of particular significance, since it was found for varieties which were similar with regard to other root and crown characters as well as culm diameter.

C. MECHANICAL PROPERTIES 1 . Straw Stiflness and Straw Strength Straw stiffness refers to the flexural rigidity of the culm (Section 11, B). It has been estimated by several methods: Measurement with a spring balance of the force required to pull horizontally a certain number of culms, growing close together in the field, to a reclining position at a certain angle (Multamaki, 1962; Oda et af., 1966); determination of the “buckling load,” which is the force required to bend an internode, fastened at the node, from an inclination of 30° to 90° (Watson and French, 1971 ) ; determination of the angle at which culms, in the field or in pots, are bent by a certain load (Baier, 1965); and the “snap test” by which plants in

229

LODGING I N WHEAT, BARLEY, AND OATS

the field are graded according to the force required to pull a handful of culms to a reclining position, and according to their resilience (Murphy et al., 1958). The snap test is apparently the most widely used method (Frey et al., 1960; Hess and Shands, 1966). Coefficients of correlation between culm rigidity and lodging resistance varied from 0.33 to 0.98 in different studies (Table 11). TABLE I1 Coefficients of Correlation between Lodging Resistance and Straw Stiffness, and Lodging Resistance and Breaking Strength Correlated characters

Crop

Lodging resistance and straw stiffness

Spring wheat Spring wheat Barley Barley Barley Oats Oats Oats Winter wheat Winter wheat Spring wheat Barley Barley Oats

Lodging resistance and breaking strength

Coefficient 0.33 0.7-0.8 0.6-0.7 0.66 0.98 0.19 0.80 0.4-0.8

0.3-0.6 0.5-0.7 0.55 0.81 0 .60 0.10

(7)

Reference Multamaki (1962) Oda el al. (1966) Oda et al. (1966) Baier (1965) Multamaki (1962) Multamilki (1962) Murphy el al. (1958) Hess and Shands (1966) Salmon (1931) Atkins (1937) Multamkki (1962) Multamaki (1962) Baier (1965) Multamaki (1962)

Since flexural rigidity of the culm is a product of its moment of inertia ( I ) and its modulus of elasticity (E), a high value for it may be due to both E and I. Oda et al. (1966) found that in barley it was due primarily to high I, whereas in wheat it originated mainly from a high E. High flexural rigidity may contribute to lodging resistance through its effect on straw strength, i.e., the highest bending moment that the culm per se is capable of resisting (Section 11, B ) . This culm property is estimated when the lodging resistance factor, cLr (Grafius and Brown, 1954), or the load bearing capacity, LBC (Miller and Anderson, 1963), is determined (Section VII, A, 3 ). 2 . Breaking Strength Breaking strength refers to the force required to break a section of certain length of the basal culm internodes. It has been studied extensively with all three cereals, various types of instrumentation being applied. Its correlation with lodging resistance has been found to vary considerably

230

MOSHE J. PINTHUS

(Table 11). However, when comparing lodging-resistant and susceptible varieties, the former were generally found to have higher breaking strength than the latter, although within each group rather wide ranges were encountered. This may be illustrated by the results reported by Strutsovkaya (1966) : The breaking strength of 222 lodging-resistant wheat varieties ranged from 1000 to 2800 g, whereas that of 148 susceptible varieties ranged from 300 to 800 g. Similar results were obtained with barley by Khramysheva (1970), and they are in line with many other studies with all three cereals (e.g., Hancock and Smith, 1963; Oda et al., 1966; Zimina, 1968). Breaking strength changes during the period from heading to maturity (Bartel, 1937) and therefore the values obtained will depend on the growth stage of the plants at the time of testing. The same applies also to some other characters, associated with lodging, which have been shown to vary during the course of plant development, e.g., chemical composition (Heyland, 1959) and straw strength (Jellum, 1962). It is obvious that breaking strength should be associated with stem lodging following fracture of the culms. However, breaking strength may also indicate lodging resistance because of its relation to the elastic limitwhich affects stem lodging, and to flexural rigidity-which is associated with both stem lodging and root lodging. 3 . Root Pulling Resistance

This resistance is the vertical force required to pull out of the soil a certain number of plants, and is expressed as force per culm or per plant. It has been investigated extensively with corn. Harrington and Waywell (1950) have investigated it with wheat, barley, and oats and have found no close correlation between it and lodging. It was found to be closely related to lodging resistance of wheat by Surganova (1967), and of barley by ZeniSEeva (1968). Our own (unpublished) work on this subject with wheat, in Minnesota and in Israel, established marked and significant differences for this character between extremely lodging-resistant and susceptible varieties. However, no correlation was found between it and the other varieties. These inconsistent results, as well as those regarding the relationship between lodging and some other characters, may be due partly to interaction effects between the variety and the conditions under which the character is tested, as, for instance, soil moisture in the present case. No effects of such interactions should be expected in the case of relationships between lodging and characters which can be determined under standard conditions, e.g, breaking strength.

LODGING IN WHEAT, BARLEY, AND OATS

23 1

D. OTHERCHARACTERS Head density and shape may affect lodging through their effect on the area that the head subjects to the wind (Grafius, 1958; Udagawa and Oda, 1967). Patterson et al. (1964) found that in oats the more dense panicle was associated with greater bending resistance. In other studies with oats (Hess and Shands, 1966), panicle density and lodging were closely correlated in progenies of some crosses, but not at all in others. The nodding angle, i.e., the angle between the head and the continuation of the culm, of all three cereals, was investigated by Hancock and Smith (1963). It may affect lodging through its effect on the torque-inducing force of the head. Awnedness may also affect lodging, through the accumulation of rain drops on the awns., thereby increasing the weight of the head. Flag-leaf shape may also affect the subjection of the plant to the wind during the critical period for lodging. Its association with lodging resistance of wheat and barley has been investigated by Kyzlasov (1969) and by Vikitenko ( 1968), respectively. An association between lodging and maturity has been established in certain cases (Mukherjee et al., 1967; Vikitenko, 1968). However, the effect of this character on lodging varies according to the time of the onset of lodging and is therefore not reliable. The association of profuse tillering with lodging resistance which is sometimes observed (Vikitenko, 1968), should be ascribed to the increase in coronal roots due to tillering (Pinthus, 1969). Certain information indicates that varietal differences in lodging resistance are associated with differences in the content of *growth-promoting or inhibiting substances (Petinov and Prusakova, 1965; Prusakova, 1964; Turkova and Suan, 1966). This seems to be in accordance with the effect of internode elongation on lodging.

V.

Environmental and Agronomic Factors Affecting Lodging

Lodging is affected very strongly by environmental conditions. Any effect on any one of the various plant characters associated with lodging will affect it to some extent. The most remarkable effects on lodging will be those exerted through the characters that are most prone to environmental effects, namely, the structure of basal culm internodes and total culm length. The spread of the coronal root system in the upper soil layer is much less influenced by environmental factors, within a considerable range, but is affected strongly by extreme conditions. Regarding the two traits mentioned above, any factor increasing elongation of internodes, particularly that of the basal ones, will promote susceptibility to lodging.

23 2

MOSHE J. PINTHUS

Increased internode elongation may be due to cell division as well as to cell elongation. Both are subject to considerable environmental effects which affect the growth-regulating mechanism within the plant. However, the transverse growth of the subapical tissues which would increase culm diameter and wall thickness, is usually quite limited (Sachs, 1965). Cell number in the transverse direction is already complete before the onset of internode elongation. Moreover, there exists an inverse relationship between the rate of cell elongation and transverse growth (Sachs, 1965). Consequently, an increased length of the internodes will be accompanied by a reduction in their diameter and wall thickness. This, together with the increased hydration which accompanies cell elongation, results in a conspicuous reduction in dry weight per unit length of culm, which has often been associated with lodging susceptibility. A.

LIGHTAND TEMPERATURE

Light intensity is a decisive factor in internode elongation. It also controls the balance between longitudinal and transverse development of vascular tissues. High intensities block the action of natural gibberellin which promotes both division an elongation of cells (Sachs, 1965). Consequently, low light intensity promotes internode elongation and reduces culm-wall thickness. It will also reduce carbohydrate assimilation, which may interfere with cell wall development and lignification (Percival, 1921). Furthermore, root growth may also be depressed by low light intensity (Campbell and Read, 1968). The effect of light intensity on cereal culm internodes has been investigated in field and pot experiments where illumination was controlled by shading. Shading resulted in an up to 25% increase in internode length (Carles et al., 1960; Holmes et al., 1960; Mulder, 1954). Culm diameter and wall thickness of oats were reduced (Mulder, 1954), solidness of the lower internodes of wheat was decreased (Holmes et al., 1960), and the bending resistance of barley culms was lowered (Hozyo and Oda, 1965). Artificial shading of field plots, which reduced light intensity during the period of elongation of the 2-4 lowest internodes by 35-75%, promoted lodging of wheat (Holmes et al., 1960; Welton and Morris, 1931) and of barley (Coenradie and Wilten, 1962; Wilten and Coenradie, 1958, 1959). The effect of light intensity on lodging is evident from numerous studies of plant density (Section VI, A, 3). In dense stands light interception is reduced, which affects the lower culm internodes and promotes lodging. It should be pointed out that the effect of shading, caused by dense stands,

LODGING I N WHEAT, BARLEY, AND OATS

23 3

may also be exerted by infestation with weeds, which does indeed promote lodging in certain cases. Very conspicuous effects of plant populations from 50 to 1600 plants per m2, on culm elongation of barley, were reported by Kirby and Faris (1970) and attributed to the effects of light on plant gibberellin. Internode elongation may presumably be affected directly by the temperature prevailing during the pertinent growth period. A significant correlation was found between the culm length of barley and the temperature during the period from seedling emergence to heading (Pasela, 1967). An increase in temperature, however, may also promote tillering (Nanda et al., 1959). This, in turn, will increase the density of the foliage, which may reduce light interception and thus affect the lower culm internodes. Another indirect effect on the promotion of internode elongation through increased temperatures may be due to its effect on the release of soil nitrogen.

B.

NITROGEN SUPPLY

The promotion of lodging due to abundant nitrogen supply is well known and has been established in many studies with various cereal crops (e.g., Bremner, 1969; Dilz, 1967; Morey et al., 1970; Mulder, 1954; Nilsson, 1972). Usually, at high nitrogen levels there is a reduction in grain yield. In most cases it may be attributed to lodging, although it should be kept in mind that lodging is not the only factor limiting yield response to high nitrogen levels (Fiddian, 1970). It is of special significance that high N levels are conducive to lodging also of semidwarf varieties. This has been reported, so far, for common wheat (Asana and Chattopadhyay, 1970; Hadiiselimovik, 1969; Sage, 1970; Sharma et al., 1970), durum wheat (Scarascia Mugnozza et al., 1965), and barley (Sage, 1970). In most cases lodging of these varieties at high N levels was accompanied by a reduction in grain yield. Lodging and reduction in grain yield of the semidwarf varieties commence at higher N levels and seem to proceed more moderately than in the case of tall varieties. Similarly, at those N levels which have been tested so far, no complete lodging of the semidwarf varieties has been encountered. Considering the information from the above-cited sources and others (e.g., Sillampaa, 1971), as well as recent local experience (Weiss, 1972), we attempted to demonstrate the comparative response of tall and semidwarf varieties to nitrogen supply (Fig. 4 ) . The effect of nitrogen on lodging should be ascribed primarily to its effect on the basal culm internodes. The results presented by Mulder ( 1954) indicate that nitrogen affected all the morphologic and anatomic culm characters associated with lodging. An increase of 10-25% in the

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MOSHE J. PINTHUS

length of the three lowest internodes due to high N level was observed in the various crops (Carles et al., 1960; Friichtenicht, 1965). Enhanced culm elongation following application of high N rates has been found also in semidwarf varieties of wheat (Koltay, 1968; Woodward, 1966) and of barley (Lovato and Venturi, 1968). High N rates may also bring about restrictions in the development of the coronal roots (Mulder, 1954). In this respect it is of special interest that root anchorage of a semidwarf wheat variety was found to be weakened due to application of high N rates r

t

a

.-)I .-C

e

0

, -Toll

Mox.r i-

/

/

- 1

/ Sernidworf

2

----

/

Nitrogen supply

-

FIG. 4. The effect of increasing nitrogen supply on lodging and grain yield of tall and semidwarf cereal varieties.

(Berlyand-Kozhevnikov et al., 1968). However, the information concerning the effects of N supply on the root growth of cereals is somewhat contradictory (Troughton, 1962). In general, it may be concluded that its effect is less on root growth than on shoot growth and therefore increased N supply will always result in an increased shoot:root ratio, which is conducive to lodging. An increase in nitrogen supply may affect the basal culm internodes also through the promotion of plant canopy development, which reduces light interception. The interaction effects of nitrogen and shading on the basal internodes have been investigated by Mulder (1954) and by Carles etal. (1960). The promotion of plant canopy and the weakening of the basal internodes due to increased nitrogen supply have been found to enhance the

LODGING IN WHEAT, BARLEY, AND OATS

235

incidence of eyespot disease (Bauer, 1963). This,in turn, may also promote lodging. In other studies, however, eyespot-induced lodging of wheat was reduced by the application of N fertilizer (Bockmann, 1964).

c.

PHOSPHORUS, POTASSIUM, AND

TRACEELEMENTS

The effect of these elements on lodging are less pronounced and less consistent than those of nitrogen. In evaluating their effects, differentiation should be made between those that originate in the repair of deficiencies and those which are due to additional supply. The former may improve lodging resistance because deficient plants in many cases suffer from poorly developed culm walls or crown roots; such effects of P and K deficiencies are evident from Casserly’s (1957) studies of lodging in oats. In many experiments no effects on lodging, or only very slight ones, were exerted following the application of either P or K (Chapman and Mason, 1969; Hernes, 1965; Morey et al., 1970; Raheja and Misra, 1955). An increased supply of phosphorus has been found to promote lodging of wheat (Miller and Anderson, 1963; Mulder, 1954; Pyatpgin and Semikhov, 1967; Shrivastava and Yawalkar, 1960) and of oats (Mulder, 1954). Reduced breaking strength of the culms was found by Miller and Anderson ( 1963), whereas increased breaking strength of the roots was reported by Spahr (1960). Increases in the length and diameter of the basal internodes of wheat, following increased P application, were reported by Skorda (1970). Based on the findings that phosphorus increases the N content and decreases the lignin content of wheat culms, Miller and Anderson ( 1965) suggested that it may promote lodging due to its enhancing of the nitrogen effect and by “reducing the ratio of mechanical tissues to proteinaceous ones.’’ An increased supply of potassium has been found to reduce lodging (Shrivastava and Yawalkar, 1960; Wahhab and Ali, 1962). It has also been found to reduce elongation of the lower culm internodes and to increase their diameter (Shrivastava and Yawalkar, 1960; Wahhab and Ali, 1962) Koch, 1969). Increased wall thickness and number of vascular bundles was also found (Wahhab and Ali, 1962). Following applications of K, an increase in culm rigidity, due to the modulus of elasticity (E), and in straw strength, was also reported LHashimoto (1959) and Koch (1969), respectively]. Nightingale (1943) ascribes the culm-strengthening effect of K to its positive effect on carbohydrate synthesis and states that “potassium is frequently recorded as favoring the development of thick cell walls and stiff straw, but in perhaps as many cases this element is reported as having the opposite effect.”

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Koval’skii and Maslyanaya (1969) claim that lodging of cereals grown on peat soil may be caused by Cu deficiency. Experiments in Germany with wheat, barley, oats and rye indicated that on Cu-deficient soils, receiving high N-dressings, the application of copper resulted in the reduction of lodging and subsequent increase in grain yield (Vetter and Teichmann, 1968). The application of manganese to barley grown on peat soil was reported to increase the breaking strength of its two lowest culm internodes (Loiko, 1968). However, Bachthaler (1969) did not find any effect on lodging resistance of winter wheat, spring wheat, or barley through the application of copper, manganese, or boron. SUPPLY D. MOISTURE#

AND

SOIL AERATION

Abundant moisture supply may be conducive to lodging due to its promoting effect on culm elongation; it may also increase the incidence of eyespot, and-when the surplus moisture is in the upper soil layerweaken the anchorage of the root system. On the other hand, dryness of the upper layer may restrict the development of the coronal-root system and thus promote lodging (Harlan, 1957). The lodging of spring wheat stressed for moisture at the onset of culm elongation, in trials at Tucson, Arizona, was attributed to the interference with normal development of upper crown roots (Day and Intalap, 1970). The interference of dryness in the upper soil-layer with coronal-root formation was also reported by Boatwright and Ferguson (1967) and by Ferguson and Boatwright (1968). Furthermore, lodging on clay soils under dry conditions may be evoked by the cracking of the soil, which damages the roots. This has been observed with wheat in Canada (Hurd, 1964). Poor soil aeration may increase susceptibility to lodging due to the effects of respiration inhibition on changes of metabolism which promote cell elongation (Turkova et al., 1965). It may, presumably, increase lodging also through its harmful effect on root development (Troughton, 1962). The promotion of lodging due to poor aeration and high moisture content of the soil is especially evident in waterlogged fields and in fen soils. Soil aeration and soil structure, however, also affect nitrogen availability, which in turn affects lodging, and therefore the effects of these factors on lodging are not clear cut (Mulder, 1954). E.

CROP ROTATION AND TILLAGE

The main effect of crop rotation on lodging is exerted through its effects on the incidence of eyespot, which concerns primarily wheat in western

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and central Europe. A close sequence of wheat and other cereals on which the disease can survive will promote its incidence (Glynne, 1963; Lelley, 1965). Green manuring and underplowing of the stubble have been reported to reduce eyespot-induced lodging (Grootenhuis, 1968). Other effects of crop rotation on lodging are probably due to its effects on soil fertility and, in particular, on nitrogen availability. In this respect the effects of the fertilizers applied to the preceding crop may be greater than those of the crop itself. Thus, lodging of barley was found to be more frequent and severe following root crops, alfalfa or well-fertilized grass than after a grain crop (Beaven, 1947; Dyke, 1967; Gately, 1968; Widdowson and Penny, 1970). Only little information is available on the effects of tillage practices on lodging. More lodging of spring wheat was found on plowed land (at Rothamsted, England) than after slit seeding into an unplowed grass sward (Hull, 1967). In Czechoslovakia, Kopeckg (1970b) found that subsoiling increased lodging of barley over that obtained on a regularly prepared seed bed, whereas rolling after sowing decreased it (Kopeckp, 1970a). A similar effect of rolling was found in Norway (Njes, 1962). These effects may perhaps be attributed to the impact of the respective seed bed preparation on nitrification in the upper soil layer and subsequent N availability to the crop. Thus, subsoiling may have increased nitrification whereas rolling may have reduced it.

F. SYNERGISTIC EFFECTS The interaction of lodging-promoting factors is apparently of a synergistic nature. Thus, increased nitrogen supply may promote lodging more under irrigated than under dryland conditions and, similarly, more in dense than in sparse stands. This may be illustrated by our (unpublished) observations in a field trial conducted by Dr. Z. Karchi (Table 111). TABLE I11 Lodging Rates (0 = No Lodging; 4 = Complete Lodging) of Wheat as Affected by Plant Density and N Application (En nor, Israel, 1965) Basic dressing of N (kg/ha) Plants per m*

0

120

50 100 150

1 .o 1.2 1.7 0.20

1.6 2.5 5.8 0.20

SE

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MOSHE J. PINTHUS VI.

A.

Prevention of lodging

CULTURAL PRACTICES

From the information presented above it is apparent that the main lodging-promoting factors are abundant moisture and nitrogen supply, dense stand, and warm temperature. All these factors, however, are also favorable to grain yield production, Therefore, cultural measures to control lodging must aim at the achievement of an equilibrium between yield promotion and lodging prevention. Factors affecting the incidence of eyespot should also be considered. 1 . Date of Sowing

The probability of the plants being at a growth stage particularly susceptible to lodging, during a period of high frequency of lodging-inducing factors, may sometimes be reduced by a suitable sowing date. Furthermore, the sowing date may affect lodging through its effects on tillering and on the period during which stem elongation will take place. Early fall-sowing of winter wheat will prolong the tillering period; and has been found to increase lodging (Hanley et al., 1961; Vez, 1968), presumably because it encourages profuse vegetative growth. Late sowing reduced lodging also because it decreased the incidence of eyespot (Vez, 1968). On the other hand, lodging of early-sown crops has sometimes been less than that of later-sown crops (Henriksen, 1961), which may perhaps be ascribed to a better developed coronal root system resulting from increased tillering. In Mediterranean and other warm regions, where spring-type varieties of cereals are grown in winter, late sowing may reduce the tendency to lodge. This was demonstrated by the results obtained with irrigated barley in Arizona (Day and Thompson, 1970), and it has been recommended to farmers in Israel. Tillering, as well as the elongation of the lower culm internodes of late-sown crops, in these regions, will occur at lower ambient temperature and will therefore be restricted. This, and in particular the restriction of the elongation of the basal culm internodes, may prevent lodging. Spring-sown cereals will enjoy warmer temperature during the periods of tillering and shooting when sown later. In this case early sowing may contribute to the prevention of lodging due to a certain retardation of growth (Rodger, 1956), as found with oats in Scotland (Bain and Morrison, 1961). On the other hand, late-sown plants also enjoy a longer daylength and will therefore reach the stage of head initiation sooner, which in turn may restrict tillering and the number of elongating stem internodes.

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This may have been the reason for the reduction in lodging of late-sown barley in Belgium (Froidment, 1968). It is concluded that adopting a suitable sowing date may contribute to the prevention of lodging. The application of this measure will, of course, be restricted to those cases in which it has no negative effect on grain yield. 2 . Depth of Sowing and Row Orientation Deep sowing increases the depth at which the root crown is located (Chambers, 1963; Foltjh and Mikala, 1971; Percival, 1921) and also its length (Table IV). This may strengthen the anchorage of the plants in the soil and thus increase their lodging resistance. However, because of increased epicotyl elongation at deep sowing, the depth of the root crown TABLE I V Effects of Sowing Depth on the Root Crown of Common Wheat (Averaged over 10 Varieties Tested a t Rehovot, Israel, in 1964)

Sowing depth (cm) 4 10 18

SE

Length of epicotyl (mm)

Length of crown

3 34 69 2.9

29 34 44 1.3

(mm)

Location of crown below soil surface (mm) 8-37 32-66 47-91

does not reach the depth of sowing (Table IV). Therefore, it seems that within the range of practicable variations in sowing depth, the effects on the root crown may be rather small. Nevertheless, deeper sowing has, indeed, been found to increase lodging resistance of barley (Socittt d’Enccouragement de la Culture des Orges de Brasserie et des Houblons en France; Rapports sur la campagne 1959). Sowing in drill rows in a direction parallel to that of the prevailing strong winds may reduce the incidence of stem lodging. This should also be taken into account while the effects are considered of plant-row direction on yield due to their influence on light interception. 3. Spacing

Numerous studies, with all three cereals and in all parts of the world, indicate that lodging may be prevented or reduced by a decrease in plant density accomplished by a reduced seeding rate (e.g., Bengtsson and Ohlsson, 1965; Furrer and Stauffer, 1970; JevtiC, 1971; Kirby, 1967;

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Lowe and Carter, 1972; Nelson and Roberts, 1961). Up to a certain seeding rate, plant density will be compensated by tillering, resulting in a rather constant shoot density. In this situation lodging resistance will benefit from low seeding rates due to the promotion, through tillering, of coronal-root formation. Beyond this rate, lodging resistance will be affected by the shading effects of plant density. The beneficial effect of low seeding rates on lodging resistance applies also to eyespot-induced lodging (Salt, 1955; Witchalls and Hawke, 1970). The prevention of lodging through a decreased seeding rate must, however, be restricted to those levels where no reduction in grain yield is to be expected in response. Moreover, the effect of plant population on grain yield is of particular significance under fertile conditions conducive to maximum yields which may be challenged by lodging. [Regarding the relationships between plant population and yield, two reviews should be consulted: Holliday (1960), and Willey and Heath ( 1969) .] Reduction in the effect of shading and concurrent maintenance of high plant population may be obtained by decreasing interrow spacing. Narrower spacing, without any change in the seeding rate, was indeed found to reduce the length and increase the diameter and wall thickness of basal culm internodes of wheat (Furrer and Stauffer, 1970; Watson and French, 1971). It also reduced lodging of wheat (Furrer and Stauffer, 1970; Humphries and Bond, 1969), and of barley (Delhaye, 1971; JevtiC, 1971), and the incidence of eyespot (Furrer and Stauffer, 1970). No effect of row spacing on lodging of wheat was obtained by Kinra et al. (1963), but in their experiments lodging was rather slight. In most of the abovecited experiments, the narrower spacing between rows, usually within the range of 8-25 cm, resulted in a certain yield increase (up to 10%) which may have been due to the reduction in lodging. Furthermore, in a review on “the effect of row width on the yield of cereals,” Holliday (1963) shows that reduced spacing ( <18 cm) has consistently given a small increase in grain yield, amounting to 2-1 0 %. In addition to its effects on lodging resistance, narrow row spacing may contribute to an increase in yield also by improving light interception. This should be of particular significance at high plant populations, which are required for the attainment of top yields (Duncan, 1969). Lodging of wheat was also reduced owing to a change in the spatial arrangement by sowing groups, 15-20 cm apart, of about five seeds per group (Forneris, 1964; Lemaire et al., 1969). It is doubtful whether high plant populations can be attained by this method, and its practical application seems to be complicated. In conclusion, narrow interrow spacing should increase lodging resistance without interfering-to say the least-with grain yield production.

.

LODGING IN WHEAT, BARLEY, AND OATS

24 1

4 . Timing and Form of N Application

The highest rates of nitrogen uptake are during the period of shooting. Its adequate supply at this time is decisive for grain yield. However, with the exception of very low available soil N, the demand for N fertilizer during the earlier growth period is rather limited. An abundant supply during this period will promote surplus tillering and extensive elongation of the lower culm internodes, which is conducive to lodging. In contrast, later application of N fertilizer hardly affects the basal culm internodes and may supply the necessary nitrogen for the attainment of a high grain yield without increasing the susceptibility to lodge. The advantage in lodging resistance and subsequent grain yield, of N dressing after the onset of stem elongation, rather than earlier application, has been reported for winter wheat (Bremner, 1969; Hadiiselimovit, 1969; Widdowson et al., 1961 ), spring wheat (Vetter and Assadolahi, 1962), barley (Prikryl, 1970; Vetter and Assadolahi, 1962), and oats (Brouwer et al., 1961; Ulmann, 1966). Under conditions of low availability of soil N, which require a basic N dressing, it has been shown that lodging of wheat could be decreased and grain yield increased by applying the nitrogen in split dressings, i.e., a certain minimum basic dressing and an additional top dressing after the onset of stem elongation (Chowdhury and Bains, 1967; Karchi and Rudich, 1964). Reduced lodging and subsequent increase in grain yield due to split spring applications of nitrogen to winter wheat, have been reported from the Netherlands (Dilz, 1967; Jonker and de Jong, 1966), Sweden (Fajersson, 196 1) , and Switzerland (Geering, 1964). Similar results have been obtained for winter-sown barley (Jonker and de Jong, 1966). Split application in these cases implies an early dressing at the onset of growth in spring and a second one during the period of intensive stem elongation. However, regarding spring barley in England, Widdowson (1962) warns against late N topdressing which may in wet years delay ripening and thus increase the risks from lodging induced by storms. It should also be mentioned that lodging following high N dressing in the form of calcium cyanamide was less severe than when equivalent amounts of N were applied as calcium nitrate or calcium ammonium nitrate (Bauer, 1963). This should be attributed to the slower N availability of the calcium cyanamide and, in the case of eyespot-induced lodging, also to the fungistatic effects of this fertilizer (Bauer, 1963; Diercks et al., 1968). 5 . Irrigation Practice Discussing the results obtained from irrigation experiments of spring wheat at Prosser, Washington, Robins and Doming0 (1962) concluded:

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MOSHE J. PINTHUS

“Reductions in early vegetative growth and plant height greatly reduce susceptibility to lodging during and following later irrigations. This suggests the advisability of withholding spring irrigation as long as possible, preferably until the early boot stage.’’ Irrigation per se is conducive to lodging (Fig. 2), which is particularly detrimental during the period of grain development (Section 111, B, 1 ) . Therefore, if the moisture requirement during this period is to be supplied or supplemented by irrigation, it may presumably be least risky at the late boot stage, in order to secure recovery by the time of heading (Section 11,C) . Trials with winter wheat in the northern Caucasus showed that lodging was promoted less by sprinkler irrigation than by furrow irrigation (Pyatggin and Semikhov, 1967).

6. Blends of Crops or Cultivars Lodging of susceptible varieties may be reduced through admixture with other varieties, preferably with more resistant ones. The blends were generally found superior to the average of the individual components grown alone. This has been reported for wheat (BorojeviC and MiSiC, 1962) and for oats (Grafius, 1966; Patterson et al., 1963). In Bulgaria, lodging of feed barley was reduced considerably by blending it with 30-50% wheat (Petrov, 1968). Improved lodging resistance of barley mixed with about 10% oats was reported from Scotland (Anonymous, 1954). The beneficial effect of blends may be ascribed to the support extended by the shorter or otherwise more resistant varieties and also to mutual support of varieties differing in growth rate and maturity. It seems that the practical use of this lodging-control measure will be restricted to feed grains or to very susceptible cereals grown for forage. 7 . Clipping and Grazing

Lodging due to excessive foliage during the period of elongation of the lower culm internodes may be prevented by clipping or grazing. This should be done before culm elongation has proceeded sufficiently for the apices to be damaged. Early studies on this method have been reviewed by Holliday ( 1956). It was successful in controlling lodging and in certain cases caused a subsequent increase in grain yield. However, in most cases grain yield was reduced following grazing or clipping. More recently, successful application of this method-which did not reduce grain yield and sometimes even increased it-has been reported from Arizona (Day el al., 1968), Britain (Aldrich, 1959; Hayes, 1959), and South Africa

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WHEAT,

BARLEY, AND OATS

243

(Lesch and Penzhorn, 1964). In other experiments this method, although effective in the prevention of lodging, caused a reduction in grain yield (Gardner and Wiggans, 1960; Nishimura and Arata, 1957). It seems that in order to secure high grain yields, the clipping or grazing should be performed without excessive compaction of the soil, and adequate moisture and nutrient supply must be available during the subsequent period. However, it is suspected that this method may interfere with the attainment of top yields.

B. APPLICATION OF 2-CHLOROETHYL TRIMETHYLAMMONIUM CHLORIDE Since the early 1960’s information has been accumulating on the prevention or reduction of lodging and subsequent increase in grain yield following the application of 2-chloroethyl trimethylammonium chloride (CCC) . The main success has been with wheat, with which the chemical is in widespread use on a commercial scale in many countries, especially under very fertile conditions where high grain yields are attainable. At present, the application of CCC is the best preventive measure against lodging of wheat: not only does it not interfere with grain yield, it may even increase it by its own merits. Unfortunately, the use of CCC has not expanded in the United States, and little information on field experiments in that country is available. The effects of this chemical and the methods of its application have been reviewed by several authors (Humphries, 1968a; Linser, 1968a,b; Wiinsche, 1970). The reference to studies cited in these reviews in similar context will not be repeated here [the citation to Wunsche (1970) indicates his experimental results rather than the literature review which precedes them]. CCC is a growth regulant which extends a retarding effect on cell division and elongation in the subapical meristem (Cathey, 1964). Consequently, it reduces the elongation of culm internodes, and this is usually accompanied by an increase in wall thickness and culm diameter. An increase in the number of vascular bundles has also been observed (Mayr and Presoly, 1963). Application of CCC at a period close to the onset of culm elongation affects the basal internodes, and this, presumably, is the main cause of its improvement of lodging resistance. In spite of their stronger effect on the shortening of the upper internodes, which often results in a greater total reduction of height, late applications are usually less effective in the prevention of lodging than the early one. Recent detailed information on the effects of application at different growth stages has been reported by Primost ( 1970) and by Wunsche ( 1970).

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Some of the beneficial effects of CCC on lodging resistance have occasionally been ascribed to its apparent effects on the promotion of root development (e.g., Chlyah, 1968). However, negative effects of CCC on the root system of cereals have also been reported (Maas, 1970; Wunsche, 1970; to mention the recent ones). In certain cases an increase in the number of coronal roots may have resulted from increased tillering, due to a delaying effect of CCC on the initiation of spike differentiation. The application of CCC may contribute to lodging resistance also by reducing the incidence of eyespot (recent publications include Maclean, 1970; Sturm and Eitel, 1968; Witchalls, 1970). The effect on eyespot, however, is not fungicidal but should rather be ascribed to the strengthening of the culm walls. Although varietal differences have been observed (e.g., Lowe and Carter, 1972), it seems that the improvement of lodging resistance induced by CCC applies to common and durum wheat in general, including semidwarf varieties (Humphries, 1970). Varietal differences in response may be at least partly due to differences in growth stage at the time of application and to differences in vegetative development, which affects the uptake of the chemical. Plants with a great number of big leaves will take up more of the chemical than plants with a poor foliage. The effects of CCC on lodging resistance of oats are less than those on wheat, although considerable culm shortening has been accomplished with it. Nevertheless, in this crop too, improvement of lodging resistance following the application of CCC has been obtained in several cases (e.g., Boland, 1969a; Humphries, 1970; Petr and PolBiek, 1971; Sturm and Jung, 1969). The results obtained with barley are rather inconsistent. The effects on lodging, as well as on culm elongation of this crop, are in most cases less than those on wheat (recent publications include Bergmann et al., 1970; Boland, 1969b; Humphries, 1970; Lovato and Venturi, 1968; Maddens and Bockstaele, 1970; Martin, 1969; Petr and PolBlek, 1971) . The best results with CCC on wheat have been obtained with foliar sprays at rates of 1-5 kg/ha. These sprays may be applied in combination with N fertilizers or with various herbicides (Peev, 1970; Rudich et al., 1969; Skorda, 1970; Sturm and Eitel, 1968). The results from soil applications or seed dressings have not been consistent, which should be attributed to differences in the decomposition of the chemical in the soil, depending on prevailing temperature and humidity. CCC sprayed onto wheat during the period of grain development, was incorporated into the seed at a rate sufficient to induce in the offspring responses similar to those obtained from direct application of the chemical (Bokhari and Youngner, 1971; Pinthus, 1967b). Promising preliminary results on the improvement of lodging resistance were obtained with this method (Pinthus, 1968), but

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subsequent trials on a larger scale failed to corroborate the original findings (M. J. Pinthus, unpublished). Although CCC has in many cases increased the grain yield of wheat even when no lodging occurred in untreated plots, a reduction in grain yield following its application has also been encountered. This should be ascribed primarily to the promotion of certain fungal diseases, e.g., Septoria nodorum and S . tritici, which, under humid conditions, may benefit from the more dense foliage and delayed ripening of CCC-treated plants.

c.

APPLICATION OF HERBICIDES AND OTHER CHEMICALS

Prevention of lodging by means of burning excessive foliage with sulfuric acid was practiced long ago (Moore, 1949). Application of this chemical has also been effective in controlling eyespot-induced lodging (Glynne, 1951; Salt, 1955). Recently, the fungicide benomyl was found to control eyespot and subsequent lodging in barley (Davies and Gareth Jones, 1971). Various herbicides improve the lodging resistance of cereals. Positive results have been obtained with certain triazines and urea compounds (Heitefuss and Bodendorfer, 1968), and with DNC, DNBP, and maleic hydrazid formulations (Reichard and Schonbrunner, 1961 ) . This may be attributed mainly to the elimination of weeds, which in turn improves light interception and may thus reduce lodging. A certain retardation of the growth of the cereal crop may also have been caused by the herbicides. Shortening and thickening of the lower culm internodes following the application of 2,4-D have been observed and suggested as means of preventing lodging (Mashtakov et al., 1954). However, relevant information is available only since the advent of CCC, from trials in which mixtures of this chemical with various herbicides, as well as the herbicides alone, have been tested. From these trials it is evident that various phenoxy compounds, in particular 2,4-D and MCPA, indeed improved lodging resistance, following their retarding effects of internode elongation (Caldicott and Nuttall, 1968; Frohner, 1965; Jung and Sturm, 1966; Rudich et al., 1969). In certain cases the admixture of these herbicides enabled a reduction in the amount of CCC applied (Jung and Sturm, 1966). However, indications of antagonistic effects between CCC and 2,4-D applied together have also been found (Rudich et al., 1969). In our trials (in cooperation with Z. Karchi and A. Zakay, unpublished) the best control of lodging of wheat was achieved with an application of 2,4-D or MCPA at the tillering stage, followed by spraying CCC at the time of elongation of the second culm internode. In this context it should, however, be pointed out that various herbicides

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may cause damage to the coronal roots of cereals and thus reduce their lodging resistance (Maas, 1968, 1970). Positive effects on lodging resistance, or on characters related to it, have been obtained with several growth regulants other than CCC. However, relevant trials have been conducted, so far, to a very limited extent only, and no marked advantages of these chemicals over CCC have been established. Bromocholine bromide (BCB) has been found similar to CCC in its effects on culm characters and lodging resistance of wheat in some Russian studies (Prusakova et al., 1967). Improved lodging resistance and subsequent grain yield were obtained in India following the application to wheat of Mendok (sodium 2,3-dichloroisobutyrate) (Mohan Ram and Rustagi, 1969). In this case also, lodging resistance was attributed to shortening and thickening of the culms. Similar effects on the culms of wheat and promising preliminary results with regard to lodging resistance were obtained with CMH [N-dimethylN-(p-chloroethyl) hydrazonium chloride] by Jung ( 1967) and with the respective bromoethyl bromide ( B M H ) by Bergmann et al. (1970). In a wheat trial in Israel, ethephon (2-chloroethanephosphonic acid) performed similarly to CCC in retarding culm elongation and preventing lodging (Karchi, 1969). Similar results were reported from Czechoslovakia (Petr and PolGek, 1971). Reduction in stem length of barley following the application of this chemical was reported from England (Murray and Dixon, 1970), whereas in the Czech experiments barley responded only very slightly and in oats a certain shortening of the lower internodes was observed (Murray and Dixon, 1970). However, Humphries ( 1970) found that barley and oat plants sprayed with ethephon lodged sooner than untreated plants. VII.

Breeding for. lodging Resistance

Improved lodging resistance is the most obvious feature to which the grain yield superiority of new cereal varieties over old ones may be ascribed. The better lodging resistance enables the new varieties to benefit from high levels of soil fertility and N applications and thus to approach their yielding potential. This has been observed in many studies (e.g., Aufhammer, 1970; Paquet, 1968). The most striking illustration, however, was presented recently in Austria when two standard winter wheat varieties were compared with an old Hungarian landrace, grown from seeds which were produced from the offspring of seeds dating back to 1877 (Ruckenbauer, 1971). The culm length of the old variety was 129 cm, 32 cm longer than that of the new varieties, it lodged badly, and yielded 40%

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less grain than the check varieties (and was also more susceptible to leaf rust and mildew). It may be concluded that better lodging resistance was achieved by deliberate breeding as well as through the selection for high yield under fertile conditions. The breeding of short-strawed varieties has contributed considerably to lodging resistance but has not eliminated the problem of lodging. Under abundant moisture and nutrient supply even the semidwarf varieties are prone to lodge and thus prevented from yielding commensurate with their potential. Data presented by Ephrat et al. (1965) indicate that the superiority in grain yield of a semidwarf wheat variety over a tall one decline from 1040 kg/ha ( 2 1 % ) in a year with little or no lodging, to 250 kg/ha when more lodging occurred. Growth regulants, such as CCC, have also not yet presented an entirely satisfactory solution to the problem and in any case their application involves extra expense. Therefore, lodging resistance still presents an important challenge in any cereal breeding program. Resistance to lodging, unlike resistance to disease or pests, is similarly to grain yield, a character of the plant population rather than of the single plant. Moreover, it is strongly affected by environmental conditions. Therefore, its evaluation is rather complicated and plant breeders have made use of various lodging indices as selection criteria. Selection according to plant character associated with lodging resistance has also been applied, especially in the evaluation of initial breeding material from rather comprehensive collections (Basistov, 1970; Kohli et al., 1967; Strutsovskaya, 1968). A.

EVALUATION OF LODGING RESISTANCE 1 . Direct Assessment in the Field

Lodging may sometimes not occur at all, or only very slightly, so that none of the tested lines or varieties are affected. On the other hand, under conditions extremely favorable to lodging, all the lines may lodge-which again will not enable any distinction to be made. Moreover, lodging is greatly influenced by variety X environment interaction effects (Fig. 5 ) . Consequently, no single “lodging nursery” may provide valid information for selection, which should rather be performed on the basis of evaluation over a wide range of environmental conditions. This has already been pointed out by various authors (e.g., Atkins, 1937; Baier, 1965; Hamilton, 1951; Murphy et al., 1958). In Denmark it was suggested to test cereal varieties at five N levels in order to obtain an estimate of lodging resistance (Pedersen, 1964). Considering the effect on lodging of the growth stage

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at which the lodging-induced conditions occur, selection should be performed within groups of lines of similar maturity. The grading for lodging resistance requires a reliable rating of the severity of lodging which should consider the prevalence as well as the degree of lodging. Unfortunately, this has not always been strictly observed and no standard quantitative method has been adopted. Furthermore, the grading should distinguish between stem lodging and root lodging (Section 11, A), and should be repeated several times throughout the period from head-

ZIG. 5. Lodging (rates from 0 = no lodging, to 4 = complete lodging, averaged ove three replications) of ten spring wheat varieties on four different fields at St. Paul, Minnesota, 1958.

ing to harvest. A single rating at harvest time may overestimate late lodging resulting from culm breakage of dry straw, and underestimate lodging prior to heading because of the recovery from it. Murphy et al. (1958) found a high correlation ( r = 0.89) for oats between the percentage of culm curvature, i.e., culms which had recovered from early lodging, and the prevalence of lodging at full ripeness. However, recovery from early lodging may sometimes increase the resistance to later lodging (Section 11, C) . Therefore, it is suggested that the rating of lodging should be based on the position of the lower culm internodes rather than on the inclination of the upper part of the culm and of the head. This is based on the assumption that if the external factors conducive to lodging had operated

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at a later growth stage, “unrecoverable” lodging of similar severity would have occurred. All these difficulties in making a valid direct assessment of lodging resistance in the field, warrant the attempts of breeders to find alternate methods. This is of vital importance for the evaluation of early breeding material consisting of a great number of lines, each with only a small quantity of seed. 2 . Auxiliary Methods Lodging resistance and associated characters of cereal plants grown in pots have been evaluated in wind tunnels (Bauer, 1964), and mobile wind tunnels have been used for this purpose in field plots (Section 111, A, 4). However, these methods are complicated and costly and their reliability with regard to root lodging is doubtful. Turkova and Suan (1966) suggested that lodging resistance be estimated by the degree of bending of the second culm internode following plant treatment with auxins and with reductases. Varietal differences in lodging had indeed been established following spraying of wheat with heteroauxin (Petinov and Urmantsev, 1964). The attempts to identify lodging resistance at early growth stages are of particular interest. Percival (1921 ) claims that wheat varieties with young spreading shoots are firmly anchored to the soil and thus resistant to root lodging, whereas erect young shoots indicate a poor spread of the root system and consequent lodging susceptibility. The relations between lodging resistance in the adult plant and mechanical strength in the seedling stage has been investigated by Baier (1965) and by Holienka and HruSka ( 1962). The latter investigators could distinguish the most susceptible varieties, whereas Baier concluded that this relation was not close and consistent enough to provide a reliable criterion of evaluation. The snap test (Section IV, C, 1) has proved useful for the evaluation of lodging resistance of differing lines of oats (Hess and Shands, 1966). 3. Lodging Indices

The recognition that lodging resistance cannot be attributed to any single plant character, the correlations which have been established between varietal differences in lodging and various characters and those found among these characters, have led to the combining of several plant characters into lodging indices. Some of these indices were closely correlated with lodging in the field and could therefore be utilized as selection criteria of lodging resistance. The ratio of culm length to diameter of basal internodes was found to be rather closely correlated with lodging resistance ( r = -0.67 to -0.85)

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in various studies of the three cereals (Basistov, 1970; Hamilton, 1941; Hansel, 1957; Wav, 1960). A little more sophisticated modification of this index is the ratio of area of culm wall cross section to culm length (Wag, 1970). Indices which take the root development into consideration are of particular interest. The ratio of culm length: number of coronal roots per culm was applied by Hansel (1957) but he did not find it superior to the first-mentioned index. The top weight :root weight ratio has been found to give an indication 01 lodging in wheat (Malkani and Vaidya, 1956) and oats (Sechler, 1961 ) . This index could be improved by adding to it an estimate of breaking strength (Malkani et al., 1959), and still better results were obtained when culm length was also included (Vaidya and Singh, 1963). Applying discriminate function analysis, Hamilton ( 195 1) developed an index in which 10 x culm diamter ( m m ) 5 x root rating (on a 1-10 scale) 1 x plant height (inches) were combined. [The detailed analytical procedure in this case is presented as Example 17-2 by Goulden ( 1952) .] With this index he could readily differentiate lodging-resistant oat varieties from susceptible ones. Similarly, ZeniSEeva and Lekes (1966) combined culm length, length of second internode, and breaking strength of culms and roots into an index ( Y ) which was found, with all three cereals, to be very closely correlated ( r = 0.90) with lodging resistance. Successful ranking of lodging resistance of winter wheat varieties was achieved by Miller and Anderson (1963) with the quotients LBC/Ht or LBC/(log Ht/3)?, where LBC (load-bearing capacity) is the product of the weight (g) supported by a culm and the horizontal displacement (cm) of the spike from the vertical position, and Ht = culm length (cm). LBC is determined by hooking a chain, of known weight per link, to the head of the plant. High values of r (-0.8 to -0.9) were found by Oda et al. (1966) for the correlation between lodging resistance of wheat and barley and the lodging index L = Z"W/wM, where 1 = culm length (cm), W = total fresh weight per tiller (g), w = culm dry weight per tiller (g), and M = bending moment at breaking ( 1 0 0 g-cm), which was determined by a special apparatus. The most widely used measure for estimating lodging resistance seems to be the cLr factor devised by Grafius and Brown (1954) and found by them to be effective for the selection of lodging-resistant lines of oats. cLr = F / b , where b = culm length (cm), and F = bending force (g), which is determined at the point where the culm stops its downward bending, as the weight of the links of a chain hanging down from the head of the plant to the ground. Close correlations between this factor and lodging resistance were also found for barley (Grafius, 1958) and for wheat

+

+

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(Roman and Muszyhska, 1962; Waa, 1960), whereas no such correlation was found by Mukherjee et al. (1967). In spite of the close correlation of the cLr with lodging resistance of oats, it was found inferior in this respect to the snap test (Section IV, C , 1) by Murphy et al. (1958) and more expensive than the snap test by Frey et al. (1960). Jellum (1962) found that the cLr values of oats changed in relation to maturity, declining during a 15-day period following anthesis and then leveling off. Bauer (1964) indicated that in wheat the cLr factor overestimates the role of culm rigidity in lodging resistance, and underestimates the role of culm length; he suggested to multiply the factor by 100/culm length. The correlation between the cLr and lodging resistance of oats was found to be affected by differences in the area of the heads (Grafius, 1958). This index should therefore apply primarily for the evaluation of lodging resistance within groups of similar panicles. An increase in the value of lodging rates assessed in a single field trial was attempted by combining them with the respective snap scores, cLr values, and estimates of culm curvatures, into a lodging-resistance index (Murphy et al., 1958). The practical value of any of the above-mentioned indices is dependent, in addition to its correlation with lodging in the field, on the number of lines which can easily and inexpensively be evaluated by it. None of them can replace, in the final stages of a breeding program, the assessment of lodging resistance in the field under a wide range of environmental conditions. B.

INHERITANCE

OF

LODGING RESISTANCE AND ASSOCIATED CHARACTERS

The earliest relevant work seems to be that of Howard and Howard (1912) in India. They investigated F, populations of crosses of common wheat varieties with strong roots and weak straw X varieties with weak roots and strong straw and concluded that strength of roots and strength of straw were independently inherited and that lodging resistance was due to the combination of both characters. From the few studies which are available on the inheritance of lodging resistance proper, the following points are apparent. Different degrees of dominance have been observed (Aastveit, 1962; Nasr et al., 1972; ZeniSEeva, 1968). Rather high heritability estimates ( > 5 0 % ) were found in some cases (Hess and Shands, 1966), intermediate (25-50%) ones in other cases (Nasr et al., 1972), and low values in still others (ZeniSEeva, 1968). Maternal effects on lodging resistance were observed in reciprocal crosses of barley (Zhivotkov, 1968). Maternal effects have also been ob-

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served on the inheritance of the length and diameter of the basal culm internodes in progenies of crosses between lodging-resistant and susceptible wheat varieties (Roman, 1962a). In other crosses between lodging-resistant and susceptible barley varieties (ZeniSEeva, 1968), incomplete dominance was found of resistance, estimated through the lodging index Y. Various degrees of dominance as well as recessiveness of lodging resistance, estimated by the cLr method, were obtained by D. A. Wheeler in different oat crosses (Jensen, 1961). Rather low heritability estimates (15% ) were obtained in this study for the F,-F, comparison; this was also the case in another study of the cLr values in segregating oat crosses (-Frey and Norden, 1959). In a cross of a lodging-resistant x susceptible wheat variety, Atkins (1938) found intermediate weight per unit length of culm with some tendency to the higher parent in F,. Significant correlations (r = 0.6) were found between the expression of this character in F, plants and F, progeny lines, and between F, plants and F, progenies. In a certain wheat cross, stem breakage was found to be controlled by a single gene, the strong straw being slightly dominant (Boyce, 1948). In another study (Kohli et al., 1970), breaking strength as well as culm diameter revealed a quantitative mode of inheritance, and transgressive segregation for both characters was observed in F,. Inheritance of stem solidness in wheat has been studied in relation to sawfly resistance. This and the inheritance of some other culm characters of wheat have been reviewed by Ausemus et al. (1967). Inheritance of the number of vascular bundles and of the size of the sclerenchyma ring was studied in crosses between lodging-resistant and susceptible wheat varieties by Jankovib ( 1966b), who also reviewed some of the earlier literature on this subject. Both characters show polygenic inheritance and certain degrees of dominance of the greater values. Similar results for vascular bundles and culm-wall thickness were obtained by Roman ( 1962a). The number and thickness of coronal roots in F, populations of crosses between lodging-resistant and susceptible wheat varieties were found to be intermediate by Roman (1962b). In barley, dominance of root tensile strength was observed by ZeniSEeva (1968). Inheritance of the length of the root crown of oats was found to be controlled by at least three factor pairs and also to be affected by many modifying genes; dominant factors may be involved in the determination of both long- and short-root crowns (Sechler, 1961 ) . It may be concluded that the inheritance of most root and culm characters associated with lodging resistance is rather complex and has not yet been sufficiently investigated. A conspicuous exception, however, is the culm length character of wheat, which has been studied extensively (Briggle and Vogel, 1968; Johnson el al., 1966; Woo and Konzak, 1969). Fac-

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tors influencing stem length were found on many chromosomes; several major, as well as many minor, genes have been shown to control this character in different crosses; the dwarfing factors are generally recessive, but dominant ones have also been observed. From the point of view of lodging resistance it is of major importance that there are indications of the existence of independent factors controlling the length of the different internodes (Paquet, 1968). C.

AND PROSPECTS OF BREEDING ACHIEVEMENTS

The combination of lodging resistance with other favorable agronomic traits through the intentional cross breeding of parental varieties excelling in these characters has been obtained in wheat (Pal, 1944), barley (Ambastha, 1962), and oats (Ponomarenko, 1971 ). More often, however, the improvement of lodging resistance should be ascribed to selection for this trait in general breeding material. In this respect the snap test (Section IV, C, 1) has been particularly effective as a selection criterion for oats (Murphy et al., 1958). Considerable success has been achieved in the selection of lodging-resistant mutant lines in all three cereals. This subject has been reviewed in detail by Scarascia Mugnozza (1965). The Swedish barley variety Pallas is one of the high-yielding and lodging-resistant varieties obtained through mutation breeding (Gustafsson and Ekman, 1967). Several other lodgingresistant barley and oat varieties, selected directly after mutagenic treatment or out of the progenies of crosses between the mutants and other varieties, have already been released (Sigurbjornsson and Micke, 1969). Rather impressive success in mutation breeding of lodging resistance has been achieved with durum wheat in Italy (Scarascia Mugnozza and Bozzini, 1968). Several of the resulting mutant lines have excelled in lodging resistance and grain yield in extensive trials at many locations throughout the Mediterranean region and the Middle East (Bogyo et al., 1969). The increased lodging resistance of the mutants has been associated in many cases with reduced culm length, but this has not always been the case. Moreover, several lodging-resistant durum mutant lines were significantly higher than their mother varieties (Scarascia Mugnozza, 1965). Mutants of the Austrian durum wheat ADUR showed less reduction in grain yield when their lodging resistance was not accompanied by reduction in height (Nagl, 1971 ) , The improved lodging resistance of various mutants could be attributed to several characters other than culm shortness: number of elongating internodes, relative length of the different internodes, culm anatomy and solidness, and structure of the basal internodes. Breeding for various anatomical culm characters related to lodging resistance and particularly for those of the basal internodes, has been sug-

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gested (Nitr, 19160; ZeniSEeva and LekeS, 1971) . However, the greatest achievements of lodging resistance through the breeding of any single character have been accomplished by reducing culm length. In addition to the famous semidwarf wheat varieties (Borojevic, 1968; Briggle and Vogel, 1968), new barley and oat varieties which owe their lodging resistance to reduced culm length have been bred. BARTELbarley in Arizona (Day et al., 1972) and RANDOM oats in Canada (Kaufmann, 1971) are only two examples of recently released varieties. Semidwarf varieties may suffer from several defects, e.g., reduced seedling emergence and increased susceptibility to various diseases, which present urgent challenges to current breeding programs (Berbigier, 1968; Briggle and Vogel, 1968). Under certain agricultural conditions their reduced straw yield has also been disadvantageous (Pal, 1966). Nevertheless, the availability of suitable genetic material, the ease of selection, and the possibility of starting selection in early generations, in addition to the previous achievements, justify and encourage the improvement of lodging resistance through the breeding of reduced culm length. Lines with improved lodging resistance were obtained following two or three cycles of selection, out of established winter wheat varieties, of plants with well-developed root systems (Il'inskaya-CentiloviE and TeterjatEenko, 1961); when selecting, the spread, number, and thickness of the coronal roots were considered. These authors claim that the improved root system of the selected types was accompanied by an increase in the thickness of cell walls and in the number of vascular bundles in the sclerenchyma of the stem. However, generally root characters have been neglected in the work of breeding for lodging resistance. This has obviously been due to the practical difficulties involved with the evaluation of the root system. However, the causal relationship between this character and root lodging, and the weak variety X environment interaction effects on the spread of the roots in the upper soil layer (Pinthus, 1967a), warrant some breeding efforts in this direction. This may be particularly rewarding with the improvement of high-yielding, short-strawed varieties which nevertheless are prone to lodge under conditions of high fertility. VIII.

Increased Exploitation of Yield-Promoting Factors Due to the Prevention of lodging

The exploitation of yield-promoting factors, such as N fertilization or irrigation, is dependent on the prevention of lodging. This may be illustrated by the following examples. In an experiment in Italy (Scarascia Mugnozza et al., 1965), the durum

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wheat CAPPELLI and its lodging-resistant mutant B 132, without N-fertilization, yielded 2628 and 2643 kg/ha, respectively. After the application of 120 kg/ha N, the grain yield of the mutant, which did not lodge, was increased by 82 % , whereas that of Cappelli, which lodged considerably, was increased by only 28%. Similarly, certain trials in Britain have shown that the differential response of barley varieties to high rates of nitrogen could be attributed almost entirely to varietal differences in lodging (Holmes, 1969). In India, grain yield of a semidwarf lodging-resistant wheat variety could be increased considerably through adequate irrigation, whereas the response of tall varieties to irrigation was considered to be limited because of lodging (Misra et al., 1969). In many cases, the prevention of lodging by the application of CCC enabled wheat to benefit from high N fertilizer rates (Humphries, 1968a; Wunsche, 1970). Similarly, under certain field conditions in Israel, CCC has increased the beneficial effects of irrigation on wheat yield. Up to the level of grain yield which has hitherto been achieved under the most favorable conditions, lodging indeed constitutes the main factor limiting the response of cereals to yield-promoting agents. Consequently, the prevention of lodging through the application of CCC as well as through the cropping of semidwarf varieties, may enable the attainment of this grain yield level. However, beyond this level, any further increase in grain yield will depend on the more effective use of ambient light. This may perhaps be achieved through the development of hybrid varieties. However, considering the dominant nature of the height-controlling genes (Section VII, B ) and some other information on hybrid wheat (e.g., Johnson and Schmidt, 1968), the hybrids are expected to be tall and therefore susceptible to lodging. On the other hand, the cereal “ideotype,” proposed by Donald (1968), wiIl be a weak competitor, to be planted densely, having a single culm with a big awned head. It may be added that long upper internodes, which should complete their elongation by the onset of grain development, would also be advantageous for the assimilation of carbohydrates and their supply to the grain. The yielding capacity of such an ideotype will obviously be limited by lodging. Consequently, further efforts to prevent lodging, whether by chemical means or by breeding lodging resistance, will be needed in future in order to benefit from the anticipated increase in grain yield potential. It may be concluded that there is a permanent requirement for increased lodging resistance which is linked to the continuous process of grain yield promotion. ACKNOWLEDGMENTS

Mr. D. Trifon, C.E. contributed considerably to Section 11, B. Mrs. V. Priel read and corrected the manuscript. Their assistance is greatly appreciated.

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537-558. Scarascia Mugnozza, G. T., and Bozzini, A. 1968. Euphyticu 17,Suppl. 1, 171-176. Scarascia Mugnozza, G.T., Bagnara, D., Bozzini, A., and Mosconi, C. 1965. Genet. Agr. 19, 195-198. Schultz, J. E. 1971. Aust. 1. Exp. Agr. Anim. Husb. 11, 450-454. Sechler, D.T. 1961.Mo., Agr. Exp. Sia., Res. Bull. 769. Sharma, K. C., Misra, R. D., Wright, B. C., and Krantz, B. A. 1970. Indian J . Agron. 15, 97-105. Shrivastava, M. M. P., and Yawalkar, K. S. 1960. Indian J . Agron. 4, 246-257. Sigurbjornsson, B., and Micke, A. 1969.Induced Mutaiions Planis, Proc. Symp., 1969 pp. 673-698. Sillampla, M. 1971.F A 0 Soils Bull. 12. Sisler, W.W.,and Olson, P. J. 1951. Sci. Agr. 31, 177-186. Skopik, P. 1969. Rostl. Vyroba 15, 265-273. Skorda, E. A. 1970.Episiemonicon Deltion (Greece) 38. Skucihska, B. 1965.Hodowla Rosl., Aklim. Nasiennictwo 9, 589-640. Spahr, K. 1960.Z. Acker- Pflanzenbau 110,299-331. Strutsovskaya, E. S. 1966. Sb. Tr. Aspir. Molodykh Nauch. Sotrudinkov., Vses. Nuitch.-lssled. Inst. Rastenievod. 7, 88-93; Field Crop Abstr. 20, 47 (1967). Strutsovskaya, E. S. 1968. Selek. Semenovod. (Moscow) 1968 (2), 28-31. Sturm, H.,and Eitel, J., 1968. Meded. Riiksfac. Landbouwwetensch., Gent 33,

1373-1 379.

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Surganova, L. D. 1967.Sb. Tr. Aspir. Molodykh Nauch. Sotrudnikov., Vses. Nauch.Issled. Inst. Rastenievod. 8, 35-40; Field Crop Abstr. 21, 1526 (1968). Syme, J. R. 1968. Aust. J . Exp. Agr. Anim. Husb. 8, 574-577. Timoshenko, S . 1940. “Strength of Materials,” 2nd ed., Part 1. Van Nostrand-Reinhold, Princeton, New Jersey. Troughton, A. 1962. Commonw. Bur. Pasture Field Crops Mimeo. Publ. 2. Turkova, N. S., and Suan, L-T. 1966. Nauch. Dokl. Vyssh. Shk., Biol. Nauki 1, 167-170;Field Crop Abstr. 20, 1519 (1967). Turkova, N. S., Vasil’eva, L. N., and Cherernukhina, L. F. 1965. Fiziol. Rust. 12, 825-831;Sov. Plant Physiol. 12,721-726 (1966). Uctum, S., and Hungerbiihler, K. 1968.Z. Acker- Pflunzenbau 128, 1-16. Udagawa, T., and Oda, K. 1967.’Proc.Crop Sci. SOC. Jap. 36, 192-218. Ulrnann, L. 1966. Rostl. Vyroba 12, 139-146. Vaidya, S. M., and Singh, B. 1963.Sci. Cult. 29, 247.

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GENESIS AND MANAGEMENT OF ACID SULFATE SOILS C. Bloomfield and 1. K . Coulter Rothomrted Experimental Station. Horpendcn. Herts. England

I . Introduction .................................................. 266 I1 . The Formation of Sulfides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267 A . Sources of Sulfur .......................................... 267 B. Sulfate Reduction in Anaerobic Soils ......................... 268 C Formation of Iron Sulfides .................................. 271 D . Environmental Factors and Sulfide Formation . . . . . . . . . . . . . . . . . 273 111 Oxidation of Sulfides .......................................... 278 A. Microbial Reactions ........................................ 278 B. Metallurgical Applications .................................. 281 C. Reactions in Soils .......................................... 282 D . Formation of Ochre in Field Drains .......................... 289 IV Mining and Corrosion Problems ................................. 290 A . Pollution ................................................. 291 B. Corrosion ................................................ 292 V . Classification and Mapping ...................................... 292 A Classification ............................................. 292 B. Mapping ................................................. 293 VI Conditions for Plant Growth .................................... 296 A . Toxicities ................................................ 297 B. Deficiencies ............................................... 305 C . Biological Factors ......................................... 307 VII . Management for Agriculture .................................... 308 A Waterlogging ............................................. 308 B. Drainage and Leaching .................................... 311 C . Liming .................................................. 313 D . Other Treatments .......................................... 314 E. Conclusions ............................................... 314 VIII. Analysis of Pyritic Soils ....................................... 315 A . Detection of Pyrite ........................................ 315 B. Measurement of Acidification ............................... 316 C. Determination of Monosulfide .............................. 316 D. Determination of Pyrite ................................... 317 IX. Conclusions .................................................. 318 References ................................................... 319

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I.

Introduction

Soil materials containing sulfides (mainly pyrites) that become very acid

on drying have been recognized for many years and the historical review by Poelman (1973a) draws attention to reports by Linnaeus in 1735 about the occurrence of “argilla vitriolacea” in swamps. In the Netherlands, the drainage of the Haarlemmermeer polder revealed unproductive areas where lime was absent, and these were attributed to the formation of “sulfuric iron oxidule .” The pale yellow mottles and general infertile nature of the soils led to the use of the term “Katteklei” (cat clay) for such soils by the Dutch farmers. This term has been widely adopted and has been used in most parts of the world where the soils have been found. More recently, however, the term “acid sulfate soil” has been introduced and this has generally supplanted the term “cat clay.” Acid sulfate soils are thus soils that have been drained, that have free and adsorbed sulfate, that show pale yellow mottles of jarosite, and that usually have a pH below 4 in water. Undrained soils with sulfides are also of agricultural importance since they may occur in situations where some form of reclamation is attempted; these are termed potential acid sulfate soils-i.e., they have the potential to develop exceptional acidity when drained. The degree of acidity that develops depends not only on the amount of sulfide but on a number of other factors, discussed in Section 111, C. Although it is very important to distinguish between actual and potential acid sulfate soils from mapping and agricultural aspects, the term acid sulfate soils will be used to cover both, distinctions being made as necessary. Dutch farmers seem to have been the first to encounter these problem soils, and Dutch scientists made the first systematic studies, although the total area in the Netherlands is quite small compared with that in other parts of the world. Soil surveys, either preceding or following development schemes, have located several million hectares, particularly in the tropics. Although some areas are not farmed at present, perhaps because of past failures, on much of these soils there is some form of agriculture, often rice cultivation. Generally the rice yields are very poor, of the order of 500-1000 kg/ha, but the contrast between these yields and those on nonacid sulfate soils was not too great until the introduction of new technologies; whereas better varieties, fertilizers, and water control can easily give yields of 4000-5000 kg/ha on normal soils, such inputs make little difference to the yields on acid sulfate soils. There have been insufficient soil surveys to give a reliable estimate of the area of acid sulfate soils throughout the world. Reviews by van Beers

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(1962) and Moorman ( 1963) give some indication of their extent, and more recent figures include those of van der Kevie (1973), 800,000 ha in the Bangkok Plain; of Moorman (1961), 2 million ha in Vietnam; of Watts (1969), 200,000 ha in West Malaysia; of Jordan (1964), 100,000 ha in Sierra Leone; and of Driessen (1 973), 2-3 million ha in Southern Kalimantan. Rocquero de Laburu and Garcia-Casal ( 1973) reported comparatively small areas in Brazil, but there are probably very large areas yet to be identified; thus Sioli (1964) states that there are 2.5 million ha of estuarine land at the mouth of the Amazon and large areas in the Orinoco delta are possibly potential acid sulfate soils. Other areas are reported in Senegal (Durand, 1967; Vieillefon, 1973) and Malagasy (Coutinet and Durand, 1966). Descriptions of some very acid soils in India and Pakistan strongly suggest an acid sulfate nature. Thus Varghese et al. (1970) described the “Pokkali” soils of Kerala state, which have pH values of 3.1 and considerable quantities of sulfate. “Kari” soils with a pH below 3.5 are referred to by Raychaudhuri and Anantharaman (1960) and Nambiar et al. (1966) record soils, also in Kerala, with pH values of 2.1, completely uncultivated except for rice grown in mounds on the fringes of the swamp. Brammer (1966) and Islam and Ullah (1968) refer to “Kosh” soils in Pakistan and state that 20,000 ha formerly good rice land, have gone out of cultivation. Such soils in East Asia in areas of dense population are, of course, of greater agricultural significance than much larger areas in thinly populated countries. In contrast to tropical countries, the areas of acid sulfate soils in temperate lands seem to be small. Apart from their well-documented distribution in the Netherlands, Sweden, Finland, Japan, Korea, and the United States, small areas have been reported in Western Australia (Teakle and Southern, 1937) and in the United Kingdom (Trafford et af., 1973). Although this review is concerned mainly with using these soils for agriculture, some attention is given to their use for fish ponds and to the problems associated with mining and engineering. II.

A.

The Formation of Sulfides

SOURCESOF SULFUR

Sulfur originates from sulfates in sea water, from ancient sediments or from biological materials. Sulfates from sea water are the source of sulfides in recent marine sediments, i.e., deltaic and coastal formations, which comprise the areas of major agricultural importance. Ancient sediments may

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contain large amounts of sulfides, and oxidation of these introduces serious problems in some lignite, bituminous, anthracite, pyrite, copper, zinc, and lead mines (Temple and Koehler, 1954). Oxidation of sulfides may provide sulfates for charging ground water in lower-lying areas and these, suggests Poelman (1973b), are the source of sulfur for further pyrite formation in these waterlogged areas. Subsequent drainage and oxidation Iead to sulfate formation and the creation of “cat sands,” sandy soils with jarosite mottles. Inland swamps at 2000 m have been described by Chenery (1953, 1954) in Uganda where the sulfur comes from surrounding formations. Sulfides weather to sulfates and encrustations of sodium sulfate appear in the nearby area, providing salt licks and soluble salts that enter the swamps in drainage water. Sulfides formed by reduction accumulate in these swamps. A similar situation has been described by Thompson (1972) in Rhodesia where the sulfates are thought to originate from deep seated springs and are then reduced in the peaty swamps in some areas. Solfataras may also provide excess sulfur in surrounding soils leading to high acidity. Sulfur from biological materials, algae, diatoms, etc., is described by Sombatpanit (1970) as the source of sulfides in some “gyttja” soils in Sweden. These soils are formed by the simultaneous sedimentation of fine mineral particles and plant and animal remains in rivers and lakes. Other gyttja deposits in Sweden and Finland originate in marine or brackish environments.

B. SULFATE REDUCTION IN ANAEROBIC SOILS When Hamlet asked, “How long will a man lie i’ th’ earth ere he rot?’ he was told, “. . . some eight year. A tanner will last you nine year.” Shakespeare may have underestimated the effect of tannins on protein, as the preservation of Iron Age bodies for 2000 years in Danish peat bogs seems to have resulted from some such process (Glob, 1971). The stomach contents of these bodies have been preserved well enough to permit identification of the various grains that constituted the last meals, so that digestive processes must have ceased quite soon after death. It seems unlikely that tannins would diffuse rapidly enough to account for this, and it has been suggested that the preservation of the stomach contents results from the action of hydrogen sulfide.

I . Sulfur Reducing Organism Hydrogen sulfide is formed in peat bogs, etc., as a product of putrefaction. Bacteria of the genus Clustridium are chiefly responsible for the anaerobic decomposition of protein, but another group of bacteria is a

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much more important source of hydrogen sulfide in anaerobic soils. These are the dissimilatory sulfate-reducing bacteria, an exclusive property of which is the utilization of sulfate in the same sense that higher organisms use oxygen-i.e., sulfate acts as the terminal electron acceptor for their respiratory processes. Postgate ( 1959 ) suggested the term assimilatory sulfate reduction to describe the production of sulfur-containing organic cell constituents, and dissimilatory sulfate reduction for the relatively much more extensive energy-yielding process. The process can be formalized as: 2CHa.CHOH.COOH

+ SO

1-

+ OCH3.COOH

+ 2C02 + 2H20 + S*-

Stoichiometric amounts of sulfide are formed, and if adequate sulfate is available, as in marine or estuarine environments, much hydrogen sulfide is formed at the expense of relatively little organic matter-as much sulfide would be formed by sulfate-reducing bacteria from 1 mole of lactic acid as would be provided by several kilograms of putrefying protein. Beijerinck described the original type species, Desulfovibrio desulfuricans, in 1895. Campbell and Postgate (1965) distinguished two genera, sporulating Desulfomaculum, and Desulfovibrio, which does not form spores (for recent reviews, see Postgate, 19.60, 1968; Roy and Trudinger, 1970; Kelly, 1970). Both occur in soils and waters. They are obligate anaerobes, but they are not killed by exposure to air, and although they do not become active unless the environment becomes anaerobic, they seem to occur in almost all damp terrestrial environments. Desulfovibrio also reduces thiosulfate, tetrathionate, and colloidal sulfur to sulfide (Postgate, 1959). In biological sulfate reduction experiments, in which the redox potential was controlled automatically, Connell and Patrick (1968) found that sulfate became unstable at about -150 mV. Under their conditions, the bacterial reduction of sulfate was confined to the pH range 6.5-8.5, which is a less acid lower limit than usual; pH 5 seems to be about the lowest value at which anaerobic sulfate reducers are active (Bloomfield, unpublished). Hydrogen sulfide diffuses readily, and, unless it is immobilized as an insoluble sulfide, it tends to enlarge the anaerobic zone and extend the environment favorable to the development of sulfate-reducing bacteria. Sulfate reducers have important effects in causing the precipitation of metal sulfides, notably of iron, in causing pollution of waters, etc., and they are responsible for the corrosion of steel buried in certain anaerobic soils. The reduction of elemental sulfur to sulfide is a widespread reaction among bacteria, yeasts, fungi, etc. (Roy and Trudinger, 1970). Bromfield ( 1953) found that, after partial sterilization with carbon tetrachloride,

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some soils evolve hydrogen sulfide when incubated aerobically with sucrose and ammonium sulfate. Partial sterilization apparently killed bacteria that inhibit the formation of hydrogen sulfide by Bacillus megatherium, which was identified as the responsible organism. 2. Sulfide Oxidizing Organisms

Certain lithotropic organisms, which use either radiant energy or the energy released by the oxidation of inorganic compounds for their synthetic processes, oxidize reduced sulfur compounds (Postgate, 1968; Kelly, 1971 ) . One group, the colorless sulfide-oxidizing bacteria, take advantage of a chemically unstable system in which dissolved air and hydrogen sulfide coexist. They occur at the interface of aerated and hydrogen sulfide-containing water, both fresh and saline. The most common members of this group are the filamentous sulfur bacteria, which often occur as a white scum in polluted water. Beggiatoa seems to be the member of this group about which most is known. It occurs in fresh and marine waters; it was originally thought to be strictly autotrophic, but heterotrophic strains have been isolated. Sulfur granules are deposited within the cell during the oxidation of sulfide, and sulfate appears later in the medium. Truper and Hathaway (1967) found that sulfur formed by strains of purple and green bacteria (Thiocystis violaces, Chromutium, and Chlorobium ) gave diffraction lines agreeing with those of orthorhombic sulfur. Photolithotropic bacteria accomplish the oxidation of sulfide under anaerobic conditions by linking the process to the photoreduction of carbon dioxide. Members of this group are colored green (Chlorobium) or purple (Chromatium), according to the relative contents of chlorophyll and carotene. Both form elemental sulfur during the oxidation of sulfide. They closely resemble the blue-green algae, some of which are also capable of oxidizing sulfide. They often occur in gelatinous masses. The various reducing and oxidizing sulfur bacteria together can form an ecosystem-the sulfuretum (Postgate, 1968). Hydrogen sulfide is generated in the anaerobic lower levels, and nearer the surface, at depths to which light can penetrate, autotrophic bacteria, including colored sulfide oxidizers, fix carbon dioxide and nitrogen, and oxidize sulfide. Higher still, at the fringe of the anaerobic zone, colorless sulfide oxidizers produce elemental sulfur which is oxidized to sulfate by Thiobacilli, which are discussed later. The cycle can continue indefinitely provided minor elements, light, air, and sulfate remain available. Sulfureta occur widely; the Dead Sea is a notable example, but they need be no bigger than a few grains of sand. 3. Development of Alkalinity The microbial reduction of sulfate in anaerobic soils is accompanied by the formation of carbon dioxide; the net result of this and the hydrolysis

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

27 1

of soluble sulfides is the formation of bicarbonate, and increased alkalinity. Verner and Orlovsky ( 1948) detected sulfate-reducing bacteria in saline soils, particularly in peaty and bog solonchaks where anaerobic conditions prevailed; they suggested that sulfate-reducing bacteria are responsible for the development of solonchaks and the accumulation of soda. Abd-ElMalek and Rizk (1963) concluded that microbial sulfate reduction was mainly responsible for the formation of natron, i.e., hydrated sodium carbonate, in Wadi Natrun in the Libyan desert. Janitzky and Whittig (1964) found an equivalent relationship between the amounts of sulfate reduced and bicarbonate formed. Ogata and Bower (1965) observed no appreciable reduction of sulfates in flooded and-zone soils, unless the organic matter content exceeded 5 % , or undecomposed plant residues were present. Szabolcs (1966) considered biological sulfate reduction to be responsible for the formation of alkali (szik) soils in Transdanubia. Hardan (1973) showed that the accumulation of carbonate in soils of the Mesopotamian plain results from microbial sulfate reduction. Thus acid sulfate soils could not form in a closed system in which the bicarbonates were preserved; mostly these are lost by leaching at the time of sulfide formation. OF IRON SULFIDES C. FORMATION

Sulfide formed in sediments tends to be precipitated by heavy metals, and such deposits are usually stained black by ferrous sulfide. Siebenthal (1915, quoted by Roy and Trudinger, 1970) considered biological sulfate reduction to have been involved in the formation of some zinc sulfide deposits in the United States; it seems to be at least a theoretical possibility that sulfate-reducing bacteria were responsible for the formation of some base metal sulfide deposits (ZoBell, 1946, see Postgate, 1960; Miller, 1950; Baas Becking and Moore, 1961; Dunham, 1961). The bacterial formation of iron sulfides is the process responsible for the accumulation of inorganic sulfides in soils and sediments, and is thus the ultimate cause of B e formation of acid sulfate soils. The conditions under which iron sulfides are formed has been intensively studied by Berner (1962, 1964, 1967, 1970, 1972), Roberts et al. (19691, and Rickard (1969a,b, 1973). According to Rickard (1973) seven iron sulfides are known: pyrrhotite; Fe,l_,,S, x = 0-0:126, hexagonal or monoclinic; mackinawite, c. FeS, tetragonal; cubic ferrous sulfide, c. FeS; griegite, Fe,S,, cubic; smythite, Fe,S,, hexagonal, possibly monoclinic; pyrite, FeS,, cubic; marcasite, FeS, orthorhombic. Rickard ( 1969a) prepared all but smythite and cubic ferrous sulfide in bacterial sulfate reduction experiments.

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In relation to the formation of acid sulfate soils, the essential aspect of sulfide formation is the accumulation of iron disulfide, which usually occurs as pyrite, but occasionally as marcasite. 1 . Formation of Pyrite and Marcasite Allen et al. (1912) prepared iron disulfides by heating sulfur and ferrous sulfide in sealed tubes. The formation of marcasite was favored by acid conditions, whereas pyrite was formed near neutrality. Pyrite and marcasite were distinguished by chemical and optical crystallographic methods. Verhoop (1940) prepared pyrite by anaerobic incubation of ferrous sulfide and elementary sulfur at room temperature. Berner (1962) investigated the effect of hydrogen sulfide on various iron compounds, and concluded that the disulfides are formed only in the presence of elementary sulfur, which in his experiments was produced by the oxidation of hydrogen sulfide by either ferric iron derived from geothite, or atmospheric oxygen. Pyrite was formed only below pH 5, and marcasite below pH 3.5. Rickard (1969b), again in inorganic systems, obtained pyrite and marcasite over the pH range 4.4-9.5; the proportion of marcasite, which predominated at pH 4.4, decreased to zero as the pH was increased to 9.5. The effect of pH on the form of the product is consistent with Rickard’s conclusion (1973) that whereas marcasite is formed by the oxidation of mackinawite by elementary sulfur, pyrite results from the interaction of makinawite and polysulfide, the latter being stable only under relatively alkaline conditions. It is interesting to note that Senarmont (1851, quoted by Allen et al., 1912) prepared the disulfide by heating ferrous salts with alkaline polysulfides. The reaction of sulfur with ferrous sulfide is quite rapid, being 50% complete after vigorous stirrings for 1 hour at 4OoC, although in unstirred bacterial sulfate-reduction experiments sulfidation of geothite was not complete after 3 months (Rickard, 1973). Kaplan et al. (1963) found elemental sulfur in recent marine sediments, but befork extraction of the sulfur the samples were treated with dilute acid to decompose monosulfide, so that if acid-soluble ferric compounds were present at least some of the sulfur could have been formed by oxidation of hydrogen sulfide by Fe3+during the preparation of the samples. As elementary sulfur is reduced by D. desulfuricans, the formation of iron disulfide in anaerobic sediments must be the net result of competition between ferrous sulfide and sulfate-reducing bacterias for sulfur, as it is formed by the reaction of hydrogen sulfide with ferric iron; it is to be expected that elementary sulfur would have only a transient existence in an anaerobic sediment.

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D. ENVIRONMENTAL FACTORS AND SULFIDE FORMATION Essential for the formation of sulfides is a supply of sulfates and organic matter, so coastal and deltaic areas, often very important agriculturally, provide optimum conditions for formation of sulfides. 1 . Physiography Knowledge of the physiological conditions for formation of sulfide-bearing muds is useful for understanding their genesis, predicting their location and mapping their boundaries. Recent coastal deposits cover very large areas, particularly in the tropics; an example is the west coast of Malaysia where the deposits may be up to 40 miles wide and 450 feet deep (Carter, 1959). Deltas form at the mouths of all rivers, but those in the tropics originate from much larger rivers, are flooded to much greater depth at certain times, and are desiccated more intensely at others. Fosberg ( 1964) has classified the main physiographic features of deltas into water (distributaries, delta channels and tidal channels, lakes and ponds of levee bank depressions, and abandoned channels), wet lands (filled lakes and ponds), and drylands (delta terraces, natural levees, and sand ridges and flats). The distributaries tend to be the larger channels in the delta; they have natural levees stabilized by vegetation, and strong currents may provide considerable scouring action. Lakes and ponds may be little subject to active tidal influence so they normally contain fresh water, often leading to freshwater peat formation. Interconnecting basins originate as areas of shallow sea that are subsequently cut off by ridges and sand bars as the delta extends seaward. In the tropics, mangrove grows along the margins and in many parts of Asia, Nipa palm, Nipa fruclecens becomes established. Lakes and ponds gradually fill with silt and organic debris; where the area is subject to tidal inundation, reeds and tall grasses dominate in the fresher water areas and mangrove in the saline areas. Interconnecting basins, lakes, and ponds, that are subject to tidal influence, thus provide the optimum environments for sulfide formation, but changes in sea level can inundate former fresh water peat areas with sea water, thus leading to sulfide formation in these as well. Van der Kevie (1972) shows that normal soils are associated with river levees and, where these are broad the areas of sulfide formation may be relatively small. Microrelief and sulfide formation are closely related; areas of slightly higher elevation may never have had any sulfides, or the higher relief may indicate sulfide-free material deposited over sulfidic muds, whereas the lower areas have had no such deposits or very thin layers only (Brinkman and Pons, 1973).

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The position of acid sulfate soils in the landscape can also be related to sea-level changes. Those formed when sea levels were higher may now be a long distance from the sea and have better drainage and consequently strongly developed acid sulfate soil characteristics. Old Pleistocene terrace soils have also been reported as having some acid sulfate soil properties (Pons and van der Kevie, 1969; Moorman, 196 1 ) . Thus potential acid and acid sulfate soils may be found in coastal areas with saline or brackish water influence, in seasonal or permanent freshwater swamps, formerly brackish, in Pleistocene terraces and in high altitude swamps with adjacent sources of sulfate. Physiographic variations and sea-level changes have thus given a variety of depositional features so that acid sulfate soils may vary from large contiguous areas to small patches of only a few hectares. Van der Kevie (1972) recorded that acid sulfate soils in Central Thailand cover an area of 800,000 ha with only small inclusions of nonacid soils; the Plain de Joncs in Vietnam also covers a very large area of uniformly acid sulfate soils. In other areas, e.g., Malaya, Sarawak, the Netherlands, acid sulfate soils often occur in patches of a few to perhaps several hundred hectares, interspersed in nonacid soils. 2 . Vegetation Although much hydrogen sulfide is formed at the expense of relatively little organic matter (Section 11, B), Rickard (1973) states that organic matter normally limits sulfate reduction; thus sources of organic matter and hence the vegetation associated with coastal sediments are of great importance. Sediments in coastal regions develop over a wide range of tidal regimes varying from continuously flooded, flooded twice daily at high tide, twice monthly or only occasionally. Tidal ranges may be very great and the salinity of the water is obviously much influenced by river flow. Parts of West Africa receive more than 4000 mm of rain in 6 months, with virtually none for the rest of the year. There the large estuarine areas are fresh during the rains and saline during the dry season. Areas flooded only occasionally by high tides may accumulate considerable quantities of salt, which render them almost sterile. Such barren flats (tannes) are extensive in Gambia and Senegal. Vegetation successions in coastal areas play a major role in the buildup of sediments by trapping the mud and controlling erosion. Mangrove successions have been particularly well studied because of the value of certain species for timber, charcoal and tanning materials. A useful summary of salt marsh vegetation in temperate zones is given by Steers (1959). Zostera sp. are early colonizers, growing on soft and wet mud, trapping silt so that banks grow sufficiently high for ill-defined creeks to form. As

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275

the creeks are cut off by further siltation, small dams form; these lead to salt pans which may remain devoid of vegetation until the drainage system changes and salts leach out. Spartina alterniflora is an important colonizer on the United States east coast. a. Mangrove. In contrast to the low-growing herbaceous plants that colonize salt marshes of temperate areas, tropical salt marshes have several tree species as primary colonizers, and mangrove, a term used to cover both the ecological group of species on tidal lands of the tropics and the plant communities that include these species (Richards, 1952), is primarily involved. There are several families of mangrove, the more important being the Rhizophoraceae, the Lythraceae, and the Verbenaceae. Rhizophora mucronate and R . conjugata occur in the Malaysian area and eastern and southern Africa (Watson, 1928; Dale, 1939; Macnae and Kalk, 1962). Rhizophora apiculata and R . stylosa are found in Queensland (Macnae, 1966). Around the Atlantic shores the three main species are Rhizophora mangle, R . racemosa, and R . harrisonii (Keay, 1953; Davis, 1940). Various species of the genus Avicennia occur in the Verbenaceae family. Avicennia germinans occurs in West Africa, A . oficinalis, A . intermedia, and A . alba in Malaysia, A . marina in Australia, eastern and southern Africa, and A . nitida in Florida. In this discussion our interest lies in the relationships, mostly indirect, between vegetation type and sulfide levels in the mud. Unfortunately studies on the colonizing vegetation seldom include any information on the muds, except perhaps on the salinity, but sulfide contents are seldom recorded. Reeds (Phragmites sp.) are usually related to sulfides in temperate area muds, but these are not primary colonizers of coastal areas. This suggests that, in these areas, excess sulfides are formed when the soils are under intermittent flooding by saline waters, i.e., brackish water swamps. Work in West Africa (Tomlinson, 1957) appears to have first drawn attention to the relationships between mangrove species and excess sulfide formation; he found that areas presently or formerly under Rhizophora racemosa developed much acidity on drainage, whereas soils from areas of Avicennia did not. He attributed this to differences in the rooting habits of the species; stilt roots of one Rhizophora tree may cover an area of 6 m diameter (Watson, 1928). In the soil these stilt roots are covered with root hairs, the major source of the peaty material which gradually builds up under this vegetation. This peaty layer may be several feet thick in West Africa, and Rosevear (1947) states that it can be cut and burned as fuel. Such thick peat deposits have not been reported from Malaysia, but in Thailand van der Kevie (1973) states that the vegetation over broad areas of sulfide muds has been swamp forest, “probably Rhizophora.” The reasons for the different amounts of fibrous peat formed

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under Rhizophora in various parts of the world may lie in the reaction of the tree to ecological factors. Watson (1928) in Malaya, and Davis (1940) in Florida, recorded that trees growing in shallow soils or areas subject to very deep inundation have the greatest mass of roots, so that large root masses would be expected in some areas of West Africa, because of the great changes in water level that occur under tidal and fresh water flooding. By contrast Avicennia sp. produce a shallow widespread root system, with small pneumatophores protruding from the surface. In West Africa, soils under this species are not usually fibrous unless previously covered with Rhizophora. On the other hand, Davis (1940) reports that in Florida deep peats are formed from the remains of both Rhizophora and Avicennia sp. Peats formed from Rhizophora remains have an abundance of reddish brown pithy roots in varying stages of decomposition. The reddish brown color distinguishes this peat from that formed by Avicennia, which is darker, has more yellow roots and is more plastic. Vann (1969) described soils under Avicennia in northeast Brazil that have 15-35 cm of partially decayed vegetation over a brownish gray clay. Because of the behavior of the different species of mangrove in peat formation, and consequently sulfide formation, mangrove successions are of interest. As they require protection from erosion, mangroves generally do not colonize exposed coastlines; on such coastlines they flourish only where there is a wide, shallow sea bed to reduce wave action, as on the west coast of Malaysia. Development more usually takes place in protected bays and behind sand bars, and in this well protected environment organic debris is not swept away, and so can supply the energy for bacterial reduction of sulfates. Mangrove successions parallel to the coast can be related to the degree of tidal immersion. Savory (1953) described such zonation in West Africa, the pioneer genus being Rhizophora, which extends to the limit of the diurnal tides and is flooded twice daily. R. racemosa is the pioneer species, and may reach heights of 40 m. R . mangle occurs at the drier inner limits of the zone as a small shrub up to 4 m high. By contrast Davis (1940) reported R . mangle in Florida as a large forest of tall trees growing in almost continuously submerged soil. In both Florida and West Africa the landward side of the Rhizophora is colonized by Avicennia nitida, on land that may be regularly or only occasionally flooded with brackish water. The succession described by Giglioli and King (1966) in Gambia is Rhizophora racemosa followed by Avicennia germinans; as the soils become drier these die out and barren flats take their place, as the occasional saline floods leave the land too salty for the mangrove. In Malaya Watson (1928) recorded a different type of succession, with Avicennia the primary colonizer. Carter (1959) stated that an accreting

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277

coastline is shown by Avicennia advancing seaward as small seedlings, a stable coastline by mature Avicennia, and an eroding coastline by Rhizophora. The more important factors that determine the colonization pattern are the erosion conditions and the nature of the mud, Avicennia colonizing sand and firm soils, Rhizophora soft muds. Andriesse et al. (1973) showed that in Sarawak the vegetation succession in deltaic areas is Nibong palm (Elncosperma filamentosa) in the higher areas, where salinity is around 0.5 mho/cm; A vicennia, Rhizophora near rivers and creeks, where the salinity is highest ( >30 mho/cm) ; and Nipa palm (Nipa fructicens) over the areas of intermediate elevations and salinities. Nipa palm appears to play an important role in sulfide formation in the Malayasia region, for acid sulfate soils very often contain the roots of this plant. b. Other Vegetation. While there are some obvious relationships between present day vegetation and sulfide-bearing muds, in many areas the vegetation of either potential or actual acid sulfate soils is often quite different from that under which the soils were originally formed. Such areas may now support a limited range of species of grasses, sedges, shrubs, and trees. Sedges (Phragmites vulgaris) and Cyperus sp. have been reported from Gambia. Pure stands of gelam, Melaleuca leucadendron have been reported from Malaya and Indonesia; Fimbristylis globulosa has also been reported from Indonesia by Driessen (1973), and Brinkman and Pons ( 1973) report several species of grasses, e.g., Imperata brasiliensis, sedges (Scleria and Rhynochospora sp.), and trees (Tabebuia insignis). Sedges seem to be the major type of vegetation in large areas of Vietnam (The Plain de Joncs) . However, these species, although useful indicators, are not specific for acid sulfate soils, but they are indicative of generally adverse soil conditions. As a conclusion, certain vegetation consociations are indicative of potential or acid sulfate soils, but none are specific; the closeness of the relationships obviously varies from one environment to another, so that extrapolation of relationships that exist, say in West Africa, to East Asia is unreliable. 3 . Climate

Acid sulfate soils occur in a wide variety of climates, but the largest areas are in the humid and monsoonal zones of the tropics, and in the moist temperate climates. The temperature obviously influences the amount and type of vegetation; although more organic matter is present in sediments of temperate areas at the time of deposition, the continuous growth of vegetation in the tropics can add larger quantities to the deposits. Rainfall distribution affects the behavior of sulfidic muds after deposition; without a marked dry season they may remain in a waterlogged and

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C. BLOOMFIELD AND J. K. COULTER

reduced state, unless drained artificially. In monsoon areas the soils dry out to a meter or more during the dry season, and strongly acid conditions can thus develop. Even in the wet tropics, prolonged dry spells, though infrequent, do occur, and Dunn (1965) reported the mass death of fish and the flocculation of sediments in a river in West Malaysia following a prolonged dry spell that caused swamp areas to dry out; subsequent heavy rain washed the sulfates into the river. The strongly contrasting climatic conditions are of great importance in management, and are discussed in greater detail in Section VII. In temperate areas the soils are usually so swampy that they seldom dry out naturally. 4. Fauna The influence of soil fauna on acid sulfate soil formation has not been widely studied, but Andriesse et al. (1973) have contributed some interesting observations on the activities of the mud lobster (Thallusinu anornula) in mangrove and Nipa palm swamps in Sarawak, where the lobsters channel to a depth of 120 cm or so and build mounds as high as 150 cm, covering as much as 40% of the land surface. Apparently the lobsters consume much of the organic debris from Nipa palms, etc., and thus have much the same effect as earthworms in dry soils. As a consequence of these deep burrowing activities, sulfidic materials are brought up from the deep subsoils, and these then develop extreme acidity (pH 2.7-3.9). Leveling the lobster mounds for agricultural development thus spreads a layer of highly acid material over the surface. Micromorphological studies by Slager et ul. (1970) on soils from Surinam and Thailand showed that crabs were active in homogenizing some of the upper soil horizons. Macnae and Kalk (1962) gave details of the soil fauna found in mangrove areas of Mozambique and described the wide variety of crabs and small fish and oysters on Rhizophoru roots, but they did not report any mound-building lobsters. Such animals appear to be absent too from any other extensive area of sea littoral tropical vegetation, but they obviously have considerable significance in the pattern of soil development. Ill.

A.

Oxidation of Sulfides

MICROBIAL REACTIONS

The acidification of mine waste has been the subject of intensive research, and our present knowledge of the oxidation of pyrite under natural conditions derives largely from the efforts of workers in this field (Temple and Koehler, 1954; Lorenz, 1962; Clark, 1966; May and Berg, 1966;

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279

Barnshisel and Massey, 1969 ) . Rasmussen ( 196 1) , considered the chemical and microbiological oxidation of pyritic soils. In 1919 Powell and Parr reported that the production of sulfate in freshly powdered coal is enhanced by inoculation with previously oxidized coal, and concluded that microbial action was involved. Carpenter and Herndon (1933) observed that pyritic coal is less prone to oxidation after sterilization; McLean (1918) found that sulfur is rapidly oxidized to sulfuric acid when composted with soil and rock phosphate, and Rudolphs (1922) found that enrichment cultures from such composts actively promoted the oxidation of pyrite. Lipman et d . (1921) isolated a sulfuric-oxidizing bacterium from soil, which they named Thiobucillus thiooxiduns. Jensen (1927) found the same bacterium in Danish soils, and considered T . thiooxiduns to be capable of oxidizing pyrite; in the light of present knowledge, it seems that Jensen did not succeed in isolating a pure culture of T . thiooxiduns. T . thiooxidans is autotrophic, obtaining energy from the oxidation of elementary sulfur, or thiosulfate. It grows optimally at pH 2.0-3.5, and can tolerate conditions very much more acid than this. Leathen and Madison (1949) found T . thiooxiduns in all the mine effluents they examined, and it is understandable that this species should have been considered responsible for catalyzing the acidification reaction. However, although it promotes the oxidation of marcasite (Leathen et ul., 1953), T . thiooxiduns has no direct action on pyrite, and an indirect mechanism based on the intermediate formation of elementary sulphur was proposed. Pyrite is oxidized by Fe3+according to the equation: FeSz

+ 2Fea+

=

+ 2s"

SFe*+

and sulfur thus formed could be the substrate for T . thiooxiduns; the oxidation of sulfur would decrease the pH and bring more Fe3+into solution. This mechanism provides an explanation for the acidification, and it is significant that Temple and Koehler (1954) found T . thiooxiduns to be more numerous at the site of oxidation than in the mine water. Nevertheless, it is clear that in the steady state the rate-determining stage of the overall process would be the reoxidation of Fez+,and, under the acid conditions considered here, this would be much too slow to account for the observed rate of the bacterially catalyzed oxidation. The resolution of the difficulty originated with the observation by Hinkle and his co-workers that the ferruginous deposits that formed in natural mine waters did not develop in artificial solutions of the same composition. Having shown that the deposits did not form.in natural mine water that had been sterilized, Colmer and Hinkle (1947) demonstrated the presence of a hitherto unknown bacterium that oxidized Fez+in acid conditions,

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C. BLOOMFIELD AND J. K. COULTER

for which Temple and Colmer (195 1 ) proposed the name Thiobucillus ferrooxidans. Gleen (1950, 1951) observed microbial catalysis of Fez+ when soils were perfused with solutions of ferrous sulfate, and as he gave no description of his soils it can probably be assumed that they were not pyritic, and that ferrous iron-oxidizing bacteria commonly occur in soil. Ashmead (1955) reported the presence of bacteria resembling T . ferrooxiduns in acid mine water in Scotland. A second iron-oxidizing bacterium was described by Leathen et al. (1956), distinguished from T . ferrooxiduns by its ability to oxidize thiosulfate, for which the name Ferrobacillus ferrooxidans was proposed, but it seems that the existence of this as a distinct species is no longer generally accepted. T. ferroxiduns is an autotroph that grows best at pH 2.0-3.5; it oxidizes Fez+, elemental sulfur or thiosulfate (Unz and Lundgren, 1961). The upper limit for its growth is between pH 3.5 and 4.0, and it commonly occurs in acid sulfate soils and in ochre deposits associated with pyritic soils (Bloomfield, 1972). In laboratory experiments the rate at which pyrite oxidizes is increased severalfold in the presence of T. ferrooxiduns. The overall course of the oxidation of pyrite in an orginally slightly alkaline soil was demonstrated by Bloomfield (1972); after 24 days' incubation the pH of the uninoculated soil decreased from 7.2 to 3.8, and during this period the iron that was mobilized persisted almost entirely in the ferrous state. The rate of oxidation was greatly accelerated once the pH fell to within the range tolerated by T . ferrooxiduns, and the presence of ferrous iron-oxidizers was shown by the predominantly ferric form of the mobilized iron. The major influence of T. ferrooxidans in promoting the oxidation of pyrite is probably indirect, operating via the catalysis of the oxidation of Fez+,but there is evidence for direct oxidation of sulfide sulfur. Ehrlich (1962) found that T. ferrooxidans promoted the oxidation of a nominally iron-free synthetic chalcocite (Cu,S), but the possibility of the presence of traces of iron in the chalcocite does not seem to have been excluded. Beck and Brown (1968) observed decreases in the abilities of aged suspensions of intact cells of T . ferroxiduns to oxidize sulfur and ferrous iron. The sulfur-oxidizing ability decreased most rapidly, and with some suspensions the ability to oxidize sulfur was completely lost, although the cells were still able to oxidize Fez+.These cells were unable to oxidize pyrite or chalcopyrite; none of the cells that could' oxidize sulfur were unable to oxidize sulfide minerals, so that from this it seems that the S- and Feoxidation systems are different, and that the former is essential for the oxidation of sulfides. Duncan et ul. (1967) found that T. ferrooxiduns oxidized iron and sulfur in CuFeS, and pyrite. When cells grown on chal-

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

28 1

copyrite were used to oxidize chalcopyrite, 68-74% of the oxygen uptake was due to the oxidation of sulfide, and 25-30% to the oxidation of ferrous iron, but with pyrite all the oxygen was consumed in oxidizing sulfur. With cells grown on ferrous sulfate, with chalcopyrite 80-90% of the oxygen uptake was initially due to oxidation of iron, but sulfur oxidation became important later. Ferrous sulfate-grown cells oxidized pyrite faster than cells grown on chalcopyrite. B.

METALLURGICAL APPLICATIONS

The practical application of the atmospheric oxidation of sulfide ores is of great antiquity. According to Mellor (1935), in the first century of our era Dioscorides described the crystallization from mine waters of what must have been ferrous and cupric sulfates, and Pliny recorded the preparation of cupric sulfate from natural waters in Spain. In De R e Metallica, Agricola (1 556) described how heaps of vitriolic earth or stone were exposed for 5-6 months and leached with water when the mass had crumbled. The leachate was concentrated, treated with strips of iron and evaporated to crystallize ferrous sulfate (“vitriol”). In De Sal-nitro Spiriti Nitro-aereo, published in Oxford in 1669, Mayow gave the following excellent account of the process: “Vitriols are produced from the stone or rather saline-sulphureous earth usually called marchasite, and from it on the application of fire the flowers of common sulfur are elicited in considerable abundance. But after this earth has been exposed for some time to the air and weather and then (as its nature is) has fermented spontaneously, it will be found to be richly impregnated with vitriol.” Kendall and Wroot (1924) described the industrial production of alum by roasting pyritic shales, in Yorkshire, in the 17th to 19th centuries. Alum was widely used in the cloth and leather industries, and processes such as this must have been of considerable importance. According to Bernal (1969), one reason why the northern clothiers favored the Reformation was their dislike of the papal monopoly in alum; it seems that trafficking in alum from rival sources was among the sins for which forgiveness could not be obtained by purchasing an indulgence. Extensive industrial use is made of T. ferrooxidans in recovering copper from ore of too low a grade for conventional methods to be economic. According to Burkin (1971) 15% of the primary production of copper in the United States is produced in this way. Leaching heaps of the ore gives a solution of cupric sulfate, from which copper is precipitated by treatment with scrap iron. The oxidation of ferrous iron in the leachate is catalyzed by T. ferrooxidans, thereby enhancing its ability to oxidize pyrite when it is returned to the dump (Le ROUX,1969; Fletcher, 1971).

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Bryner and Jameson (1958) isolated two chemosynthetic autotrophs (apparently T. ferrooxiduns and T . thiooxidans) from leaching streams in Bingham Canyon, Utah. The former oxidized free sulfur, Fez+, pyrite, molybdenite, and several copper sulfide minerals, whereas the second had no action on the sulfide minerals (see also Bryner et al., 1954, 1967; Bryner and Anderson, 1957; Bryner and Jones, 1965; for recent reviews, see Le ROUX,1969, 1971; Trudinger, 1971; Tuovinen and Kelly, 1972; Wadsworth, 1972). Elemental sulfur or pyrite can be added to compensate for acid neutralized by gangue material (Napier et al., 1968). Marchlewitz et ul. (1961) found that selected strains of T. thiooxiduns could tolerate concentrations of 8 g of Fe, 0.5 g of Cu, or 2.5 g of Zn per liter; after adaptation 10 g of Cu or 50 g of Zn per liter was tolerated. After adaptation, T. ferrooxidans alone was almost as effective as in the presence of T. thiooxiduns. Sadler and Trudinger ( 1967) have considered toxic effects of heavy metals to micoorganisms in relation to geochemical processes. It seems highly probable that bacterial leaching as a means of recovering metals will become increasingly important iii the near future, and that the process will be used industrially for the extraction of metals other than copper. Laboratory studies have shown the extraction of zinc, cadmium, molybdenum, and uranium to be theoretically feasible.

c.

REACTIONS IN SOILS

Quispel et al. (1952) noted that in 1886 van Bemmelen reported that the acidification associated with the formation of acid sulfate soils was caused by the oxidation of mono- and disulfides. The difficulty of determining ferrous monosulfide in soil is discussed later; allowing for the considerable uncertainty of the estimates, it seems that the concentration of monosulfidic sulfur in anaerobic soils seldom exceeds 100-200 ppm, whereas pyrite contents of several percent are not uncommon. The oxidation of pyrite is thus the process essentially responsible for the formation of acid sulfate soils. Murakami (1966) identified pyrite by X-ray diffraction in the residues obtained by treating lake muds with hydrofluoric acid. The sulfur contents of the insoluble matter agreed well with the amounts of oxidizable sulfur that was insoluble in HCl or soluble in aqua regia, and Murakami concluded that the muds contained only small amounts monosulfide and free sulfur. Hesse (1958) concluded that sulfur occurs in the mud of Lake Victoria mostly in organic form, but the method used to determine organic sulfur was such as to include pyritic sulfur. Bloomfield et al. (1970) found

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283

pyrite in mud from the same source, and concluded that there is no apparent reason to postulate the presence of unusual organic matter. Hart made an extensive study of the oxidation of sulfidic mangrove swamp soils in Sierra Leone (1959, 1962, 1963), but he followed earlier Dutch workers (Quispel et al., 1952; Harmsen, 1954) in wrongly assuming the first products of the biological oxidation of pyrite to be ferric oxide and sulfur. Although he noted the presence of ferrous iron-oxidizing bacteria in his soils he did not appreciate their significance, and concluded that T . thiooxidans is solely responsible for the catalytic action. The fact that Hart's turbidimetric method for determining elementary sulfur in soils (1961) seems to overestimate the amount actually present (Bloomfield, 1972) no doubt tended to support him in this conclusion. Wiklander et al. (1950), and Hart (1959) considered that liming increases the rate at which pyrite oxidizes. The effect of pH on the rates of both the chemical and the microbiological processes suggests that the opposite would be true; Trafford et al. (1973) measured the rates at which pyrite oxidized in undisturbed cores of limed and unlimed soil, and found that oxidation is inhibited by liming.

1. Products of Acidity The oxidation discussed in Section 111, A can be summarized as follows (Temple and Koehler, 1954) : Initial chemical reaction in moist conditions :

Action of Thiobacillus ferrooxidans: '2FeS04

+ 0 + H2S0, = Fe2(S04)3 + H20

Subsequent chemical reactions:

+ FeSz 0S + 6 FeZ(S04)a + 8Hz0 Fe*(SO4)3

=

SFcS04

=

+ 0s

10FeS04

+ 8HzSO4

Reaction by Thiobacillus thiooxidans: S

+ SO + HzO

=

YH+

+ Sod*-

a. Formation of Jarosite. Weathering pyrite gives very acid products, the maximum acidity being produced when all the iron is oxidized and hydrolyzed to solid ferric oxide (van Breemen, 1973). However, the reaction does not normally go to completion; in the absence of sufficient bases, normally calcium carbonate, to neutralize the acid, basic iron sulfates are formed of which the most widely reported is undoubtedly jarosite. This

284

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AND J. K. COULTER

is a member of the alunite group with the formula AB,(SO,),(OH),, where A may be K, Na, Pb, NH,, or H 3 0 and B may be Fe3+or AP’ (Brophy et al., 1962). Jarosite, KFe3(S04)z(OH)o, is a pale yellow material insoluble in water but soluble in HCl, commonly found along old root channels, on the sides of peds, and on drain spoil. Brown tubes, also along old root channels, may accompany the yellow material, which itself may have a thin reddish brown coating; Clarke et al. (1961) concluded that the brown tubes were soil particles cemented together by iron sulfide, sulfate and possibly oxides. There have been a large number of investigations into the formation of jarosite by the oxidation of pyrite, and these have been summarized by van Breemen (1973). Some of this work has been concerned with the preferential uptake of iron over aluminum and of potassium over sodium. Van Breemen found that even when the sodium concentration in the soil solution exceeded that of seawater, virtually all the “A” positions were filled with potassium. The sodium member, natrojarosite, was formed only on depletion of all available potassium. Jarosite forms in a matter of weeks or months on exposure of pyritic muds to oxidizing conditions. It has been suggested by Warshaw (1956) that it is precipitated when leaching and oxidation take place. It has also been reported as pseudomorphic after pyrite (Furbish, 1963). In the laboratory, jarosite is unstable above pH 3.0, hydrolyzing to ferric oxide and giving SO,2+and K+ ions. On the other hand, it often occurs in soils with a pH above 4 and is sometimes so stable that certain soils have been called “fossil” acid sulfate soils. The slow hydrolysis at apparently higher pH levels in the field may reflect the inaccuracy of measurements of pH in bulk samples, as the pH in the immediate vicinity of the jarosite may be very acid. The problem of determining the pH of very acid soils is discussed in Section VIII, B. b. Other Sulfates. In addition to jarosite, sulfates of sodium, magnesium, calcium, and aluminum are formed. Sodium and magnesium sulfates leach readily from the profile as soon as adequate drainage is provided. Calcium sulfate (gypsum) is somewhat less soluble, but leaches in wetter conditions. Gypsum accumulates as nests of crystals in drier areas and has been recorded in rice soils in Malaysia, and it can contribute to the increased conductivity of suspensions of such soils. Under strong drying conditions, some soluble aluminum sulfates may appear as effloresr cences on the surface of the soil. Using chemical and X-ray analysis, van Breemen (1973) detected sodium alum, NaA1(S0.,)2.12H2O, and tamurgite, NaA1(SO,),*6H2O, as well as gypsum and sodium chloride in surface crusts from Thailand. Herbillion et a!. (1966) have reported alunite, KA1, (SO, ) (OH) on the surface of acid sulfate soils in Vietnam.

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

285

Considerable quantities of aluminum occur in solution in water samples from oxidized pyritic muds. In an experiment on oxidizing pyritic mud, van Breemen (1973) found that the leachates had pH values between 1.8 and 4, aluminum concentrations from 58 to 0.1 1 mmoles/liter, and sulfate concentrations of 260-12 mmoles/liter. In groundwater samples from the same area (Thailand), he reported pH values from 2.8 to 5.5 and aluminum concentrations from 2.12 to 0.023 mmoles/liter. Allbrook (1973) extracted aluminum from acid sulfate soils in Malaysia using a 1 : 1 soil water ratio and reported 8.5 me/lbO g of soluble aluminum from a soil which had 3 % sulfur. Van Breemen (1973) gave a comprehensive account of attempts to prove the existence of a basic aluminum sulfate with the stoichiometric formula, AIOHSO,. However, the existence of this mineral could not be detected by X-ray studies on soils. A basic aluminum sulfate with this formula and the composition AI,(OH) ,(H,O) (SO,) ,.2H,O has been prepared by Johansson (1962); he stated that the crystals are readily soluble in water, forming a clear solution; after standing or dilution a precipitate is formed. It would appear therefore that his compound does not have a long-term stability. Hollingworth and Bannister ( 1950) reported the presence of hydrobasaluminite Al,SO,(OH) ,,.36H,O and basaluminite AI,SO,(OH) lo.5H,0 at the junction of pyritic ironstone orerlying limestone; they suggested that this was formed by the downward movement of aluminum sulfate-bearing waters into the zone of calcium bicarbonate saturation, causing precipitation of amorphous compounds, eventually forming crystalline products. Such compounds might thus be formed in areas where calcium bicarbonate-saturated flood waters exist. Van Breemen (1973) suggested that neither gibbsite nor basaluminite can theoretically exist below approximately pH 4.5, and that therefore they normally do not influence dissolved aluminum. It can be concluded therefore that definitions of the aluminum sulfate compounds in these soils are somewhat speculative. 2. Results of Acidification a. Changes in Mineralogy. Lynn and Whittig (1966) examined the clay minerals from cat clay formations in San Francisco Bay; these soils, exposed to an oxidizing regime for 6 years before sampling, had characteristic pale yellow jarosite mottles, a pH of 3.0-3.5, and red mottles of amorphous iron oxide. An adjacent area, drained for more than 60 years, had jarosite and iron mottles to a greater depth but had about the same pH. Lynn and Whittig reported that the same mineral suite-mica, montmorillonite, vermiculite, chlorite, kaolinite, and interstratified chlorite-vermiculite-was present in both the reduced sediments and the recently oxidized ones.

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C. BLOOMFIELD AND J. K. COULTER

In the older drained area the same mineral suite was present, but the diffraction peaks were less sharp, and very little chlorite was present. The authors suggested that additional montmorillonite was formed as the chlorite disappeared. In fact chlorite seems to be a fairly ephemeral clay mineral, appearing quickly in clay samples incubated under reducing conditions but then disappearing again. Kaolinite has been reported as the dominant clay mineral in several tropical areas (Herbillion et al., 1966;Horn and Chapman, 1969; van Breemen, 1973;Allbrook, 1973);this reflects the highly weathered nature of the parent material of the sediments, although there is also some evidence for the formation of kaolinite by breakdown of 2:l minerals. Although mineralogical studies give qualitative information on the changes taking place under the intense acid attack, quantitative changes are much more difficult to assess. b. Neutralization of Acidity. The final pH of the soil depends on the amount of pyrite and the buffering capacity of the soil. The pH values often reported are those obtained after allowing small samples to dry under laboratory conditions; these values may be a pH unit or more below those of samples oxidized in field conditions (Section VIII, B) . For several hundred samples from Malaysia, Bloomfield et al. (1968) gave a modal value of 3.4 in the subsoils (30-60 cm). Lowest pH values are reported in very sandy soils, e.g., pH 1.5 by James (1966) in quartzitic material from goldmines. There are two sources of bases: (a) minerals, mainly calcium carbonate, and (b) metal cations on the exchange complex, for neutralizing the acid. According to van Beers (1962)many marine sediments in Holland contain 10-20% calcium carbonate, whereas river sediments have somewhat less. In the United States, on the other hand, Edelman and van Staveren (1958) stated that the marsh soils have little or no calcium carbonate. Many of the sediments in the wet and wet-dry tropics contain little carbonate, as the catchment areas of their rivers are in zones of base-poor rocks. Pons (1964a) stated that the carbonate content of sediments of the Amazon is less than 0.3%. Certain exceptions do occur, and in these, base-rich flood waters may contain sufficient bicarbonates to neutralize all or much of the acidity; such areas have been reported in Thailand (Pons and van der Kevie, 1969). Evans (1966) gives examples from Guyana where local concentrations of carbonate neutralize the acidity, giving soils with excellent structure and high yield potential. There is no satisfactory evidence that other minerals contribute significant amounts of bases; release of such bases is normally rather slow. Pons and van der Kevie (1969) have postulated that some of the green iron silicate minerals, such as glauconite, break down rather readily under very acid conditions to provide bases for

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

287

neutralization, and they suggest that each gram of green minerals has the potential for neutralizing 200-300 mg pyrites. It is difficult, however, to find supporting evidence and laboratory experiments do not show any lessening of acidification when pyrite is incubated with such minerals (Trafford et al., 1973). Exchangeable bases react with the acids; van Breemen (1973) stated that marine clays contain 75-200 me/100 g soil of bases; unless the bases of soluble salts, i.e., magnesium and sodium, are included where the environment is saline, these values appear too high, especialhy ,since kaolinite is reported as the dominant clay mineral in tropical areas (Section 111, C). c. Exchangeable aluminum. Exchangeable bases are removed by acids and replaced by H+, but there is ample evidence that hydrogen clays undergo almost spontaneous decomposition to form clays saturated mainly with aluminum ions (Coleman and Craig, 1961). Thus in many acid soils virtually no exchangeable H' can be found (Coulter, 1969). However, it would appear that under certain conditions strongly acid soils may retain some exchangeable H'. Yuan (1963) noted that acid soils, pH 4.8 in 1 N KCl, had more exchangeable H+ than A13'. Using soils from a liming experiment Coulter (1966) reported that those of pH 3.1 in 0.01 M CaCl, had 1 . 1 me H+ and 7.2 me A13+per 100 g; above pH 4.8 no exchangeable H+was found. Frink ( 1973) discussed evidence supporting the observation that the amount of exchangeable A13+produced in a soil is related to the concentration of exchangeable H'. Although the evidence is slender, it is thus possible that some exchangeable Ht does exist on the exchange complex at the pH levels usually found in acid sulfate soils. The source of the exchangeable A13+formed by the decomposition of H clays is mainly the layer silicates. These silicates usually have coatings of hydroxyaluminum and iron compounds that are positively charged. Some of these are presumably attacked by the sulfates and release aluminum into solution; acid sulfate soils have large pH-dependent charges, the C.E.C. at the pH of the soil being only about half that at pH 8.2. Aluminum that is exchangeable to neutral salts plays a major role in determining the physical and chemical characteristics of soils, and its toxic effects on plants have been widely studied. Both monomeric, Al( O H ) 2+, and polymeric species, e.g., Al,(OH),,3+, of aluminum are reported to occur in the soil solution. Frink (1973) suggested that simple monomeric hydrolysis can be used to calculate the pH and aluminum ion activities at low basicities; at higher basicities, significant amounts of polynuclear hydroxyaluminum cations may be present. Gibbsite, Al(OH),, seems to control the activity of aluminum in the soil solution at higher pH's. There is considerable evidence that organic matter and aluminum can

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form stable complexes, and accumulation of organic matter in allophane soils has been attributed to the formation of organic aluminosilicate complexes. Many acid sulfate soils have peaty top soils, e.g., muck soils in Malaysia and “pegassy” clays in Guyana; most also have some buried organic matter, and it is therefore conceivable that considerable quantities of aluminum are absorbed by organic matter in these peaty horizons. Lefebre-Drouet ( 1967) found that destruction of organic matter in acid soils with H,02 liberated large quantities of aluminum. McLean et al. (1965) found that the pH-dependent C.E.C. decreased drastically when top soils were limed or the organic matter destroyed, and that, at pH 4.8, NH,OAc extracted considerably more aluminum than did 1 N KCl. They concluded that most of the pH-dependent C.E.C. sites were due to organic matter which complexed with aluminum. This could be displaced by the NH,OAc, and precipitated as Al(OH),. Mutatkar and Pritchett ( 1966) found that saturating a muck soil from the Florida Everglades with aluminum and adjusting to pH 4 produced less CO, on incubation than did a similar calcium-saturated soil, adjusted in the same pH. The evidence therefore points to a strong interrelationship between aluminum and organic matter in acid soils. What the evidence does not show, however, is whether the aluminum in the soil solution, which is the important factor for plant growth, is lessened with increased organic matter content. Field observations certainly suggest that at low pH levels crops grow better on peaty acid sulfate soils than they do on equally acid mineral soils. Most of the studies on aluminum have been done on acid soils in the absence of sulfate, but acid sulfate soils have considerable quantities of sulfates, and the reactions of aluminum under these conditions have received little attention. The behavior of aluminum is of importance in liming studies. Calculations of lime requirements based on the pH of acid sulfate soils shows the need for enormous and generally quite uneconomic quantities. The neutralization of an acid soil involves the neutralization of exchangeable Hi (normally virtually absent but possibly present to some extent in acid sulfate soils) and also of exchangeable aluminum and acid charges on edge sites of minerals and on organic matter. The latter more or less correspond to the pH-dependent charges. Increasing the pH by liming should increase the hydiolysis, and hence the rate of disappearance, of jarosite, but there seems to be no confirmatory experimental evidence of this. d. Aluminum and Physical Conditions. Scheltema and Boons (1973) described “pseudo” acid sulfate soils as soils of good physical properties, due to a high proportion of aluminum on the absorption complex, yet lacking the toxic properties of acid sulfate soils. Evans (1966) reported that

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289

soils formed by the weathering of pyrite, in which the acid reacted with shell material in the spoil from the drains, had very good structure. Frink (1973) reviewed recent work on the effect of aluminum on soil structure, and showed that it is aluminum rather than iron that seems to be responsible for cementing soil particles into structural units. When waterlogged, acid sulfate soils present a special situation, as much ferrous iron is mobilized; when oxidizing conditions set in, iron is reprecipitated, presumably in a finely divided and “active” state. Waterlogging had long been used in Guyana as a method of restructuring sugar cane soils, but the actual mechanism of the recovery has not been investigated. e. Profile Development. Van Breemen (1 973) has used a chronosequence to demonstrate profile development in acid sulfate soils. In the youngest soils the pyrite distribution reflects the situation in the original mud. Shallow drainage results in acidification of the surface soil, but jarosite has not yet appeared. In the next stage jarosite appears, and as the soils become older and better drained, the horizons of jarosite and pyrite occur at progressively greater depths; as the jarosite horizon moves downward, hydrolysis of jarosite causes ferric oxide to accumulate in the upper horizons. The change from a horizon containing little pyrite to one with a large content is abrupt, so that oxidation is apparently confined to a narrow zone. D. FORMATION OF OCHREIN FIELDDRAINS

The blocking of field drains by ochre is known in most areas in which underdrainage is practiced (Grass, 1969). Two distinct forms of ochre are known. The first of these occurs in near-neutral peaty areas and is associated with filamentous, or sheath-forming, bacteria. The microbiological origin of this form of ochre was demonstrated by Winogradsky, who isolated from ferruginous spring water a bacterium that oxidized ferrous iron and deposited ferric hydroxide in its sheath. The formation of the ferric hydroxide sheath accounts for the dark brown color of this form of ochre, and for its typical “raglike” consistency. The iron bacteria comprise several genera, most of which, but not all, are filamentous. Some are capable of oxidizing manganese as well as iron compounds (Alexander, 1961; see also Pringsheim, 1949; Puustjarvi and Juusela, 1952; Wolfe, 1964; Mulder, 1964; Parr, 1969). Spencer et al. (1963) found six genera of iron and other bacteria in ochre deposits from different parts of drains in citrus groves in Florida. The second form of ochre occurs in areas of pyritic soil, and is formed by the action of T. ferrooxiduns. As mentioned earlier, it was the precipi-

290

C. BLOOMFIELD

AND J. K. COULTER

tation of ferric oxide in acid mine waters that led to the discovery of T. ferrooxiduns by Colmer and Hinkle (1947), but the association of this bacterium and pyritic soils with ochre deposits in drains seems to have been appreciated only recently (Rasmussen, 1961). Bloomfield (1967, 1972) reported the formation of bright orange-red ochre deposits in drains and ditches at a reclaimed open-cast coal site, where the very acid (pH 3.2) ditch water contained nearly 1.5 g of SO,*- per liter. Ochre from this and several widely separated similar sites contained bacteria that oxidized ferrous iron and sulfur. Reports on the effect of copper in preventing the formation of ochre are conflicting (Puustjarvi and Juusela, 1952). The inconsistency may have arisen from failure to distinguish the pyrite-T. jerrooxiduns and filamentous bacterial forms of ochre. Puustjarvi and Juusela (1952) mention that not all Finnish ochre deposits have the raglike consistency of filamentous ochre, and of the 20 or so Danish samples examined by Petersen (1966), 9 contained more than 1% SO,, so that both types of ochre were probably included in the samples considered by these workers. T . ferrooxiduns can tolerate large concentrations of copper (Marchlewitz et al., 1961), and it is hardly to be expected that the formation of ochre by this bacterium would be affected by copper wire, although’it is conceivable that the growth of filamentous iron bacteria would be affected (Bloomfield, 1972). Sulfate is readily reduced under anaerobic conditions at pH values of about 5 and above, and the occurrence of black ferrous sulfide a few millimeters below the surface of the bright orange-red ochre in ditches is a common occurrence at pyritic sites. Ford et ul. (1968) reported the clogging of porous drain-surrounding materials by ferrous sulfide. As the rate at which pyrite oxidizes decreases with increasing pH, liming the soil should decrease the amount of iron available for the formation of ochre, and thus extend the effective life of the drainage system. In an experiment with undisturbed cores of pyritic soil, Trafford et ul. (1973) found that with a total drainage of about 1000 mm over 12 months, treating the soil with 42,000 kg of CaCO, per hectare decreased the amount of iron leached from the soil to about 20% of the amount leached from the unlimed core, so that the benefits of liming pyritic soils could well be 2-fold. IV.

Mining and Corrosion Problems

It has been noted (Section 111, A) that the acidification of mine waste has been thoroughly examined; this interest has arisen because of metallurgical applications of sulfide oxidation and the pollution problems of mine spoil.

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

A.

29 1

POLLUTION

Mines and their spoil often contain large quantities of pyrites, which oxidize on exposure to the air and render the spoil almost sterile to plant growth, thus adding to the danger and ugliness of the heaps; water draining from spoil tips and mines may be so acid that whole watersheds are polluted. Temple and Koehler (1954) give a comprehensive account of the problems in bituminous coal mining areas of the United States. Not all areas are affected, but those that are produce sulfuric acid in such large amounts that pumps, pipes, and concrete structures are corroded. Brayley (1954) estimated that the bituminous coal fields of western Pennsylvania produced about one million tons of sulfuric acid per annum, all of which found its way into the Ohio River and its tributaries. Acid mine water comes from the large tips of overburden or unsalable coal; in these oxidation may be stopped by suitable consolidation. A second source is the roofs of disused mines, which gradually disintegrate, continuously exposing pyrite-bearing formations to oxidation; these can supply acid mine water for at least 50 years after abandonment. Indeed where the mines drain by gravity, crumbling mine roofs may provide acid drainage water almost indefinitely, and abandoned shaft and strip mines have been reported by Martin and Hill (1968) to contribute over 60% of the acid pollution in coal mining areas of the United States. The problem may be less spectacular in other regions, but it exists in many mining areas; Doubleday (1969) stated that the area of derelict land in Great Britain exceeds 40,000 ha, much of it from coal mining. Such areas have been increasing yearly and there is now strong pressure to reclaim these, mainly for recreational uses. James (1966) describes similar problems in the slime tips of South Africa’s goldfields. Much of this material is quartzitic, and very low pH values (1.5) can be caused by quite small amounts of pyrite. Strip mining in Denmark has covered several thousand hectares with sand, gravel, and pyrite-bearing clay. According to Petersen et al. (1968), some of these tippings have remained bare of vegetation for 50 years; in these the pH of the soil is 2.3. The problems of reclamation vary greatly, and several factors are involved. Thus Doubleday (1971 ) showed that the maximum acidity (pH 2.5) develops in some tips at a depth of about 20 cm; this is the maximum depth of drying out, and depends on the rainfall and the exposure; southfacing slopes dry out more deeply. Wind and water erosion may expose fresh material, and loose tipping allows aeration to considerable depths. Deep aeration leads to formation of sulfates which appear in spring lines on the sides or base of the tip, giving zones of high toxicity. Regrad-

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C. BLOOMFIELD AND J. K. COULTER

ing to provide level or gentle slopes may also expose new zones of pyrite.

B. CORROSION Corrosion from acid sulfate waters is a common problem in mining; the corrosion of concrete in acid sulfate soils has been described by van Holst and Westerveld (1973); sulfate corroded the surface of concrete piles, giving soft and porous surfaces. Similar conditions are likely to arise with the engineering structures of irrigation projects in acid sulfate soils in the tropics. The solution is probably the use of sulfate-resistant blastfurnace cement, or bituminous coatings on concrete. V.

Classification and Mapping

A.

CLASSIFICATION

It has long been recognized that there are considerable variations in the agricultural potential of acid sulfate soils, but until recently attempts at their classification have been based largely on the amount of sulfide sulfur or the acidity that develops on drying. Generally pH values of air-dry material below 4.0, commonly about 3.5 have been taken as the values below which soils may be regarded as acid sulfate soils. Recently the importance of these soils have been recognized in classification studies (Soil Taxonomy, 1970), and a distinction has been made between horizons that have already developed acidity i.e., acid sulfate soils, and those that have the potential to do so, i.e., potential acid sulfate soils. A sulfuric horizon is defined as “a mineral or organic horizon with a pH lower than 3.5 (1 : 1 in water) and with yellow jarosite mottles with hues 2.5 or yellower and chromas 6 or more in the Munsell notation.” Sulfidic materials are defined as waterlogged mineral or organic soil materials that have 0.75% (on a dry weight basis) or more total sulfur, mostly in the form of sulfides, and less than three times 2s much carbonates (CaC03 equivalent) as sulfur. Another international definition is that in the legend of the Soil Map of the World (Dudal, 1968) where a thionic unit is defined as one containing sufficient sulfur compounds to cause acidification of the soil, when oxidized, to a pH (in KCl) of less than 3.5,within 100 cm of the surface. The term “pseudo-acid sulfate soil” occurs in the literature; although no definitive terms have been given, it seems to refer to a soil containing jarosite, but with a pH in water above 4.0, a good structure, and insufficient acidity in the form of exchangeable aluminum to prevent good crop growth.

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293

In the classification proposed in “Soil Taxonomy,” the great soil group of sulfaquepts has been introduced. This comprises strongly acid soils with a sulfuric horizon with yellow jarosite mottles and a pH (1 : 1 in water) less than 3.5 in some part of the top 50 cm of the profile; where the acidic horizon is between 50 and 150 cm in depth, sulfic subgroups of other aquepts are distinguished. These would be regarded as buried cat clays. Thus many of the acid sulfate soils of the tropics would be classified as Typic Sulfuquepts or SuZfic Tropuquepts (van der Kevie, 1973). In the temperate areas they would be mainly Typic Sulfaquepts and SuZfic Haplaquepts. Acid sulfate soils may be buried by layers of peat or muck, in which case they may be Histic Sulfuquepts or Histic Sulfic Tropaquepts. Sulfohemists are organic soils with a sulfuric horizon within 50 cm of the surface. Potential acid sulfate soils, i.e., those with sulfidic horizons, are classified as Typic Sulfaquents if the pH (1 :1 water) of the dried soil is less than 3.5 in the upper part of the profile. Potential acid sulfate soils that are dominantly organic are classified as Sulfihemists. Very soft, unripened, swamp soils that gave a pH upon drying below 4.5 in the upper 25 cm or more may be classified as Sulfic Hydraquents. Sulfic Tropaquents and Sulfic Fluvuquents are similar soils but with some profile development. Van der Kevie (1973) drew attention to sulfidic soils that may be saline under natural conditions and suggested hulk subgroups for these. Similarly some of the sulfuquepts may also be saline where they occur in swamps, subject to very infrequent flooding with saline water, but with a strong dry season leading to oxidation of sulfides. Table I, from van der Kevie (1973), summarizes the properties and main classes as they are placed in the Soil Survey of the U.S.(Soil Taxonomy) and in the legend of the Soil Map of the World.

B. MAPPING Potential acid sulfate areas are swampy and usually difficult of access and often covered in heavy vegetation, either mangrove or other swamptolerant trees, or extremely tough tall grasses in the tropics, and reeds in temperate areas. Apart from drying the samples and determining the acidity, or other laboratory methods, including microscopic examination, there are no completely positive ways of identifying these soils, or at least of determining how acid they will become on drainage. Several morphological features are indicative; soft muds with buried organic matter, particularly if the remnants can be identified as halophytic, dark gray rather than greenish gray colors, yellow mottles of jarosite in spoil from ditches, etc., are all useful indicators. As discussed in Section 11, D, physiographic relationships

TABLE I International Classifications of Acid Sulfate Soilsa Climatic zone

World wide

Soil Taxonomy

Typic Sulfaquenta

Main characteristics=

Potmh'al acid sulfatc soils pH (1: 1 water) of dried soil <3.5 within 50 cm if n 1.0: within SO cm if

Worldwide

Sulfic Hydraquents

World Soil Map

Thionic fluvisols

>

n < 0.7 pH (1: 1 water) of dried soil Thionic fluvisols <4.5 in upper 45 cm, or more acid-between 50 and 100 cm; n > 0.7 between 80 and 50 cm Gleyic solonchaka

Dystric fluvisols

Wet tropics and monsoon

Sulfic Tropaquents*

Temperate Worldwide

Sulfic Fluvaquents Typic Sulfihemists

Acidity requirements of sulfic hydraquents, but n < 0.7 between 80 and 50 cm Same as Sulfic Tropaquents Sulfidic materials within 100 cm; pH (1: 1 water) of dried soil <5.5

Thionic fluvisols, gleyic solonchaks, dystric fluvisols

Thionic fluviSols

t d

W

P

Main characteristics

pH (KCl) of dried soil <5.5 within 100 cm

Some t h a t are less acid than sulfaquents but sufficiently acid t o be included in Sulfic Hydraquents; nonsaline Salic horizon and saline at some time of the year; part that meets acidity requirements for Sulfic Hydraquents but not for Thionic Fluvisols Not sufficiently acid for Thionic Fluvisols but meets requirements for Sulfic Hydraquents; nonsaline As above

As above

hU 4 ?

8 s

Worldwide

Typic Sulfihemists

Worldwide

Typic Sulfaquepts

Wet tropics and monsoon

Sulfic Tropaquepts

Acid sulfate soils pH ( 1 : l water) <3.5 within 50 cm pH (1:1 water) <3.5 within 50 cm pH ( 1 : l water) <4.0 between 50 and 150 cm and/or 3.5 to 4.0 within 50 cm

Thionic fluvisols

As above

Thionic fluvisols

As above

Thionic fluvisols Humic gleysols Dystric gleysols

As above pH(KC1) 2 3.5; umbric or 0 horizon pH(KC1) 2 3.5; ochric A

Wet tropics

Histic Sulfic Tropaquepts

Acidity as in Sulfic Tropaquepts; Histic epipedon

Thionic fluvisols Humic gleysols

Monsoon and semiarid

Vertic Sulfic Tropaquepts

Acidity as in Sulfic Tropaquepts; cracks (1 cm) a t 50 cm when dry

Thionic fluvisols Humic gleysols Dystric gleysols

Acidity as in Sulfic Tropaquepts; Umbric or Histic epipedon Acidity as in Sulfic Tropaquepts; Ochric epipedon Acidity as in Sulfic Tropaquepts; sodium saturation > 15 in half or more of upper 50 cm; mostly saline in some part of t h e year

Thionic fluvisols Humic gleysols

Humid temperate

Sulfic Humaqueptsb

Temperate

Sulfic Haplaquepts

Monsoon and semiarid

a

Sulfic Halaqueptsb

From van der Kevie (1973).

a Tentative subgroups suggested by van der Kevie (1973). I value: an estimate of the degree of ripening (development).

Thionic fluvisols Dystric gleysols Thionic fluvisols Gleyic solonchaks

horizon As above Umbric or 0 horizon pH(KC1) 2 3.5; 0 horizon As above pH(KC1) 2 3.5; umbric or 0 horizon pH(KC1) 2 3.5;ochric A horizon As above pH(KC1) 2 3.5;umbric or

0 horizon As above pH(KC1) 2 3.5; ochric A horizon As above pH(KC1) 2 3.5;salic horizon and/or saline at some time of the year

n m

5 *z zm

U

5

z

Em 5 cU2

2 r T *4I m m

0,

rl t3

W

v1

296

C. BLOOMFIELD AND J. K. COULTER

and vegetation type can have strong local correlations with sulfidic materials, and are useful in mapping on aerial photographs, on which the different mangrove species, sedges, gelam (Melaleuca) are easy to identify. A complicating feature for soil mapping is the very strong macro- and microvariation in levels of sulfur. Microvariation arises because of the nature of pyrite formation related to the uneven distribution of organic matter; sampling should be replicated unless large samples are taken. Macrovariation arises from the relationship between physiographic features and pyrite formation. The degree of variation is illustrated by Westerveld and van Holst (1973), who stated that delineation of acid sulfate areas requires maps on a scale of 1:25,000 to 1 :10,000 in the more homogeneous areas and a scale as large as 1 :500 in the most heterogeneous areas. Because of the environment it is logistically impossible to map potential acid sulfate soils at such scales in the tropics. However the decision on whether to develop them for agriculture usually rests more on the percentage of the total area which will be affected by severe acidity rather than the actual location of the areas affected. The former can be decided by adequate sampling; because of difficulties of access random sampling is usually impossible, so that some form of grid sampling is necessary; a random grid, i.e., one in which the spacing of the grid lines is determined but the direction of the lines is decided at random, is possibly the best solution. Having obtained an estimate of the area likely to be affected by strong acidity, it can be decided whether the development project can support a limited area of very infertile soils that require expensive ameliorative measures, or whether the area affected is large enough to have a serious detrimental effect on the agricultural prospects of the whole project. Mapping soils that have already developed acid sulfate characteristics is less difficult, for jarosite mottles are usually evident, and pH values can be measured by a portable meter; agricultural development may have cleared the area, so that the state of crop growth can be ascertained, and the physiographical features can be clearly seen on the ground, or on aerial photographs. However, the problems presented are usually not so much those of identification of acid sulfate soils, but rather of assessing the seriousness of acidity, the limitations on agriculture and the probability of improvement. None of the soil classifications so far proposed can be related directly to a land capability classification of this sort.

VI.

Conditions for Plant Growth

We have seen that acid sulfate soils are characterized by low pH values, whereas potential acid sulfate soils have pH values near neutrality but are

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strongly reduced. Rorison (1973) has listed the factors detrimental to plant growth under strong acid conditions. These include: 1 . Direct effect due to injury by H+ions 2. Direct effect due to low pH ( a ) Impaired absorption of calcium and nitrogen (b) Increased solubility, and thus toxicity, of iron, aluminum and manganese (c) Decreased availability of phosphorus, caused by aluminumphosphorus interactions, and of molybdenum 3. Low base status, leading to deficiency of calcium, magnesium, and potassium 4. Abnormal biotic factors, such as impairment of the nitrogen cycle and mycorrhizal activity, and increased virulence of pathogens.

Most of these have been studied on acid soils, but a few on very acid soils. In addition, the presence of aluminum salts could lead to salt injury. Under strong reducing conditions the following factors may contribute to poor plant growth: ( 1 ) production of hydrogen sulfide; ( 2 ) mobilization of ferrous and manganous ions; (3) production of organic acids. In temperate areas cropping of acid sulfate soils takes place after the soils have been drained, so that in these regions we are concerned only with the effects of acidity. In the tropics, such soils may be drained for annual or perennial crops or temporarily waterlogged for rice, and in these regions we are concerned with toxic factors under both oxidizing and reducing conditions. A.

TOXICITIES

I. Hydrogen Ion and p H At the pH levels of acid sulfate soils some Htmay be present, and whereas root injury as a direct result of Htions below pH 4 has been suggested by work in solution culture, Rorison points out that plants may tolerate relatively large concentrations of Htions, so long as the concentrations of other cations are large, and the concentration of toxic polyvalent cations is small. Thus it is likely that the detrimental effects of aluminum and manganese in the soil solution far outweigh those of H+ ions (Adams and Pearson, 1967). Low pH inhibits the conversion of ammonium to nitrate, so that NH,' ions accumulate. Some plants take up both ammonium arid nitrate ions, but calcicole species may give poor or no growth when supplied with at this NHN , at pH 4.2, whereas calcifuge plants flourish with NH,-N pH (Rorison, 1973). Since conditions more acid than these are common

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.C. BLOOMFIELD AND J. K. COULTER

in surface soils of acid sulfate areas, the behavior of tropical species, particularly in their reaction to NH,-N and NOs-N, is obviously of interest. 2. Aluminum Aluminum is normally the major exchangeable cation in very acid soils. Little Fe3+appears to exist in exchangeable form, but both aluminum and iron exist in fairly accessible hydroxy forms as coatings and on edge sites. Little Fe3+can exist in solution at pH > 3.5 so that ferric iron is unlikely to be a cause of toxicity, except in very acid conditions, such as might occur in the subsoil where active pyrite oxidation is taking place. Aluminum, on the other hand, is appreciably soluble above this pH. The oft quoted work of Magistad (1925) gives the solubility of aluminum as 0.3 ppm at pH 4.50 and 76.4 ppm at pH 3.11. This refers to the A13+ion, but other aluminum ions, e.g., Al(OH)2+,may have a less steep increase in solubility with increasing acidity. Tanaka and Navasero (1966a) found that the concentration of aluminum in culture solution was less than 1 ppm when the pH > 5.5, regardless of the amount added. Tolerance to aluminum differs greatly between and within species, and, at least for a number of temperate crop plants, this tolerance has been thoroughly studied; the uptake of aluminum has been reviewed by Jackson (1967). Foy and Brown (1964) showed that oats yielded 75% of the maximum yield with 6 ppm of aluminum in solution, whereas the yield of mustard was only 7%. Reid et al. (1969) showed that within-species tolerance is genetically controlled, and could be detected in greenhouse trials. Of interest in this respect is the work of Chadwick and Salt (1969), who examined the tolerance of Agrostis tenuis, a frequent colonizer of colliery tip spoil. By sampling areas with a known history of colonization, they showed that tolerance to aluminum toxicity could probably evolve in about ten generations. Except for rice, tropical crops do not seem to have had the same attention as regards aluminum tolerance. Rubber, oil palms, and coconuts grow well in soils of pH 4 or above. Bananas and cassava also grow well at this value, and pineapples at below pH 4.0. Adams and Lund (1966) demonstrated the detrimental effect of aluminum to cotton, which appears particularly sensitive to aluminum toxicity and/or calcium deficiency, and Turner and Bull (1967) described aluminum toxicity symptoms in oil palms. Aluminum toxicity to rice plants was first reported by Miyake in 1916, who showed that 1.2 ppm of aluminum in solution was toxic. Cate and Sukhai (1964) summarized the literature on toxic levels for rice, and gave values varying from the 1.2 ppm of Miyake to 270 ppm given by Hart (1959). Tanaka and Navasero (1966a), using water culture, found that

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the critical concentration in the culture solution was about 25 ppm for plants with adequate contents of other nutrients, particularly phosphorus. However, their work illustrates the difficulties of using aluminum in culture solution, for even when 200 ppm was added to the solution, only 49 ppm of soluble aluminum was found on analyzing the culture solution; even at pH 3.5, they found only 175 ppm in solution, when 500 ppm had been added. Thus it would appear that split root techniques or mist spray cabinets are essential to keep large amounts of aluminum in solution. In Section 111, C we recorded groundwater samples from Thailand with 2.12 mmoles of aluminum per liter, and such levels would obviously be extremely toxic to rice. Tanaka and Navasero (1966b) leached small samples of acid sulfate soils from Vietnam and Malaya, with initial p H s of about 3.5, and found that the first leachate had a pH of 3.7 and contained 70 ppm of aluminum; rice plants grown in this leachate died, but normal growth was obtained in the fifth successive leachate, which had a pH of 3.8 and contained 21 ppm of aluminum. The toxicity of aluminum to rice plants is not in doubt, but the amount in the soil solution after the acid soils have been waterlogged for some time, is in doubt. Thus Tanaka and Navasero (1966b) reported a pot experiment in which initial soil leachate contents of 35 ppm dropped to less than 1 ppm with 3 weeks flooding or 30 days of incubation. These experiments showed an increase in pH of less than half a unit, i.e., from about 3.5 to 3.8, a critical range for aluminum, but they offer no other explanation for the large decrease of aluminum in solution. They record a very large increase in ferrous iron in the leachates after flooding or after incubation. Patrick and Wyatt (1968) have suggested that the reaction Fe(OH)z

+e

--t

Fe(OH),

+ OH-

is responsible for the increase in p H on waterlogging, but the existence of Fe(OH), under these conditions seems improbable, though it is often postulated. The formation of ammonia from decomposing plant material is probably the major factor in raising the pH of a waterlogged soil. It is hydroxyl that is responsible for neutralizing aluminum, rather than ferrous iron, as Cate and Sukhai (1964) suggested. Increases in pH, many of them greater than those reported by Tanaka and Navisero, have often been recorded. Ponnamperuma et al. (1973) reported rises from about pH 3.5 to 6.1 in 12 weeks’ flooding of acid sulfate soils from Vietnam, much of the increase taking place in the first 2 weeks. Nhung and Ponnamperuma (1966) reported an increase from pH 3.6 to pH 4.7 in 16 weeks’ flooding, whereas Tomlinson (1957) reported an increase from 2.7 to 6.2 when mangrove soils in Sierra Leone were

3 00

C . BLOOMFIELD

AND J. K. COULTER

flooded with rainwater. Kanapathy (1973) gave an increase from pH 2.6 to 6.3 in 60 days’ waterlogging. Beye (1973) found increases that varied with the soil treatment. In some polders the pH increased from 3.8 to 5.7; in others to less than 4.0. Soils in pots might be expected to behave differently from those in fields, especially if soluble salts were leached in the field. In conclusion it would appear that, whereas aluminum toxicity is certainly a very important factor in dryland agriculture, in rice culture, in which the land is flooded before and during the crop-although admittedly this is not always possible on these soils-aluminum toxicity is unlikely except in the early stages of submergence.

3. Iron Unless the pH falls below about 3.5, ferric iron is not soluble. Thus few examples of ferric iron toxicity would be expected, although Martin and Evans (1964) have reported that sugar cane can accumulate toxic amounts, giving reddish or rust-colored leaf symptoms. However, the concentration of ferrous iron increases greatly under reducing conditions. Nhung and Ponnamperuma (1966) report that the concentration of Fez+ reached 800 ppm after 6 weeks’ submergence. Hart (1959) extracted 500 ppm of Fez+with 0.2 M KC1 from mangrove soil at 65% moisture and a pH of 6.5, and 900 ppm at a pH of 5.5 and 50% moisture. In drier conditions (40% moisture) less than 100 ppm was extracted. Tanaka and Navasero (1966b) also reported very large increases in the iron contents of leachates in flooded conditions, with or without incubation, values of 800 to 1700 ppm being obtained. Ferrous iron concentrations of 5000 ppm, 2 weeks after submergence, were reported by Ponnamperuma et al. (1973), but values of 500-1000 ppm are more common; however, some soils apparently give very little. Toxic concentrations of ferrous iron are given as about 500 ppm by Nhung and Ponnamperuma. Tanaka and Navasero (1966b) concluded that iron was the main cause of poor growth of rice on acid sulfate soils. However, not all acid sulfate soils give large amounts of iron on reduction; this can be attributed to small iron contents, or the absence of “easily reducible” iron oxides, an ill-defined term. Iron oxides are plentiful in many nonacid sulfate rice soils, yet no toxic symptoms develop. Takijima ( 1965) suggested that under certain conditions, e.g., in peaty soils, rice roots lose their ability to form a protective zone around them. Iron in the rice plant gives some indications of the conditions in the soil, for Tanaka and Navasero (1966b) showed that contents may reach 6000 ppm in plants severely affected by iron toxicity, whereas normal plants contain about 200 ppm. In their liming experiment, rice roots had

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

301

1600 ppm in unlimed pots and 230 ppm in soils receiving 5 g of calcium carbonate per kilogram of soil. Tanaka et al. (1966) reported that rice leaves containing more than 300 ppm of iron exhibit iron toxicity symptoms. In culture solution, 100 ppm of iron and a pH of 3.7 may give toxicity symptoms, but normally more than 500 ppm are needed; young plants are more susceptible to iron toxicity. Rorison (1973) reviews information on the plant mechanisms of tolerance to toxicity; in waterlogged soils these have been related to the evolution of oxygen from roots, so precipitating ferric oxide and lessening the transpiration rate. Rice plants obviously do cause precipitation of iron oxide round their roots, yet under normal conditions they absorb sufficient iron to maintain healthy growth, even though the crop has a large need for this nutrient. 4 . Manganese Little is known about the toxicity of manganese in acid sulfate soils for most attention has been given to aluminum toxicity in dryland soils and iron toxicity in reduced soils. However, soils rich in manganese and with a low pH give manganese toxicity, particularly on alternate wetting and drying. The temporary acidity brought about by using acid hydrolysis fertilizers, e.g., monocalcium phosphate; can also give manganese toxicity (Agricultural Research Council, 1967). Perhaps few acid sulfate soils contain any appreciable quantities of manganese, having lost much of it during the soil formation process. Manganese is readily mobilized in rice soils, and accumulations of manganese dioxide often occur in a horizon below that of iron accumulation. Tanaka and Navasero ( 1 9 6 6 ~ )stated that manganese toxicity is rare in rice, and they found (1966b) that the manganese content of rice plants was low, irrespective of the amount in the soil solution. Lockard (1959) obtained no symptoms of toxicity in plants receiving 2 ppm manganese, but did so with 8 ppm in culture solution. He also found a strong varietal difference in the uptake of manganese; at 8 ppm of manganese in the culture solution one variety had 200 ppm in the leaves, another over 4000 ppm. 5 . Salt Eflects

There are large increases in soluble salts when pyritic soils are dried and oxidized; Ponnamperuma et al. ( 1973 ) give specific conductance levels (mmho/cm) exceeding 10 in some acid sulfate soils. Very frequently reports on conductivity do not define whether soil suspensions, solutions, or saturation extracts were used, so that comparisons are impossible. It would appear, however, that serious salt injury is possible in many soils. Not only are salts formed on oxidation, but considerable amounts of neu-

302

C. BLOOMFIELD AND

J. K. COULTER

tral salts may be left by periodic flooding with sea water (Section I ) . Such salts are washed out by the early rains and by subsequent flooding by fresh water during the wet season.

6 . Hydrogen Sulfide Hydrogen sulfide formed in anaerobic soils is not always completely immobilized, and plant growth suffers where this occurs. Vamos (1964) reported that damage by hydrogen sulfide in some paddy fields in Hungary is usually preceded by decreases in the temperature and atmospheric pressure; in one instance, enough hydrogen sulfide was released from a pond to kill unfledged birds in the neighborhood. Postgate (1960) described a spectacular evolution of hydrogen sulfide off the coast of South West Africa in the winter of 1950, when poisoned fish were strewn to a depth of several feet on the shore of Swakopmund. Morton (1965) recorded examples in Florida where dredging mangrove swamps released so much hydrogen sulfide from buried mangrove debris that buildings were discolored and, on one occasion, workmen were killed. Rice is the crop principally concerned in hydrogen sulfide toxicity, although Dommergues et al. (1969) describe similar effects on lucerne and broad beans on saline soils in Tunisia; Ford and Calvert (1969) reported hydrogen sulfide toxicity to citrus in Florida, 0.5 ppm hydrogen sulfide in the groundwater causing death of citrus roots. Ford (1973) demonsstrated a time-H,S concentration relationship with root damage. The physiological disease of rice associated with hydrogen sulfide is known in Japan as akiochi (autumn decline). The respiratory activity of the roots is impaired; affected plants are deficient in silica and bases, and at later stages of growth, in N and K as well (Okajima and Takagi, 1953, 1955, 1956a,b; Baba et al., 1953; Baba and Harada, 1954; Mitsui et al., 1954; Yamada and Ota, 1958; Vamos, 1967; Park and Tanaka, 1968). Plants affected by akiochi are susceptible to Helminthosporium leaf spot, and infection with this fungus is taken as an indicator of akiochi (Baba and Harada, 1954; Mitsui, 1956; Tanaka and Yoshida, 1970). The iron content of rice affected by akiochi tends to be greater than in healthy plants; Tanaka et al. (1968) found that sulfide decreased the root respiration of rice plants grown in water culture, even in the presence of excess Fez+,and increased the iron content of the shoots. It seems that the oxidizing power of the roots is diminished by the effect of hydrogen sulfide, and the roots lose their ability to absorb nutrients and the plants become susceptible to Helminthosporium and other diseases. The plants seem to become more sensitive to hydrogen sulfide when vigorous growth is checked by overcast weather, presumably because their oxidizing power is decreased (VBmos, 1964). Vimos (1958b) found that the application

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

303

of nitrate fertilizers inhibited sulfide formation. Ponnamperuma et al. ( 1965) corrected “suffocation disease” of rice by applying manganese dioxide to the soil before it was flooded. Brusone, another disease of rice, is caused by Piricularia oryza, and seems also to be associated with damage caused by hydrogen sulfide (VBrnos, 1958a, 1959a,b; Zsoldos, 1962). Soils on which akiochi occurs are characterized by being iron deficient, and the persistence of free hydrogen sulfide is ascribed to the lack of sufficient iron to react with all the sulfide formed in the waterlogged soil. It seems that hydrogen sulfide toxicity is not an intrinsic property of these soils, in that they do not contain excessive amounts of sulfate, but that it arises from the use of artificial fertilizers that contain sulfate (Baba and Harada, 1954); nowadays akiochi seems to be no longer a serious problem in Japan (Tanaka and Yoshida, 1970). Sulfide toxicity in akiochi soils can be prevented by incorporating subsoil, etc., to increase the iron content (Shiori and Tanada, 1954), but Yamane and Sat0 (1961) found that adding hydrated ferric oxide to a muck paddy soil caused little decrease in the amount of free hydrogen sulfide that formed in the flooded soil. Allam (1971) has also reported that, in Louisiana rice soils, the Fez+concentration had no appreciable effect on hydrogen sulfide accumulation, and suggested that it was sorbed on the clay fraction. Pitts (1971) working with the same soils postulated that a flexibacterium, that is capable of destroying hydrogen sulfide, exists in rice soils. Rodriguez-Kabana et al. (1965) examined the influence of hydrogen sulfide on nematodes in rice soils and recorded considerable control. They found 0.1 to 1 ppm hydrogen sulfide in the soil-water phase 5-7 days after flooding with as much as 30 ppm in some soils after 100 days’ flooding. Although these levels killed the nematodes, the authors report no damage to the rice. When discussing the immobilization of sulfide in flooded soils, Japanese writers consistently refer to “active ferric oxides,” but we have found no definition of this quantity.’ However, it is implicit in the use of this term that not all the soil iron is capable of reacting with sulfide. It is to be expected that flooding a soil would increase the reactivity of the iron it contains, and it is significant that mud from river beds, etc., is more effective than hill soil as an amendment to degraded paddy soils (Baba and Harada, Motomura and Yokoi (1969) distinguished active and inactive ferrous iron, the former being extracted by 0.2% aq. AICI, followed by 1 N NaOAc, pH 3; inactive ferrous iron was calculated as the difference between total Fez+ extracted by HF/HzS04 and the active fraction. It is unlikely that this distinction has any real significance, as Pruden end Bloomfield (1969) showed that both AICI, and HF give spurious values for ferrous iron in soils.

304

C. BLOOMFIELD AND J. K. COULTER

1954). Bloomfield (1969) found that a slight excess of a laboratory-prepared hydrated ferric oxide, relative to the total sulfate, was sufficient to immobilize all the sulfide formed in microbiological sulfate-reduction experiments. However, when soil containing a severalfold excess of iron was substituted for the artificial ferric oxide, under the same conditions a considerable proportion of the sulfide was not trapped. Less free hydrogen sulfide was obtained with a periodically waterlogged soil than with a soil from a well-drained site, although the HC1- and dithionite-soluble iron contents of the two soils were almost identical. The greater reactivity of iron in the periodically flooded soil was illustrated by the amounts of iron dissolved when the two soils were incubated anaerobically with plant matter, without added sulfate-about 3 times as much iron was dissolved from the poorly drained as from the well-drained soil. The proportion of free hydrogen sulfide decreased asymptotically as the proportion of soil in the incubation mixture was increased, so that in this respect the relationship between active and total iron was not linear (C. Bloomfield, unpublished). Further, different proportions of free hydrogen sulfide were obtained with different forms of plant matter, although without added sulfate, weight for weight the two forms of plant material dissolved the same amounts of iron in anaerobic incubation experiments. It thus seems that biochemical factors also influence the extent to which sulfide combines with iron in anaerobic soils. Sulfate-reducing organisms do not operate in very acid conditions (Section 11, B) so hydrogen sulfide toxicity is unlikely in acid sulfate soils, except where the acidity decreases after prolonged waterlogging. Some toxicity in dryland crops is therefore possible when the acid sulfate horizons are waterlogged to counteract acidity, but none has been reported. The more vigorously the rice plant is growing the better it can cope with hydrogen sulfide in the soil solution, by the detoxification' mechanisms of the roots, possibly oxidation, and/or by proliferation of its root system to compensate for root destruction. The latter has been reported from Malaya (Annual Report, 1957) where injection of hydrogen sulfide saturated solution into the soil doubled the weight of the roots, root proliferation being greatest near the surface.

7. Organic Acids Hollis and Rodriguez-Kabana ( 1967) showed that acetic, propionic, and n-butyric acids, the latter is very small amounts, accumulated in Louisiana rice soils. Acetic acid was dominant, with a concentration of 3X me per liter in the soil solution. The undissociated molecule is regarded as the toxic factor, and as dissociation is pH dependent, an increase in pH from 4.5 to 5.5 decreases the concentration of this 10-fold.

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

305

Tanaka and Navasero (1967) also showed that acetic and butyric acids had a deleterious effect on growth in a culture solution of pH 4.0, but had no effect at pH 6 or 8. They concluded that as the pH of most rice soils rises above 6, the concentrations of organic acids are normally not great enough to cause damage. B.

DEFICIENCIES

I . Phosphorus

Rorison ( 1973 ) states that aluminum inhibits the uptake of phosphorus and seriously limits the growth of susceptible species, but Jackson ( 1 967) draws attention to aluminum accumulator plants, like tea, that contain normal amounts of phosphorus in the aboveground portions, even when they take up large amounts of aluminum. Precipitation of aluminum phosphate may occur outside the root and also in the intercellular spaces of the cortex. The large amounts of exchangeable aluminum in acid sulfate soils, under dryland conditions, could cause severe phosphate deficiency in susceptible crops, but few investigations on phosphate behavior have been reported, though many reports show the need for phosphate by rice on acid sulfate soils. Tanaka and Navasero (1966a) found that acid sulfate soils from Vietnam and Malaya had little available phosphorus, plants in pot culture having very small amounts. Heavy dressings of phosphate eliminated iron toxicity symptoms and gave normal growth of the plants. Moorman (1961) found that 800 kg of rock phosphate per hectare had no residual effect in the second year on rice soils in Vietnam. Hesse (1963) and Watts (1969) reported large retention of phosphorus by fresh mangrove muds, and Watts also reported very low levels of phosphorus in the water of fishponds in acid sulfate soils in Malaya. Adding phosphate to the water greatly increased the yield of fish. Conditions for residual effects probably vary, for there are reports from Senegal of residual responses after 5 years from phosphate application (IRAT, 1971 ). It is likely that phosphate deficiency is very widespread in acid sulfate soils and that good responses will be obtained when other limiting factors are removed. It is uncertain, however, whether the deficiency can be attributed to acidity per se, or to overall shortage of phosphates. Variscite and strengite are the most likely stable end products of phosphate reactions in acid soils. In the crystalline form both are of low solubility except at very acid p H s ; Bache (1963) found that, in pure systems, the pH of the equilibrating solution had to be below 3.1 for the phosphate concentration in the solution to be controlled by the solubility product of variscite. However, the initial precipitation products are possibly amorphous compounds

306

C. BLOOMFIELD AND J. K. COULTER

adsorbed on the hydroxy iron and aluminum materials, and the release of phosphate from these would not be controlled by pH. Under the reducing conditions of rice soils, iron phosphate compounds become available ta the plant (Patrick and Mahapatra, 1968). Thus the reactions of phosphate in acid sulfate soils may depend on the timing of application. If applied when the soils are dry and are at their maximum acidity, with large amounts of aluminum in solution, aluminum phosphate may be precipitated. Although this is likely to be in an amorphous form, it would crystallize on aging and hence be of limited solubility as soon as the pH increased with waterlogging. Phosphate added after the soils are flooded and reduced would react with the ferrous iron to form ferrous phosphate, which would remain available to the rice plant. 2 . Copper Deficiency Copper deficiency in pineapples has been reported by Moorman (1961). This may be associated with the rather higher organic contents of the soil, as pineapples show copper deficiency on nonacidic peat soils. Grant (1973) reports copper contents of 10-100 ppm, mainly in the form of chalcopyrite, in muds in Hong Kong. In Nigeria, copper sulfate gave a 40% increase in rice yields when applied to mangrove muds (Annual Report, 1962).

3. Cations Bases are removed as sulfates and replaced on the exchange complex by aluminum, and to some extent magnesium, during the formation of acid sulfate soils. Acid sulfate soils are therefore likely to be deficient in calcium and potassium, but exchangeable magnesium may be quite high; however, Turner and Bull (1967) state that oil palms of acid sulfate soils frequently show symptoms of severe magnesium deficiency. Reports on the amounts of bases show large differences. Sombatpanit (1970) quotes 3.5-5.0 me/100 g exchangeable calcium and 3.0-3.2 me/100 g exchangeable magnesium in the top 35 cm of an acid sulfate soil in Thailand. Amounts of this order are also given by Nhung and Ponnamperuma (1966) for a soil from Vietnam. The figures for the nonacid sulfate soil from the same area are 5.5-10 me/100 g calcium and 5.3-6.1 magnesium. Nonacid sulfate soils derived from marine alluvium in Malaya also have exchangeable calcium contents of 5-10 me/100 g (Coulter, 1972), but the well-weathered soils on nonalluvial materials have often less than 1 me/100 g exchangeable calcium. As many tropical crops have relatively small needs for calcium, these values for the acid sulfate soils are not unduly small. Pham et al. (1961) give 3.0 me/100 g ex-

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

307

changeable calcium in the 0-35 cm horizon, 2.9 in the “cat” clay horizon, and 3.6 in the reduced horizon; corresponding figures for magnesium are 4.1, 5.7, and 9.0; similar values are given by Vieillefon (1969) for acid sulfate soils from Senegal. In Sarawak, on the other hand, Andriesse et al. (1973) show that soils from lobster mounds, which had become oxidized and leached, had a maximum of 1.6 me/100 g exchangeble calcium with none in some horizons. Although the hinterland rocks from which these soils are derived are relatively poor in bases, recent marine deposits in the same area had 5 to 6 me/100 g exchangeable calcium, and it would therefore seem that under high rainfall and virtually continuous leaching very small amounts of exchangeable bases will be retained. Where there is a prolonged and intense dry season, as in Thailand and Vietnam, there is less leaching of bases. In temperate countries, e.g., the Netherlands, exchangeable calcium and magnesium contents are quite large, the values at the surface reflecting the addition of lime; even in the deep subsoil of drained profiles 3-5 me/100 g exchangeable calcium has been reported. Potassium may be deficient in some acid sulfate soils but, as in the case of calcium and magnesium, no detailed investigations have been reported. Clays of marine origin often contain much potassium, and Sombanpanit (1970) found 1.2-1.7% total potassium in soils from Thailand. C.

BIOLOGICAL FACTORS

Little is known of the biological conditions in acid sulfate soils, other than those reported for the sulfur cycles. Much research has been done on the general effects of acidity on microorganisms, and many studies have reported on the effects of acidity on Rhizobia. Tropical species are apparently much more tolerant of acidity than temperate species, a reflection of their tolerance of aluminum, though they are susceptible to large amounts of manganese. Cover crop legumes grow on acid sulfate soils with a pH of about 4.0 (Bloomfield et al., 1968) and, given adequate phosphate, legumes such as Centrosema and Pueraria flourish at low pH. Nitrogen fixation by nonsymbiotic microorganisms has been reported as occurring around the roots of rice plants (IRRI, 1971). The amounts of nitrogen fixed are relatively small, but if fixation ceases under very acid conditions, then the supply, already low in many rice soils, will be worsened. Mycorrhiza contribute substantially to the uptake of phosphorus in phosphate-poor soils; although they are extremely tolerant of acidity, they are likely to be affected at the pH values of acid sulfate soils.

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C. BLOOMFIELD AND J. K. COULTER

VII.

Management for Agriculture

The reclamation and improved use of acid sulfate soils cannot be discussed on the merits of the soils alone. Other environmental factors like climate, and also social and economic considerations, must play a major role in any decisions on investments in improved agriculture. Thus there will be no single panacea for the betterment of these soils, and this discussion on improvement can deal only in broad terms with a few major concepts. The factors of the physical environment that influence their use include the degree of acidity that develops on drainage, the depths of nonacid sulfate soil covering buried acid or potential acid horizons, the geographical distribution of acid sulfate soils vis A-vis nonacid soils, i.e., whether they comprise small areas in a larger mass of nontoxic soils or large contiguous areas, rainfall distribution, i.e., intensity of the dry season, and ease of water-table control during the dry season. Their utilization for biological projects other than agriculture, e.g., fish ponds and forestry, requires consideration in an economic and social context. There are vast areas of these soils used for agriculture, and farmers themselves have devised means of farming them at an acceptable, albeit low, level of production. In temperate areas cereals, grass, and sugar beet have been grown, though grass is probably the major crop. In the tropics both annual and perennial crops are grown, and rice is by far the most important crop. We have seen from the discussion in Section VI, A that the major toxicity factors are likely to be aluminum in the dry soils and ferrous iron and hydrogen sulfide in the waterlogged soils; thus ameliorative treatments are broadly aimed at dealing with these toxicities. Ponnamperuma et al. (1973) have summarized the ameliorative treatments that have been suggested by scientists or applied by farmers. These include prolonged submergence, leaching with rain or sea water or a succession of these, additions of lime or manganese dioxide or various combinations of these treatments. Farmers’ systems consist basically of keeping the land waterlogged and growing rice, increasing the depth of nontoxic topsoils by ridging, growing tolerant crops and, in nontropical areas, deep ploughing to mix in calcareous horizons, liming, fertilizing, and water table control. A.

WATERLOGGING

I. Rice The flat alluvial soils under mangrove and other brackish water-tolerant vegetation have been cleared for rice in many parts of the tropics. Inevita-

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GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

bly then this has lead to the opening up of areas with considerable sulfide levels. In Sierra Leone rice has been grown in the tidal areas adjacent to the rivers and creeks for nearly 100 years. Mangrove was cleared and rice planting followed immediately, yields of the order of 2000-2500 kg/ha being obtained. During the rainy season these areas are flooded twice daily as the fresh river water is backed up by the tide, whereas in the dry season, with <150 mm of rainfall in 6 months, the soils are flooded at spring tides with salt water. In attempts to extend rice cultivation into areas of permanent salinity in Sierra Leone, perimeter bunds were constructed around some areas so that saline water could be excluded. In the Rice ReTABLE I1 Yields (kg/ha) of Rice, as Affected by Water Control, Rokupr Research Farm, Sierra Leone (Annual Report, 1959) Year"

Block No. 22 23 94 25

26 27

19351943, average

1944

1945

1946

1947

1850 2310 2545 1900 2560 3160

860 1170 2055 1755 755 1185

10 200 655 135 255 620

SO 0

0 35 145 235 0 55

PO0

65 10 35

1948

1949

1950

1951

1952

800

1955 2670 3010

1670 2455 2970 2735 3160 2625

2625 2570 2670 2910 1910 2535

5270 2960

1255

1120 1980 955 935

5280

2070 2280

3595

5870 3425

a 1955-1943, farm under tidal influence; 1944-1947, tidal influence excluded; 1948-1952. tidal influence restored by breaking bunds.

search Station at Rokupr such bunding was done after the station had been in use for several years, and Table I1 gives the yields for 8 years prior to the bunding, 4 years during the bunding, and 5 years after the restoration of tidal influence during the dry season. This and other work in Sierra Leone illustrates very well the detrimental effects of dry season desiccation, and the rapid restoration to relatively good yields once dry season waterlogging is provided. Farmers in Indonesia, Vietnam, and Thailand have also evolved systems for cultivating rice on these soils. In Indonesia (Driessen, 1973), Bandjarese farmers of South Kalimantan manage the potential acid soils by a very shallow tillage to deal with weed growth, leaving the potential acid soil undisturbed; they use several transplantings of rice seedlings so that in the final transplanting the seedlings are large enough to cope with deep flooding.

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In Vietnam, Moorman (1961 ) reports that the farmers, by maintaining waterlogged conditions as much as possible, grow rice over quite a proportion of the Mekong delta on soils with a pH, when dry, of 2.8. In Thailand, also, van der Kevie (1972) reports that rice, often the floating variety that tolerates deep flooding, is the major crop on these soils. The farmers’ successful technique of waterlogging these soils is supported by pot and field experiments in other parts of the world. In Guyana, Cate and Sikhai (1964) used pot experiments to demonstrate the value or prolonged preplanting flooding in using toxic soils for rice. Experiments in the Medina experimental polder in Senegal (Beye, 1973; IRAT, 1971 1, where different intensities of drainage were installed, showed the detrimental effects of intense drying. Although very large areas of potentially toxic soils are farmed in this manner, there are several disadvantages which make it desirable to improve the system. These include: 1. Yields are generally low, commonly 800-1000 kg/ha, though farmers in Sierra Leone have reached over 2000 kg/ha. 2. Opportunities for improving yields, using fertilizers and better varieties, are limited, although considerable responses to nitrogen by the new rice varieties is reported in the Medina polder in Senegal (IRAT, 1971 1. 3. Dry spells during the rainy season can lead to soil drying, with consequent strong acidification and very low yields. 4. In some areas, the system appears to break down. Thus Driessen (1973) reported that changes in the drainage conditions in South Kalimantan lowered yields to 500 kg/ha, so that the rice fields were eventually abandoned. Van der Kervie ( 1973 ) also reported decreased yields in such areas. 5. Extensive areas may be flooded by very acid floodwaters leading to destruction of rice on nontoxic soils. Moorman ( 1961 ) and Pons and van der Kevie (1969) describe how flood waters with pH values of 2.5-3.5 damage the crops. 6. Waterlogging does not eliminate, and may exacerbate, the effects of reducing conditions, i.e., ferrous iron and hydrogen sulfide toxicity. Other detrimental effects include the absence of good potable water supplies, the flocculation of clay suspensions in the canals by the acid sulfates, necessitating frequent cleaning, and the problems of controlling salinity in coastal areas owing to the detrimental effects of bunding. 2. Other Crops

Complete waterlogging is obviously out of the question for dryland crops, but a measure of water-table control has proved advantageous where a toxic horizon is covered by a nontoxic deposit. In these, deep drainage

GENESIS AND MANAGEMENT OF ACID SULFATE SOILS

31 1

leads to oxidation of the sulfides and, under appropriate drying conditions and watertable levels, large amounts of acid sulfates and/or neutral salts can accumulate at the surface (Section 111, C ) . Provided the rise of salts is controlled, comparatively shallow layers of nontoxic soils give acceptable yields. Zuur (1952) concluded that sugar beet was successful in Holland where the toxic horizon was below 40 cm, although fruit trees were affected at this depth, and Bloomfield et al. (1968) suggested that oil palms in Malaya were little affected by toxic layers below 75 cm. The effectiveness of this technique obviously depends on the crops obtaining sufficient nutrient from a shallow depth of soil. In certain conditions this depth is lessened by the presence of a peaty surface horizon which dries out irreversibly (Bloomfield et al., 1968). Roots grow poorly in this horizon, and shallow rooting crops may suffer serious damage. Examples of controlled watertables giving good crops have been recorded by Chenery (1953), who observed that, in Ruanda, peat swamps, similar to those in Uganda described in Section I, were under intensive cultivation with sweet potatoes and sorghum, using a cropping system of banks with the watertable within 50 cm of their crest. Coulter (1973) reported the considerable improvement in oil palm yield by raising the watertable and keeping the acid sulfate layer flooded. Van der Kevie (1972) has reported a combination of ridging and flooding in Thailand so that the drains alongside the ridges are fairly full of water. If the ridges are too high, i.e., soil is removed from the toxic horizon, then the ridge-tops become very acid. Van Breemen (1973) suggested that this should be avoided, but it would appear that in Vietnam the farmers do this deliberately to promote oxidation and leaching, meanwhile growing very acid-tolerant crops (pineapples) on the ridges. B.

DRAINAGE AND LEACHING

We have shown that soluble salts are formed during oxidation, and that some of these are toxic to plants. Consequently, it has been frequently proposed that potential acid sulfate soils should be intensively drained and the resultant soluble salts leached away in the drainage water. Apart from the costs and logistical problems, other difficulties include the nearly completely aluminum-saturated soil that could result, (Section 111, C), and the considerable quantities of jarosite, which will hydrolyze at higher pH’s, and thus provide sulfate ions over a considerable time. Many laboratory experiments have been reported on the rate of oxidation of pyrite, and on the requirements for leaching the sulfates. Hart et al. (1963) estimated that one field season’s drying would oxidize about half the pyrite present. Another laboratory experiment in Sierra Leone

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(Annual Report, 1959) showed that daily leaching with sea or fresh water would remove half the titratable acidity of the oxidized soils after using five times the weight of soil, the rates of leaching being the same for both fresh and sea water. After leaching a soil of pH 2.6 with 15 times its weight of water, its lime requirement (to pH 5.2) was lowered from 38 to 8 tons of CaC03 per hectare per 15 cm. Kivenen (1950) reported an increase in pH from 2.5 to 3.7 when small samples of acid clays were leached with copious quantities of water. The conditions for oxidizing and leaching small, well homogenized samples in the laboratory are of course very different from those in the field, or even of undisturbed cores in the laboratory. The latter have much lower rates of oxidation and leaching (Bloomfield, 1973). Well controlled, properly monitored field experiments on oxidation and leaching have not been reported, although a number of one-season trials have been described. In Sierra Leone it is reported (Annual Report, 1958) that leaching by rain, where the excess of rainfall over evaporation in the rainy season may exceed 1200 mm, is an extremely slow process and may take 10 years to complete. Other evidence for slow leaching rates in field conditions has been discussed by Coulter (1973); he reviewed circumstantial evidence that pyrite contents can be lowered from 2 or 3% to about 0.5% in 5-10 years and suggested that 10 years is an optimistic estimate for the time taken to oxidize sulfides and remove the sulfates under good drainage conditions. Other evidence on the slow removal of sulfur by oxidation and leaching and the infertile nature of the resulting soil is shown by the work on mine spoils discussed in Section IV, A and also by observations on drain spoil and bunds. Evans (1966) has reported that the spoil from canals in sugar estates in toxic soils in Guyana remains barren for a long period, even though conditions for oxidation and leaching are obviously good. Toxic sulfates apparently do not move downward rapidly for he found that, on making vertical mulch slits through the toxic spoil into the soil beneath and filling the slits with filter press mud, good sugar cane growth was obtained in the slits. Experiments on leaching with sea or brackish water have been reported from Sierra Leone (Hart et al., 1963) and Guyana (Evans and Cate, 1962). It has been suggested that the saline water acts in the same way as a neutral salt in laboratory experiments so that exchangeable aluminum is displaced from the soil by the bases in the sea water. Evidence for this is inconclusive in view of the difficulty of removing the aluminum ion from the exchange complex. Leaching with saline water is obviously of potential value, where large quantities can be obtained easily. Although there are theoretical advantages to be derived from the oxidation and leaching of acid sulfate soils, the practical difficulties in all but

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a few areas are very great. Intensive drainage is obviously necessary, copious supplies of water are needed and, most important of all, if it is necessary to wait 5-1 0 years before the oxidizable sulfur components are leached and the soil is limed and cropped, the initial investment will be largely discounted.

C. LIMING Acidity can obviously be corrected by liming, and acid sulfate soils have been successfully reclaimed in Europe where lime is cheap relative to the value of the land. The major problems in using lime in tropical areas are lack of convenient supply-some countries have to import lime-poorly developed road systems for transporting the large amounts needed, and lack of implements for distribution and for deep ploughing into the soil. These disadvantages are often accompanied by a lack of capital for purchasing the material. This suggests that, for liming to be effective over a large area, its purchase and distribution by governments as a capital input would be necessary. The quantities of lime needed to be effective have been variously estimated at anything from 4 to about 100 tons of calcium carbonate per hectare, but there is a dearth of critical field experiments for determining optimum amounts. Kivenen (1950) used rates of 7, 14, and 21 tons of lime per hectare on fodder crops in Finland and reported about the same yields, with each, averaged over 10 years. On rice, in Sierra Leone, Hart et al. (1963) increased yields from zero with no lime to 1900 kg/ha with 5 tons/ha and 2000 kg/ha with 10 tons/ha, in the absence of seawater leaching. In conjunction with seawater leaching, 2.5 tons of lime per hectare gave as good yields. as 10 tons/ha. However, yields in the succeeding year were much smaller with all treatments. Evans (1966) suggested using aluminum saturation (me A1 displaced by neutal salt as percentage of total displaceable cations) the critical value being 60%, above which liming would be required to lower it to that figure. It is doubtful, however, whether this would be widely applicable even for one species. In Malaya, a wide range of crops are grown on soils of >80% aluminum saturation (Coulter, 1972). Furthermore, different strengths of salt extractant will extract varying amounts of aluminum so that it is not possible to fix a critical aluminum saturation. Normally the subsoil is more acid than the top soil and lime must be introduced into the subsoil, an expensive undertaking and obviously only possible with the use of heavy machinery. Experience in liming very acid grassland soils in the United Kingdom shows that most of the lime is retained in the grass-mat on the surface (Johnston, 1972). On the other hand, Kanapathy (1973) has shown some movement of lime into the sub-

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soil when limestone was broadcast on the surface. He measured the pH values of the 0 to 15 cm, 15 to 30 cm, and 30 to 45 cm horizons of an oil palm area in Malaya before liming with 5, 10, and 15 tons of ground limestone per hectare and 5 years later; 5 tons increased the pH of the 0 to 15 cm horizon from 3.9 to 4.3 and of the 30 to 45 cm horizon from 2.9 to 3.5; 15 tons increased the values from 3.8 to 4.8 and from 2.9 to 4.2. Care is needed, however, in interpreting such results, especially in the absence of adequate replication to measure the variation. The detrimental effect of ferrous iron on rice has been discussed in Section VI, A, and liming has been suggested as a control for this. Nhung and Ponnamperuma (1966) found that, in pot experiments, 0.8% CaC03 (8000 kg/ha, 15 cm) depressed the Fez+ in the soil solution from 490 ppm to 130 ppm by raising the pH at planting from 3.7 to 5.5. Where large amounts of toxic ferrous iron are produced on waterlogging, adding lime in considerable quantities may thus be beneficial. It is not known, however, how long the effects of such dressings last. The effects of liming can be achieved by deep ploughing where there is a calcareous layer at depth. Pons (1956) suggested that in the region of 8% calcium carbonate is necessary for this.

D.

OTHERTREATMENTS

Nhung and Ponnamperuma (1966) and Pomamperuma et af. (1973) added manganese dioxide (0.5 and 1 % ) to an acid sulfate soil and found that it retarded the fall in redox potential, depressed the aluminum and iron in the soil solution and apparently retarded sulfate reduction. In pot experiments manganese dioxide alone or in combination with lime improved yields. This treatment has not been reported on in field trials; there are obvious difficulties under field conditions where the quantities, about 10,000 kg/ha, and the mobility of manganese, leading to rapid removal from the surface layers might render it ineffective after a season or two. E. CONCLUSIONS

There are a number of techniques for the reclamation of acid sulfate soils. Experiments in pots and in the field confirm that these treatments do improve yields, but little information is available on long-term reclamation. Controlling the watertable and using lime are the most promising techniques; selecting varieties of dryland crops for tolerance to aluminum toxicity and of rice to ferrous iron toxicity could be worthwhile. Where amelio-

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rative treatments are used, raising the fertility, by the addition of phosphates and probably of nitrogen, potassium, and copper, may be essential. Improved productivity of these soils in areas of dense population will be needed but otherwise they are better left alone or used for forestry or, in limited areas, for fish ponds. Investigations on these have been reported by Prowse (1968) in Malaya, where additions of lime and phosphorus to the pond water were necessary for satisfactory fish growth; in Hong Kong, Grant (1973) has recorded that ponds in acid sulfate soils have had to be abandoned because of poor fish yields.

VIII.

Analysis of Pyritic Soils

The detection of actual acid soils presents no real difficulty-the pH, the presence of jarosite incrustations on exposed surfaces of spoil from ditches etc., and of ferruginous deposits in ditches are usually sufficient indication. The recognition of potential acid s,ulfate soils in undrained areas is more difficult (Section V, B ) . The presence of black stains of ferrous sulfide, that rapidly turn brown on exposure, is a valuable indication that the soil may contain pyrite. The smell of hydrogen sulfide produced when a specimen is acidified, or the blackening of a lead acetate paper, allows very small amounts of sulfide to be detected. A.

DETECTION OF

PYRITE

Pyrite gives hydrogen sulfide when heated with an acid solution of stannous chloride, or with zinc and dilute acid, and this has been proposed as a field test (Neckers and Walker, 1952). Unfortunately hydrogen sulfide is formed from soil organic matter under these conditions (Smittenberg et al., 1951; Melville et al., 1971), so that in unskilled hands this test could lead to confusion. Edelman, quoted by Brinkman and Pons (1973) modified Feigl’s spot test for sulfide by adding detergent, taking the extent of foaming as a measure of the sulfide content of the soil. The test depends upn the catalytic decomposition of azide by sulfide, and it seems that soil organic matter also gives a positive reaction (Pons, 1970). Pyritic sulfur is readily oxidized by hydrogen peroxide, and an appreciable fall in pH can indicate the presence of pyrite. However, partial oxidation of organic matter with hydrogen peroxide also causes acidification, and confusion could arise with soils containng much organic matter and little pyrite. Poelman ( 1973b) and Ford and Calvert (1970) avoid this difficulty by assessing sulfate visually as barium sulfate.

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B.

MEASUREMENT OF ACIDIFICATION

The degree of acidification produced after exposing pyritic soils to atmospheric oxidation is often used to identify potential acid sulfate soils. In many instances, emphasis is placed on air-drying the soil rather than on oxidation as such. Some investigators expose the soil for several months after air-drying, and others dry and rewet several times before measuring the final pH. It is unlikely that appreciable oxidation of pyrite would occur in the dry state, and as air-drying a partially oxidized pyritic soil inactivates ferrous iron-oxidizing bacteria, only the relatively slow chemical oxidation process would operate in the rewetted soil. Ideally the soils should be kept permanently moist and aerated. Polythene is permeable to oxygen, and extensive acidification of moist samples stored for several weeks in thin polythene bags has been observed; this could perhaps be the most convenient way of making the test. Van Breemen (1973) found that oxidizing a pyritic soil in the laboratory always gave a pH 1-2 units lower than the value attained by the same soil when drained in the field, so that a large proportion of the acid formed in the laboratory is either not formed in the field, or is neutralized or eliminated in some way (Brinkman and Pons, 1973). Presumably the difference between the acidities developed in the field and in the laboratory results from samples tending to be more completely oxidized in the laboratory and not being subjected to leaching, th,at the hydrolysis of ferric and aluminum sulfates is minimal, and acid oxidation products are not removed from the system. Because the pH of a water slurry of an acid sulfate soil is a function of the dilution, Doemel and Brock (1971 ) measured the pH at various dilutions and extrapolated the readings to zero dilution.

c.

DETERMINATION OF MONOSULFIDE

The monosulfides are readily decomposed by dilute acid, and several convenient methods for determining the liberated hydrogen sulfide are available. However, the monosulfide contents of sulfidic soils are usually too small to be significant. The speed with which ferrous sulfide oxidizes on exposure to air precludes drying and adequate mixing to obtain representative samples, and as ferrous sulfide is usually concentrated around decaying root fragments, and generally sporadically distributed, prohibitively large samples would need to be used to obtain representative results. As well as these mechanical difficulties,the chemical determination of ferrous sulfide in soil is subject to uncertain errors caused by the presence of acid-soluble ferric compounds, so that some hydrogen sulfide is oxidized by Fe3+ when the sample is acidified. Pruden and Bloomfield (1968)

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limited errors from this cause to a degree t;*,rtwas acceptable in laboratory incubation experiments by using a solution of stannous chloride in hydrochloric acid to liberate hydrogen sulfide. However, pyrite also yields hydrogen sulfide with this reagent, so that this method is not applicable to normal field samples. It has been suggested that iron monosulfides can be determined indirectly by determining the ferrous iron liberated by dilute acid. Under these conditions Fe3+is reduced by both hydrogen sulfide and soil organic matter (Pruden and Bloomfield, 1969), so that results obtained by this method would have no significance.

D. DETERMINATION OF PYRITE Pons ( 1964b) described a microscopical method for determining pyrite in soils; the method gave good correlation with chemically determined values. Pyrite can be determined chemically as the difference between the sulfate contents before and after oxidation, hydrogen peroxide being perhaps the most convenient oxidizing agent. Tabatabai and Bremner (1970) used alkaline hypobromite prior to determining total sulfur as sulfate, and this has the advantage of giving an iron-free extract. However, the absence of iron is essential only if sulfate is to be determined turbidimetrically-a method that we find unreliable. Iron can be removed with an ion exchange resin if sulfate is to be determined as barium sulfate, but interference from iron can be avoided more readily by adding ascorbic acid to reduce Fe3+ before precipitation. Iron does not interfere in the reduction of sulfate to hydrogen sulfate with hydriodic acid (Luke, 1943); absorption of the hydrogen sulfide in sodium hydroxide and titration with mercuric acetate solution, with dithizone as indicator (Archer, 1956) is a very precise method for determining small amounts of sulfate. The basic ferric and aluminum sulfates formed in acid sulfate soils are relatively insoluble, and fairly drastic conditions are necessary to ensure complete extraction; 20-30 minutes of digestion with 2 N hydrochloric acid, on a water bath, is usually adequate. The rate of oxidation of pyrite by Fe3+is appreciable, so that the acid extraction should not be prolonged unduly, and for the same reason it is preferable to use separate samples for the before- and after-oxidation sulfate determinations. Bloomfield et al. (1968) observed that oxidizing acid sulfate soils with hydrogen peroxide gave consistently slightly smaller total sulfur values than ignition with vanadium pentoxide (Bloomfield, 1962). The difference between the two values probably represents organic sulfur not oxidized by hydrogen peroxide, and as such would have little significance in this context.

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Rasmussen (1961) determined the pyrite content of soils by X-ray diffraction, with magnesium oxide as internal standard. Petersen ( 1969) used the same method, making a correction for interference by quartz. For survey purposes, the determination of total sulfur by X-ray fluorescence spectroscopy provides a rapid method for the initial screening of large numbers of samples. Brown and Kanaris-Sotiriou (1969) found that the generally large and variable organic content of Malayan acid sulfate soils caused serious matrix effects, but the application of a correction factor based on the loss on ignition gave acceptable results.

IX.

Conclusions

Acid sulfate soils cover relatively small areas in temperate lands, though they may be important locally in drainage projects. Pyritic materials in mining spoils are of considerable importance in many regions. Acid sulfate soils cover large areas in the tropics, and where they occur in densely populated zones urgently need improvement for agriculture. Much research has been done on the factors governing the formation of sulfides in sediments and on the mechanisms involved in the oxidation of the sulfides, so that the conditions leading to extreme acidity are now well understood. However simple routine methods that are rapid and reliable are needed for detecting potential acid sulfate soils, and for predicting the degree of acidity that would develop on drainage; this is necessary for soil suitability ratings. Whereas the progress of acidification on drying has been determined in laboratory experiments, very little work has been done in field conditions or on undisturbed cores, which would be the nearest approximation to the field state. Rates of oxidation are so very different under these conditions from those in laboratory samples that much more quantitative information is needed. Much of the field evidence available on oxidation and leaching comes from reclaimed polders where the progress of soil changes has not been closely monitored. Leaching of sulfates has been thoroughly studied in the laboratory, but very little information is available for field conditions. The rates at which sulfides oxidize, the rates at which the resulting sulfates are leached and the degree of acidity that develops on oxidation and leaching are obviously of the greatest importance in the improvement of these soils for agriculture. In the tropics many short-term ad hoc field experiments on the reclamation and improvement of acid sulfate soils have been reported, but few long-term experiments have been described. In dryland crops the large amount of aluminum that appears in the soil sollition when the soils be-

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come very acid is probably the major factor limiting plant growth, so that techniques for limited oxidation by drainage control, and liming for counteracting acidity, need more investigation. In waterlogged conditions the toxic factors are less well defined. Ferrous iron and hydrogen sulfide are both toxic to rice, but methods for identifying the precise soil conditions under which these toxicities arise are not well developed. Finally, it is important to note that the appropriate ameliorative treatments will vary depending on the physical environment; as well as the soils, the climate and the social and economic aspects of the region must be considered. Where population pressure is not serious such soils would best be left out of consideration for agricultural use. In despoiled mining areas, a somewhat different -emphasis is needed. The ability to mine valuable ores without ruining large tracts of country is likely to be emphasized more in future, so that methods of preventing extreme acidity developing, and of reclaiming those areas already despoiled, will be needed. REFERENCES Abd-El-Malek, Y.,and Rizk, S. G. 1963. J. Appl. Bacteriol. 26, 7-13, 14-19, and 20-26. Adams, F., and Lund, Z. F. 1966. Soil Sci. 101, 193-198. Adams, F., and Pearson, R. W. 1967. In “Soil Acidity and Liming” (R. W. Pearson and F. Adams, eds.), Agron. Monogr. No. 12, pp. 161-206. Amer. SOC. Agron., Madison, Wisconsin. Agricultural Research Council. 1967. Agr. Res. Corrnc. Cent. A f r . , Annu. Rep. p. 26. Alexander, M. 1961. “Introduction to Soil Microbiology.” Wiley, New York. Allam, S. W. 1971. Ph.D. Thesis, Louisiana State University, Baton Rouge. Allbrook, R. F. 1973. Proc. I n t . Symp. Acid Sulpliate Soils, 1972 (in press). Allen, E. T., Crenshaw, J. S., and Johnson, J. 1912. Amer. 1. Sci. 33, 169-236. Andriesse, J. P., van Breemen, N., and Blokhuis, W. A. 1973. Proc. Int. Symp. Acid Sulphate Soils, 1972 (in press). Annual Report. 1957. Malaya, Annu. Rep. Dep. Agr., p. 32. Annual Report WARRS 1959. West Afr. Rice Res. Sta., Rokupr. Sierra Leone, Annu. Rep. p. 32. Annual Report. 1962. Wesr Afr. Rice Res. Sra., Rokrrpr. Sierra Leone, Annu. Rep. p. 22. Archer, E. E. 1956. Analyst 81, 181-182. Ashmead, D. 1955. Colliery Guardian 190, 684-698. Baas Becking, L. G. M., and Moore, D. 1961. Econ. Geol. 56, 259-272. Baba, I., and Harada, T. 1954. l a p . 1. Breed. 4, 101-151. Baba, I., Takahashi, Y., and Iwata, I. 1953. Proc. Crop Sci. SOC.Jap. 21, 235-236. Bache, B. W. 1963.1. SoilSci. 14, 113-123. Barnshisel, R. I., and Massey, H. F. 1969. Soil Sci. 108, 367-372. Beck, J. V., and Brown, D. G. 1968.1. Bucteriol. 96, 1433-34.

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MALTING BARLEY IN THE UNITED STATES' G . A . Peterson and A . E. Foster Department of Agronomy. North Dakota State University. Fargo. North Dakota

I. Introduction . . . . . . ........................................ 328 I1. History of Malting B Production in the United States . . I11. The Malting Process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 A . Preparing the Barley . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Steeping . . . . . . . . . . . . . . . . . . . . . . . . ...................... 333 C . Germination ......................................... 333 D . Kilning . . . . ................. .................... 334 E. Handling of Malt . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334 IV . Uses of Malt . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334 V. Classification of Cultivated Barleys of th States . . . . . . . . . . . . 335 A . MANCHURIA-O.A.C. 21-ODERBRUCKER Group . . . . . . . . . . . . . . . . . . 335 B. Two-Rowed Group . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 336 C Coast Group . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 336 D . Tennessee Winter Group . . . . . VI Grading Standards of Malting Barley VII . Requirements of Malting Barley . . . . A Acceptable Varieties of Malting 342 B Kernel Plumpness and Test Weight .......................... C . Skinned and/or Broken Kernels ............................ 342 D . Germination Percentage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343 E . Moisture Percentage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343 F. Sound Barley . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343 G . Other Grains and Foreign Material . . . . . . . . . . . . . . . . . . . . . . . . . . 343 H. Kernel Protein Content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344 I . Soluble Protein .... .. .................... 344 J . Extract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 345 K . Enzymatic Activity . . . . . . . . . . . . . . . . . . 345 VIII . Sources of Variability in Malting Quality Factors . . . . . . . . . . . . . . . . . . 345 IX . Barley and Malt Intercharacter Correlations . . . . . . . . . . . . . . . . . . . 347 X . Genetics and Breeding of Malting Barley . . . . . . . . . . . . . . . . . . . . . 350 350 A . Genetics and Heritability Studies . . . . . . . . . . . . . . . . . . B. History of Acceptable Malting Barley Varieties . . . . . . . . . . . . . . . . 352 C . Malting Barley Breeding Accomplishments . . . . . . . . . . . . . . . . 355 XI . Hybrid Malting Barley . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 358 Procedures Used to Develop Acceptable Malting Barley ................................................ 360 . . . . . . . . . . . . 361 Test . . . . . . . . . . . . . . . . . . . . . . . . . . B . Macro and Micro Malting . .............................. 362

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1 Contribution from the North Dakota Agricultural Experiment Station and Department of Agronomy as Journal Series Article N o . 375 .

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C. Pilot Malting and Brewing .................................. D. Carlot Quality Evaluation . .............................. XIII. Malting Barley Production Prac s ............................ A. Choice of Variety . . . . . . . . . . . . . . . . .................... B. Seed Quality and Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Type of Seedbed and Seedbed Preparation .................... D. Seeding Practices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Fertilizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. Control of Pests . . . . . . .................... G . Harvesting and Threshing . . . . . . . . . . . . . . . . . H. Handling and Storage . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I.

363 3 64 3 64 3 65 3 66 366 368 370 372 373 374 375

Introduction

Malting barley is a specialty crop grown for a raw material used for a specific purpose. The crop is produced for the grain, which must meet a relatively narrow range of performance for several quality characteristics established by the industrial users of malt. The barley is converted to malt by the process known as malting. Malting is a controlled, limited germination process of the barley grain used to activate and synthesize enzyme systems. The conversion of barley to malt also includes other physical and chemical changes. Although barley, wheat, rye, sorghum, corn, and rice are malted throughout the world, only the first three are malted commercially in the United States in substantial quantities (Kneen and Dickson, 1967). Barley is used in much larger amounts than wheat or rye for several reasons (Reid et al., 1968). These three cereals produce two enzymes, a-amylase and p-amylase, when germinated. Hydrolysis of starch to dextrins and fermentable sugars is more efficient with combinations of the two enzymes than either alone. Only barley, of the three grains, has the “hulls” (lemma and palea) adhering to the caryopsis or kernel, and they remain attached after threshing. The hulls prevent damage to the coleoptile during the malting process, resulting in more uniform germination. Also, the hulls aid in filtration of soluble materials from undissolved particles in the processing of malt for brewing, malt syrups, and many other uses. Steeped barley has a somewhat firmer kernel texture than wheat or rye and can be handled with less damage at these high moisture levels. II.

History of Malting Barley Production in the United States

The early history of American barley production was reviewed by Harlan et al. (1925) and Weaver (1950). The first barleys introduced into

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North America were brought to the Atlantic seaboard colonies by the earliest settlers from the Old World. Records show that barley was grown on Martha’s Vineyard and the Elizabeth Islands as early as 1602. These early colonial varieties primarily were produced as a raw material for the production of beer and were cultivated types from the home regions of colonists from England and Continental Europe. The first production of barley along the Atlantic seaboard was not particularly successful since growing conditions were unfavorable. Also, the late-maturing, two-rowed varieties from England, such as CHEVALIER and THORPE, were not well adapted to the area. A more favorable environment for barley was encountered by settlers moving into western New York. The two-rowed variety, HANNA, and the six-rowed varieties of the European continent were better adapted to this area than the two-rowed varieties from England. The combination of a favorable environment and adapted varieties caused New York to emerge as the leading barley-producing state. Nearly two-thirds of the total United States barley production was estimated to have been grown in New York by 1820. New York continued as the dominant barley producing state until‘l849. Barleys of North African origin were introduced into southwestern United States by Spanish settlers. from Mexico in the 1700’s. These varieties of the Coast group were grown near settlement areas as a feed grain. The discovery of gold in California in 1848 caused an increased demand for barley by the brewing industry and resulted in increased acreage. This increased production, used both for feed and malting, moved California ahead of New York as the leading barley-producing state. By 1889, California produced more than one-half of the nation’s total barley. Concurrent with the dominance of California’s barley production was a persistent movement of centers of production westward from New York as agriculture advanced into the Midwest. The demand for malting barley stimulated production around population centers such as Detroit, Cincinnati, St. Louis, and Chicago. During the period from 1889 to 1919, the total United States barley production increased dramatically, from 80,790,000 bushels to 225,067,000 bushels. Important regional redistribution of barley production accompanied the increase, and the North Central States produced nearly 63% of the nation’s barley by 1920. Southeastern Wisconsin, southeastern Minnesota, and western Iowa developed as three very important centers of barley cultivation. In the 1890’s, the malting industry began to build additional facilities in Wisconsin and neighboring states to meet increased consumer demands and to be close to centers of barley production. Areas in eastern Oregon and Washington and northwestern Idaho were growing barleys of the type found in California during this time. Also, northwestern Kansas and central Nebraska developed as barley production areas. The major movement of the total barley acreage

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began to develop arqhe turn of the 20th century. First, an acreage increase occurred in western Minnesota and eastern South Dakota; however, by 1919 the Red River Valley and adjacent areas in North Dakota, Minnesota, and South Dakota had become one of the major regions of barley culture in the nation. The six-rowed varieties of the Manchurian type grown in the heavy producing areas of the North Central States were the primary source of malting barley for the industry. The areas of barley production remained stable during the two decades between World Wars I and 11, partly because new frontiers for agricultural production were no longer abundant. However, the national barley acreage expanded locally, and production increased to 31 1,278,000 bushels in 1940. An advance in barley varietal improvement was a major factor contributing to the increased barley acreage in the United States. During the period, winter barleys of the Tennessee Winter type increased in the South, and both dryland and irrigated production expanded in the intermountain areas of the West. However, production in these two areas was minor compared to the continued dominance of the North Central States. A second westward movement of the major areas of barley production began about 1940. In the North Central States, barley acreage was reduced in Wisconsin, Iowa, and in southern Minnesota and South Dakota while the crop became more firmly established in the agricultural programs of the Red River Valley and adjacent areas. The “acceptable” six-rowed malting varieties were the types generally grown. This northwesterly movement of the barley acreage was caused by several factors, among them, the competition from the expanding use of hybrid seed corn and the new crop, soybeans. Also, damage from diseases reduced barley yields and its competitiveness with other crop alternatives. The susceptibility of both barley and corn to scab (Gibberella spp. and Fusurium spp.) discouraged the inclusion of these two crops in the same rotation, and decreased barley production in the Corn Belt areas. Spot blotch (Helrninthosporiurn sutivum Pam., King, and Bakke) was very destructive in 1943 and 1944 and discouraged the planting of barley in the more humid areas of the North Central States. The continued development of irrigation in the intermountain areas of the western United States provided the opportunity to expand production of suitable two-rowed malting barleys. This second westward movement of the barley production area generally stabilized in the mid1950.’~and has continued until the present time with seasonal variations but only minor acreage shifts. Since 1955, the national annual production of barley has been near or above 400,000,000 bushels. The malting industry in the United States purchases approximately 25 to 30% of this production annually, but the amount depends upon total production and suitability of the crop for malting.

MALTING BARLEY IN THE UNITED STATES

331

The present major areas of supply for the malting industry are North Dakota, South Dakota, and Minnesota in the Upper Midwest, and California, Washington, Oregon, Colorado, Idaho, and Montana in the West. The average production of barley used for malting, shown in Table I, was estimated for the period 1963 to 1967 by Fraase and Anderson (1970). TABLE I Estimated Annual Supply of Malting Barley by State, Average Bushels for the Period 1963-1967" Type Area and state

Six-row

8 8 ,2 3 7 ,1 2 9 North Central total Minnesota 2 0 ,8 0 8 ,6 3 3 North Dakota 63,412,809 South Dakota 2 ,6 7 3 ,9 3 7 Total 86,895,379 Illinois 251,400 Michigan 328,800 Wisconsin 729,150 Iowa 32,400 Total 1 ,3 4 1 ,7 5 0 Western total 8 $ 5 0 5 ,5 9 8 Montana 1 ,1 7 9 ,9 3 6 Idaho 93,370 Wyoming 74,696 Colorado 275,600 Washington 1 ,6 1 6 ,4 7 9 Oregon 499,880 California 4 ,7 6 6 ,0 4 4 Total estimated US. supply 96,742,727 Imports, estimated 3 ,5 0 0 ,0 0 0 Total supply 100,242,727 Total supply of six-row and two-row barley 118,908,656 a

Two-row

14,583,504 4 ,6 8 2 ,8 7 1 728, 286 485,524 2 ,2 0 4 ,8 0 0 3 ,1 5 5 ,2 2 9 2 ,7 4 7 ,1 4 0 579,654 14,583,504 4,082,425 18,665,929

Adapted from Fraase and Anderson (1970).

The estimate includes barley produced in the United States and also that which is imported from Canada and other countries. Although an increase of approximately 10,000,000 bushels of barley over the 1967 estimate, or 128,300,000 bushels (Katz, 1971), are used for malting at the present time, the proportionate production within the various states is similar to the estimate. The principal areas of malting barley production in 1972 are shown in Fig. 1.

332

G. A. PETERSON AND A. E. FOSTER

Ill.

The Malting Process

Malting involves a series of chemical and physical processes which convert the barley grain into malt. Although different techniques are used by various maltsters, there are certain common basic steps. These steps are discussed to illustrate the importance of some of the requirements of barley used in the production of malt. A more extensive review of the malting

FIG. 1. The principal malting barley producing areas in the United States in 1972.

process is available in six chapters of a book, “Barley and Malt” edited by Cook (1962) and from other sources (Kneen and Dickson, 1967; Reid et al., 1968; Witt, 1970). A flow diagram of the steps involved in a malthouse operation is given in Fig. 2. A.

PREPARING

THE

BARLEY

All foreign material must be cleaned from barley to be malted because malt is used in products for human consumption. Thin and broken barley kernels are removed, and the barley is sized by kernel width into two or three assortments to assure uniform steeping and germination. New crop barley usually is stored for at least three months before malting to permit an afterripening process during which obscure chemical and physical changes take place.

333

MALTING BARLEY IN THE UNITED STATES

B. STEEPING The cleaned barley of uniformly sized kernels from individual varieties is placed in steep tanks to raise the kernel moisture level to 42-45%. In addition to supplying water to the barley, steeping also allows removal of any remaining foreign material from the barley. The rate of water absorption and time of steeping are influenced by temperature, type, and variety of barley, and physical characteristics of the kernel, such as size, endoDUST AND CHAFF

DUST, CHAFF

OATS. WHEAT,

CORI(AND WEED SEEDS

CRACKEDEARLEY WEED SEEDS, ETC.

d*/

SEPARATOR

--b

UNDERSIZED KERNELS

t

GRADER

BARLEY

\

DRIED SPROUTS

FIG. 2. Flow diagram of the steps in a malthouse operation. (Reproduced from Fraase and Anderson, 1970).

sperm texture, degree of skinning, and hull adherence. Respiration increases with increased moisture content, and aeration is provided to prevent loss of germinating ability.

C. GERMINATION The steeped barley is transferred to compartments or drums for the germination step of the malting process. Germination proceeds under controlled conditions of moisture, oxygen supply, and temperature. The primary reason for germinating the barley is to produce or activate enzymes which are important for subsequent uses, without a substantial loss of dry matter from respiration and growth. The rate of production and the quantities of the several enzymes developed are influenced by malting conditions

334

0. A. PETERSON AND

A.

E. FOSTER

(Shands et al., 1942; Dickson et al., 1947; Kneen and Dickson, 1967). Germination is allowed to proceed until the coleoptile of a majority of the kernels has grown to about seven-eighths of the full length of the kernel. Germination requires 3-6 days for six-rowed barley and longer periods, up to 10 days, for two-rowed types. The length of the germination period depends upon the variety of barley (Shellenberger and Bailey, 1936; Kneen and Dickson, 1967), the temperature, moisture, and oxygen supply under which the barley is germinated, and the characteristics of the malt desired. Germinating barley kernels which have reached the desirable stage of development but still retain the rootlets and relatively high levels of moisture are called “green” malt. D.

KILNING

The green malt is moved to kilning compartments, or kept in the same compartment in the fleximalt system, for drying and stopping germination. Kilning proceeds through various stages, and kernel moisture content is reduced from about 45% to 3.5-4.0% with initial drying temperatures of about 90°F and final temperatures of 175O-195OF for brewer’s malt. High temperatures cause chemical reactions between sugars and amino acids which produce the aroma and flavor of the kilned malt as well as considerable enzyme destruction. Color of the solubilized products of malt also is enhanced by the use of high temperatures in the kilning schedule. The subsequent use of the malt determines the time schedule, usually ranging from 48 to 72 hours, and temperature used in kilning to obtain a balance among aroma, flavor, color, and enzymes.

E. HANDLING OF MALT Finished malt is cooled, then moved through malt cleaners to remove rootlets, loose hulls, and dust before storage. Sometimes the malt is stored prior to cleaning. The finished malt is stored for several weeks to several months to develop uniform moisture levels among kernels and to allow other desirable changes, which are not well understood, to take place. Separate binning of malt of the several sizes from each of the several types or varieties, areas of production, or specific malting procedures is practiced. Individual lots of malt are blended according to purchaser’s specifications before shipment. IV.

Uses of Malt

About 85% of the malt produced in the United States is utilized by the brewing industry, slightly less than 10% by the distilling industry, and

MALTING BARLEY IN THE UNITED STATES

335

slightly over 5% for food uses (Dickson, 1969). The most important uses of malt and by-products are given in Table 11. The “screenings,” or barley kernels considered too small for malting, and other “cleanout” are sold as feed. V.

Classification of Cultivated Barleys of the United States

A classification of barley based more on physiological characters rather than morphological, given by Wiebe and Reid (1961), has been useful TABLE: I1 TTses of Barley hlalt and Malt By-Productsa Brewer’s malt Beverages-beer, ale, malt extracts Export Brewer’s grains for dairy feeds Brewer’s yeast for animal feed, human food, and fine chemicals IXstiller’s malt Alcohol Distilled spirits and whiskey Export Distiller’s grains )for livestock and poultry feeds Distiller’s soluhles Specialty malts High dried Dextrin for breakfast cereals, sugar colorings, dark beers, and coffee substitutes Caramel Black Malt-enriched food products Malted milk concentrates, malted milk beverages, and infant foods Malt flour for wheat flour supplements and for human and animal food products Malt syrups for medicinal, textile, haking, breakfast cereals, and candies Malt sprouts for dairy feeds, vinegar manufacture, and industrial fermentations

1

a

Reproduced from Reid et al. (1968).

in categorizing malting varieties (Kneen and Dickson, 1967; Reid et al., 1968). A description of each group follows. A.

MANCHURIA-O.A.C. 21-ODERBRUCKER GROUP

The varieties in this group are believed to have originated in Manchuria or neighboring countries and to have been introduced at various times into the United States and Canada through Europe. The first introduction probably was in 1861 (Harlan and Martini, 1936), and distribution to farmers was made by the Wisconsin station in 1873 (Harlan et al., 1925). Intro-

336

G . A. PETERSON AND A. E. FOSTER

ductions from this group, improved selections, and later varieties of hybrid origin have been grown extensively in the major barley-producing areas of the Midwest. Approximately 90% of the malt in the United States is made from the midwestern six-rowed barleys of this group. The varieties LARKER, DICKSON, and CONQUEST account for practically all the present malt production. The varieties comprising this group are spring-type, six-rowed, awned barleys with intermediate kernel size. The plants generally are medium to tall in height, midseason in maturity, and with lax, nodding spikes. The varieties shatter badly when grown in a dry climate. The better samples of these varieties are medium-to-high in kernel protein, vigorous in germination, and produce high enzymatic activities when malted. These barleys are used for both brewer’s and distiller’s malts, the higher protein lots being selected for the latter. Malts for food uses also are made from these varieties.

B. TWO-ROWEDGROUP Varieties of the two-rowed group are of two types: the HANNCHENtype of European origin and the COMPANA-SMYRNA type of Turkish origin. The HANNCHEN-HANNA type was introduced into the United States near the beginning of the 20th century (Harlan and Martini, 1936), but the acreage and number of varieties did not increase markedly until 1950. Introductions such as PIROLINE, BETZES, FIRLBECKS 111, MoRAVIAN, and HANNCHEN, and the two new varieties, VANGUARD and SHABET, are grown in the Northwest and intermountain areas for use in malting. The COMPANA-SMYRNA type is used for feed. The varieties of the HANNCHEN-HANNA type used for malting are tworowed, awned, spring-type, intermediate in height, and midseason to midlate in maturity. Desirable samples of these varieties have large kernels, thin hulls, and relatively low protein content. They germinate vigorously and produce malts intermediate in enzymatic activity and high in extractable materials, primarily starch. Malts from two-rowed types are blended with malts from midwestern six-rowed types for brewing, mainly to increase extract yield. HANNA

C. COASTGROUP The first varieties of the Coast group were introduced from arid sections of North Africa into southwestern United States and California. Prior to World War I1 large quantities of this western six-rowed type, grown in California, were exported to England for malting. At present, relatively small amounts of this type grown in the central valleys of California are malted and used in blends with midwestern-type six-rowed varieties for brewing. The Coast or Bay Brewing varieties were grown earlier, but have

337

MALTING BARLEY IN THE UNITED STATES

been replaced by small acreages of ATLAS and its backcross derivatives and WINTER TENNESSEE. The Coast varieties are characterized as spring types but usually are fall- or winter-sown in mild climates, early maturing, midtall to short in height, and resistant to shattering of grain from the spike. Varieties usually TABLE 111 Typical Analyses of Malts from Three Types of Barley"

Property Kernel weight (mg, dry basis) Growth of malt 0 t o !/a (%I !i t o !i (%) 36 to 94 (%I t o 1 (%I Overgrown Kernel size assortment On 764 screen (%) On 964 screen (%) On 964 screen (%) Through 5.64 screen (%) Moisture (%) Extract (dry basis) : Fine grind (%) Coarse grind (%) Difference (%)

Midwestern 6-Rowed

Western %-Rowed

California &Rowed

32.0

37 . 0

41.0

2.0 3.0 9.0 83.0 3.0

2.0 4.0 10.0 83.0 1.0

3.0 4.0 17.0 76.0 0.0

25.0 56.0 17.0 2.0 4.5

85.0 10.0 1. 0 0.0 4.5

79.0 24.0 4.0 0.0 4.7

76.5 74.5 2.0

80.5 79.0 -

77.0 74.8

1.5 __

9.2 __

1.5

1.0

1.3

12.0 38.0 195.0 40.0

10.0 38.0 90 . 0 25.0

11 . o 33.0 60.0 30.0

N

Color, laboratory wort ("IA)* Protein (dry basis) Total (%) Soluble (%) of total Diastatic power (degrees)c a-Amylase (90' units)d

~

__

Reproduced from Reid et al. (1968). Degrees Lovibond, a unit of wort color. c Degrees, a unit of amylase activity. d 2O0C dextrinizing units, a unit of a-amylase activity.

a

b

have large, bright kernels, thick hulls, medium protein content, rather slow physical and chemical modification, and low enzymatic activities after malting. Typical analyses of malts prepared from the Coast group (California six-rowed), the MANCHURIA-O.A.C. 214DERBRUCKER group (Midwestern six-rowed), and the two-rowed group (Western two-rowed), as given by Dickson (Reid el al., 1968), are shown in Table 111.

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G. A. PETERSON AND A. E. FOSTER

D. TENNESSEE WINTERGROUP The winter barleys were of little importance in the United States prior to 1920. Increases in acreage have occurred and now 20-30% of the total barley acreage of the United States (Reid et al., 1968) is planted to winter barley. The principal region of winter barley production lies south and east of a curved line running from New York City through Kansas City and western Texas. Other areas of production outside this region are located around the eastern Great Lakes, in the Pacific Northwest, in some intermountain areas of western United States, and as far north as South Dakota in the Great Plains. Very little winter barley is malted. Factors causing unsuitability for malting are : unacceptable barley varieties, too high kernel protein content, and severe kernel discoloration from excessive moisture at harvest. Varieties such as WHITE WINTER grown in northwestern United States, and HUDSON,grown in the East, are used for malting to a minor extent. VI.

Grading Standards of Malting Barley

Official grain standards of the United States are established for barley moving in commerce and passing through inspection points or made available to grain inspection laboratories. The Grain Division, Consumer and Marketing Service, United States Department of Agriculture is the agency responsible for developing and providing information on these standards. Commercial grain grading agencies, supervised and licensed by the USDA, grade grain and furnish the information to “interested parties” such as grain handlers, shippers, and buyers, and grain exchanges. Barley is divided into three market classes: Barley, Western Barley, and Mixed Barley. The class Barley is further subdivided into three subclasses: Malting Barley, Blue Malting Barley, and Barley. Numerical grades from U.S. No. 1 to 5 and Sample grade are assigned to barley lots within each market class or subclass, except numerical grades 1-3 for the Malting Barley subclass. Special grades may be added to the grade designation to indicate certain characteristics of the grain which are of interest to barley buyers, such as “Tough” for moisture contents slightly above desired storage levels or “Blighted” for grain with more than 4% blighted kernels. “Barley” offered for sale on the commercial market is described, if officially graded by a licensed inspector, in terms of several physical characteristics, as shown in Table IV. Some of these characteristics are useful to those who require the barley for malting purposes. Meeting the standards for the subclass “Malting Barley” does not, in itself, indicate whether suitable malt can be made from the barley. The description of certain physical

TABLE I V Grades and Grade Requirements for the Subclasses Malting Barley and Blue Malting Barley of the Class Barley‘ Minimum limits of

Grade

U S . No. 1 U.S. No. 2 U.S. No. 3

Test weight per bushel (pounds)

Sound barley (%)

47.0 45.0 43 0

97.0 94.0 90 0

Maximum limits of

Damaged kernels

Foreign material

Skinned and broken kernels

Thin barley

(%I

(%I

(%I

(%I

2.0 3.0 4.0

1.o 2.0 3 0

4.0

7 0 10.0 15.0

6.0 8.0

Black barley Other grains (%I (%) 0.5 1 .o 0.0

2.0 3.0 5.0

a Reproduced from “Official Grain Standards of the United States” published by USDA, Consumer and Marketing Service, Grain Division, as revised, February, 1970.

W W

\o

340

G. A. PETERSON AND A. E. FOSTER

characteristics, however, does provide a basis for judging the desirability of the raw material used for malting. The barley used by the malting industry is mainly midwestern-grown six-rowed barley with white or blue aleurone. Grade and grade requirements for these types of barley are given in Table IV. The subclass Malting Barley shall be six-rowed barley of the class Barley which has 90% or more of the kernels with white aleurone; which is not semisteely in mass; and which, after the removal of dockage, contains not more than 5 % tworowed and/or other varieties of barley unsuitable for malting. The Blue Malting Barley subclass has the same requirements as the subclass Malting Barley except that the kernels must have a blue aleurone. Two-rowed barley used for malting may be of the market class Western Barley or Barley. The special grade, Choice Malting Two-Rowed, can be assigned to tworowed barley of the class Barley meeting special requirements, or tworowed barley meeting the requirements for grade U.S. No. 1 of the class Western Barley and other special requirements. The special grade, Malting Two-Rowed, can be given to two-rowed types of the class Barley or Western Barley which meet requirements of the grades U.S. No. 1 to U.S. No. 3 of the class Western Barley and other special requirements. Certain varietal and other physical standards also must be met to obtain these two special grades for two-rowed barley.

VII.

Requirements of Malting Barley

The agronomic and disease resistance requirements of a malting barley can be defined quite precisely, and varieties for production can be chosen on the basis of their performance under certain conditions. Although many of the characteristics of malting quality can be measured with as much precision as agronomic and disease evaluations, the definition of malting quality is difficult. No universal description of requirements for the quality factors of malting barley can be applied. The requirements differ with the processes employed by the maltsters and ultimate users of malt, by the type of products to be made from the malt, and somewhat by traditional concepts of standard malt characteristics. The requirements often can be expressed in terms of characteristics expected in an acceptable malting barley variety widely grown in a malting barley producing area. Now in the United States, malt specifications established by industry would correspond to characteristics within good quality grain of the variety LARKER for the white aleurone, six-rowed type; CONQUEST barley for the blue aleurone, sixrowed type; and HANNCHEN or BETZES for the two-rowed barleys. In the development of a new malting variety, a change in malting characteristics

MALTING BARLEY I N THE UNITED STATES

34 1

may represent an improvement in the malting quality of the barley. However, these changes are accepted rather reluctantly, if at all, by industry because modification of their operation may result in a slightly different end product or affect the economics of production. Thus, specifications for malt often include the amounts of the barley varieties desired as the raw material, along with standards for other properties. Certain factors are used to evaluate malting quality. Some of these factors can be determined ,from the barley grain while others are evaluated on the malt. Anderson et al. (1943) gave an excellent discussion of malting quality characteristics for Canadian barleys. A report from the Brewing and Malting Barley Research Institute, Winnipeg, Manitoba, in 1967, defined the standards for many of the malting quality properties. Specific standards for malting quality factors desired by the United States industry have not been published, but the general requirements have been discussed by Dickson and Burkhart (1956), Sfat (1963), Olson (1963), Rosenbusch (1966), Hunt ( 1968), and Seidl ( 1972). Various committees involving industry, state, and federal personnel have attempted to establish desirable ranges for the measured quality factors. Eflbrts coordinated by the Malting Barley Improvement Association, Milwaukee, Wisconsin, are continuing toward this objective. Grain buyers at the local market and malting barley merchandisers at the terminal grain markets use characteristics of the barley grain to determine price and quality premiums. Barley variety, protein content, kernel plumpness, and kernel discoloration are the major factors involved. Other values established through assignment of the official grade of barley provide supplemental information for the malting barley merchandisers and the maltsters purchasing barley. General requirements of desirable malting barley as defined by industry representatives will be discussed. Major emphasis will be devoted to standards for midwestern grown six-rowed barley used for brewer's malt because this represents over three-fourths of the total malt production in the United States. A.

ACCEPTABLE VARIETIES

OF

MALTINGBARLEY

A list of acceptable malting barley varieties is established as a result of collaborative quality testing programs of Agricultural Experiment Stations from malting barley-producing states with industry, represented by the Malting Barley Improvement Associaton, Milwaukee, Wisconsin. Varieties show distinct differences in the way they react during malting and brewing and acceptable varieties can be processed more efficiently. Carload lots of a single variety are desired by industry, which provides a raw mate-

342

0. A. PETERSON AND A. E. FOSTER

rial of known genetic performance within a range of environmental variability. Processing a known variety by the maltster is less difficult than processing a mixture and allows blending of different finished malts to meet specifications of malt users. B.

KERNELPLUMPNESS AND TESTWEIGHT

Kernel size of malting barley is defined by two different agencies. Country elevators and malting barley buyers in areas of production or major terminal markets near production areas define “percent plump” barley as those barley kernels staying on top of a sieve having slotted perforations of 8/04 inch by 5/4 inch. Official grain standards of the Consumer and Marketing Service, Grain Division, USDA, define “percent thin” barley in the class Barley as “barley and other matter that will pass readily through a 744 )( 5/4 (inch, slotted perforations) sieve” and “percent thin” in the class Western Barley shall be “barley and other matter that will pass readily through a 51/,/64 X % (inch, slotted perforations) sieve.” “Thin barley” is determined after the removal of dockage in official grading by the Licensed Inspector. Probably “plump barley” also is determined after the removal of dockage in the country elevator or before the malting barley buyer applies a plump percentage in the central or terminal market. Thin barley and other matter that passes through a %j4 X % inch sieve is not used for brewers malt and represents an economic loss. Uniformity in kernel size, obtained through use of seives, and in kernel shape through handling of single variety lots, is important for uniform steeping, germination, and grinding in the malt mill. Test weight is used to determine the suitability of barley for malting as an approximate indicator of malt extract potential. Although test weight has some merit as a measure of extract potential, it is less accurate than kernel plumpness. Test weight can be influenced greatly by closeness of threshing with higher values obtained by skinning or hull removal. C.

SKINNEDAND/OR BROKENKERNELS

Skinned kernels are those in which one-third of the lemma or palea is removed, or which have the lemma loosened or removed over the embryo. A broken kernel of barley is one that is broken regardless of the extent or size of the pieces. The official grain standards of the United States allow a maximum of 8% skinned and/or broken kernels within the subclasses for six-rowed malting barley and 10% within the special grades of tworowed malting barley. A lower level of skinned kernels is preferred since the hull (lemma and palea) helps regulate water and oxygen absorption

MALTING BARLEY I N THE UNITED STATES

343

and prevents mechanical injury of the coleoptile during the malting process. Greater uniformity of germination among the kernels and a more complete modification of the barley to malt is experienced with nonskinned kernels. Also, the brewer uses the hull as a filter aid in the brewing process so that a low hull percentage may give an undesirable separation of the solubilized wort. Broken kernels which cannot be removed in the cleaning process will reduce the quality of the malt because they will seldom germinate.

D. GERMINATION PERCENTAGE Germination is basic to the malting process. The germination percentage should be above 95% to assure that the proper chemical and physical changes occur to produce high quality malt. The vigor and uniformity of germination among the barley kernels is important in the rate and the degree to which the changes take place. The percentage and vigor of germination are influenced by the many factors that determine soundness of the kernel and by post-harvest dormancy.

E. MOISTUREPERCENTAGE Since barley usually is stored for at least 3 months prior to malting, kernel moisture content should be 13% or less. Storage above 13% moisture may result in damage due to the growth of microorganisms on or within the kernel, or from an increase in temperature within the grain. These factors may cause loss of viability and of germination vigor, or cause undesirable chemical changes within the kernel to render the barley unsuitable for malting.

F. SOUND BARLEY Sound barley refers to whole kernels and pieces of kernels of barley which are not classified as “damaged.” There are many factors that influence soundness, such as disease, heat, sprouting, frost, ground damage, and weathering. The standards of the maltster for soundness are higher than those listed for malting barley in the official grain standards of the United States. Low tolerances are set by maltsters because most of the damaging factors reduce germination or cause chemical changes in the kernel which affect flavor, or color, or cause processing difficulties in products made from malt. G.

MATERIAL OTHER GRAINSAND FOREIGN

The use of barley which is not contaminated with other agricultural crop seeds, with weed seeds, or with foreign material of any type is the goal

344

0. A. PETERSON AND A. E. FOSTER

of the maltster. Economic loss as a result of dockage removal or a reduction in the quality of the malt may occur if contaminants cannot be separated from the barley. H.

KERNELPROTEINCONTENT

Protein content of malting barley is one of the most important considerations because of the effect protein has on the malting and brewing processes as well as on the resultant end products of these processes (Olson, 1963). High kernel protein tends to lengthen the steeping time and causes uneven germination in the malthouse. Blends of high and low protein barley increase the problem of uneven germination. High protein barley increases malting losses from higher respiration and rootlet losses. Also, high protein may cause a flinty appearance within the endosperm and as a result, mellowness of the malt is reduced. Protein is necessary for the development of many of the key analytical properties of malt. Excessive levels of kernel protein in barley decrease the amount of soluble material that can be extracted from both fine or coarsely ground malt and ultimately decreases the percent of extractable material. Enzymatic activity, as measured by diastatic power and u-amylase in the malt, and soluble protein in wort obtained from the filtered extract of malt, increase with the use of high-protein malting barley. These increases may cause undesirable changes in the processing and end products of malt. The malting and brewing industry has defined protein specifications for barley that meet the standards desired in their raw material, barley. Acceptable upper protein limits for barley on a percent dry basis are 13.5% for the Midwestern six-rowed type, 13.0% for the Western two-rowed type, and 11.O% for the Western six-rowed type, which includes the Coast and Winter Tennessee groups. However, preferred levels for these three types are 12.5%, 12.0%, and 9.0%, respectively. Protein levels of barley that is grown in the United States are rarely too low (Olson, 1963).

I. SOLUBLEPROTEIN Soluble protein is that portion of the nitrogenous compounds in malt which is solubilized in the mashing process. Although determination of soluble protein is made after malting, the amount of barley protein and proteolytic activity potential is basic to this factor. Fermentation efficiency, related to yeast metabolism, and amount of soluble protein. in the finished product of brewing are important factors dependent on the soluble protein in the wort. Individual brewers specify ranges for soluble protein, but standards for the industry as a whole have not been established.

MALTING BARLEY IN THE UNITED STATES

J.

345

EXTRACT

The amount of extractable material in barley or malt can be measured. The requirements for extract have no upper limit since this factor is associated with brewhouse yield. Among the acceptable varieties, the tworowed varieties tend to have higher extract levels than six-rowed types. The difference between extracts obtained from finely and coarsely ground malts is used as an indication of the efficiency with which extractable solids can be recovered in the brewing process and is a measure of the degree of modification. A barley which can produce a well-modified malt would have a low fine-coarse extract difference. The fine grind extract measures the yield potential, but the coarse grind extract relates to the yields obtained in actual brewhouse practice.

K.

ENZYMATIC ACTIVITY

One of the main reasons why barley is used more extensively than other grains for malting is the presence of or ability to develop acceptable levels of the proper enzymes. The amylases or starch-splitting enzymes are of major importance since they must act on the starch of the barley endosperm as well as on the adjunct of other grains added in the mashing process during brewing. Diastatic power, determined on barley or malt, and a-amylase determined on malt, are measures of the activity of these amylolytic enzymes. Industry-wide standards have not been established for diastatic power and a-amylase, but individual companies have specified requirements. Normally, the acceptable enzymatic activity ranges are within those that can be provided by the widely grown acceptable malting varieties. Specifications for the proteolytic enzymes are not given for barley or malt but are reflected in the soluble protein or percentage of soluble protein relative to total protein values. Other enzyme systems are known to be important in malting barley, but requirements have not been established for conventional commercial malting. As they become better understood with further research, additional enzyme specifications may be added by the users of malt. One of these may be p-glucanase because of its importance in modification of the kernel during malting.

VIII.

Sources of Variability in Malting Quality Factors

The sources of variation associated with chemically determined malting quality factors have not been studied as extensively and are less understood than agronomic characteristics and most of the physical quality factors of

346

G . A. PETERSON AND A. E. FOSTER

malting barley. However, studies on varieties (Shellenberger and Bailey, 1936; Anderson et al., 1943; Harris and Banasik, 1952) and experience by industry (Kneen and Dickson, 1967) have established that both genotype and environment influence the chemical composition of the barley kernel. The range of values for quality characteristics, such as percentage of barley or malt protein, extract percentage, and diastatic power of a malting barley variety over environments, usually would be expected to be greater than for several malting barley varieties grown under one environment. As an example, Anderson (1944) indicated that protein content of varieties grown under identical conditions rarely differs by more than 1.5 percentage units, but the protein content of the same variety grown under widely different conditions may vary by as much as 10 percentage units. The influence of environment on malting quality of barley has been categorized as the effects of location and season (Harris and Banasik, 1952; Rasmusson and Glass, 1967). The environmental factors that cause the greatest amount of variability in malting quality is not consistent among all studies. Undoubtedly, soil moisture levels, temperatures during the growing period, and availability of essential nutrients for plant growth are three of the most important constituents in determining the physical and chemical properties of malting barley. A relatively universal generalization exists, that any limitation or deficiency among these constituents which stress the barley plant growth normally renders the resulting barley grain less suitable to meet desirable malting barley standards. This deficiency or limitation may cause a lowering of the level of one or more quality factors or a disruption of the balance of factors essential in the raw material for malt. Studies on the effects of environment on malting quality factors show that kernel protein content is among the factors affected to the greatest extent and that diastatic enzymatic level is among those factors affected least. Because of the seasonal effect on physical and chemical properties of malting barley, the commercial malting industry periodically adjusts its raw material procurement standards in order to obtain the best material available. This adjustment, of course, causes some changes in malt user specifications and commercial plant operations in order to produce their desired end products. As expected for any biological entity, the genotype x environment component of variability contributes to levels of performance of barley quality. References listed previously in this section indicate the significance of many first-, second-, and third-order interactions, and genotypes usually are involved in these interactions. Although agreements are noted among certain interactions, discrepancies can be expected because varieties of different maturities and physiological types are involved, and because of very

MALTING BARLEY IN THE UNITED STATES

347

diverse growing conditions. Several heritability studies involving hybrid populations which elucidate the importance of variables affecting malting quality factors have been reported and will be discussed in the section relating to breeding malting barleys. IX.

Barley and Malt lntercharacter Correlations

Numerous studies have reported the correlations existing among physical and chemical properties of barley and malt in attempts to predict intercharacter relationships. Intravarietal correlations, association of characters within a variety, are interesting to the users of malt because they supply a certain degree of confidence in the expected performance of some of the malting characteristics of a particular barley variety. Also, the barley breeder uses intravarietal data to select parents for crosses. Intervarietal correlations and relationships obtained on segregating barley populations are of greatest interest to barley breeders in their efforts to combine desirable traits into individual genotypes. A sample of values and ranges of simple correlation coefficients obtained using determinations made on only barley grain characteristics, barley grain and malt properties, or only malt determinations, are given in three separate columns of Table V. Only statistically significant correlation coefficients are reported from the 15 studies which involve a diversity of barley genetic material and environmental conditions (Anderson et al., 1941; Meredith et al., 1942; Meredith, 1943; Anderson, 1944; Lejeune, 1946; Den Hartog, 1950; Harris and Banasik, 1952, 1953; Hsi and Lambert, 1954; Peterson, 1956; Banasik and Harris, 1957; Rasmusson and Glass, 1965; Streeter and Pfeifer, 1966; Foster el al., 1967; Rutger et al., 1967). The data are not intended to typify exact intercharacter associations that may be found in any specific barley variety, but certain consistent relationships indicate that some generalizations can be made regarding barley varieties grown under a wide range of conditions. The usual expec-, tation that large physical kernel measurements will result in low kernd protein or nitrogen levels is not substantiated by several of the correlation coefficients. The independence of kernel size and protein content is important to those procuring barley for malting since levels of both characteristics need evaluation to meet required standards. In general, maltsters can relate larger kernel size with higher extracts and lower protein contents within an individual barley variety. The r values in Table V and other studies involving partial correlation coefficients indicate malting quality improvements are possible through breeding, but more basic information on chemical relationships on barley and malt is required to accelerate progress.

TABLE V Simple Correlation Coefficients among Barley Grain or Malt Characteristics Important to Malting Barley as Compiled from Fifteen Different Studies

W

P,

Determinations (r value or range) made on Characters correlated Grain yield vs plump kernels Grain yield vs protein or nitrogen Grain yield vs diastatic power Grain yield vs extract % Plump kernels vs protein or nitrogen % Plump kernels vs diastatic power % Plump kernels vs extract % Plump kernels vs fine-coarse extract difference % Thin kernels vs kernel weight % Thin kernels vs test weight % Thin kernels vs protein or nitrogen % Thin kernels vs diastatic power % Thin kernels vs extract % Thin kernels vs fine-coarse extract difference Kernel weight vs test weight Kernel weight vs protein or nitrogen Kernel weight vs diastatic power Kernel weight vs extract Test weight vs extract Test weight vs soluble/total nitrogen Test weight vs protein or nitrogen Protein or nitrogen vs diastatic power Protein or nitrogen vs extract Protein or nitrogen vs a-amylase

Barley 0.29 -0.20 to -0.25 to 0.4% to 0.25 to -0.75 0.54 to

-0.48 -0.28 0.65 0.40 0.55

-0.71 to -0.86 -0.49 to -0.70 -0.41 0.70 to -0.53 -0.58 0.29 -0.47 -0.47 0.51 0.45

to to to to to

0.71 0.27 -0.55 0.71 0.58

0.28 to 0.97 -0.28 to -0.90

Barley and malt

Malt

0 ?

-0.55 -0.28

cd

m 4 m

-0.55 to -0.49 -0.58 0.52 to 0.54 -0.56

F!

0

z a-

s ? P

0.42 to 0.44 0.65 -0.50 to 0.55 0.45

;3 a 0.60 0.69 0.25 0.50 0.41 -0.50 0.41

to 0.99 to 0.96 to -0.96 to 0.65

0.44 to 0.74 -0.30 to -0.90 0.50 to 0.60

Protein or nitrogen vs soluble protein or nitrogen Protein or nitrogen vs soluble/total protein or nitrogen Protein or nitrogen vs proteolytic activity Protein or nitrogen vs malting loss Protein or nitrogen vs malt recovery Diastatic power vs diastatic power Diastatic power vs extract Diastatic power vs a-amylase Diastatic power vs soluble protein or nitrogen Diastatic power vs fine/coarse extract difference Extract vs extract Extract vs a-amylase Extract vs soluble protein or nitrogen Extract vs soluble/total protein or nitrogen a-Amylase vs soluble protein or nitrogen a-Amylase vs soluble/total protein or nitrogen Soluble protein or nitrogen vs soluble/total protein or nitrogen Soluble protein or nitrogen vs fine-coarse extract difference Soluble/total protein or nitrogen vs fine-coarse extract difference

0.65 t o 0.76 -0.64 0.85 0.69

0.53 to 0.66 -0.55 to - 0 . 6 2

-0.95 0 . 7 9 t o Oi91 -0.27 to -0.86

-0.87

-0.54 t o - 0 . 7 9 0.34 to 0 . 5 5 0 . 5 0 to'O .64 -0.54

0 . 8 9 to 0.97

0.68

Fr

=! z

0

0.41 t o -0.53 -0.43 to -0.48 0.46to0.57 0 . 5 3 to 0 . 5 5 0.65 0.80

-0.36 -0.59

m r

.e

z

4

E

m m

w P W

350

0. A. PETERSON AND A. E. FOSTER

X.

Genetics and Breeding of Malting Barley

Wiebe (Reid et al., 1968) has indicated that cultivated barley ranks among the top half-dozen plant species in the amount of genetic information available. Genetic analyses have established the number of genes and linkage relationships for many of the morphological and disease characteristics of barley. Although the physiological and biochemical characters that relate to malting quality are heritable, the exact mode of inheritance is unknown. The inheritance of many of these malting quality characteristics is complex, and their expression is influenced by the environment in which the barley plant is grown. Although the plant breeder does not have a complete understanding of the inheritance of the malting quality characteristics, improvement of the characteristics through breeding has been possible. However, this lack of knowledge has slowed improvement of the malting quality characteristics compared with several of the qualitatively inherited agronomic and disease characteristics. Breeding for malting quality has been aided by correlation studies which contribute to the knowledge of what can be expected in hybrid progeny, and by heritability studies which aid in the understanding of the reliability of selection. Acceptable malting varieties have been developed by bringing favorable levels of malting quality characteristics into a single variety. Once these favorable associations are established within a variety, they assist the barley breeder by serving as genotypes which can be used as parents in effecting further improvements. Genetic linkages can be a deterent to breeding improvements when the breeder attempts to introduce a desirable gene or genes which are associated with unfavorable agronomic, disease, or malting quality characteristics. Undesirable genetic linkages often occur when exotic germplasm is used as parents in a breeding program. Bell and Lupton (1962) have aptly described the breeding of malting barley varieties and the associated problems. One factor emphasized is that quality standards are not universal. The barley breeder’s efforts must be to develop varieties which contain suitable levels of agronomic and disease characteristics for given environments and the proper combination of malting quality traits. These quality traits may vary with the type of barley, area of production, and maltster and brewer requirements. A.

GENETICSAND HERITABILITY STUDIES

The literature on the inheritance of many of the agronomic and disease characteristics desired in a malting barley variety is extensive. Smith

MALTING BARLEY IN THE UNITED STATES

35 1

(1951) and Nilan (1964) have made excellent reviews of these studies. The complexity of inheritance of agronomic characteristics ranges widely from traits such as maturity and plant height, where individual F, plant selection is effective, to grain yield, which requires extensive progeny testing in replicated trials. Most of the disease characteristics are relatively simply inherited and can be manipulated in a breeding program if either natural or artificial epiphytotics are available to obtain a selection differeential. A common experience encountered, however, is that the desired disease resistance often is available only in exotic, unadapted material containing undesired genes. Several crosses with adapted malting barley varieties or the growing of extremely large populations of single crosses often are required to break the linkages between the disease resistance gene or genes and the undesired genes. The genetics of malting quality characteristics are less understood than most of the agronomic and disease characteristics handled by the barley breeder. The unavailability of adequate testing procedures to most breeders and the complexity of inheritance of quality characteristics have been contributing factors to the lack of understanding. The recognition of the relationship of kernel protein levels to malting quality caused the initation of some of the first genetic studies of quality to be made on kernel protein. Recent genetic studies have been concerned with enzymatic activity and other quality characteristics. Reviews of these inheritance studies along with application of the results to development of improvement of malting quality have been made by Smith (1951 ), Nilan (1964), Bell and Lupton (1962), and Meredith et al. (1962). The development of “prediction tests” which involve chemical analyses of the barley grain for percent protein, potential diastatic power, and percent extract has provided the barley breeder with a means for predicting malting quality of lines in early generations. The prediction test frequently is supplemented by kernel plumpness evaluations. Sisler and Banasik (195 1 ) found that selection in the F, generation of a barley cross for kernel weight, percent nitrogen, diastatic power, and percent extract increased the proportion of lines with acceptable quality. The effectiveness of selection for the individual characters was not presented. Bendelow and Meredith (1955) showed the prediction test was 79 % effective in selecting lines which were favorable for quality, based on later malting quality tests. They indicated that in some instances desirable lines would be discarded, but knowledge of the parentage would be helpful in the selection of lines. Some of the most useful information that can be used by the plant breeder in selecting for malting quality characteristics is provided by recent studies on estimates of heritabilities and genetic variances (Day et al., 1955; Rasmusson and Glass, 1965, 1967; Rutger et al., 1966; Foster et al.,

352

0. A. PETERSON AND A. E. FOSTER

1967; Baker et ul., 1968). With the exception of results by Rutger et al. (1966), these studies are based on tests on the barley grain rather than on malt. Although heritability estimates from the various studies cannot be compared directly because of different methods of computation, genetic variance of populations, and different generations involved, a general evaluation of the effectiveness of selection in hybrid populations can be made for the various malting quality characteristics. Quality measurements made on an individual F, plant basis appear unsatisfactory. Selection for potential diastatic power, which is primarily a measure of p-amylase in these studies, is effective using grain from a single F, plot. Results from single plot data in the F, generation indicate that selection would be advantageous for barley extract, kernel plumpness, and kernel weight. Of course, delay of selection to the F, or F, generation would improve chances of retaining desirable hybrid lines. Heritability estimates for barley protein or nitrogen have been quite variable. Variable estimates are expected because of the large influence of the environment on this characteristic. However, selection in the F, generation for barley protein or nitrogen appears to have merit if genetic variances are adequate. The use of more than one replication, location, or year improves the selection advantage, but the extra expense and time involved does not appear to override the use of Fa selection for barley protein or nitrogen. Rutger et al. (1966) evaluated several physical and chemical quality properties on both barley and malt in the F, generation and found heritability estimates exceeding 0.67 for all characteristics except barley nitrogen and wort nitrogen. Although heritability values may be satisfactory for the measurable quality characteristics, the barley breeder must combine desirable levels of the several traits into a single genotype which meets the standards of the user of malt. These levels must be maintained under fluctuations in the environment that occur in the area of production. Another problem of great concern to the barley breeder is the inability to select for some quality characteristics of importance to the brewer, because techniques to evaluate these characteristics are not available to test hybrid progenies in a breeding program. Flavor and filtration in the brewhouse are examples of such characteristics.

B. HISTORY OF ACCEPTABLE MALTINGBARLEYVARIETIES The classification of a barley variety as acceptable for malting and brewing involves much testing. The types of quality evaluations to which a barley line is subjected before achieving quality acceptance will be discussed in a later section. Collaboration between agricultural experiment stations

MALTING BARLEY IN THE UNITED STATES

353

and the malting and brewing industry is involved in the classification of a variety as acceptable for malting. Several industrially sponsored organizations dating back to the 1930’s have been concerned with the testing and classification of malting barley varieties (P. E. Pawlisch, personal communication). Initially, the United States Maltsters Association and the Barley Improvement Council coordinated the industry effort to improve malting barley and assisted in the establishment of the USDA National Barley and Malt Laboratory. The Malt Research Institute was established in 1939, and one of its functions was to evaluate varieties and submit their approval of those acceptable for malting. The Midwest Barley Improvement Association was organized in 1945 and renamed the Malting Barley Improvement Association in 1954. The Malt Research Institute merged with the Malting Barley Improvement Association in 1959 and since then the Malting Barley Improvement Association has been the sole organization sponsored by industry for the evaluation and approval of malting barley varieties. Members of this organization consist of commercial maltsters, malting brewers, the United States Brewer’s Association and Master Brewers Association of America. In addition to the aforementioned functions, they have been involved in several other pursuits with malting barley including financial support to malting barley breeding programs at several state agricultural experiment stations. A compIete list of varieties that have been approved as acceptable malting and brewing types in the United States is given in Table VI. Under present-day standards, most of the older varieties on the list no longer are acceptable. All the varieties have the spring growth habit. Several other spring and winter types not on the list have been or are being used by industry, but they occupy a relatively minor part of the total market. Examples of some of these varieties are six-rowed varieties such as ATLAS and WINTER TENNESSEE and the two-rowed types, MORAVIAN and CARLSBURG 11. Although some of the acceptable malting varieties are more widely adapted than others, all the varieties generally produce favorable quality barley only when grown in those environments for which they were specifically selected. Malting barley varieties available to producers have been the result of direct introductions from foreign countries, of selections by breeders or farmers from introductions with mixtures of barley types, or of hybridization followed by one of several breeding methods. The older barley varieeties used by the malting and brewing industry primarily were introductions or selections from introductions. Suitable quality in these types usually was a matter of chance. More recently, varietal release has resulted from plan-

T A B U VI Barley Varieties Classified as Acceptable Malting and Brewing Types in the United States

Variety

Year introduced or released to producers

HANNCHEN O.A.C. 91 ODESSA ODERBRUCKER MANCHURIA 38 WISCONSIN KINDRED BAY MONTCALM MOORE HANNA

1908 1910 1914 1917 1990 1999 1949 1945 1945 1948

PARKLAND TIUILL

1956 1956 1957 1961 1961 1964 1965 1965 1966 1971 1971 1973 1973

BETZES LARKEH

TROPHY DICKSON CONQUEST

PIROLINE FIRLBECKS I11 SEABET VANGUARD BEACON KLAGEB

?

Source USDA Ontario Agricultural College South Dakota Wisconsin North Dakota Wisconsin North Dakota Michigan Macdonald College Wisconsin California Brandon, Manitoba North Dakota Montana North Dakota North Dakota North Dakota Brandon, Manitoba Idaho, Washington California, Oregon Montana Washington North Dakota Idaho, USDA

CI No. 531 1470 182 4666 2947 5105 6969 7113 7149 7951

8106 10001 9438 6998 10648 10647 10968 11638 9558 10088 13847 11868 15480 15478

Row No.

e 6 6 6 6 6 6 6 6 6 9 6 6

a 6 6 6 6

a a e e 6

a

Aleurone color Colorless Blue Blue or colorless Colorless Blue Colorless Colorless Colorless Blue Colorless Colorless Blue Colorless Colorless Colorless Colorless Colorless Blue Colorless Colorless Colorless Colorless Colorless Colorless

w

v, P

Origin Introduction Selection from introduction Introduction Selection from introduction Selection from introduction Hybrid selection Farmer selection Hybrid selection Hybrid selection Hybrid selection Selection from introduction Hybrid selection Hybrid selection Introduction Hybrid selection Hybrid selection Hybrid selection Hybrid selection Introduction Introduction Hybrid selection Hybrid selection Hybrid selection Hybrid selection

F ? cd

B

1 B gd

8Z ? B

MALTING BARLEY IN THE UNITED STATES

355

ned crosses with specific quality objectives in mind. The breeding of malting barley varieties in the United States is relatively new. A concentrated effort has been devoted to this objective only within the last three decades. The history of malting barley breeding involving the six-rowed types of barley is slightly older than for the two-rowed barleys. TRAILLwas the first six-rowed barley released to producers in the United States in which a primary breeding objective involved acceptability as a malting variety. TRAILL maintained the quality performance of KINDRED, a farmer’s selection which fortunately contained the quality characteristics desired by the maltsters and brewers. KINDRED raised the level of performance for quality above any six-rowed barley previously available and became the standard of quality for industry. The short history of two-rowed malting barley breeding in the United States is attested to by the fact that until the recent release of SHABET and VANGUARD, all two-rowed varieties used by industry were of foreign origin. SHABETand VANGUARD are varieties developed through the use of hybridization. Present malting barley breeding programs in the United States involve planned crosses of selected parental varieties followed by one of several selection and testing procedures. The majority of the malting barley varieties released in the last two decades in the United States have been through the use of the pedigree method of breeding, or this method with slight modifications. SHABETis the only variety in Table VI which was developed using the backcross breeding method.

C. MALTINGBARLEYBREEDINGACCOMPLISHMENTS The history of the development of malting barley varieties in the United States contains some interesting trends. Most of the information for this section will pertain to barley production in the principal six-rowed malting barley growing areas of the midwestern United States, but similar patterns exist for other areas of malting barley production in this country. The acceptance of new barley varieties by producers has been more rapid in recent years than that experienced 15 years ago. Rapid increases of seedstocks, improved methods of seed distribution, and an awareness of producers to advantages of using improved seedstocks are some of the reasons for the accelerated rate of new variety acceptance. Varietal history also shows that the length of time a variety stays in production has decreased in recent years. One of the undesirable features noted in the varietal history of barley has been the trend toward a one variety culture. A single variety grown over a large area is vulnerable to attack by various crop hazards, as clearly pointed out by Horsfall et al. (1972). Varieties with acceptable malting quality have been the dominant barleys grown in the Midwest.

356

0. A. PETERSON AND A. E. FOSTER

These malting types also are suitable for feed purposes, and in most instances perform as well as the better feed varieties. Generally, new varietal releases have been an improvement over the older varieties in production and have tended to dominate the barley acreage. Much effort by state agricultural experiment stations is devoted to developing barley varieties having superior performance while maintaining a required level of genetic diversity among varieties. This effort must continue in order to reduce the risk of loss of malting barley supplies and to give both the producers and users a varietal choice to fit their particular need. However, only the acceptance of a variety by producers and users over time determines its success. Peterson (1972) made an overall assessment of the progress in the development of improved barley varieties by studying changes in agronomic, disease, and quality characteristics over the past four decades. Agronomic, disease, and quality values for the most popular varieties grown in the Midwest during this period are given in Table VII. Compared with varieties such as MANCHURIA and WISCONSIN 3 8, which are relatively undesirable by present day standards, grain yields were increased significantly with TRAILL and were raised again with DICKSON. A new level of improved straw strength was achieved with TRAILL and has been maintained since that time. Further improvements in this characteristic are a critical need for the more productive areas. Short, stiff-strawed types may help solve the lodging problem. Although present malting barley varieties are slightly earlier and shorter than older ones, changes since KINDRED up until now in these characteristics have been slight. The variation in test weight also has been relatively small in the popular varieties. The most significant improvements in barley varieties have been in the area of improved disease resistance. Stem rust (Puccinia graminis tritici Eriks. and Henn.) resistance was found in KINDRED and has been introduced into every variety of six-rowed malting barley released since KINDRED. Resistance to the prevalent leaf spotting diseases was not attained was the first variety with field resisuntil DICKSON was released. DICKSON tance to three prevalent leaf spotting diseases, spot blotch (Helminthosporium sativum Pam., King, and Bakke), net blotch (Helminthosporium teres Sacc.), and Septoria leaf blotch (Septoria pusserinii Sacc.). DICKSON has been a significant factor in stabilizing production in certain parts of the major midwestern malting barley producing areas since varying levels of these leaf spotting diseases may occur either singly or in all combinations each year. The new variety BEACON has resistance to loose smut [Ustilago nudu (Jens.) Rostr.] added to the disease resistance levels present in DICKSON. Loose smut resistance also is present in the blue aleuroned vari-

TABLE VII Agronomic, Disease, and Quality Comparisons of Six-Rowed Barley Varieties Produced in the Midwestern United States and Utilized for Malting and Brewing During the Past Four Decades0

Variety

Year released to producers

Grain yield (bu/acre)

Straw lodging

Plump kernels

Kernel protein

Malt extract

(%)

Leaf spot score (1-10)b

(%I

(%)

(%I

66 64 79 44 43 41 41

5.0 6.0 6.7 6.7 6.0 6.5 3.5

29.0 46.0 31.5 a1 .o 40.6 55.9 34.6

14.6 15.3 14.6 14.0 14.1 14.6 13.8

72.8 69.6 73.0 73.8 74.3 74.8 74.9

F

F

=! z

Diastatic power ( V

0 W

9

P

r m

.e MANCHURIA WI~CONSIN 38 KINDRED

TRAILL TROPHY LARKER DICKSON

1990 1929 1942 1956 1961 1961 1964

51.3 47.8 50.8 59.8 61 . O 61.6 68.2

189 154 233 204 227 226 225

2 J

E C

5J

m U [n

Data obtained from a period of years and locations summary of barley grown in North Dakota (Peterson, 1979). b Combined disease score for spot blotch, net blotch, and Septoria leaf blotch. 1 = no symptoms, 10 = severe symptoms. Degrees Lovibond, a unit of wort color.

Z ,

H

5

z

358

G. A. PETERSON AND A. E. FOSTER

eties, CONQUEST and BONANZA. Recent evidence indicates that introduction of resistance to leaf rust (Pucciniu hordei Otth.) and (Septoria avenue Frank f. sp. trilicea T. Johnson) into the six-rowed malting types may be needed. The changes in kernel plumpness due to shifts in predominant barley varieties has shown a cyclic trend over the last four decades. With the difficulty of obtaining simultaneous improvement of all important characteristics with each new varietal release, it appears that occasionally a sacrifice has been made in kernel plumpness in order to improve other traits. Since all the varieties listed in Table VII which occupied substantial acreages in the Midwest have been acceptable malting types, consideration of the trends of quality characteristics is of interest. Although changes in kernel protein percent, malt extract percent, and diastatic power have occurred as a result of shifts in varieties, none of these changes since the KINDRED era were very drastic. In fact, differences among recent varieties often have not been greater than that expected from year-to-year quality variations within a variety. The deviations in quality characteristics of sixrowed, white aleurone types since KINDRED have not been nearly as great as those for many of the agronomic and disease traits.

XI.

Hybrid Malting Barley

Cultivated barley is a highly self-fertilized crop in most environments. The characteristics which inhibit cross-pollination make it difficult to obtain hybrids through natural crossing. Barley pollinates while the spike is partially to completely enclosed in the flag leaf sheath in many areas of the United States and Canada. Opening of the florets is inhibited by the flag leaf sheath and only a limited amount of pollen escapes from the flower into the air. Attempts are being made to increase cross-pollination percentages by incorporating genes for head emergence prior to flowering, anther extrusion from florets, and increased pollen load into adapted varieties (Foster and Schooler, 1971; Hockett and Eslick, 1971). Barleys from the USDA world collection and interspecific crosses have served as sources of germplasm. Genetic male sterility first was reported in barley by Suneson (1940). Since that time many other genetic male steriles have been found (Hockett and Eslick, 1971) and 19 different loci have been identified. Male steriles probably existed long before their first being reported because discovery of at least one male sterile plant in a field of barley is not uncommon. Hockett and Eslick (1969) reported a spontaneous mutation rate for genetic male sterility of one in 40,000 plants. However, the genetic male

MALTING BARLEY IN THE UNITED STATES

359

sterility could not be used to produce hybrid barley seed in large quantities because production of entire populations of male sterile plants was not possible. Wiebe (1960) proposed use of the chemical DDT in combination with genetic male sterility to produce populations of male sterile plants. He proposed that a gene for susceptibility to DDT, Ddt, could be tightly linked to a gene for male fertility, Ms. Spraying a population segregating for Ms-Ddt ms-ddt with DDT would leave only male sterile plants. The failure to find an ms gene linked close enough to the ddt gene to severely restrict crossovers has prevented this scheme from becoming operational. Ramage (1965) proposed the use of a balanced tertiary trisomic (BTT) system for production of hybrids. He proposed that the extra chromosome carry a M s gene close enough to the breakpoint of the translocation to prevent crossovers. In addition, a mature plant character, such as kernel size, kernel shape, or plant color, would be linked to Ms so that trisomic plants could be identified easily. Several feed-type hybrid barleys are being produced commercially and utilize the BTT system without benefit of the mature plant character. More recently, Wiebe and Ramage (1971) proposed incorporating a gene for albinism into the system so that hand rogueing would not be necessary. Wiebe (1972) reported additional modifications of the BTT and other systems for production of hybrids. A basic requirement for the BTT system to work properly is that the extra chromosome is not transmitted through the pollen. Matchett (1972) found that rate of pollen transmission of the extra chromosome depended on varietal background and varied from 4 to 17%. Transmission of the extra chromosome through the pollen results in fertile trisomics in the desired male sterile female block of a hybrid seed production field. If these fertiles are not removed, they provide pollen to surrounding male sterile plants, and male sterile plants will be present in a farmers F, hybrid field. Eslick (1971) presented alternative.methods to the BTT system for production of hybrid barley. He proposed the use of balanced male steriles in combination with dominant preflowering selective genes. The proposed systems require close linkages between male sterility genes and dominant preflowering genes, and the genetic stocks have not been established. Schooler (1967) reported finding a cytoplasmic male sterile in the progeny of an interspecific cross with H . jubatum cytoplasm. However, undesirable plant types associated with the cytoplasm and fertility restoration have prevented the use of these stocks in developing acceptable F, hybrids. Pfeifer (1 972) reported that the variety “Pennrad” has a normal cytoplasm and nonrestorer genes and that many other varieties have sterile cytoplasms and fertility restorer genes. He indicated that no undesirable side effects were observed and that fertility restoration was complete in the F, hybrids.

3 60

G. A. PETERSON AND A. E. FOSTER

The malting quality of F, barley hybrids is of concern to the industrial processors and to the barley breeders. A number of quality tests on F, hybrids have been made. Most of the tests have been on small amounts of material because hybrid plants were the result of hand pollination and often of hand emasculation. Lofgren and Peterson (1962) made prediction tests on unmalted barley and found that percent extract and percent plump kernels usually were similar to the mean of the high-parent. Diastatic power and percent nitrogen, although variable, were most often intermediate to the parents and near the mean of the low-parent, respectively. These results were substantiated by Rasmusson et al. (1966) when they performed malting tests on 28 F, hybrids involving 8 parents of diverse malt quality. Average percent extract was intermediate between the mid- and high-parent mean, and average percent malt nitrogen and percent plump kernels were similar to the low-parent and high-parent averages, respectively. The average of all F,’s was not different from the mid-parent average for percent wort nitrogen, ratio of wort to malt nitrogen, diastatic power, a-amylase, or p-amylase. The F, hybrids with the best quality usually had one parent with acceptable malting quality, and they suggested that both parents of a hybrid should have good malting quality in order to have the best chance of obtaining an F, hybrid with good quality. Foster and Peterson (1967) evaluated a diallel cross among four barley varieties for quality. They noted that F, hybrids were similar in kernel plumpness, slightly lower in kernel protein, and slightly higher in percent extract and diastatic power than the mid-parental means. Foster (1971) reported results of malting tests on hybrid barley produced in large plots. The F, hybrids had parents with unsuitable malting quality, and the hybrids also had unsuitable malting quality. Grain yields of barley F, hybrids have not been outstanding (Armstrong et al., 1970; Foster and Peterson, 1967; Foster, 1967, 1969, 1971; Grissom, 1969). The F, hybrids have performed better, relative to the parents, under good environmental conditions than under unfavorable environmental conditions. Present barley varieties which can serve as potential parents have intermediate straw strength. Improvement in straw strength and reduction in plant height of the parents will be necessary for the.F, hybrids to express their yield potential under high fertility conditions.

XII.

Quality Testing Procedures Used to Develop Acceptable Malting Barley Varieties

Tests have been developed which aid in the evaluation of hybrid selections and introduced material for their potential as future malting barley

MALTING BARLEY IN THE UNITED STATES

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varieties. In many barley breeding programs a series of tests for quality are used. The complexity and number of determinations of the tests increases as the amount of grain available for testing and homozygosity of lines increases with advancing generations. Also, the number of hybrid selections which can be evaluated in later generations becomes less because of the complexity of the tests and expense involved. Selection based on the preliminary tests aids in reducing numbers of selections in advanced generations. The purpose of this section is not to give a detailed discussion of the methods used in evaluating barley or malt, but to illustrate the steps a barley breeding team usually follows from making the initial cross to final naming and releasing of an acceptable malting variety. Methods for barley quality evaluation were reviewed by Dickson and Burkhart (1956) and Dickson (1965). Meredith et al. (1962) extensively reviewed the methods of quality evaluation used for barley and malt in several of the quality laboratories in Canada, the United States, and Europe. Dickson (1969) discussed tests used for malting quality, and Anderson et al. (1943) extended such information to include an interpretation of analytical data on barleys and malts with this interpretation helpful to plant breeders in their selection programs. New methods of quality evaluation are constantly being investigated and incorporated into testing procedures on hybrid selections as new basic biochemical and physiological information becomes available. Much effort by quality laboratories involves improvement in the efficiency and speed with which barley selections can be analyzed for quality. The success of a malting barley breeding program is closely related to the number of barley selections which can 'be evaluated for quality along with agronomic and disease characteristics. The ability of small-scale quality tests to aid the barley breeder in selecting for quality characteristics can only be determined by their relationship to plant scale malting and brewing tests. A.

PREDICTION TEST

The prediction test involves the determination of protein content, potential diastatic power, and percent extract on the barley grain. Kernel size assortment also is determined using the standard %4 inch X % inch and the %;4 inch x % inch sieves. Although 60 g are submitted for the prediction tests, actual evaluations usually involve only 36 g of barley grain. The prediction test is conducted on grain from individual plant progenies normally beginning in the F, generation and may continue until the F, or as long as selections are carried as individual lines. Barley in any generation can be analyzed by the prediction test. However, Foster et al. (1967) have

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shown that use of the method was ineffective for selection on an individual F, plant basis. Bendelow and Meredith ( 1955) have described prediction test procedures based on several earlier studies conducted by Canadian researchers. Results of a micro method of extract determination using 3.5 g of barley correlated well with the results of prediction tests normally using 20 g (Banasik and Harris, 1959). This micro method for extract determination could be used for very small samples, but normally individual plant progeny rows furnish sufficient grain for the 20 g test. A computer evaluation system for the barley prediction data has been designed to provide greater uniformity of laboratory results (Banasik et al., 1966). The more rapid compilation of the data has been of great benefit to the program. B.

MACROAND MICROMALTING

The macro malting test normally is used on barley selections upon their initial entry into performance trials which include grain yield determinations. Although the macro malting test often is initiated on F, selections, tests beginning with F, to F, generation lines are more common. The macro malt quality evaluations continue as rong as barley selections are retained in small plot or rod-row type performance trials. The USDA National Barley and .Malt Laboratory uses the macro malt test on entries of the several regional nurseries grown throughout the United States. Approximately 250 g of barley are malted, and determinations are made according to standardized procedures which have been developed by the American Society of Brewing Chemists (Anonymous, 1958). The characteristics listed in Table I11 are obtained from the macro malt analysis. In addition, kernel discoloration, malt recovery, percent of total protein that is soluble, and p-amylase often are reported. Banasik et al. (1956) developed a micro malting method which modified some of the steps in the macro malting procedure without an appreciable loss in the accuracy of the determinations. The changes primarily involved modification of the steeping process, a 3-day germination period instead of 5 or 6 days, and a two-stage kilning process. A major advantage of the micro malting method is the use of only 60 g of barley grain. Often in preliminary performance trials of barley selections, the amount of available grain may be a limiting factor for the macro malting test. The Department of Cereal Chemistry and Technology at North Dakota State University is using the micro malting test on barley selections in preliminary and advanced performance trials. Wort color and p-amylase are two of the characteristics that are not obtained by the micro malt test, but are determined in the macro malts.

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An automated analysis for both malt diastatic power and @-amylaseactivity that was recently reported (Banasik, 1971) is being used on a routine basis. This modified procedure has shown precision equal to manual procedures and has greatly decreased the time required for the determination of these enzymes. The computer evaluation and compilation of malting quality data (Banasik et al., 1966) mentioned previously for barley quality data also are being used. These modifications are helpful in a barley breeding program because the time period from submitting samples for quality testing to the need for the quality data to make selections for planting of the promising lines is relatively short. Micro brewing methods which only require 120 g of barley grain are available. This micro brewing evaluation has been used on advanced barley selections in performance trials at North Dakota State University, but the number of selections which can be handled is limited. The micro brewing data do assist in making quality decisions on the advancement of barley selections in a breeding program.

c.

PILOT MALTINGAND BREWING

Pilot-scale malting and brewing tests are conducted in industry laboratories. These tests are attempts to obtain quality results which simulate plant-scale operations. Only the most promising barley selections from plant breeding programs are submitted to the Malting Barley Improvement Association for distribution to various industry participants which collaborate in the pilot-scale malting and brewing tests. The physical and chemical properties of the barley, malts, and brews which are determined are the same as those determined from plant scale operations. These characteristics from malting have been discussed by Witt (1970) and from brewing by Ohlmeyer and Matz (1970). Industry laboratories which pilot malt generally use 1 to 10 pounds of barley. Industry collaborators which perform pilot-scale tests on both malts and brews generally require 12-30 pounds. Appropriate checks are submitted along with the advanced selections. Usually not more than five barley selections are submitted from any, single breeding program. Pilot malting and brewing are conducted on barley lines which show considerable promise for agronomic and disease characteristics in tests over locations and years. Pilot scale testing usually is conducted only for a one-year period but can extend beyond this time. Usually the agricultural experiment stations submit one bushel of barley from one or more locations on which preliminary evaluation for protein content, kernel plumpness, and kernel discoloration are satisfactory. An overall performance rating of the barley selections, and a recommendation regarding further advancement is made

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through a technical committee of the Malting Barley Improvement Association to the breeder for his consideration.

D. CARLOTQUALITYEVALUATION The final step in the quality evaluation of a barley selection is carlot testing on a plant scale basis. Selections do not reach this stage unless they show very great potential as a barley variety. This quality evaluation is made by industry through coordination with the Malting Barley Improvement Association. The handling of experimental barleys usually is similar to that of commercial malting operations, and direct comparisons with commercially grown check varieties are made. The amount of grain needed for a plant-scale evaluation depends on a particular malting company, but a minimum of 2000 bushels generally is required. Usually a maximum of approximately 10,000 bushels is desired by the Malting Barley Improvement Association for these tests. As with the pilot-scale evaluation, an overall evaluation and a recommendation regarding further testing is made by a technical committee of the Malting Barley Improvement Association. Final acceptance or rejection is made by the full membership of this organization. The recommendation for acceptance is made on satisfactory performance on a plant scale basis for two years or two of three years. Rejection can be based on one or more years of unacceptable performance. Naming and release of an acceptable malting barley is done by the agricultural experiment stations upon consideration of the complete results from agronomic, disease, and quality evaluations. Usually 10 to 14 generations have been grown before naming and release. The minimum time from the initial cross to release of an acceptable malting barley variety is eight years. The minimum number of years is less than the minimum number of generations because winter greenhouse crops and winter increases in Mexico or the southern United States makes possible the growth of more than one generation per year. XIII.

Malting Barley Production Practices

Although the barley grower cannot be assured of producing a crop suitable for malting barley, there are several important management decisions which affect his chances of success. Many of the practices recommended for the production of barley for feed or seed also apply to its production for malting barley (Shands and Dickson, 1953; Reid et aZ., 1968; Hunter, 1962). Maximum grain yields of bright, plump kernels produced under conditions that provide minimum losses due to weeds, diseases, and insects are a common goal. However, some of the decisions involved in the pro-

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duction of barley for the malting market are more critical than for other uses because the physical and chemical properties of the harvested grain are of primary concern in the market. Three general considerations confront a producer interested in growing acceptable malting barley. First, the area of production must have the potential of growing grain of suitable quality. This factor is largely a matter of environment, and past climatic history should provide the answer. There are new frontiers for malting barley where history may be of little value in determining successful production. However, these are small in number and generally are associated with new irrigation developments or areas where cropping practices can be changed in established irrigation districts. Second, adapted barley varieties of acceptable quality must be available. Third, a market for malting barley must be available. After these general criteria have been met, several specific management decisions remain. The general requirements of malting barley have been known for a long time in relation to the period of time that this crop has occupied an important place in American agriculture. Information on barley production practices was summarized by Derr (191 1) and in bulletins by Harlan (1918, 1932) and Harlan and Wiebe (1943). Each of these authors referred to culture of malting barley. Most states with significant malting barley acreages have published results on production practices and made these available to barley growers through extension bulletins and circulars. Although some of the recommended practices have been modified as new research data have been published, it is interesting to note the validity of recommendations made several decades ago to malting barley producers. A.

CHOICE OF VARIETY

Selection of a variety by a malting barley grower involves two major considerations. First, the variety must be adapted to the area and should have as many of the agronomic characteristics as possible to fit the specific conditions provided by the individual grower’s farming operations. Medium to late maturity in spring barley for early sowing, in order to utilize more of the growing season, and resistance to loose smut [Ustilago nuda (Jens.) Rostr.] are examples of specific characteristics that may be used in varietal decisions. Second, the variety must have the potential as a suitable raw material for malt. The various agricultural experiment stations in states with malting barley breeding programs collaborate with the malting and brewing industry through the Malting Barley Improvement Association in the evaluation of potential malting barley varieties. Acceptable malting barley varieties are made known to growers through publications listing the varieties available for production or, in some states, the

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recommended malting barley varieties. However, growing of an acceptable malting variety does not assure the production of acceptable grain. Standards for kernel protein percentage, kernel plumpness, percentage of skinned and broken kernels, kernel discoloration, and other factors must be met.

B. SEED QUALITYAND TREATMENT Numerous investigators with several crops have dealt with the effect of seed quality on grain yield and the components of yield as well as on other agronomic characteristics. Although barley is considered a superior competitor against weeds, compared to other small grain cereals and flax, seed of high germination, good plumpness or weight, and freedom from weed seeds, diseases, and inert mixtures is recommended to produce optimum plant stands as measured by seedling emergence and vigor. Kaufmann and McFadden (1963) and Peterson and Foster (1964) found seed size to be associated positively with grain yield, especially under conditions of plant stress often experienced with late sowing. The number of spike-bearing tillers was the yield component most affected by seed size. The barley plant appears to compensate for seed and seedling deficiencies during the growing season if the environment is favorable for barley grain production. Seed quality factors are important to malting barley in the way that they affect kernel size or plumpness of the resultant crop in addition to the usual criteria of agronomic performance. Kernel plumpness of harvested grain has been shown to be maintained at a higher level when plump seed is used for late planting (Peterson and Foster, 1964). The use of chemical seed treatment is a recommended malting barley production practice found to be effective in controlling certain seed-borne diseases (Dickson, 1962; Reid et al., 1968). Also, protection of germinating seeds and young seedlings against harmful organisms in the soil is obtained. Seed treatment is more likely to prevent losses from diseases which weaken plants or prevent spikes from producing seed than to prevent losses from diseases which reduce or impair quality of the harvested grain. Kernel plumpness and protein percentage can be influenced by diseases if interplant competition is altered or nonthrifty plants contribute to the total production. Recommendations of state agricultural experiment stations should be followed closely in the use of seed treatments on malting barley.

c.

TYPEOF SEEDBED

AND

SEEDBED

PREPARATION

The best soils for growing malting barley are well-drained loams and clay loams (Harlan and Wiebe, 1943; Reid et al., 1968). Barley is more

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susceptible to damage than several other crops from water-saturated soil. Light, sandy soils in the subhumid and semi-arid regions often produced drought stress of plants, resulting in low yields. The fertility level of the soil is extremely important for malting barley and will be discussed in a subsequent section. Most of the malting barley in the United States is spring sown. Most of the spring barley is sown on land which was cropped the preceding year. A common practice is to fall plow, especially fine-textured soils of the Red River Valley of North Dakota and Minnesota or where winter erosion is not a problem. Seedbed preparation of fall-plowed land involves shallow tillage in the spring to control weeds, to prevent deeply buried weed seeds from being brought to the surface, and to reduce soil moisture loss. Disking or field cultivating followed by a harrowing often is used in the spring on land previously seeded to a row crop. In less humid areas where malting barley is grown on previously cropped land, the most common practice is to spring plow or to use other implements which leave some of the crop residue on the surface. Spring soil moisture often is more favorable with spring than with fall tillage because of snow cover held during the winter. Also, the standing crop residue reduces erosion during the winter. Under irrigated conditions, as used for malting barley in many western areas of the United States, the land is preferably plowed. Some spring-sown malting barley is planted on summerfallow. Generally, this is not a recommended practice because protein content of the grain produced may be too high. However, some summerfallow fields may not have excessive soil nitrogen levels (Wagner et al., 1970) and are suitable for malting barley production. Shallow tillage for seedbed preparation is recommended for land which has been summerfallowed. Fall-sown winter or spring malting barleys usually are shown on nonfallow land. Plowing followed by various tillage operations to prepare a firm, level seedbed often is used if large crop residues exist. If crop residues are of minor consequence, seedbed preparation is similar to that mentioned for spring-sown barley on row-crop land. A small amount of fall-sown malting barley is seeded on summerfallow and seedbed preparation is similar to that for spring-sown barley. Malting barley usually is grown in a crop sequence. The kind of sequence varies with the other crops adapted to the region, length of growing season, availability of moisture, soil type, soil fertility, and disease problems (Reid et al., 1968). Barley following barley is not a recommended cropping practice, particularly in areas where inoculum of destructive diseases can build up on residues in the soil and on the surface. Barley following corn or wheat is undesirable in areas where scab is a problem unless clean cultivation and sanitation are practiced. In the more humid regions

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where summerfallowing is not practiced, malting barley production following row crops such as sugar beets, potatoes, and sunflowers has been successful if soil nitrogen levels are not excessive. Occasionally malting barley is used as a companion crop with a legume or legume-grass mixture in these areas or where irrigation is used. Malting barley follows wheat in many rotations in the major producing areas of the North Central States. Fallow-wheat-barley is a common crop sequence for less humid malting barley growing areas.

D. SEEDINGPRACTICES Malting barley usually is seeded with a grain drill, often equipped with press wheels and a fertilizer attachment (Reid et al., 1968). Most drills have disk furrow openers which place the seeds in rows 6-8 inches apart. Hoe drills, with about 9 inches between rows, are used in some areas of the Pacific Northwest on clean fallowed land, and in some of the less humid regions of the upper Midwest. The desired plant population for a specific set of environmental conditions is obtained by selecting an appropriate rate of seeding. Variety, date of sowing, soil moisture, and conditions affecting seedling emergence are the most important factors affecting the number of spike-bearing tillers per unit area. Varieties with large seeds and low tillering capacity require higher seeding rates. A delay in date of seeding, which often reduces tillering or stand reductions due to poor seedling emergence in nonfriable soils, also dictates use of higher seeding rates to compensate for below optimum stands. Lower rates of seeding ordinarily are used in drier areas because less dense stands reduce stress due to interplant competition. Competition from excess weed growth requires that barley be seeded at higher rates than normal (Woodward, 1956). Grain drills meter out the barley seed by volume, and seeding rate recommendations normally are made on this basis. Planting 1.5 to 2 bushels of barley per acre is a general practice in the more humid area of the North Central States and in irrigated regions of Western United States. One to 1.5 bushels are seeded in the less humid malting barley growing areas of the Midwest. Seeding by volume is one reason the grower adjusts seeding rate by variety or kernel size. Berdahl (1967) was not able to show any difference in grain yield when rates from 0.75 bu/acre to 1.75 bu/acre were seeded in North Dakota by volume, weight, or number of seeds per unit area. These results, along with an increase in the number of spike-bearing tillers with the use of large seed (Kaufmann and McFadden, 1963; Peterson and Foster, 1964), indicate the compensation in rate of seeding may be less important than growers believe. Studies with barley show that similar grain yields are obtained over a wide range of seeding

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rates (Meredith and Olson, 1942; Woodward, 1956; Berdahl, 1967). An important factor to the malting barley grower, however, is that the range of seeding rate for the production of quality grain is more critical than for quantity. Higher seeding rates than required for optimum stands reduce kernel size (Meredith and Olson, 1942; Woodward, 1956; Peterson, 1966). Date of seeding of malting barley is influenced by latitude, altitude, climatic conditions, cropping practices, and use of spring or winter varieties (Reid et al., 1968). Most of the malting barley for processing by the malting industry is obtained from spring-sown barleys. The general recommendation for these production areas is that seeding should begin as soon as a good seedbed can be prepared. In the North Central States the earliest seeding date ranges from about March 10 to May 10. The range of preferred dates of seeding spring barley in the Pacific Northwest and intermountain areas is from March 15 to April 30. Some winter barley is sown in these areas from September 1 to October 15. In California, spring varieties are sown from late October to mid-January. The benefits of early spring seeding regarding performance for yield and other agronomic characteristics have been established by numerous investigators (Woodward, 1956; Beard, 1961; Jackson et al., 1962; Peterson, 1966; Berdahl, 1967; Hoag and Geiszler, 1968; Zubriski et al., 1970). Seeding date is among the most important factors involved with malting barley production. Although grain yield response to seeding date may differ with varieties (Beard, 1961; Berdahl, 1967) or with years or locations (Woodward, 1956; Zubriski et al., 1970), the advantage of early seeding of barley is affirmed. Reduction in grain yield with delayed seeding appears to have a linear trend in some studies and nonlinear in others. A delay of one month from the optimum seeding date for malting barley in North Dakota resulted in grain yield reductions of 53% (Peterson, 1966), 22% (Berdahl, 1967), and 7% (Hoag and Geiszler, 1968). Most studies show yield losses to be within the range of the North Dakota studies, with the position within the range depending on the variety and/or the environment under which the trials were conducted. The effect of date of seeding on characteristics of harvested grain is important to the grower since the influence on grade and suitability for malting have a direct impact on economic return. In addition to a loss in yield, losses in kernel weight, kernel plumpness, and test weight per bushel appear to be some of the most consistent effects indicated in date of sowing studies (Meredith and Olson, 1942; Woodward, 1956; Beard, 1961; Jackson et al., 1962; Peterson, 1966; Berdahl, 1967; Hoag and Geiszler, 1968; Zubriski et al., 1970). Kernel protein percentage increases with late seeding (Meredith and Olson, 1942; Hoag and Geiszler, 1968; Zubriski et al.,

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1970) and levels are often in excess of those suitable for malting (Table VIII), Undesirable decreases in barley extract (Beard, 1961) and malt extract (Meredith and Olson, 1942) were found as a result of late seeding. Expected increases in diastatic power in the barley grain accompanying the increase in kernel protein levels were found by Beard (1961). TABLE VIII Influence of Seeding Dates and Rates of Nitrogen and Potassium Fertilizers on Average Grain Yields, Percentage Plump Kernels, and Protein Content of Graina

Rate of N or K

(WA) 0.0 20.0 40.0 60.0 0.0 12.5 25.0

N N N N K K K

Average

Average yields

Average plump kernels

(WA)

(%I

Average protein content (%)

Early seeded

Late seeded

Early seeded

Late seeded

Early seeded

Late seeded

48.6 53.3 56.2 58.5 53.6 54.3 54.4 54.1

44.2 49.2 49.9 51.5 47.7 49.1 49.2 48.7

75.8 75.9 75.9 75.6 74.8 76.1 76.5 75.8

66.2 67.1 65.6 65.1 64.5 66.3 67.2 66.0

12.8 13.1 13.2 13.5 13.2 13.1 13.1 13.1

13.4 13.6 13.9 14.2 13.8 13.7 13.8 13.8

Adapted from Zubriski et al. (1970).

Barley should be sown at a depth at which moisture is available, but the depth should not be so great that the energy requirement for emergence exceeds the supply available in the barley kernel. In general, the depth of seeding is 1-2 inches in the more humid malting barley growing areas and 2-3 inches in the drier regions. E.

FERTILIZERS

One of the most important management decisions for the malting barley producer is the amount of fertilizer to apply to the soil. High yields of good quality grain is the goal of the barley grower. Protein content and kernel plumpness are two properties of the harvested grain used to evaluate malting quality and must be at desirable levels if the barley is to be purchased by the malting industry. These properties are greatly influenced by the supply of available nutrients, particularly nitrogen, in the soil in relation to the minimum amount required for dry matter production. Other

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variables affecting grain quality are the barley variety, moisture, and temperature conditions under which the variety is produced, and diseases or other pests detrimental to favorable plant growth. The close relationship of soil nitrogen levels to yield and protein content of the grain has been recognized for a long time. Hopkins (1936), Jackson et al. (1962), Zubriski el al. (1970), and Bishop and MacEachern (1971) found nitrogen fertilizer increased average grain yields on nitrogen-deficient soils. Protein content of the grain increased significantly when excessive nitrogen fertilizer was used. Protein content of the grain appears to increase to the greatest extent after the maximum grain yield level is reached. When the yield curve begins to level off as greater amounts of nitrogen (are made available, protein content of the barley grain increases rapidly. If the nitrogen available to the plant exceeds that required for optimum yield in relation to the other soil nutrients and environments, kernel protein levels above those desirable for malting barley often result. Nitrogen fertilization appears to influence kernel plumpness or size less than grain yield or protein. Kernel plumpness and size are most seriously reduced if use of fertilizer or other factors induce lodging at a relatively early growth stage. Grain yield and kernel protein responses in barley with the addition of different levels of nitrogen fertilizer show considerable variability as reported by many workers. Also, significant interactions with years, locations, and varieties have been indicated (Olson et al., 1942; Frey et al., 1952; Pendleton el al., 1953; Zubriski et al., 1970). The discrepancies in response to different amounts of nitrogen fertilizer indicated among the various reports probably result from not considering the amount of nitrogen in the soil profile available to the barley plant before fertilizer application and from uncontrolled environmental variables. Soper and Huang (1962) showed a highly significant correlation of 0.95 between nitrate nitrogen in the soil to a 4-fOOt depth and yield response to nitrogen. Also, the correlation between uptake of nitrogen in the grain and nitrate nitrogen in the soil profile plus nitrogen added at seeding time was r = 0.90. The need for a certain amount of nitrogen fertilizer to enhance malting barley production on land which has been cropped previously is well understood. Many producers have thought summerfallow to be unsuitable for growing malting barley because of suspected high levels of nitrate-nitrogen in the soil which would lead to higher levels of protein in the grain produced. Recent summaries show that about 15% of the summerfallowed fields in the Red River Valley of North Dakota and Minnesota and adjacent areas contain less than 100 pounds/acre of nitrate nitrogen (Wagner et al., 1970). Acceptable malting barley can be produced on these summerfallow fields. Producers utilizing the NO, soil test to predict the amount

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of nitrogen available for crop growth can make reliable decisions on choice of land to use for malting barley and how much nitrogen, if any, to apply. Malting barley has shown favorable responses to phosphorus and potassium applied to soils in which these elements are deficient. Grain yield increases, reduced lodging, increased kernel plumpness, and reduced protein content of grain are the major benefits attributed to applications of phosphorus (Hopkins, 1936; Norum et al., 1953; Pendleton et al., 1953; Atkins et al., 1955). Response of barley to phosphorus fertilizer often is observed on both fallow and nonfallow land. The use of potassium fertilizer on malting barley has given less consistent responses than nitrogen or phosphorus with agronomic and quality characteristics (Hopkins, 1936; Pendleton et al., 1953; Bauer and Vasey, 1964; Zubriski et al., 1970). An increase in percent of plump kernels and often an accompanying decrease in kernel protein content by application of potassium fertilizer are among the more frequent favorable responses observed. The use of nitrogen, phosphorus, and potassium fertilizers on malting barley should be based on soil test results along with other production variables, such as soil moisture, soil type, and date of seeding. Fertilizer recommendations for malting barley, made by state agricultural experiment stations such as those presented by Wagner et al. ( 1970), consider the several variables in suggesting the levels to be applied. The need for a balanced level of nutrients available to the barley plant for best grain quality has been recognized (Hopkins, 1936; Pendleton et al., 1953; Jackson et al., 1962; Zubriski et al., 1970; Bishop and MacEachern, 1971). Most soils used for malting barley production appear to have satisfactory levels of micronutrients.

F. CONTROLOF

PESTS

A large array of pests can influence malting barley production and the quality of harvested grain. The effects can be either through competition with the barley plant, as with weeds, or by direct attacks on different parts of the plant by diseases or insects. The loss or damage is a result of an interaction between the barley genotype and pest as influenced by the environment. Control of any pest may be accomplished through the use of one or a combination of practices which include cultural methods, sanitation, chemical treatments, resistant varieties, or timing of management operations. A lengthy discussion on pests of malting barley will not be included because of the number and variability of effects. Some known effects of pests on malting barley are grain yield reductions, decreased kernel size and weight, discoloration and blighting of the grain, increased kernel protein, and changes in chemical constituents of the kernel. Reviews of pests and their control in barley include those for weeds (Reid et al.,

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1968), insects (Reid et al., 1968), and diseases (Dickson, 1962; Reid et al., 1968).

G. HARVESTING AND THRESHING The primary method of harvesting and threshing malting barley in the major producing areas in the North Central region of the United States is windrowing followed by combine threshing of the windrows. Cutting and direct threshing of the standing grain, termed direct or straight combining, is a common practice in Western United States. Windrowing has two main advantages. First, shattering is avoided since considerable moisture is contained in the straw and grain at the time of windrowing. This feature especially is applicable to the midwestern grown six-rowed Manchurian types because of their tendency to shatter at maturity. Second, weed mixtures and barley of uneven maturity are permitted to dry enough to allow proper threshing and usually reach a kernel moisture content adequate for safe storage. Several workers (Harlan, 1920; Harlan and Pope, 1923; Dodds and Dew, 1958; Koenig et al., 1965; Brewer and Poehlman, 1968; Pomeranz et al., 1971) have shown that the deposits of dry matter in the barley kernel cease as the kernel moisture content reaches the 3 5 4 2 % level. The barley kernel is termed physiologically mature when the addition of dry matter to the grain ceases. Changes from the 35-42% level of kernel moisture to maturity have been considered to be primarily dehydration. Grain yield and kernel weight are not reduced by windrowing of malting barley at physiologic maturity with subsequent threshing when the grain has a moisture content of 15% or less. Windrowing at high levels of kernel moisture has affected the variability of chemical characteristics used to measure quality of malting barley more than it has affected the variability of grain yield and kernel weight. Optimal properties for some of the chemical characteristics appear to be reached when the barley is windrowed or harvested at kernel moisture contents below 3 5 4 2 % . Malt modification, as measured by fine-coarse extract difference, a-amylase activity, and protein solubility (expressed as the wort nitrogen-to-malt nitrogen ratio) are factors that benefit from barley maturation. Windrowing when the kernel moisture ranges from 18 to 35% appears suitable in order to obtain desirable chemical properties in the grain for malting barley (Dew and Bendelow, 1963; Koenig et al., 1965; Pomeranz et al., 1971). The moisture content of barley grain when threshed is important to malting quality. Watson et al. (1962) found that with direct combining, germination was reduced below an acceptable level for malting barley if the moisture content was above 21.5%. Although other malting quality characteristics were satisfactory in grain with higher moisture content, me-

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chanical damage was responsible for poor germination at these levels. Malting barley should not be threshed if the moisture content is above

20%. Threshing malting barley is a critical operation for the producer because acceptable grain can be made unsuitable for malting by improper threshing. The principal factor which causes reduction in, or the elimination from, the malting barley grades is skinned and broken kernels. Excessive cylinder speeds of the combine mainly are responsible for skinned and broken kernels (Vogel, 1958). Concave clearance of the combine should be adjusted in relation to correct cylinder speed to properly thresh without excessive damage to the grain (Kucera, 1972). Sieves and air should be adjusted for minimum tailings in the return to prevent kernel damage caused by barley passing through the cylinder a second time. Kernel damage from threshing is greatest when moisture content is too low or high. The moisture content of the grain varies with the time of day, and therefore, combine adjustments should be made according to prevailing conditions.

H. HANDLING AND

STORAGE

Most malting barley is stored in bulk in bins of various sizes. Grain elevators are used in transferring the barley into and out of these bins. If a blower type of elevator is used, excessive fan speeds should be avoided to prevent skinned or broken kernels (Vogel, 1958). For safe storage of malting barley for long periods, kernel moisture content should be less than 13% (Tuite and Christensen, 1955). Grain should be dried to a moisture content of 13% or less to prevent heating and possible deterioration in malting quality characteristics, especially loss of germination. Barley intended for malting purposes should be harvested at a kernel moisture content of 20% or lower and not be subjected to drying air temperatures above 130°F (Watson et al., 1962). Lower drying air temperatures should be used as kernel moisture levels increase. High air velocity and temperature are being used in some of the new drying units, and extreme care should be exercised in use of this equipment on malting barley to prevent loss of quality. In the post-ripening process that takes place in newly threshed and stored barley, the moisture and temperature tend to increase. If the moisture content is above 13 %, molds develop and temperatures continue to rise and cause the grain to deteriorate. Tuite and Christensen (1955) found that storage molds became active when kernel moisture content was above 13 % , resulting in decreased germination. The storage molds were the main cause of germination loss since mold-free grain retained viability when stored for 15-30 days at room temperature and at moisture contents up

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to 19.4%. Invasion of the kernels by the storage molds, Aspergillus spp. and Penicillium spp., took place after harvest. Fungi such as Alternuria spp., Cladosporium spp., and Fusarium spp. are sometimes abundant in the pericarp of the kernels and under the hulls before maturity, but decrease after barley is placed in storage. These fungi are associated with kernel discoloration and blight in harvested grain. Dickson (1962) made an extensive review of the kernel diseases of barley and their effect on malting quality. Barley infested with insects or rodents will deteriorate in storage and may become “unfit for human use,” thus not classifying as malting barley in the marketplace. Sanitation and use of recommended chemicals on storage facilities before use can help alleviate these problems. REFERENCES Anderson, J. A. 1944. Wallerstein Lab. Commun. 7, 179-191. Anderson, J. A., Sallans, H. R., and Meredith, W. 0. S. 1941. Can. J . Res. 19, 278-29 1. Anderson, J. A., Meredith, W. 0. S., and Sallans, H. R. 1943. Sci. Agr. 23, 297-314. Anonymous. 1958. “Methods of Analysis,” 6th ed. Amer. SOC.Brew. Chem., Madison, Wisconsin. Armstrong, J . F., Howell, D. R., Little, J. W., Dennis, R. E., and Osborne, W. E. 1970. 1969 Barley Newslett. 13, 3-6. Atkins, R. E., Stanford, G., and Dumenil, L. 1955. J . Agr. Food Chem. 3, 609-614. Baker, R. J., Bendelow, V. M., and Buchannon, K. W. 1968. Crop Sci. 8, 446-448. Banasik, 0. J. 1971. Wallerstein Lab. Cornmiin. 34, 45-51. Banasik, 0.J., and Harris, R. H. 1957. Brew. Dig. 32,60-65. Banasik, 0. J., and Harris, R. H. 1959. Wallerstein Lab. Commun. 22, 81-87. Banasik, 0. J., Myhre, D., and Harris, R. H. 1956. Brew. Dig. 31, 50-55 and 63-67. Banasik, 0. J., Gilles, K. A., Holoien, M. O., and Peterson, D. E. 1966. Proc. Amer. SOC. Brew. Chem. pp. 192-198.. Bauer, A., and Vasey, E. H. 1964. N . Dak. Farm Res. 23, 19-22. Beard, B. H. 1961. Crop Sci. 1, 300-303. Bell, G. D. H.,and Lupton, F. G. H. 1962. In “Barley and Malt: Biology, Biochemistry, Technology” (A. H. Cook, ed.), pp. 45-99. Academic Press, New York. Bendelow, V. M., and Meredith, W. 0. S. 1955. Can I . Agr. Sci. 35, 252-258. Berdahl, J. D. 1967. M.S. Thesis, North Dakota State University, Fargo. Bishop, R. F., and MacEachern, C. R. 1971. Can. J . Soil Sci. 51, 1-11. Brewer, D. H., and Poehlman, J. M. 1968. Agron. J . 60, 472-474. Cook, A. H., ed. 1962. “Barley and Malt: Biology, Biochemistry, Technology.” Academic Press, New York. Day, A. D., Down, E. E., and Frey, K. J. 1955. Agron. J . 47, 163-165. Den Hartog, G. T. 1950. Ph.D. Thesis, University of Minnesota, Minneapolis. Derr, H. B. 1911. US.Dept. Agr., Farm Bull. 443. Dew, D. A., and Bendelow, V. M. 1963. Can. J . Plant Sci. 43, 534-541. Dickson, A. D. 1965. Cereal Sci. Today 10,284-290.

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Dickson, A. D. 1969. In “Cereal Science” ( S . A. Matz, ed.), pp. 97-117. Avi, Westport, Connecticut. Dickson, A. D., and Burkhart, B. A. 1956. Proc. Amer. SOC. Brew. Chern. pp. 143-155. Dickson, A. D., Olson, W. J., and Shands, H. L. 1947. Cereal Chern. 24, 325-337. Dickson, J. G. 1962. In “Barley and Malt: Biology, Biochemistry, Technology” (A. H. Cook, ed.), pp. 161-206. Academic Press, New York. Dodds, M. E., and Dew, D. A. 1958. Can. J . Plant Sci. 38,495-504. Eslick, R. F. 1971. In “Barley Genetics 11” (R. A. Nilan, ed.), pp. 292-297. Washington State Univ. Press, Pullman. Foster, A. E. 1967. Proc. Barley Improvement Conf., 1967, Minneapolis pp. 36-41. Foster, A. E. 1969. Proc. Barley Improvement C o n f . , 1969, Minneapolis pp. 48-51. Foster, A. E. 1971. Proc. Barley Improvement Conf., 1971, Minneapolis pp. 48-51. Foster A. E., and Peterson, G. A. 1967. Agron. Abstr. 59, 9-10. Foster, A. E., and Schooler, A. B. 1971. In “Barley Genetics 11” (R. A. Nilan, ed.), pp. 316-318. Washington State Univ. Press, Pullman. Foster, A. E., Peterson, G. A., and Banasik, 0. J. 1967. Crop Sci. 7, 611-613. Fraase, R. G., and Anderson, D. E. 1970. N. Dak., Agr. E x p . Sta., Bull. 487. Frey, K. J., Robertson, L. S., Cook, R. L., and Down, E. E. 1952. Agron. J . 44, 179-182. Grissom, D. B. 1969. Proc. Barley Improvement C o n f . , 1969, Minneapolis pp. 45-48. Harlan, H. V. 1918. U.S., Dep. Agr., Farmers’ Bull. 968. Harlan, H. V. 1920.1. Agr. Res. 19, 393-429. Harlan, H. V. 1932. U S . , Dep. Agr., Farmers’ Bull. 1464. Harlan, H. V., and Martini, M. L. 1936. Yearb. Agr. ( U S . Dep. A g r . ) pp. 303-306. Harlan, H. V., and Pope, M. N. 1923. J. Agr. Res. 23, 333-360. Harlan, H. V., and Wiebe, G. A. 1943. U S . , Dep. Agr., Farmers’ Bull. 1732. Harlan, H. V., Martini, M. L., and Pope, M. N. 1925. U S . , Dep. Agr., Bull. 1334. Harris, R. H., and Banasik, 0. J. 1952. Cereal Chern. 29, 148-155. Harris, R. H., and Banasik, 0. J. 1953. Brew. Dig. 28, 161-164. Hoag, B. K., and Geiszler, G. N. 1968. N . Dak.. Farm Res. 25, 13-15. Hockett, E. A., and Eslick, R. F. 1969. Crop Sci. 9, 23-24. Hockett, E. A., and Eslick, R. F. 1971. In “Barley Genetics 11” (R. A. Nilan, ed.), pp. 298-307. Washington State Univ. Press, Pullman. Hopkins, J. W. 1936. Sci. Agr. 17, 250-258. Horsfall, J. G., Brandow, G. E., Brown, W. L., Day, P. R., Gabelman, W. H., Hanson, J. B., Holland, R. F., Hooker, A. L., Jennings, P. R., Johnson, V. A., Peters, D. C., Rhoades, M. M., Sprague, G. F., Stephens, S. G., Tammen, J., and Zaumeyer, W. J. 1972. “Genetic Vulnerability of Major Crops.” Nat. Acad. Sci., Washington, D.C. Hsi, C. H., and Lambert, J. W. 1954. Agron. J . 46, 470-474. Hunt, L. A. 1968. Proc. Red River Valley Barley Day, 1968, Grand Forks, North Dakota pp. 20-24. Hunter, H. 1962. In “Barley and Malt: Biology, Biochemistry, Technology” (A. H. Cook, ed.), pp. 25-44. Academic Press, New York. Jackson, T. L., Foote, W. H., and Dickason, E. A. 1962. Oreg., Agr. Exp. Sta., Tech. Bull. 65, 1-20. Katz, P. C. 1971. Proc. Barley Improvement Conf., 1971, Minneapolis pp. 74-78. Kaufmann, M. L., and McFadden, A. D. 1963. Can. J . Plant Sci. 43, 51-58.

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Kneen, E., and Dickson, A. D. 1967. Encyl. Chem. Technol. 12, 861-886. Koenig, R. F., Robertson, D. W., and Dickson, A. D. 1965. Crop Sci. 5, 159-161. Kucera, H. L. 1972. Proc. Red River Valley Barley Day, 1972, Grand Forks, North Dakota pp. 24-30. Lejeune, A. J. 1946. Sci. Agr. 26, 198-21 1 . Lofgren, J. R., and Peterson, G. A. 1962. Agron. Abstr. 54, 77. Matchett, R. W. 1972. 1971 Barley Newslett. 15, 47-49. Meredith, W. 0. S. 1943. Sci. Agr. 23, 355-361. Meredith, W. 0. S., and Olson, P. J. 1942. Sci. Agr. 23, 237-246. Meredith, W. 0. S., Olson, P. J., and Rowland, H. 1942. Sci. Agr. 23, 135-153. Meredith, W. 0. S., Anderson, J. A., and Hudson, L. E. 1962. I n “Barley and Malt: Biology, Biochemistry, Technology” ( A . H. Cook, ed.), pp. 207-270. Academic Press, New York. Nilan, R. A. 1964. The Cytology and Genetics of Barley, 1951-1962. Res. Stud., Mongr. Suppl. 3, pp. 1-278. Washington State University, Pullman. Norum, E. B., Young, R. A., Zubriski, J. C., and Haley, L. E. 1953. N . Dak. Bimon. Bull. 3, 108-1 1 1 . Ohlrneyer, D. W., and Matz, S. A. 1970. In “Cereal Technology” ( S . A. Matz, ed.), pp. 173-220. Avi, Westport, Connecticut. Olson, P. J., Meredith, W. 0. S., Laidlaw, H. C., and Lejeune, A. J. 1942. Sci. Agr. 22, 659-673. Olson, W. J. 1963. Proc. Barley Improvement Conf.,1963, Minneapolis pp. 19-26. Pendleton, J. W., Lang, A. L., Dungan, G. H. 1953. Agron. J. 45, 529-532. Peterson, G. A. 1956. M.S. Thesis, University of Minnesota, Minneapolis. Peterson, G. A. 1966. Proc. Red River Valley Barley Day, 1966, Grand Forks, North Dakota pp. 5-8. Peterson, G. A. 1972. Proc. Red River Valley Barley Day, 1972, Grand Forks, North Dakota pp. 3-12. Peterson, G. A., and Foster, A. E. 1964. Annu. Rep. lni. Crop Imp. Ass. 46, 49-52. Pfeifer, R. P. 1972. Agron. Absir. 64, 17. Pomeranz, Y., Standridge, N. N., and Shands, H. L. 1971. Crop. Sci. 11, 85-88. Ramage, R. T. 1965. Crop Sci. 5, 177-178. Rasmusson, D. C., and Glass, R. L. 1965. Crop Sci. 5, 389-391. Rasmusson, D. C., and Glass, R. L. 1967. Crop Sci. 7, 185-188. Rasmusson, D. C., Upadhyaya, B. R., and Glass, R. L. 1966. Crop Sci. 6,339-340. Reid, D. A., Wiebe, G. A., Dahms, R. G., Dickson, A. D., Harlan, J. R., Moseman, J. G., Olien, C. R., Price, P. B., Shands, R. G., Shaw, W. C., and Suneson, C. A. 1968. U S . , Dep. Agr., Agr. Handb. 338, 1-127. Rosenbusch, H. K. 1966. Proc. Red River Valley Barley Day, 1966, Grand Forks, North Dakota pp, 24-32. Rutger, J. N., Schaller, C. W., Dickson, A. D., and Williams, J. C. 1966. Crop Sci. 6, 231-234. Rutger, J. N., Schaller, C. W., and Dickson, A. D. 1967. Crop Sci. 7,325-326. Schooler, A. B. 1967. 1. Hered. 5 8 ( 5 ) , 206-211. Seidl, S. F. 1972. Proc. Red River Valley Barley Day, 1972, Grand Forks, North Dakota p p . 23-24. Sfat, M. R. 1963. Rep. Nat. Malting Barley Growers Ass. pp. 1-1 1 . Shands, H. L., and Dickson, A. D. 1953. Econ. Bot. 7, 3-26. Shands. H. L., Dickson, A. D., and Dickson, J. G. 1942. Cereal Chem. 19,471-480.

378

G . A . PETERSON AND A. E. FOSTER

Shellenberger, J. A., and Bailey, C. H. 1936. Cereal Chem. 13, 63 1-655. Sisler, W. W., and Banasik, 0. J. 1951. Agron. J . 43, 616. Smith, L. 1951. Bot. Rev. 17, 1-51, 133-202, and 285-355. Soper, R. J., and Huang, P. M. 1962. Can. J. Soil Sci. 43, 350-358. Streeter, J. G., and Pfeifer, R. P. 1966. Crop Sci. 6, 151-154. Suneson, C. A. 1940. J . Hered. 31, 213-214. Tuite, J. F., and Christensen, C. M. 1955. Cereal Chem. 32, 1-1 1. Vogel, S. L. 1958. Proc. Red. River Valley Burley Day pp. 33-36. Wagner, D. F., Zubriski, J. C., and Dahnke, W. C. 1970. N . Dak. Coop. Ext. Circ.

SF

13.

Watson, C. A., Banasik, 0. J., and Pratt, G. L. 1962. Brew. Dig. 37, 44-48. Weaver, J. C. 1950. “American Barley Production.” Burgess, Minneapolis, Minnesota. Wiebe, G. A. 1960. Agron. J . 52, 181-182. Wiebe, G. A. 1972. 1971 Barley Newslett. 15, 44-46. Wiebe, G. A., and Ramage, R. T. 1971. In “Barley Genetics 11” (R. A. Nilan, ed.), pp. 287-291. Washington State Univ. Press, Pullman. Wiebe, G. A., and Reid, D. A. 1961. U S . , Dep. Agr., Tech. Bull. 1224. Witt, P. R., Jr. 1970. I n “Cereal Technology” (S. A. Matz, ed.), pp. 129-172. Avi, Westport, Connecticut. Woodward, R. W. 1956. Agron. J. 48, 160-162. Zubriski, J. C., Vasey, E. H., and Norum, E. B. 1970. Agron. J . 62, 216-219.

Author Index Numbers in italics refer to the pages on which the complete references are listed.

A Aastveit, K., 251, 256 Abd-El-Malek, Y.,271, 319 Adamczewski, K., 81, 120 Adams, F., 58, 73 297, 298, 319 Adams, H. R., 187, 205 Adams, W. E., 58, 61, 73, 96, I20 Ahlrich, V. E., 49, 75 Aldrich, D. T . A., 242, 256 Alexander, M., 289, 319 Ali, R., 235, 263 Ali-Khan, S . T., 141, 160 Allam, S. W., 303, 319 Allan, 0. N., 59, 73 Allbrook, R. F., 286, 319 Allen, E. T., 272, 319 Allen, G. P., 106, 120 Allen, S. E., 20, 41 Allison, F. A,, 11, 44 Altschul, A. M., 195, 202 Ambastha, H. N. S., 253, 256 Amberger, A., 241, 257 Amemiya, M., 90, 120 Amos, J. M., 51, 64, 73 Ananthraman, P. V., 267, 324 Anderson, D. E., 331, 333, 376 Anderson, G., 8, 41 Anderson, J. A., 341, 346, 347, 351, 361, 375, 377 Anderson, K . L., 229, 235, 250, 260 Anderson, R. J., 21, 34, 35, 36, 45, 282, 320 Andriesse, J. P., 277, 278, 307, 319 Ansari, A. Q., 171, 202 Ansiaux, J. R., 210, 256 Anthony, W. B., 49, 59, 61, 74, 75 Arata, H., 243, 260 Archer, E. E., 317, 319 Argikar, G. R., 141, 142, 143, 145, 160 Ariel, D., 118, 122 Armiger, W. H., 298, 324 Armstrong, D. E., 11, 18, 19, 44, 45 379

Armstrong, J. F., 360, 375 Armstrong, W. D., 187, 207 Army, T. J., 91, 119, 120, 121 Arnon, I., 141, 143, 145. 160 Arnott, R. A., 94, 98, 120 Asai, J., 197, 204 Asana, R. D., 233,256 Ascherson, P., 48, 73 Ashley, T. E., 61, 73 Ashmead, D., 280, 319 Aso, S . , 302, 323 Assadolahi, A,, 241, 263 Atkins, I. M . , 225, 229, 247, 252, 256 Atkins, R. E., 126, 141, 143, 145, 151, 160, 161, 372,375 Atkinson, M. R., 167, 190, 191, 195, 202, 206 Atkinson, R. J., 9, 42 Attanandana, T., 299, 300, 301, 308, 314, 323 Aufhammer, G., 246, 256 Ausemus, E. R., 252, 256 Aylesworth, J. W., 30, 31, 41 Ayyangar, G. N . R., 136, 160

B Baas Becking, L. G. M., 271, 319 Baba, I., 302, 303, 319 Bache, B. W., 7, 41, 305, 319 Bachthaler, G., 84, 112, 118, 120, 236, 256 Baetcke, K. P., 69, 76 Baeumer, K., 92, 97, 113, I20 Bagnara, D., 233, 253, 254, 256, 262 Baier, A., 224, 225, 228, 229, 247, 249, 256 Bailey, C. H., 334, 346, 377 Bain, R., 238, 256 Bains, S. S., 241, 257 Baker, R. J., 352, 375 Bakermans, W. A. P., 84, 93, 96, 105, 109, 113, 114, 120 Baltaga, S . V., 226, 258

380

AUTHOR INDEX

Banasik, 0. J., 346, 347, 351, 362, 363, 373, 374, 375, 376, 377, 378 Bancroft, T. A., 58, 74 Bange, G. G. T., 165, 176, 182, 202, 206 Bannister, F. A., 285, 321 Barber, S. A,, 12, 41, 97, 120, 182, 202 Barley, K. P., 90, 120 Barnes, B. T., 96, 122 Barnes, D. K., 126, 136, 137, 138, 152, 161 Barnshisel, R. I., 279, 319 Barr, C. E., 180, 202 Bartel, A. T., 230, 256 Bartholomew, W. V., 11, 42 Basistov, A. A,, 247, 250, 256 Bass, M. H., 63, 73 Bauer, A., 372, 375 Bauer, F., 211, 216, 228, 229, 235, 241, 249, 251, 256 Baumgartner, G., 223, 256 Beale, 0. W., 107, 120 Bear, F. E., 187, 202 Beard, B. H., 369, 370, 375 Beatty, M. T., 32, 40, 43 Beaty, E. R., 49, 73 Beaven, E. S., 237,256 Beck, G., 302, 321 Beck, J. V., 280, 282, 319, 320 Beckett, D. H. T., 10, 45 Beckham, C. M., 64, 73 Beil, G. M., 141, 143, 145, 160 Bell, G. D. H., 350, 351, 375 Belville, B. C., 290, 321 Bement, R. E., 107, 121 Bendelow, V. M., 351, 352, 362, 373, 375 Bender, J., 81, 120 Bengtsson, A., 239, 256 Bennett, H. W., 56, 68, 73 Berbigier, A., 254, 256 Berdahl, J. D., 368, 369, 375 Berg, W. A., 278, 322 Bergmann, H., 244, 246, 256 Berlyand-Kozhevnikov, V. M., 234, 256 Bernal, J. D., 281, 320 Berner, R. A., 271, 212,320 Berry, L. J., 48, 76 Bertagnolli, B. L., 204

Beye, G., 299, 300, 301, 308, 310, 314, 320, 323 Bhamonchant, P., 224, 231, 256, 261 Biever, K. J., 259 Biggar, J. W., 2, 5 , 14, 24, 41 Birge, E. A., 24, 38, 42 Bishop, R. F., 371, 372, 375 Black, A. L., 91, 120 Black, C. A,, 12, 30, 32, 41, 44, 45 Blake, G. H., Jr., 64, 73 Bledsoe, C., 190, 202 Bleier, H., 68, 73 Blevins, R. L., 90, 94, 95, 108, 120 Blinks, L. R., 167, 202 Blokhuis, W. A., 277, 278, 307, 319 Bloomfield, C., 267, 280, 282, 283, 286, 287, 290, 304, 307, 311, 312, 316, 317, 320, 324, 325 Blount, C. L., 61, 73 Blum, A., 141, 143, 145, 160 Boatwright, G. O., 236, 256, 257 Bockmann, H., 216, 223, 235, 256 Bockstaele, L., 244, 260 Bodendorfer, H., 245, 258 Boehm, W., 98, 108, 121 Boerner, H., 96, 120 Bogyo, T. P., 253, 256 Bokarev, K. S., 246, 261 Bokhari, U. G., 244,256 Boland, P., 244, 256 Bolt, G. H., 9, 43 Bolton, E. F., 30, 31, 41 Bond, J. J., 90, 91, 120 Bond, W., 240, 259 Bondurant, J. A., 30, 31, 41 Boone, F. R., 84, 85, 88, 122 Boons, H. ch. P. M., 288, 324 Bormann, F. H., 23,41 BorojeviC, S., 242, 254, 256 Borrill, M., 142, 160 Borthwick, H. A., 129, 130, 138, 160, 161 Boseck, J., 49, 52, 66, 75 Bosse, O., 81, 84, 87, 93, 94, 96, 101 120, 121 Boszormenyi, Z., 187, 202 Bower, C. A., 271, 323 Bowling, D. J. F., 171, 202, 203 Boyce, S. W., 252, 256

38 1

AUTHOR INDEX

Bozzini, A., 233, 253, 254, 262 Brabec, D. J., 14, 45 Brackeen, L. O., 62, 73 Bracker, C. E., 167, 193, 196, 204 Brammer, H., 267,320 Brandow, G. E., 355, 376 Brayley, S. A., 279, 280, 291, 320, 322 Bregger, J . T., 67, 73 Bremner, J. M . , 233, 241, 256, 317, 325 Brewer, D. H., 373, 375 Briggle, L. W., 217, 252, 254, 256 Briggs, G. E., 164, 165, 202 Brill, G. D., 6, 28, 43 Brink, N., 21, 22, 23, 31, 41 Brinkman, R., 273, 277, 315, 316, 320 Britten, E. J., 68, 73 Brock, T. D., 3 16, 321 Broeshart, H., 166, 182, 186, 203 Bromfield, S. M., 8, 19, 41, 269, 320 Brooks, D. H., 102, 120 Brophy, G. P., 284, 320 Brouwer, W., 241, 256 Browrnan, M. G., 9,44 Brown, D. G., 280, 319 Brown, G., 282, 3 18,320 Brown, H. D., 195, 202, 211, 229, 240, 250, 258, 259 Brown, J. C., 298, 321 Brown, W. L., 83, 120, 59, 61, 75, 355, 376 Broyer, T. C., 164, 167, 190, 204 Bryan, E. H., 35, 37, 41 Bryner, L. C., 282, 320 Buchanan, A. S., 271, 324 Buchanan, G. A., 49, 74 Buchannon, K. W., 352,375 Buehrer, T. F., 9, 41 Buhtz, E., 84, 87, 93, 94, 96, 120 Buie, T. S., 54, 73 Bulfin, M., 81, 120 Bull, R. A., 298, 306, 325 Burgess, H. E., 49, 74 Burk, D., 180, 205 Burkhart, B. A., 341, 361, 376 Burkin, A. R., 281, 320 Burrows, W. C., 91, 101, 121, 122 Burstrom, H., 190, 205 Burton, J. C., 59, 73 Burwell, R. E., 25, 27, 29, 39, 44 Butler, G. W., 164, 165, 202

Butt, V. S., 195, 204 Byrd, M., 49, 75 C Caddel, J. L., 137, 139, 160 Caldicott, J. J . B., 245, 256 Caldwell, A. G., 32, 44 Caldwell, R. M . , 211, 231, 242, 261 Calvert, D. V., 290, 302, 315, 321 Campbell, C. A., 232, 256 Campbell, F. R., 25, 26, 39, 41 Campbell, L. L., 269, 320 Campbell, M. H., 113, 123 Camel, R. Q., 96, 112, 121 Carasso, F. M., 254, 257 Carden, E. L., 49, 60, 74 Carles, J., 232, 234, 257 Carlise, A,, 20, 41 Carpenter, A. I., 311, 312, 313, 321 Carpenter, L. V., 279, 320 Carreker, J. R., 28, 44 Carter, D. L., 30, 31, 41 Carter, J., 273, 276, 320 Carter, 0. G., 218, 221, 240, 244, 260 Carter, R. L., 28, 44 Casserly, L. M., 235, 257 Cate, R. B., 298, 299, 310, 312, 320, 32 1 Cathey, H. M., 130, 160, 243, 257 Catt, J. A., 282, 320 Cereijido, M., 173, 202 Chadwick, M. J., 298,320 Chailakhian, M. Kh., 129, 160 Chakravart, S. N . , 7, 41 Chambers, L. A., 282, 323 Chambers, S. C., 239, 257 Chance, B., 197, 202 Chandler, W. V., 6, 9, 44 Chang, S. C., 19, 41 Chang, S. L., 21, 43 Changeux, J. P., 183, 206 Chapman, F. M . , 235, 257 Chapman, S. L., 286, 322 Chappell, J. B., 197, 198, 202 Charles, A. H., 106, 121 Chase, S. S., 137, 161 Chattopadhyay, N. C., 233, 256 Chavan, V. M., 141, 142, 143, 145, 160 Chavda, D. H., 143, 160

382

AUTHOR INDEX

Chenery, E. M., 268, 311, 320 Cherernukhina, L. F., 236, 262 Chiang, M. S., 141, 143, 144, 145, 160 Ching, T. M., 57, 73 Chinoy, J. J., 233, 260 Chizhova, S. I., 246, 261 Chlyah, H., 244, 257 Chowdhury, S. L., 241, 257 Christensen, C. M., 374, 377 Christianson, A. G., 20, 27, 29, 45 Clark, C. S.,278, 320 Clark, H. E., 129, 160 Clarke, J. S., 284, 320 Clarke, N. A., 21, 43 Clement, C. R., 94, 98, 120 Coats, R. E., 60, 61, 73, 74 Coenradie, J., 222, 232, 257, 263 Cohen, J. M., 20, 45 Cole, C. V., 9, 41, 190, 202 Coleman, N. T., 287, 320 Collander, R., 165, 166, 180, 186, 203 Collins, D. L., 102, 121 Collins, F. C., 145, 160 Colmer, A. R., 279, 280, 290, 320, 325 Combremont, R., 302, 321 Compton, L. E., 211, 231, 242, 261 Connell, W. E., 269,320 Cook, A. H., 332, 375 Cook, D., 90, 120 Cook, R. L., 371, 376 Cooke, G. W., 31, 38, 41 Coombe, D. E., 48, 73 Cooper, C. F., 23,41 Cope, J. T., Jr., 52, 53, 57, 5 8 , 59, 60, 61, 63, 64, 65, 66, 67, 73 Corbett, D. C. M., 81, I21 Corey, R. B., 2, 5 , 9, 14, 24, 32, 40, 41, 43, 44 Cosgrove, D. J., 8, 41 Coster, H. G. L., 170, 203 Coulter, B. S., 287, 320 Coulter, J. K., 286, 306, 307, 311, 312, 313, 317, 320 Courtice, A. C., 187, 206 Coutinet, S., 267, 320 Cowen, W., 17, 40, 41 Craig, D., 287, 320

Cram, W. J., 165, 166, 167, 173, 174, 175, 176, 177, 178, 188, 189, 191, 203 Creel, J. M., 54, 70, 74 Crenshaw, J. S., 272, 319 Crornwell, R. O., 63, 76 Cross, M. W., 94, 97, 98 113, 121 Cross, 0. E., 33, 42 Crowder, L. V., 54, 73 Cruzado, H. J., 126, 136, 137, 138, 152, 156, 161 Cseh, E., 187, 202 Culp, R. L., 21, 43 Czeratzki, W., 81, 84, 85, 88, 121

D Dahms, R. G., 217, 224, 257, 328, , 335, 337, 338, 350, 364, 366, 367, 368, 369, 372, 373, 377 Dahnke, W. C., 367, 371, 372, 378 Dainty, J., 167, 169, 172, 175, 178, 179, 203, 205 Dale, I. R., 275, 321 Dalton, L. C., 158, 160 Das, K. C., 218, 225,257 Daurn, R. M., 30,31,42 Davies, J. M. L., 245, 257 Davis, A. R., 180, 190, 204, 207 Davis, D. B., 282, 320 Davis, F. L., 5 8 , 59, 73 Davis, J. H., 275, 276, 321 Davis, R. F., 179, 204 Dawkins, P. A., 101, 122 Dawson, M. G., 102, 120 Dawson, R. N., 96, 120 Day, A. D., 219, 220, 222, 238, 242, 254, 257, 351, 375 Day, P. R., 355, 376 Debruck, J., 94, 96, 98, 101, 102, 108, 112, 121 DeCillis, E., 73 Defalque, J., 240, 259 de long, G. Y., 241,259 DeKock, P. C., 165,205 Delhaye, R. J., 240, 257 Delouche, J. C., 57, 74 Den Hartog, C. T., 347,375 Dennis, R. E., 360, 375

AUTHOR INDEX Derr, H. B., 365, 375 Deters, D. W., 195, 206 Dew, D. A., 373, 375,376 De Wit, C . T., 84, 93, 96, 105, 109, 113, 114, 120 Diamond, J. M., 166, 172, 185, 186, 187, 201, 203 Dickason, E. A., 369, 371, 372, 376 Dickey, D. D., 83, 120 Dickson, A. D., 219, 222, 257, 328, 332, 334, 335, 337, 338, 341, 346, 347, 350, 351, 352, 361, 364, 366, 367, 368, 369, 372, 373, 375, 376, 377 Dickson, J. G., 334, 366, 373, 375, 376, 377 Diercks, R., 241, 257 Dilley, R.A., 197, 203 Dilz, K., 233, 241, 257 Dion, H. G., 9, 42 Dixon, I. J., 246, 260 Dodds, J. J . A., 195, 203 Dodds, M. E., 373, 376 Doemel, W. N., 3 16, 321 Doggett, H., 159, 160 Dorningo, C. E., 241, 261 Dommergues, Y.,302, 321 Donald, C. M., 255, 257 Donelly, E. D., 52, 53, 56, 57, 58, 59, 60, 61, 63, 64, 65, 67, 73, 75 Dorofeev, V. F., 210, 228, 257 Doster, D. H., 114, 121 Doubleday, G. P., 291, 321 Down, E. E., 351, 371, 375, 376 Downes, R. W., 137, 160 Driessen, P. M . , 267, 277, 309, 310, 321 Drolsom, P. N . , 143, 160 Dudal, R., 292, 321 Dudinskii, Ya. A., 216, 257 Dudley, J. W., 147, 161 Duggar, J. F., 48, 59, 65, 66, 73, 74 Dumenil, L., 372, 375 Duncan, D. W., 280,321 Duncan, W . G., 240, 257 Dungan, G. H . , 371, 372, 377 Dunharn, K., 271, 321 Dunklee, D. E., 32, 33, 43 Dunlop, J., 171, 203 Dunn, I. G., 278, 321 Durand, J. H., 267, 320, 321 During, C., 94, 97, 98, 113, 121

383

Dyke, G. V., 237, 257 Dzydevich, G. S., 8, 42

E Eadie, G. S., 180, 203 Eckerrnan, G., 190, 191, 202 Eckert, H., 244,246, 256 Eckert, R. E., 107, I21 Edelman, C. H., 286, 321 Edwards, D. G., 165, 205 Edwards, W. M., 19, 20, 23, 24, 25, 26, 30, 39, 40, 44 Eguchi, H., 221, 258 Ehlers, W., 85, 86, 97, 98, 108, 120, 121 Ehrlich, H. L., 280, 321 Eisenrnan, G., 166, 185, 187, 189, 199, 201, 203 Eitel, J., 244, 262 Ekrnan, G., 253, 258 Elkins, D. M., 5 5 , 74 Elliott, I . L., 32, 42 Elliott, J. R., 48, 56, 76 Ellis, B. G., 31, 42 Ellis, F. B., 96, 112, 121, 122 Ellis, R. J . , 33, 42, 195, 203 Elrod, J. M., 56, 74, 75 Elzarn, 0. E., 181, 187, 197, 203 Emery, F. C., 66, 74 Emery, K. O., 272, 322 England, J. M., 96, 122 Ephrat, J., 247, 257 Epstein, E., 164, 165, 166, 173, 180, 181, 182, 183, 186, 187, 203, 205, 206, 207 Erdrnan, L. W., 59, 67, 74 Erickson, A. E., 31, 42 Eslick, R. F., 358, 359, 376 Esteves, I. A., 225, 257 Etherton, B., 166, 170, 171, 175, 177, 178, 182, 203, 204 Evans, A. C., 82, I21 Evans, C. E., 20,41 Evans, E. M . , 49, 74 Evans, H., 286, 288, 300, 312, 313, 321, 322 Evans, L. T., 129, 140, 161 Evans, R. A., 101, 107, 121 Evans, T. D., 8, 44

384

AUTHOR INDEX

Evans, W. J., 195, 202 Everson, A. C., 107, 121

F

Fuller, W. H., 12, 42 Furbish, W. J., 284, 321 Furrer, 0. J., 239, 240, 258

G Fairbanks, G. E., 104, 111, 122 Fajersson, F., 241, 257 Faris, D. G., 233, 259 Favilli, R., 50, 68, 74 Fayemi, A. A,, 5 5 , 74 Fergus, E. N., 57, 74 Ferguson, F. A., 21, 42 Ferguson, G. E., 5 , 3 6 , 4 2 Ferguson, H., 236, 256, 257 Fiddian, W. E. H., 233, 257 Fippin, E. O., 26, 42 Fisher, D. W., 23, 41 Fisher, J. D., 167, 193, 194, 196, 203 Fletcher, A. W., 281, 321 Floyd, R. A., 189, 206 Folt);n, J., 239, 257 Foote, B., 164, 203 Foote, W. H., 369, 371, 372, 376 Ford, H. W., 289, 290, 302, 315, 321, 325

Forneris, F., 240, 257 Forsberg, R. A., 251, 260 Fosberg, F. R., 273, 321 Foster, A. E., 347, 351, 358, 360, 361, 366, 368, 376, 377 Foster, R. J., 166, 170, 171, 182, 204 Foth, H. D., 240, 259 Foury, A., 48, 74 Fox, R. H., 12.42 Foy, C. D., 298,321, 324 Fraase, R. G., 331, 333, 376 Freeman, J. F., 96, 122 French, S. A. W., 228, 240, 263 Freney, J. R., 315, 323 Frey, K. J., 219, 220, 224, 229, 247, 248, 251, 252, 253, 257, 260, 261, 351, 371, 375, 376 Fried, M., 166, 180, 182, 186, 203, 206 Frink, C. R., 18, 38, 39, 42, 287, 289, 321

Fripiat, J. J., 9, 42 Frohner, W., 245, 257 Froidment, F., 239, 257 Friichtenicht, K., 234, 258 Fruh, E. G., 32, 40, 43

Gabelman, W. H., 355,376 Gadet, R., 232, 234, 257 Galkovskaya, L. T., 226, 258 Garber, L. F., 78, 121 Garcia-Casal, J., 267, 324 Gardner, C. O., 159, 161 Gardner, F. P., 243, 258 Gardner, W. R., 5 , 42, 107, 121 Gareth Jones, D., 245, 257 Gastuche, M. C., 9, 42 Gately, T. F., 221, 237, 258 Gauch, H. G., 164, 182, 204 Gburek, W. J., 16, 43 Gee, R., 195, 196, 201, 205 Geering, J., 241, 258 Geiszler, G. N., 369, 376 Gerechter-Amitai, Z., 247, 257 Gerhart, J. C., 183, 204 Gerson, D. F., 171, 182, 204 Giglioli, M. E. C., 276, 321 Gilbertson, C. B., 33, 42 Gill, J. B., 61, 74 Gilles, K. A., 362, 363, 375 Glass, R. L., 346, 347, 351, 360, 377 Gleen, H., 280, 321 Glob, P. W., 268, 321 Glynne, M. D., 217, 237, 245, 258 Gobin, C. A., 284, 320 Gotz, A., 241, 256 Golden, J. D., 306, 323 Goldina, S. M., 245, 260 Goldman, D. E., 179, 204 Gorbunov, N. I., 8, 42 Gore, A. J. P., 20, 42 Goring, C. A. I., 11, 42 Goulden, C. H., 250, 258 Graebner, P., 48, 73 Graff, O., 82, 121 Grafius, J. E., 211, 229; 231, 242, 250, 251, 258 Graham, D., Jr., 150, 161 Grama, A,, 247, 257 Grant, C. J., 306, 315, 321 Grant, M., 190, 191, 202

AUTHOR INDEX

Grantham, A. E., 66, 74 Grass, L. B., 289, 321 Graves, J. S., 179, 204 Greaves, M. P., 11, 42 Green, D. E., 197, 204 Green, H. B., 64, 75 Greenland, D. J., 11, 42 Gregory, P. H., 217, 258 Grinchenko, A. L., 218, 219, 263 Grissom, D. B., 360, 376 .Grootenhuis, J. A., 237, 258 Gruener, N., 195, 204, 206 Guenzi, W . D., 96,121 Guild, W. J., 82, 121 Gulline, H., 165, 166, 177, 178, 207 Gustafsson, A., 21, 22, 23, 31, 41, 253, 258 Guy, H. P., 5, 36, 42 H Haarhoff, K. N., 197, 198, 202 Hadiiselimovif, S., 233, 242, 258 Hansel, H., 224, 225, 228, 250, 258 Hageman, R. H., 147, 161 Hagen, C. E., 166, 180, 182, 203, 204 Halevy, A. H., 222, 261 Haley, L. E., 372, 377 Hall, J. L., 193, 195, 204 Hallgren, G., 283, 326 Hallock, D. L., 109, 121 Hamilton, D. G., 224, 225, 226, 247, 250, 258 Hamner, K. C., 129, 161 Hanapel, R. J., 12, 42 Hancock, N. I., 214, 224, 230, 231, 258 Handley, R., 166, 181, 187, 204, 2u5 Hanks, R. J., 91, 120 Hanley, F., 238, 258 Hannapel, R. J., 186, 187, 205 Hansen, D., 167, 193, 196, 203, 205 Hanson, J . B., 164, 187, 195, 196, 197, 203, 204, 205, 355, 376 Hansson, G., 195, 196, 201, 204 Harada, T., 302, 303, 319 Harbor, A. R., 66, 75 Hardan, A,, 271, 321 Harlan, H. V . , 236, 258, 328, 335, 336, 365, 366, 373, 376

385

Harlan, J. R., 328, 332, 335, 337, 338, 350, 364, 366, 367, 368, 369, 372, 373, 377 Harmsen, G. W., 282, 283, 315, 321, 324 Harrington, J . B., 219, 228, 230, 258 Harris, R. A., 197, 204 Harris, R. F., 8, 9, 10, 11, 13, 14, 15, 16, 17, 18, 19, 20, 34, 36, 40, 42, 44, 45 Harris, R. H., 346, 347, 362, 375, 376 Harrold, L. L., 90, 92, 121 Hart, G. E., 133,162 Hart, M. G. R., 283, 298, 300, 311, 312, 313, 321 Harvey, C., 144, 161 Hasche, D., 282, 290, 322 Hashimoto, T., 216, 222, 235, 258 Hathaway, J. C., 270, 325 Haunold, A., 259 Haupt, W., 128, 161 Hawke, M. F., 240, 263 Hayes, J. D., 242, 258 Hayes, 0. E., 27, 28, 43 Hays, S. B., 63, 64, 73, 74, 75 Heald, W . R., 16, 43 Heath, S . B., 240, 263 Heitefuss, R., 245, 258 Helmer, J . C., 57, 74 Hem, J. D., 38, 45 Hemwall, J. B., 7, 42 Hendricks, H. E., 59, 66, 74 Hendricks, S. B., 129, 130, 138, 161, 189, 190, 204 Henriksen, J. B., 238, 258 Henson, P. R., 66, 74 Herbillion, A. J., 284, 286, 321 Herndon, L. K., 279, 320 Hernes, O., 235, 258 Herzog, R., 81, 84, 93, 94, 96, 101, 120, 121 Hesketh, J. D., 137, 138, 161, 162 Hess, D. C., 229, 231, 249, 251, 258 Hesse, P. R., 282, 305, 321 Hetting, L. J., 23, 40, 42 Heyland, K U., 226, 230, 241, 256, 258 Hiatt, A. J., 186, 187, 189, 190, 200, 204

386

AUTHOR INDEX

Higinbotham, N., 164, 165, 166, 167, 169, 170, 171, 174, 175, 176, 177, 178, 179, 180, 182, 203, 204, 205, 206 Hill, A. V., 184, 204 Hill, D. D., 57, 73, 291, 322 Hillsman, G. A., 107, 123 Hingston, F. J., 9, 42 Hinkle, M. E., 279, 290,320 Hirano, J., 221, 258 Hirth, C. R., 8, 43 Hoag, B. K., 369, 376 Hoagland, D. R., 164, 167, 180, 190, 204 Hockett, E. A., 358, 376 Hodges, T. K., 166, 167, 182, 184, 187, 188, 190, 193, 194, 195, 196, 197, 198, 203, 204, 205 Hofstee, B. H. J., 180, 204 Holienka, J., 249 258 Holland, R. F., 151, 162, 355, 376 Holliday, R., 240, 242, 258 Hollingworth, S. E., 285, 321 Hollis, J. P., 303, 304, 321, 324 Hollowell, E. A., 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 59, 60, 61, 63, 64, 66, 67, 68, 74, 75, 76 Holmes, M. R. J., 255, 258 Holmes, N. D., 232, 258 Holoien, M. O., 362, 363, 375 Holt, C. L. R., Jr., 32, 40, 43 Holt, E. C., 66, 74 Holt, R. F., 12, 17, 25, 27, 29, 39, 43, 44, 45 Hood, A. E. M., 102, 113, 121 Hoogerkamp, M., 107, I21 Hooker, A. L., 355, 376 Hope, A. B., 164, 165, 179, 202, 204 Hopkins, H. T., 180, 182, 204 Hopkins, J. W., 371, 372, 376 Hore, F. R., 30, 31, 41 Horn, M. E., 286, 322 Horowitz, C. T., 195, 196, 204 Horsfall, J . G., 355, 376 Hoveland, C. S., 49, 54, 55, 60, 70, 74 Howard, A., 251, 258 Howard, G. L. C., 251, 258 Howell, D. R., 360, 375 Howse, K. R., 96, 122 Hozyo, Y., 216, 232, 258, 259

HruSka, L., 249, 258 Hsi, C. H., 347, 376 Hsu, P. H., 7, 8, 9, 17, 42 Huang, P. M., 371, 377 Hudson, L. E., 351, 361,377 Huffman, E. O., 7, 42 Hull, R., 237, 259 Hullinger, D. L., 20, 44 Humphries, E. C., 218, 221, 240, 243, 244, 246, 255, 259 Hungerbiihler, K., 216, 262 Hunt, L. A., 341,376 Hunter, H., 364, 376 Hunter, W., 32, 40, 43 Hunzicker, R. R., 32, 44 Hurd, E. A., 226, 236, 259 Hurd, R. G., 200, 205 Hyder, D. U., 107, 121

I Igel, H., 81, 94, 121 Il’inskaya-CentiloviE, M. A., 254, 259 Intalap, P, 236, 257 Ireland, C. F., 5 8 , 75 Iseri, K. T., 2, 43 Ishiwara, T., 302, 323 Islam, A., 267, 322 Ittihadieh, F., 30, 31, 42 Iwata, I., 302, 319

J Jackson, E. B., 254, 257 Jackson, M. L., 6, 7, 9, 19, 27, 28, 41, 42, 43, 44, 369, 371, 372, 376 Jackson, P. C., 164, 182, 187, 204, 205 Jackson, W. A., 298, 305, 322 Jacob, F., 183, 206 Jacobson, L., 166, 167, 181, 182, 186, 187, 189, 190, 200, 205, 206 Jacoby, B., 190, 193, 195, 196, 205, 206 James, A. L., 286, 291,322 James, E., 52, 56, 58, 68, 74 Jameson, A. K., 282, 320 Janitzky, P., 271, 322 Jankovi6, M., 219, 220, 252, 259 Jarvis, R. H., 238, 258 Jaworski, N. A., 23, 40, 42

AUTHOR INDEX

Jeffery, J. W. O., 311, 312, 313, 321 Jellum, M. D., 242, 230, 251, 259 Jennings, D. H., 164, 205 Jennings, P. R., 355, 376 Jensen, A. T., 291, 323 Jensen, H. L., 279, 322 Jensen, L. A., 57, 73 Jensen, N. F., 252, 259 Jeroch, H., 244, 246, 256 Jeschke, W. D., 188, 205 Jevtit, S., 239, 240, 259 Joffe, J. S., 279, 322 Johansen, C., 165, 205 Johansson, G., 285, 322 Johnson, H. P., 5 , 6, 15, 24, 42 Johnson, J., 272, 319 Johnson, V. A., 252, 255, 259, 355, 376 Johnson, W . H., 114, 115, 116, 122 Johnston, A. E., 313, 322 Johnston, W. R., 30, 31, 42 Johnstone, W. C., 57, 7 4 Jones, G. D., 84, 93, 94, 107, 108, 116, 121, 298, 324 Jones, J. N., 90, 91, 97, 98, 100, 101, 121 Jones, L. W., 282, 320 Jongmans, A. G., 278,324 Jonker, J. J., 241, 259 Jonsson, E., 283, 326 Jordan, D. O., 11, 42 Jordan, H. D., 267, 322 Jordan, J. W., 303, 324 Jouan, B., 240, 259 Juday, C., 24, 38, 42 Juncu, A. M., 225, 260 Jung, J., 218, 244, 245, 246, 259, 262 Juusela, T., 289, 290, 324 K Kafkafi, U., 9, 11, 18, 42 Kahn, J. S., 187, 205 Kahnt, G., 93, 94, 97, 98, 121 Kalk, M., 275, 278, 322 Kambal, A. E., 141, 143, 145, I61 Kanapathy, K., 300, 313, 322 Kanaris-Sotiriou, R., 286, 307, 3 11, 3 17, 318, 320 Kapelyushnikova, L. M., 246, 261

387

Kaplan, I. R., 272, 322 Kapp, L. C., 66, 74 Karchi, Z., 241, 244, 245, 246, 259, 262 Karilchi, Z., 247, 257 Karper, R. E., 126, 127, 132, 136, 141, 143, 145, 147, 148, 149, 151, 152, 153, 155, 156, 158, 161, 162 Katz, P. C., 331, 376 Kaufmann, M. L., 254, 259, 366, 368, 376 Kay, B. L., 107, 121 Keay, R. W., 275, 322 Kedem, O., 167, 205 Keenan, T. W., 167, 193, 196, 204 Kelly, D. P., 269, 270, 282, 322, 325 Kelso, W . I., 267, 283, 287, 290, 325 Kendall, P. F., 281, 322 Kenny, R., 57, 7 4 Kensel, N. A., 280, 322 Kephart, L. W., 48, 54, 55, 57, 67, 74 Kerns, K. R., 129, 160 Keulemans, N. C., 139, 161 Keup, L. E., 7, 8, 22, 38, 42, 43 Khramysheva, L. I., 230, 259 Kiesling, R. L., 211, 258 Kiesselbach, T . A., 126, 161 Kight, T. G., 49, 61, 74 Kilgore, B. W., 66, 74 Kincade, R. T., 106, 110, 114, 121 King, D. F., 276, 321 King, H. M., 166, 181, 187, 205 Kinra, K. L., 240, 259 Kirby, B. W., 106, 121 Kirby, E. J. M., 233, 239, 259 Kirby, J. S., 141, 143, 145, 161 Kirkham, D., 96,123 Kitasato, H., 180, 205 Kittrick, J. A., 7, 42 Kivenen, E., 312,322 Kivi, E. I., 222, 259 Kleinzeller, A., 171, 206 Kline, C. K., 96, 122 Kluesener, J., 34, 42 Kneen, E., 328, 332, 334, 335, 346, 376 Knight, A. H., 165, 205 Knight, W. E., 49, 50, 51, 52, 53, 54, 55, 56, 57, 60, 61, 63, 64, 66, 67, 68, 69, 70, 71, 74, 75, 76 Knoblauch, H . C., 6, 28, 43 Koch, E. J., 298, 324

AUTHOR INDEX

388

Koch, K., 235, 259 Koehler, W. A., 268, 278, 279, 283, 291, 325 Koenig, R. F., 373, 377 Kohli, S. P., 210, 224, 231, 247, 251, 252, 259, 260 Kohnke, H., 92, 121 Kolodny, L., 6, 28, 43 Koltay, A., 234, 259 Konzak, C. F., 252, 263 Kopeck$, M., 237,259 Koshland, D. E., 166, 183, 184, 189, 194, 198, 201, 205 Koval'skil, V. V., 236, 259 Kramer, N. W., 141, 143, 145, 162 Krantz, B. A., 233, 262 Kroetz, M. E., 92, 122 Kucera, H. L., 374, 377 Kuipers, H., 80, 121 Kumazawa, K., 302,323 Kunishi, H. M., 10, 14, 15, 16, 17, 40, 43, 44 Kylin, A., 195, 196, 201, 204, 205 Kyzlasov, V . G., 231, 259

L Lahav, N., 9, 43 Lahr, K. A., 141, 143, 145, 162 Laidlaw, H. C., 371, 377 Lakshmanarn, C., 288, 322 LaMaster, J. P., 66, 75 Lambert, J. W., 347, 376 Landesman, J., 280, 321 Lane, H. C., 126, 130, 139, 161 Lang, A., 129, 161, 371, 372, 377 Langbein, W. B., 2, 43 Langdale, G. W., 107, 120 Langford, W. R., 66, 75 Langston, R., 13, 43 Larsen, J. E., 13, 43 Larson, R. I., 232, 258 Larson, W. E., 91, 95, 96, 101, 121, 122, 123 Laties, G. G., 165, 182, 189, 200, 203, 205, 207 Latterell, J. J., 12, 17, 43, 45 Laude, H . H., 219, 220, 222,259, 261 Lawton, G. W., 32, 40, 43 Leathen, W. W., 279, 322

Lee, B., 187, 206 Lee, G. F., 1, 17, 32, 40, 41, 43 Lee, H . S., 69, 75 Lefebre-Drouet, E., 288, 322 Leggett, J. E., 180, 182, 204, 205 Lejeune, A. J., 347, 371, 377 Lekes, J., 219, 250, 254, 259, 263 Lelley, I., 237, 259 Lemaire, J. M., 240, 259 Leng, E. R., 147, 161 Leonard, R. T., 166, 167, 182, 184, 193, 194, 195, 196, 198, 204, 205 Leopold, A. C., 126, 129, 132, 135, 161 Le Roux, N . W.,281, 282, 322 Lesch, S. F., 243, 259 Lessman, L. J., 150, 161 Levitzki, A., 183, 205 Lewis, W. M., 110, 11 1, 121 Liang, G. H., 141, 142, 143, 144, 145, 161, 162 Lienhard, M., 57, 74 Likens, G. E., 23, 41 Lillard, J. H., 90 91, 97, 98, 100, 101, 121, 122 Lim, S. M., 57, 75 Lindsay, W. L., 7, 43 Lineweaver, H., 180, 205 Linser, H., 243, 260 Lipman, J. G., 279, 322 Lips, S. H., 200, 207 Little, J. W., 360, 375 Lockard, R. G., 301, 322 Loe, R., 301, 325 Lofgren, J. R., 360, 377 Lolko, A. N . , 236, 260 Loneragan, J. F., 165,205 Lorenz, W. C., 278, 322 Lorrirnore, J. C., 32, 44 Lovato, A., 234, 244, 260 Love, R. M., 48, 76 Lowe, L. B., 218, 221, 240, 244, 260 Lowery, J. C., 66, 75 Lucas, W. J., 200, 205 Luke, C. L., 3 17, 322 Lund, E. J . , 167, 205, 207 Lund, Z. F., 298,319 Lundeglrdh, H., 190, 205 Lundgren, D. G., 280,325 Lupton, F. G. H., 350, 351, 375

AUTHOR INDEX Luttge, U., 176, 182, 205, 206 Lynn, W. C., 285, 322

M Maas, G., 226, 244, 246, 260 McCalla, T. M., 33, 42, 96, 119, 121, 122 McCarty, P. L., 3, 21, 32, 40, 43 McCaughey, W. F., 242, 257 Maclean, L. E. R., 244,260 McClure, J. W., 144, 161 MacDonald, I. R., 165, 205 McDonald, M. J., 8, 9, 45, 232, 258 MacEachern, C. R., 371, 372, 375 McFadden, A. D., 366, 368, 376 Machado, W. C., 64, 75 McIntyre, L. D., 279, 322 McKee, G. D., 8, 43 McKee, R., 54, 56, 75 Mackenthun, K. M., 1, 2, 8, 43 McKercher, R. B., 8, 9, 43, 44 Macklon, A. E. S., 175, 177, 178, 205 McLean, E. O., 288,322 McLean, H. C., 279, 322 MacLennan, D. H., 195, 205 Macnae, W., 275, 278, 322 McNeal, F. H., 252,256 MacRobbie, E. A. C., 164, 167, 169, 171, 172, 173, 174, 175, 176, 191, 192, 205 Maddens, K., 244, 260 Madison, K. M., 279, 322 Magistad, 0. C., 298, 322 Mahapatra, I. C., 306, 323 Malkani, T. J., 250, 260 Manning, S . H . , 210, 217, 260 Marchant, W. H., 233, 235, 260 Marchlewitz, B., 282, 290, 322 Marinos, N. G., 164, 20bi Martens, D. C., 84, 93, 94, 97, 108, 116, 121, 122 Martin, F. J., 291, 322 Martin, J. P., 12, 43, 300, 322 Martin, K. H., 221, 244, 260 Martini, M. L., 328, 335, 336, 376 Mashtakov, S. M., 245, 260 Maslyanaya, M. K., 236, 259 Mason, J. L., 235, 257 Massey, H. F., 6, 27, 28, 43, 279, 319

389

Matchett, R. W., 359, 377 Matelski, R. P., 7, 44 Matz, S. A., 363,377 May, R. F., 278, 322 Mayr, H. H., 243, 260 Mayton, E. L., 49, 74 Mehard, C. W . , 197, 206 Meijer, C. L. C., 182, 202 Mellor, J. W., 281, 323 Melville, G. E., 315, 323 Mendel, G., 146, 161 Meredith, W. 0 . S., 341, 346, 347, 351, 361, 362, 369, 370, 371, 375, 377 Metwally, A., 187, 204 Met'zler, D. F., 21, 43 Micke, A., 253, 262 Middleton, F. M., 21, 43 Midgley, A. R., 32, 33, 43 Mielke, H., 210, 217, 260 Mielke, L. N., 32, 44 Mikala, F., 239, 257 Mikolenko, T. A., 216, 257 Miladinovic, N., 218, 221, 260 Milifa, .C. I., 225, 260 Millar, C. E., 32, 43 Millar, W. E., 38, 40, 43 Miller, F. L., 126, 136, 137, 138, 139, 152, 156, 161, 229, 235, 250, 260 Miller, L. P., 271, 323 Miller, R. B., 20, 43 Minshall, N. E., 25, 26, 39, 40, 43, 45 Mishra, D. N., 250, 260 Mi%, T., 242, 256 Misra, K. P., 235, 261 Misra, R. D., 233, 255, 260, 262 Mitchell, P., 197, 198, 201, 206 Mitsui, S., 302, 323 Miyake, K., 323 Mohan, Ram, H. Y . , 246, 260 Moldenhauer, W. C., 5, 6, 15, 24, 42 Money, N. S., 267,325 Monod, J., 183, 206 Moody, J. E., 90, 100, I21 Moore, C. L., 197, 206 Moore, D. P., 186, 187, 205, 271, 319 Moore, H. I., 210, 245, 260 Moore, R. P., 60, 75 Moorman, F. R., 267, 274, 305, 306, 310, 323 Morey, D. D., 233, 235,260

390

AUTHOR INDEX

Morley, F. H. W., 56, 75 Morris, V. H., 218, 232, 263 Morrison, D., 238, 256 Morton, J. F., 302, 323 Moschler, W. W., 84, 93, 94, 97, 100, 107, 108, 109, 116, 117, 121, 122 Mosconi, C., 233, 254, 261 Moseman, J. G., 328, 332, 335, 337, 338, 350, 364, 366, 367, 368, 369, 372, 373, 377 Moser, F., 58, 75 Motomura, S., 303, 323 Mott, P. A., 60, 74 Mott, R. L., 186, 207 Mukherjee, K. K., 210, 224, 231, 247, 251, 252,259, 260 Mulder, E. G., 218, 221, 222, 223, 225, 232, 233, 234, 235, 236, 260, 289, 323 Muljadi, D., 9, 43 Mulleriyawa, R. P., 302, 325 Multamaki, K., 224, 226, 228, 229, 260 Murakami, H.,282, 323 Murdock, J. T., 8, 11, 44 Murphy, H. C., 229, 247, 248, 251, 253, 260 Murphy, J. V., 197, 207 Murray, R., 246, 260 Murthy, K. N., 141, 161 Musick, G. J . , 102, 121 Muszynska, K., 251, 262 Mutatkar, U. K., 288, 323 Myhre, D., 362, 375

N Naftel, J. A., 52, 57, 58, 75 Nagal, K., 253, 260 Nagur, T., 141, 161 Nair, T. J., 267, 323 Nambiar, E. P., 267, 323 Nanda, K. K., 137, 161, 233, 260 Napier, E., 282, 323 Nasr, H. G., 251, 260 NBtr, L., 225, 254, 260 Navasero, S. A,, 298, 299, 300, 301, 305, 325 Neal, 0. R., 6, 43 Neckers, J. W., 315, 323

Neirinckx, L. J . A., 165, 176, 206 Nelson, C. E., 240, 260 Nelson, D. W., 27, 39, 43 Nelson H., 195, 206 Nelson, N., 195, 206 Nerncek, O., 171, 206 Neucere, N. J., 195, 202 Neumann, J., 195, 204,206 Newbould, P., 96, 122 Nhung, M. M., 299, 300, 303, 306, 314, 323 Nichols, M. S., 25, 26, 39, 40, 43, 45 Niehaus, N. H., 141, 144, 145, 161 Nightingale, G. J., 235, 260 Nilan, R. A., 351, 377 Nilsson, H. E., 216, 260 Nilsson, L. G . , 233, 260 Nishimura, S., 243, 260 Nissen, P., 166, 182, 184, 206 Nitsch, J. P., 140, 161 Njgis, A., 237, 260 Nobel, P., 191, 206 Noggle, J. C., 180, 182, 203, 206 Norden, A. J . , 219, 220, 224, 229, 251, 252, 257, 260, 261 Norstadt, F. A., 96, 121, 122 Norum, E. B., 369, 370, 371, 372, 377, 3 78 Nuttall, A. M., 245, 256 Nykvist, N., 17, 43 0 Oberlander, H. E., 182, 203 Oda, K., 211, 212, 216, 219, 224, 228, 229, 230, 231, 232, 250, 259, 261, 262 Ogata, G., 271, 323 Ohle, W.,1, 43 Ohlmeyer, D. W., 363,377 Ohlsson, I., 239, 256 Okajirna, H., 302, 323 Olien, C. R., 328, 332, 335, 337, 338, 350, 364, 366, 367, 368, 369, 372, 373, 377 Olsen, S. R., 9, 41, 43 Olson, P. J., 219, 220, 262, 347, 369, 370, 371, 377 Olson, W. J., 334, 341, 344, 376, 377

AUTHOR INDEX

Ordin, L., 167, 182, 189, 190, 200, 205, 206 Orlovsky, N. V., 271, 325 Osborne, W. E., 360, 375 Osmond, C. A., 108, 110, 122 Osterhout, W. J. V., 166, 167, 180, 206 Ota, Y., 302, 326 Otzen, D., 282, 283, 315, 324 Overstreet, R., 166, 181, 186, 187, 204, 205, 206 Owen, R. E., 107, 121 Ozanne, P. G., 13, 43

P Paden, W. R., 58, 59, 75 Page, N. R., 58, 59, 75 Pal, B. P., 253, 254, 261 Paleev, A. M . , 210, 261 Pallaghy, C. K., 165, 166, 173, 176, 177, 178, 206, 207 Pallas, J. E., 96, 120 Palmer, C. M., 21, 43 Palmer, R., 282, 320 Pape, G., 92, 97, 98, 108, 113, 120, I21 Paquet, J., 246, 253, 261 Pardee, A. B., 183, 204 Park, J. K., 64, 75 Park, Y. D., 302, 323 Parker, D. T., 83, 91, 95, 98, 100, 101, 122 Parker, E. M., 54, 73 Parker, F. W., 12, 44, 63, 64, 76 Parker, M. C., 57, 73 Parr, J. F., 289, 323 Parr, S. W., 279, 324 Parrish, L. P., 8, 43 Pasela, E., 233, 261 Patanothai, A., 126, 141, 143, 151, 161 Patrick, R., 289, 325 Patrick, W. H., 269, 299, 306, 320, 323 Patterson, F . L., 21 1, 224, 231, 242, 256, 261 Patterson, R. M., 59, 61, 75 Pauli, A. W., 142, 162, 219, 220, 222, 259, 261 Pearson, R. W., 58, 75, 297, 319 Pecrot, A., 284, 286,321 Pedersen, E. J. N., 247, 261 Peev, H., 244,261

391

PeiIakhov, U. I., 234, 256 Pendleton, J. W., 219, 220, 223, 261, 263, 371, 372, 377 Penniston, J. T., 197, 204 Penny, A., 237,241,263 Penth, B., 182, 206 Penzhorn, E. J., 243, 259 Peperzak, P., 32, 44 Percival, J., 216, 226, 232, 239, 249, 261 Peters, D. C., 355, 376 Peters, R. A., 102, 106, 122 Petersen, L., 290, 291, 318, 323 Peterson, A. E., 32, 40, 43, 362, 363, 3 75 Peterson, G. A,, 347, 351, 356, 357, 360, 361, 366, 368, 369, 376, 377 Peterson, L. K., 232, 258 Petinov, N. S., 219, 231, 249, 261 Petr, F., 229, 247, 248, 251, 253, 260 Petr, J., 244, 246, 261 Petrov, G., 242, 261 Pfeifer, R. P., 347, 359, 377 Pham, H-A., 306, 323 Phillips, R. E., 90, 94, 95, 108, 120 Phillips, S. H., 90, 120 Phillips, W. M . , 105, 110, 118, 122 Phinney, B. O., 133, 161 Picard, J., 69, 75 Pickett, R. C., 141, 144, 145, 160, 161 Pierce, R. S., 23, 41, 165, 166, 174, 175, 176, 177, 178, 179, 206 Pierre, W. H., 12, 44 Pieters, A. J., 48, 51, 75 Pikush, G. R., 218, 219, 263 Piland, J. R., 58, 75 Pillsbury, A. F., 30, 3 1, 42 Pinck, L. A., 11, 44 Pinthus, M. J., 218, 222, 226, 228, 231, 244, 245, 254,261, 262 Pirjol, L., 225, 260 Pitman, M. G., 165, 174, 175, 176, 177, 178, 180, 187, 188, 199, 200, 206 Pitts, R. G., 303, 323 Poehlman, J. M., 373, 375 Poelman, J. N . B., 266, 268, 315, 323 PolBIek, J., 244, 246, 261 Polya, G. M., 167, 190, 195, 202, 206 Pomeranz, Y . , 373, 377

392

AUTHOR INDEX

Ponnamperuma, F. N., 299, 300, 301, 303,306,308, 314,323 Ponornarenko, A. D., 253, 261 Ponomarev, V. I., 210, 257 Pons, L. J., 273, 274, 277, 278, 286, 310, 314, 315, 316, 317, 320, 323, 324 Poole, R. J., 171, 177, 178, 182, 188, 189, 204, 206 Pope, M. N., 328, 335, 313, 376 Posner, A. M., 9, 11, 18, 42, 43 Postgate, J. R., 269, 270, 271, 302, 320, 324 Potts, E. C., 66, 74 Poux, N., 193, 206 Powell, A. R., 279, 324 Powell, J. D., 49, 73 Powell, R. W., 96, 122 Power, J. F., 91, 120 Pratt, G. L., 373, 374, 378 Prescott, J. A., 9, 44 Presoly, E., 243, 260 Preston, J. B., 61, 75 Price, P. B., 328, 332, 335, 337, 338, 350, 364, 366, 367, 368, 369, 312, 373, 377 Primost, E., 218, 243, 261 Prince, A. L., 187, 202 Pringsheim, E. G., 289, 324 Pritchard, A. J., 68, 75 Pritchett, W. L., 288, 323 Prokudina, P. I., 245, 260 Prowse, G . A., 315, 324 Pruden, G., 267, 283, 287, 290, 316, 317, 324, 325 Prusakova, L. D., 231, 246, 261 Puustjarvi, V., 289, 290, 324 Pyatygin, A. V., 235, 242, 261 Pykhtin, N. I., 218, 219, 263

Q Quinby, J. R., 126, 127, 128, 131, 135, 136, 137, 138, 139, 140, 142, 143, 144, 145, 147, 148, 151, 152, 155, 156, 157, 158, 162 Quirk, J. P., 9, 11, 18, 42, 43 Quispel, A., 282, 283, 315, 324

132, 141, 149, 161,

R Rachie, K. O., 158, 162 Racker, E., 195, 206 Raheja, P. C., 218, 225, 235,257, 261 Rains, D. W., 166, 181, 182, 186, 189, 191, 192, 203, 206 Rarnage, R. T., 359, 377, 378 Rarnaswamy, K. R., 225, 226, 261 Rampton, H. H., 48, 53, 55, 67, 75 Randolph, N. M., 64, 75 Rao, V. P., 136, 160 Raven, J. A., 167, 191, 192, 200, 206 Rasmussen, K., 279, 290, 291, 318, 323, 324 Rasrnusson, D. C., 346, 347, 351, 360, 377 Ratner, A., 193, 195, 196, 206 Raven, J . A., 167, 191, 192, 200, 206 Raychaudhuri, S. P., 267, 324 Read, D. W. L., 232, 256 Reddy, T. V., 136, 160 Reed, J. K., 64, 75 Reichard, T., 245, 261 Reicosky, S. C., 288, 322 Reid, D. A,, 298, 324, 328, 332, 335, 337, 338, 350, 364, 366, 367, 368, 369, 372, 313, 377,378 Reisenauer, H. M., 58, 75 Rennie, D. A., 9, 44 Rhixon, L., 95, 122 Rhoades, M. M., 355,376 Rich, C. I., 9, 44 Richards, P. W., 275,324 Rickard, D. T., 271, 272, 274, 324 Rittenberg, S. C., 272, 322 Rizk, S. G., 271, 319 Robbins, C. W., 30, 3 1, 41 Robeck, G. G., 27, 29, 45 Roberts, H. A., 101, 122 Roberts, S., 240, 260 Roberts, W. M. B., 271, 324 Robertson, D. W., 373, 377 Robertson, L. S., 240, 259, 371, 376 Robertson, R. N., 164, 165, 190, 191, 197, 202, 206, 207 Robins, J. S.,241, 261 Robinson, G. S., 94, 97, 98, 113, 121 Robinson, R.,113, 122

AUTHOR INDEX

Rocquero de Laburu, C., 267, 324 Rodger, J. B. A., 224, 238, 261 Rodriguez-Kabana, R., 303, 304,321,324 Rogers, H. T., 6, 44, 52, 57, 68, 70, 75 Rohlich, G. A,, 1, 44 Roman, A., 252, 261, 262 Roman, T., 251, 262 Romkens, M. J. M., 27, 39, 43 Rorison, I. H., 297, 301, 305, 324 Rosenbusch, H. K., 341,377 Rosene, H. F., 167, 207 Rosevear, D. R., 275, 324 Ross, C., 190, 202 Roth, C. B., 9, 44 Rotunno, C. A., 173, 202 Rowland, H., 347,377 Roy, A. B., 269, 271, 324 Ruckenbauer, P., 246, 262 Rudich, J., 218, 241, 244, 245, 259, 261, 2 62 Rudolphs, W., 279, 324 Ruhm, E., 84, 8 5 , 88, 121 Russell, E. J., 9, 44 Rustagi, P. N., 246, 260 Rutger, J. N., 347, 351, 352, 377 Ryden, J. C., 8, 9, 10, 11, 13, 14, 15, 16, 17, 18, 20, 34, 36, 40, 42, 44 S

Sachs, R. M., 232, 262 Saddler, H. D. W., 177, 178, 180, 188, 206, 207 I Sadler, W. R., 282, 324 Sage, G. C. M., 233,262 Sagher, A., 19,44 Salisbury, F. B., 129, 140, 162 Sallans, H. R., 341, 346, 347, 361, 375 Salmon, S. C., 229, 262 Salt, G. A., 240, 245, 262 Salt, J. K., 298, 320 Sandal, P. C., 69, 75 Sarkissian, I. V., 133, 162 Sato, J., 303, 326 Saunders, W. M. H., 6, 8, 44, 45 Savory, H. J., 276, 324 Sawhney, K. L., 233, 260 Sawyer, C. N., 2, 21, 44 Scarascia, Mugnozza, G. T., 233, 253, 254, 256, 262

393

Scarseth, G. D., 6, 9, 44 Schafer, J. F., 211, 231, 242, 261 Schaller, C. W., 347, 351, 352, 377 Scheltema, W., 288, 324 Schertz, K. F., 132, 133, 135, 148, 162 Schilling, G., 244, 246, 256 Schmidt, B. L., 90, 92, 114, 122 Schmidt, D., 55, 75 Schmidt, J. W., 239, 240, 252, 256, 259 Schonbrunner, J., 245, 261 Schooler, A. B., 358, 359, 376, 377 Schraufnagel, R. H., 32, 40, 43 Schultz, J. E., 218, 262 Schwarta, D., 282, 290, 322 Schwerdtle, F., 81, 96, 101, 102, I22 Scott, B. I. H., 165, 166, 173, 176, 177, 178, 206, 207 Scott, C. O., 9, 41 Scott, E. S., 284, 320 Scott, N. M., 8, 9, 45 Sears, R. D., 109, 121 Sechler, D. T., 224, 226, 228, 250, 252, 262 Seidl, S. F., 341, 377 Sell, 0. E., 54, 73 Semikhov, V. F., 235, 242, 261 Sethi, K. L., 224, 231, 247, 251, 252, 259, 260 Sexton, R., 195, 207 Sfat, M. R., 341, 377 Shah, R., 6, 7, 44, 45 Shands, H. L., 229, 231, 249, 251, 258, 260, 334, 364, 373, 376, 377 Shands, R. G., 328, 332, 335, 337, 338, 350, 364, 366, 367, 368, 369, 372, 373, 377 Shanholtz, V. O., 90, 91, 100, 101, 122 Shapiro, R. E., 180, 203 Sharma, K. C., 233, 255, 260, 262 Shaw, W. C., 328, 332, 335, 337, 338, 350, 364, 366, 367, 368, 369, 372, 373, 377 Shear, G. M., 84, 93, 94, 97, 98, 100, 107, 108, 109, 117, 121, 122 Shellenberger, J. A,, 334, 346, 377 Shen, M. J., 9, 44 Shepherd, W. D., 204 Sherman, M. S.,11,44 Shiori, M., 303, 324 Shipp, R. R., 7, 44

3 94

AUTHOR INDEX

Shrivastava, M. M. P., 235, 262 Shukla, S. S., 18, 44 Sieglinger, I. B., 144, 162 Sigler, K., 171, 206 Sigurbjornsson, B., 253, 256, 262 Sillampla, M., 233, 262 Simpson, E. C., 19, 20, 23, 24, 25, 26, 30, 39, 40, 44 Singer, L., 187, 207 Singh, B., 250, 262 Singh, V. P., 255, 260 Sioli, H., 267, 324 Sirohi, G. S., 233, 260 Sisler, W. W., 219, 220, 262, 351, 377 Skopik, P., 226, 262 Skorda, E. A., 235, 244, 262 Skou, J. C., 188, 192, 193, 196, 207 Skuciikka, B., 225, 262 Slager, S., 278, 324 Slater, E. C., 197, 207 Slayman, C. L., 179, 207 Smika, D. E., 91, 122 Smillie, G. W., 9, 19, 44 Smith, D. D., 5 , 45 Smith, E. L., 104, 107, 122, 214, 224, 230, 231, 258, 350, 351, 377 Smith, F. A., 200, 205, 207 Smith, J. D., 141, 143, 144, 145, 160 Smith, K. E., 5 5 , 75 Smittenberg, J., 315, 324 Snellgrove, R. A., 284, 320 Sokolski, S., 9, 42 Solomon,A. K., 172, 203 Sombatpanit, S., 268, 306, 307, 324 Sommers, L. E., 11, 44 Soper, R. J., 371, 377 Soubies, L., 232, 234, 257 Southern, B. L., 267,325 Spahr, K., 226, 228, 235, 262 Spanswick, R. M., 179,207 Spencer, W. F., 289,325 Sprague, G. F., 355,376 Sprout, P. N., 284, 320 Staltenberg, H. A., 21, 43 Standridge, N. N., 373, 377 Stanford, G., 372, 375 Stanley, R. L., 64, 75 Starling, T. M., 298, 324 Stauffer, W., 239, 240, 258 Steers, J. P., 274, 325

Stelly, M., 58, 61, 73 Stephens, J. C., 61, 75, 141, 143, 145, 151, 162 Stephens, S. G., 355, 376 Stephenson, H. F., 7, 43 Stevens, P. G., 165, 204 Steward, F. C., 186, 189, 207 Stewart, F., 49, 52, 58, 62, 66, 75 Stewart, K. M., 1, 44 Stewart, R. K., 22, 38, 43 Stibbe, E., 118, 122 Stickler, F. C., 104, 111, 122, 142, 162 Stief, K. J., 164, 187, 205 Stitt, R. E., 56, 75 Stoltenberg, N. L., 6, 27, 28, 44 StranBk, A., 96, 122 Streeter, J. G., 347, 377 Strutsovskaya, E. S., 225, 228, 230, 247, 262 Sturnm, W., 8, 44 Sturm, H., 218, 244, 245, 259, 262 Suan, L-T., 23 1, 249, 262 Subramoney, N., 267, 323 Sukhai, A. P., 298, 299, 310, 320 Sullivan, S. L., 69, 75, 76 Sullivan, W. T., 20, 44 Sumpter, N. A., 133, 162 Suneson, C. A., 328, 332, 335, 337, 338, 350, 358, 364, 367, 368, 369, 372, 373, 377 Surganova, L. D., 230, 234, 256, 262 Sutcliffe, J. F., 164, 195, 200, 205, 207 Sutton, P., 108, 110, 122 Suzuki, M., 216, 224, 228, 229, 230, 250, 261 Swanson, N. P., 32, 44 Syers, J. K., 6, 7, 8, 9, 10, 11, 13, 14, 15, 16, 17, 18, 19, 20, 34, 36, 40, 42, 44, 45 Sylvester, R. 0.. 20, 23, 30, 31, 35, 44 Syme, 1. R., 218, 262 Szabolcs, I., 271, 325

T Tabatabai, M. A., 317, 325 Takagi, S., 302, 323 Takahashi, Y.,302, 319 Takijima, Y.,300, 325 Takimoto, A., 130, 162

395

AUTHOR INDEX

Talibudeen, O., 7, 41 Tammen, J., 355, 376 Tanada, T., 303, 324 Tanaka, A., 298, 299, 300, 301, 302, 303, 305, 323, 325 Tash, I. C., 38, 40, 43 Taylor, A. W., 2, 10, 14, 15, 16, 17, 19, 20, 23, 24, 25, 26, 30, 38, 39, 40, 43, 44 Taylor, T. H., 57, 73, 96, 104, 107, 122 Teakle, L. J. H., 267, 325 Teetes, G. L., 64, 75 Teichmann, W., 236, 263 Temple, K. L., 268, 278, 279, 280, 283, 291, 325 Templeton, W. C., 96, 104, 107, 122 Teorell, T., 169, 172, 207 TeterjatEenko, K. G., 254, 259 Thampi, P. S . , 267, 325 Thimann, K. V., 140, 144, 162 Thomas, G. W . , 28, 44, 94, 95, 97, 108, 120, 122 Thomas, J. G., 63, 64, 76 Thomas, R. C., 179, 207 Thompson, J. G., 268, 325 Thompson, R. K., 238, 242, 254, 257 Tirnmons, D. R., 12, 17, 25, 27, 29, 39, 43, 44 Timoshenko, S., 214, 262 Tippens, H. H., 63, 64, 7 6 Tomlinson, T. E., 92, 94, 122, 275, 299, 325 Toole, E. H., 55, 76 Toosey, R . D., 107, 113, 122 Torii, K., 182, 200, 207 Trafford, B. D., 267, 283, 287, 290, 325 Triplett, G. B., 90, 92, 93, 94, 97, 100, 107, 108, 109, 110, 114, 115, 116, 121, 122 Troughton, A., 226, 234, 236, 262 Trudinger, P. A., 269, 271, 282, 324, 325 Triiper, H. G . , 270, 325 Tuite, J. F., 374, 377 Tunik, B. M., 8, 42 Tuovinen, 0. H., 282,325 Turk, L. M., 32, 43 Turkova, N. S., 231, 236, 249, 262 Turner, J. S . , 190, 207 Turner, P. D., 298, 306, 325 Twenhofel, W. M., 37, 45

U Uctum, S., 216, 262 Udagawa, T., 211, 212, 216, 219, 224, 228, 229, 230, 231, 250, 261, 262 Ullah, S . M., 267, 322 Ulrnann, L., 241, 262 Ulrich, A., 189, 190, 200, 207 Unger, P. W., 118, 122 Unz, R. F., 280, 325 Upadhyaya, B. R., 360, 377 Urmantsev, Ju. A., 219, 249, 261 Ussing, H. H., 165, 167, 169, 172, 207

V Vaadia, Y . , 182, 200, 204, 207 Vaidya, S. M., 250, 260, 262 Virnos, R., 302, 303, 325 van Beers, W. E. J., 266, 286, 325 van Breemen, N., 277, 278, 283, 284, 285, 286, 287, 289, 307, 310, 311, 316, 319, 325 van den Honert, T. H., 166, 180, 207 van der Kevie, W., 267, 273, 274, 275, 286, 293, 295, 310, 311, 324, 325 Van Doren, D. M., 90, 93, 94, 97, 100, 108, 109, 110, 114, 115, 116, I22 Van Duin, R. H. A,, 91, 122 van Holst, A. F., 292, 296, 325, 326 Van Keuren, R. W., 107, 121 Vann, J. H., 276,325 Van Ouwerkerk, C., 84, 85, 88, 122 van Staveren, J. M., 286, 321 Van Wijk, W. R., 91, 101, 122 Varghese, T., 267, 325 Vasey, E. H., 12, 41, 369, 370, 371, 372, 375, 378 Vasil’eva, L. N., 236, 262 Vasington, F. D., 197, 207 Vaughn, C. E., 56, 76 Venkateswarlu, P., 187, 207 Venturi, G., 234, 244, 260 Verhoop, J. A. D., 325 Verner, A. R., 271, 325 Vetter, H., 236, 241, 263 Vez, A., 82, 84, 113, 122, 123, 238, 263 Vieillefon, J., 267, 307, 325, 326 Vielvoye, L., 284, 286, 321 Viets, F. G., 186, 207

396

AUTHOR INDEX

Vikitenko, Z. I., 231, 263 Vlamis, J., 190, 207 Voelcker, W. M., 37, 45 Vogel 0. A., 217, 252, 254, 256 Vogel, S. L., 374, 378 Voigt, R. L., 137, 138, 162 Vollenweider, R. A., 1, 3, 19, 45 von Gliemeroth, G., 54, 76 von Horn, A., 48, 76 von Willert, K., 176, 206 Voorhees, E. B., 65, 66, 76 Vorobiev, L. N . , 170, 207 Vullioud, P., 84, 113, I23 W Wadsworth, M. E., 282, 326 Wagner, D. F., 367, 371, 372, 378 Wahhab, A., 235,263 Waisel, Y.,195, 196, 204 Waksman, S. A., 279, 322 Walden, C. C., 280, 321 Waldschmidt, U., 84, 87, 93, 96, 120 Walker, A. L., 271, 324 Walker, C. R., 315, 323 Walker, J. M., 12, 41 Walker, M. E., 233, 235, 260 Walker, R. B., 282, 320 Walker, T. W., 6, 7, 8, 19, 44, 45 Walton, G., 21, 43 Wang, W. C., 14, 45 Waring, G. A,, 38, 45 Warren, G. F., 13, 43 Warshaw, C. M., 284, 326 Wa?, L., 228, 250, 251, 263 Watanabe, F. S., 9, 43 Watson, C. A., 373, 374, 378 Watson, D. J., 228, 240, 263 Watson, J. G., 275, 276, 326 Watts, J. C. D., 267, 305, 326 Way, J. T., 30, 45 Waywell, C. G., 219, 228, 230, 258 Wear, J. I., 58, 59, 76 Weaver, J. C., 328, 378 Weaver, R. N . , 16, 43 Webb, B. K., 64, 75 Webb, R. M., 81, 121 Webber, L. R., 25, 26, 39, 41 Webster, H. L., 54, 70, 74 Webster, 0. J., 141, 143, 145, 161

Weeks, D. C., 190, 207 Weibel, D. E., 137, 139, 141, 160 Weibel, R. O., 219, 220, 223, 263 Weibel, S. R., 20, 21, 27, 29, 34, 35, 36, 45 Weidner, R. B., 20, 21, 29, 45 Weigl, J., 176, 182, 190, 206, 207 Weiss, J., 233, 263 Welch, L. F., 107, 123 Welch, R. M., 182, 207 Wellensick, S. J., 128, 162 Wellhausen, H. W., 49, 61, 74 Welton, F. A., 218, 232, 263 Werkhoven, C. H., 92, 121 Westerveld, G. J . W., 292, 296, 325, 326 Westgate, J. M., 48, 54, 66, 76 Wexelsen, H., 68, 76 Wheeler, J. L., 113, 123 White, D. E., 38, 45 White, E., 16, 20, 45 White, E. J., 20, 41 White, J. L., 6, 27, 28, 44 White, R. W., 10, 45 Whitear, J. D., 238, 258 Whittig, L. D., 271, 285, 322 Wick, H., 241, 257 Wicks, G. A., 91, 106, 122, 123 Widdowson, F. V., 237, 241, 263 Wiebe, G. A., 328, 332, 335, 337, 338, 350, 359, 364, 365, 366, 367, 368, 369, 372, 373, 376, 377, 378 Wier, D. R., 12, 45 Wiese, A. F., 91, 118, 120, 122 Wiggans, S . C., 243, 258 Wiklander, L., 283, 326 Wilke, J., 25, 26, 39, 45 Wilkins, M. J., 190, 207 Wilkinson, S. R., 107, 123 Wilkinson, W., 82, 123 Willey, R. W . , 240, 263 Williams, C. H., 315, 323 Williams, E. G., 6, 8, 9, 45 Williams, G. R., 197, 202 Williams, J. A., 9, 41 Williams, J. C., 351, 352, 377 Williams, I. D . H., 7, 8, 9, 11, 18, 19, 44, 45 Williams, R. J. B., 31, 38, 41, 241, 263 Williams, W. A., 48, 56, 76

397

AUTHOR INDEX

Willis, W. O., 90, 91, 96, 120, 123 Wilmouth, R. R., 84, 93, 94, 108, 116, 121 Wilson, D. G., 282, 320 Wilson, J. R., 60, 74 Wilson, M. J., 11, 42 Wilten, W., 222, 232, 257, 263 Wischmeier, W. H., 5 , 45 Witchalls, J. T., 240, 244, 263 Witt, P. R., Jr., 332, 363, 378 Witzel, S. A., 25, 26, 39, 40, 43, 45 Wolf, F. A., 63, 76 Wolfe, R. S., 289, 326 Woo, S. C., 252, 263 Wood, R. A,, 282,323 Woods, W. R., 33, 42 Woodward, R. L., 21, 34, 35, 36, 43, 45, 234, 263, 368, 369, 378 Wright, B. C., 233, 255, 260, 262 Wright, E. M., 166, 185, 186, 187, 201, 203 Wroot, H. E., 281,322 Wiinsche, U., 243, 244, 255, 263 Wyatt, R., 299, 323 Wybrew, J. E., 114, I23

Y Yamada, N., 302, 326 Yarnane, I., 303, 326

Yasu, T., 302, 325 Yawalkar, K. S., 218, 225, 235, 257, 262 Yokoi, H., 303, 323 Yoshida, H., 221, 258 Yoshida, S., 302, 303, 325 Youker, R. E., 90, I21 Young, K. B., 32,40,43 Young, R. A., 372,377 Youngner, V. B., 244, 256 Yuan, T. L., 287,326 Yuan, W. L., 303, 323 Yueruer, N., 97, 123

Z Zadontsev, A. I., 218, 219, 263 Zaumeyer, W. J., 355,376 ZeniHEeva, L. S., 219, 230, 250, 251, 252, 254, 259, 263 Zhivotkov, L. A., 251, 263 Zimina, T. K., 224, 230, 263 Zioni, A. B., 200, 207 Zohary, M., 48, 76 Zsoldos, F., 303, 326 Zubriski, J. C., 367, 369, 370, 371, 372, 377, 378 Zuur, A. J., 31 1, 326

Subject Index

A

D

Absorption root, ions, 163-207 Accumulation ratio, 165-170 Active ion transport, 167-180 Agopyron repens, 106, 107 Ahiocho, 302, 303 Aluminum, 298-300, 305

Dallisgrass, 61 Diabrotica longicornis, 102 Diffusion potential, 178-180, 200 Digitaria ischaemum, 102 Digitaria sanguinalis, 106

E

B

EPTC, 63 S-Ethyl dipropylthiocarbamate, 63 Eyespot, 216-217, 236, 245

Bahiagrass, 61, 67 Banana, 298 Barley, lodging in, 209-263 malting, 327-378 Bermudagrass, 60, 61, 67, 107 Boron, 58 Brassica fodder, 107, 113, 117 Breeding, lodging resistance, 246-254 malting, 327-3 7 8 Brusome, 303

F Flowering, genetics of, 127-129, 155 photoperiod, 136-137, 139 physiology of, 129-131, 155 temperature and, 137-138 Flux-ratio analysis, 172-178

G C

Calcium, 166, 181, 187 Cassava, 298 Cenchrus incertus, 111 Centrosema, 307 Cercospora zebrina, 63 Cercosporella herpotrichoides, 102, 216 Chloride, 187, 192 2-Chloroethyl trimethylammonium chloride (CCC), 218,223, 243-245,255 [(4-Chloro-o tolyl) oxy] acetic acid, 63 Chlorpropham, 62 Clover head weevil, 63 Copper, 306 Corn, 97, 100, 109, 114-117 Corn rootworm, 102 Cotton, 298 Crimson Clover, 47-76 Cymadothea trifolii, 63 Cynodon dactylon, 107 398

Genetics, crimson clover, 68-71 growth, of, 132-136 malting barley, 350-360 sorghum, 125-162 Gibbsite, 287 Grazing land, 65-66 companion crops, 61-62 Green manure, 66-67 H

Herbicides, lodging effect, 243-246 weed control, 62-63, 104-106, 118 Helminthosporium sativum, 356 Helminthosporium teres, 356 Hybrid vigor, 126 genetic control, 146-151 morphological effects, 141-146

399

SUBJECT INDEX

Hydrogen sulfide, 302-304 Hypera meles, 63, 64 Hypera nigrirostris, 63

I Ion absorption, 163-207 Iron, 300-301 Irrigation, 241-242 Isopropyl carbanilate, 62 Isopropyl m-chlorocarbanilate, 62

J Jarosite, 283-284, 285 Johnsongrass, 61

K Kudzu, 61

L Lamium amplewicaule, 62 Lespedeza, 61 Lesser clover weevil, 63 Liming, 313-314 Light, ion transport, 191 Lodging, 209-263 Loose smut, 356, 365

M Magnesium, 193 Maize, 109, 114-117 Malting barley, 327-378 Malting process, 332-334 Malt, uses of, 334-335 Manganese, 301 Mangrove, 273, 275-277 MCPA, 63

N Nernst equation, 169-172 Net blotch, 356 Nitrogen, grain yield, 371-372 lodging relationship, 233-235, 236, 24 1

soil distribution, 94-95, 108-109 0

Oats, 98, 112 lodging in, 209-263 Ochre, 289-290 Ophiobolus graminis, 102, 216

P Panicum dichotomifiorum, 106 Pasture renovation, 106-107 Phosphorus, 235 absorption of, 97-98 acid sulfate soil, 305-306 runoff, 1-45 soil distribution, 93-94, 108 Photoperiod, temperature, 54-55 Pineapple, 306 Pisum sativum, 128 Plant breeding, 156-160 Plant growth, acid sulfate soils, 296-307 genetics of, 132-136 zero-tillage effects, 95-103 Pollution, mines and spoil, 291-292 Potassium, 171, 178, 181, 184, 194, 235 legume crops, 58 nutrient absorption, 97-98 soil distribution, 93-94 Prediction test, 361-362 Propham, 62 Putcinia graminis tritici, 356 Pueraria, 307 Pyritic soils, 265-326

R Rhizophora, 275-277 Rice, 266, 298-299, 300, 301, 302-303, 306, 309 Root, ion absorption, 163-207 Rose clover, 56 Ryegrass, 61

S Sclerotinia rrifoliorum, 54, 63 Septoria passerinii, 356

400

SUBJECT INDEX

Soil, acid sulfate, genesis and management of, 265-326 mapping, 293-296 moisture, 87-91 organic matter, 82-84, 94 phosphorus, 7-14 structure, 80-8 1, 84-87 tilled and untilled compared, 80-95 Sorghum bicolor, 110, 126 Sorghum, genetic control of, 125-162 Soybean, 110 Spot blolch, 356 Stem rust, 356 Straw, decomposition, 82-83 Straw strength, 214-216, 228-229 Sugar beet, 112 Sugar cane, 300 Sulfides, formation of, 267-278 oxidation of, 278-290

T Temperature, ion absorption, 165 lodging and, 232-233 photoperiod and, 137-138 Tillage, 236-237 zero, 77-123 Tillering, 143

Trifolium hirturn. 56 Trifolium incarnatum, 48, 50 Trifolium vesiculosum, 49

U Universal Soil Loss Equation, 5 Vstilago nuda, 356, 365

V Vernalization, 54

W Water, phosphorus in runoff, 1-45 soil moisture, 87-91, 96 Waterlogging, 308-3 1 1 Watershed, agricultural runoff, 25-31, 39 forest runoff, 22-24 manured land, 32-33 urban runoff, 33-36, 40 Weed control, 62-63, 104-106, 118 Wheat, 97, 98, 110, 112 lodging in, 209-263

2 Zea mays, 126, 133, 146 Zero-tillage, 77-1 23

4

B S C D E F G H 1 J

6 7 B 9 O 1 2 3