Advances in Agronomy, Volume 23

ADVANCES IN

AGRONOMY VOLUME 23

CONTRIBUTORS TO THIS VOLUME

MARTINALEXANDER

J . G . CADY JOHN L. CREECH R. B. DANIELS C. L. FOY

E. E. GAMBLE M. G . HALE W. W. HECK

H. E. HECCESTAD CHARLES S. HELLINC YOSHIAKI ISHIZUKA PHILIP C. KEARNEY B. A. LAKHDIVE

ROBERT B. MUSCRAVE DALEN . Moss RAJENDRAPRASAD G . B. RAJALE LOUISP. REITZ F. J. SHAY

ADVANCES IN

AGRONOMY Prepared under the Auspices of the AMERICAN SOCIETY OF AGRONOMY

VOLUME 23

Edited by N. C . BRADY

Roberts Hall, Cornell University, Ithaca, New York ADVISORY BOARD

W. L. COLVILLE W. A. RANEY 1. J . JOHNSON J . R. RUNKLES R. B. MUSGRAVE G . W. THOMAS 1971

ACADEMIC PRESS

New York and London

COPYRIGHT 6 1971, BY ACADEMIC PRESS,h C . ALL RIGHTS RESERVED NO PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM, BY PHOTOSTAT, MICROFILM, RETRIEVAL SYSTEM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION PROM THE PUBLISHERS.

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LIBRARY OF CONQRESS CATALOG CARD

NUMBER: 50-5598

PRINTED IN THE UNITED STATES OF AMERICA

CONTENTS CONTRIBUTORS TO

VOLUME 23 ....................................................................

PREFACE.................................................................................................... ERRATA for Volume 22 .................................................................................

ix xi

xiii

PLANT GERM PLASM NOW A N D FOR TOMORROW JOHN L. CREECH A N D LOUISP. REITZ

......................................................... I. Introduction ...... II. Ill. IV. Where Germ Plasm Comes from ... V. Collecting and Assembling Germ P ........................... VI. Evaluation, Increase, and Maintena VII. How Germ Plasm Is Used VIII. Germ Plasm Collections ..._.............. IX.

i

4 6 9 12 17 24 37 45 47

THE RELATION BETWEEN GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D GENESIS R. B. DANIELS,E. E. GAMBLE, A N D J. G. CADY

I. II.

51

111. IV.

V. Summary ................................, ........................................................ References .......................................................................................

53 55 62 84 86

FACTORS AFFECTING ROOT EXUDATION M. G. HALE, C. L. FOY,A N D F. J. SHAY 1. 11.

Introduction ..................................................................................... History ...................................., ., . ., , ., ., ............................................ V

89 92

vi

CONTENTS

111.

IV V. VI. VII. VIII.

Sources of Exudate and Pattern of Root Exudation .......... Interactions of Organic Nitrogen Sources and Exudation ......................... Effects on Carbon and Nitrogen Balance in Plants ... Foliarly Applied Compounds and Root Exudation .................................. Root Exudation-Mineral Nutrient-Mi Effects of Environment on Root Exudation ...............................

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

93

95 95 97 101

I03 107

I07

NATURE, EXTENT, AND VARIATION OF PLANT RESPONSE TO AIR POLLUTANTS H. E. HEGGESTAD A N D W. W HECK 1. Introduction. ........................................................................ Nature of Plant Response ................................... I I I. Extent of Response ......... 1V. Variation in Rtsponse as R V. Discussion ............................................................................. V1. Summary .............................. References ............................................................................

Ill

11.

140

BEHAVIOR OF PESTICIDES IN SOILS CHARLES

s. HELLING,PHILIP c .

KEARNEY. AND

MARTIN

ALEXANDER

I. Introduction ................................... 11. Processes Affecting Pesticides in Soils

I l l . Effect of Pesticides on Soil Community ................................................ IV. Implications ................................... V. Summary ............ References .....................................

208

PHYSIOLOGY OF THE RICE PLANT YOSHlAKl I. II. 111. IV.

ISHIZUKA

Introduction ..................................................................................... Static Approach: Analytical Studies of the Growth of the Rice Plant ......... Dynamic Approach: Fundamental Research for Higher Yield .................. Conclusion .......... ........... References .......................................................................................

241

243 275 309 3 I0

CONTENTS

vii

PHOTOSYNTHESIS A N D CROP PRODUCTION D A L EN . Moss I.

II. IV. V. VI. V11. V I 11.

AND

ROBERTB. MUSCRAVE

itro iction ..................................................................................... Yield and Net Photosynthesis Breeding for Photosynthetic Efficiency ................................................ Selecting for Low I' Traits in High I' Species ...................... Selecting for Photosynthetic Rates within Species ................................ Breeding for Plant Type ........................................................ Managing Photosynthesis ...................................................................

17 3 I7 32 0 327 327 328 33 1 334 334

NITRIFICATION RETARDERS A N D SLOW-RELEASE NITROGEN FERTILIZERS R A J E N D RPRASAD. A G. B. RAJALE,A N D B. A. L A K H D I V E

............................................. ultural Chemicals ..... Nitrification Retarders .............................. Slow-Release Nitrogen ........................................ Coated Fertilizers ............................................................. Concluding Remarks ............. .................... ...............................................................................

337 342 345 358 37 I 375 376

Author Index .............................................................................................. Subject Index .............................................................................................

385 405

I. 111. IV. V. VI.

Introduction

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CONTRIBUTORS TO VOLUME 23 Numbers in parentheses indicate the pages on which the authors’ contributions begin.

MARTIN ALEXANDER ( 147), Department of Agronomy, Cornell University, Ithaca, New York J. G . CADY(5 l ) , Department of Geography and Environmental Engineering, The Johns Hopkins University, Baltimore, Maryland JOHN L. CREECH ( I ) , Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland R. B. DANIELS (5 I ) , North Carolina Agricultural Experiment Station, Raleigh, North Carolina C. L. FOV(89), Department of Plant Pathology and Physiology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia E. E. GAMBLE (5 I ) , North Carolina Agricultural Experiment Station, Raleigh, North Carolina M . G . HALE(89), Department of Plant Pathology and Physiology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia W. W. HECK( I I I), Environmental Protection Agency, North Carolina State University, Raleigh, North Carolina H. E. HEGGESTAD ( 1 I I), Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland CHARLESS . HELLING( 147), Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland YOSHIAKI ~ S H I Z U K A(24 I), Emeritus Professor, Hokkaido University, Japan; Asian and Pacific Council, Food and Fertilizer Technology Center, Taipei, Taiwan PHILIP C. KEARNEY ( 147), Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland B. A. LAKHDIVE (337), Division of Agronomy, Indian Agricultural Research Institute, New Delhi, India DALE N . MOSS (317), University of Minnesota, St. Paul, Minnesota ROBERT B. MUSGRAVE(3 17), Cornell University, lthaca, New York RAJENDRAPRASAD (337), Division ofAgronomy, Indian Agricultural Research Institute, New Delhi, India G . B. RAJALE(337), Division ofAgronomy, Indian Agricultural Research Institute, New Delhi, India LOUISP. REITZ( 11, Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland. F . J. SHAV(891, Department of Plant Pathology and Physiology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia ix

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PREFACE

I n recent years the value of science to society and in turn the obligation of society to support science have become widely questioned. Some national leaders have expressed the feeling, likely shared by many laymen, that science and technology are inherently evil. In their view, pressing human problems such as pollution, crime, and even poverty are caused directly or indirectly by technological developments. Students, joined by irate taxpayers, are concerned about the seeming irrelevance of most scientific endeavors. They see no pay-off to society from the public inputs supporting scientific research, and they are concerned with the apparent independence of scientists who follow their own disciplineoriented curiosities rather than addressing themselves to the solution of human problems. Fortunately, one has little difficulty justifying, even to the pragmatist, the benefits to society of agronomic research. The eight articles appearing in this volume exemplify this fact. Each of them reviews the state of knowledge on subjects of considerable importance to man. Concern with factors affecting the quality of the environment is demonstrated through reviews on pesticides in soils, plant response to air pollutants, and slowrelease nitrogen fertilizers. Man’s ability to feed himself is the direct or indirect concern of papers dealing with rice physiology, the world’s plant germ plasm base, and factors affecting photosynthesis and crop production. Two other papers concern the state of our knowledge of important soil and plant processes. I t is quite appropriate for the scientist to justify his existence to society as a whole and especially to those who support him and his work. Likewise, the scientist has an obligation to inform not only his immediate colleagues but the larger scientific community as well of his accomplishments and failures. Reviews such as those presented in this volume are important components of the world-wide scientific communication system. They represent the first step in fulfilling an important obligation of scientists to society. N . C . BRADY Ithaca, N e w York August, 1971

xi

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ERRATA Volume 22 Page 163, Eq. (3), the fraction 4/3 should he enclosed in parentheses Page 168, Eq. (7). the left-hand side should read: k + H ) ( a c / a r ) + c ( a H / a t ) ;helow Eq. (7). c ' should read c ' . ~ Page 168, line 12, the ratio y/H should be enclosed in parentheses Page 173, Eq. (15), the second term should read ( W u / L ) Page 187, Eq. (22). the second equals sign should he a minus sign Page 342, line 4 should read: This would equal 5.0 mg of Mg per 100 g of soil

...

Xlll

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ADVANCES IN

AGRONOMY VOLUME 23

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PLANT GERM PLASM NOW AND FOR TOMORROW John 1. Creech and Louis P. Reitz Agricultural Research Service, U.S. Department of Agriculture, Beltsville, Maryland

I. Introduction ..................................................................................... 11. Germ Plasm Definitions ..................................... .................................................... 111. Our Needs for Germ Plasm. ............................... IV. V A. Seed Germ P ......................... B. Vegetatively VI. Evaluation, lncre A. Small Grain

.................................................... VII.

VIII.

A.

Cereal Grains

C.

Horticultural

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

................................................... A. Number of Items .............................................................

IX. Programs for the Future ......................................

I.

I 4 6 9 12 14

IS 17 18 22 24 25 29 31

35 37 37 39 44 45 47

Introduction

Modern crop husbandry is based on an exceedingly small segment of the plant kingdom. These efficient crops are the cumulative results of man’s research. But in this generation and for the future, plant breeders will be dependent for raw materials on the genetic resources that occur in the “gene centers” of the world. Such centers may be the geographic origins of the parental species or cultivation centers where primitive varieties have been handed down and improved by farmers over generations. Many of these progenitor types and weedy relatives of crops have been the principal sources of pest resistance and unique traits essential to successful recent crop improvement. If they are allowed to be displaced 1

2

JOHN L. CREECH A N D LOUIS P. RElTZ

and destroyed, these genetic resources cannot exert their particular influence on modern plant breeding. These irreplaceable genetic resources are seriously threatened with depletion by overgrazing and related malpractices, or through the replacement of “land races” by improved varieties. This fact has not attracted the attention of enough scientists. The impact of such losses is difficult to relate to our immediate circumstances of high crop yields, and this has produced complacency. However, it does not require much imagination to appreciate the need for genetic diversity in the face of the current threat to production by serious diseases, such as corn leaf blight (Helminthosporium maydis), or the first discovery of leaf rust (Hemileia vastatrix) of coffee in the Western Hemisphere in January 1970. The latter disease eliminated coffee production in Ceylon prior to 1900 and caused a shift to tea production. Recognizing that these resources are essential to agriculture in developed and developing countries alike, international organizations such as the Food and Agriculture Organization of the United Nations (FAO), the International Biological Program ( I BP), and The Rockefeller Foundation have encouraged the development of national and international programs to attack the problem of dwindling germ plasm reserves. To emphasize this goal and lay the scientific foundations for action programs, an international Technical Conference was held in Rome, September 18-26, 1967, under the auspices of FAOlIBP ( I 967). The conferees proposed that there be greater coordination among nations concerned with the exploration, conservation, and utilization of plant resources for agriculture and forestry. This would include existing institutions, such as botanic gardens and arboretums, agricultural and forestry research stations, agencies dealing with seed distribution, and international organizations which undertake programs of agricultural development anywhere in the world. The recommendations urged surveys to determine plants that are threatened by imminent destruction in their natural habitats and by decline in existing collections. Such surveys would permit priorities to be established so that the species and areas of greatest danger of genetic erosion would receive first consideration. I t would be anticipated that the scientists with special knowledge of local and regional conditions with respect to special plant groups could be encouraged to provide the needed information. It was recommended that institutions engaged in the study of variation of plants serve as centers to train young scientists in the field of phytogeography, tactics of plant exploration and collection, and related matters as a means of developing facilities and staff for national and international

P L A N T GERM P L A S M N O W A N D FOR T O M O R R O W

3

centers for regional exploration activities in developing countries or groups of countries with common needs. Concern was also expressed for the development of improved systems of evaluation and exchange of primitive stocks and other cultivars so as to make these essential materials equitably available and to avoid excessive duplication of effort. This would require international accord for the treatment, storage, and retrieval of genetic information which is becoming of increasing significance as the available germ plasm expands and the evaluations become more complex. This will require specialists concerned with methods to standardize climatic, ecological, phytogeographic, and taxonomic data, as well as the basic plant characteristics which are to be considered for standardization. The conference encouraged national programs to protect genetic resources habitats and to develop seed banks by drawing up plans which would create programs for national germ plasm maintenance. The members recognized that sophisticated storages in every country are unrealistic and urged that those storages now in operation, or under construction, accept international responsibilities as an interim means of protecting germ plasm. The Society for Economic Botany, in cooperation with the International Biological Program (US1BP/U M), organized a symposium at Columbus, Ohio, on September 5 , 1968, to focus attention on the urgent need to protect, conserve, and properly utilize the world’s plant resources [see Econ. Bot. 23(4) ( 1 969)]. The Symposium was designed to support the recommendations of the 1967 F A 0 Technical Conference on Exploration, Utilization, and Conservation of Plant Gene Resources. It provided a forum for alerting a segment of the U.S. biological community to our dependence on foreign sources of crop germ plasm and the needs for national and international cooperation in rescuing and conserving these irreplaceable resources. Although much is known of the origins and centers of diversity of our crop plants, American biologists were asked to consider how best to sample this diversity, ways and means to utilize germ plasm, conserve it for the future, and be alert to opportunities for international cooperation in these efforts. The Symposium was prompted by the realization that the problem of dwindling germ plasm resources is not being attacked in the United States in a coordinated fashion. There are Federal and other agency programs involved with the introduction, evaluation, and conservation of crop germ plasm. Some of these have been in effect for many years and provide a basic service to American plant science, but they have not pooled their efforts for maximum impact on this broad problem. There has been some encouraging progress. Recently, a Crop Evolution Labora-

4

JOHN L. CREECH A N D LOUIS P. RElTZ

tory was established at the University of Illinois. The mission of this Laboratory is largely concerned with the origins and evolution of cultivated plants and their relationships to wild relatives. The work of the Laboratory will nicely complement action programs for the collection and objective evaluation of crop breeding stock. There are also provisions in the Plant Gene Pools objectives of US1 BPlUM to give leadership to this overall problem area and to develop national working groups to implement the broad recommendations of the International Biological Program. Thus, I BP is promoting international recognition of the problem and is providing a framework for more meaningful cooperation on a worldwide basis. The objectives that are realistic for specific action to be undertaken by scientists in the United States are as follows: 1. To conduct national surveys of primitive and wild genetic resources of plants held by institutions and scientists in the United States; and to identify the scope, quality, and usefulness of these gene resources; 2. To assemble, analyze, and retrieve this information through use of automatic data processing; and to disseminate results of the survey to I BP, FAO, Agency for International Development (AID), institutions and scientists here and in other nations; 3. To cooperate in national programs to use and perpetuate this base of genetic variability utilizing existing facilities and proposing additional ones; and to develop information on these resources from a genetic, agricultural, and other scientific standpoint and to fully exploit their diversity; 4. To participate with IBP, AID, and other institutions in developing priorities for urgent germ plasm collecting in threatened biological and geographical areas. In keeping with the concepts of these various recommendations, the present paper is an effort to describe the current activities that have an impact on the future of germ plasm in the United States. As a nation so dependent on the world’s plant resources for raw genetic materials, we are obligated to assume a leadership role in the use and conservation of these essential inputs to plant breeding. As scientists, we would indeed be less than responsible to future generations if we do not give high priority to measures that will protect these dwindling resources from deterioration. The paper serves also to identify the various agencies and institutions that have expressed a commitment to germ plasm. II.

Germ Plasm Definitions

Germ plasm has become a standard term in agricultural research. It has been employed most extensively in dealing with crop improvement.

PLANT GERM PLASM N O W A N D FOR TOMORROW

5

Crop germ plasm has been applied to individual donors of genetic traits at one extreme to large assemblages of breeding stocks at the other extreme. A number of related terms are beginning to appear in the literature, and it seems appropriate to attempt in this paper to define some of these terms as they relate to the use and conservation of the world’s plant resources. Crop germ plasm can be defined as the array of plant materials, assembled or not, that serves as a basis for crop improvement, or related research. In this sense, germ plasm is a generic term, but its chief characterization is that of a reservoir of genes to meet the needs of plant breeders. It allows for a range of plant materials that may be as narrow and specific or as broad and widely represented as is necessary to meet the objectives of the user. I t also implies documentation of the components and continuity of this material. Collections of germ plasm fall into two major categories. Working collections are held in adequate storage, documented, and available for immediate use. Working collections are usually specific crops and may acquire the title of a world collection when the number and geographical origin of accessions has reached such a magnitude as to result in worldwide requests for seed. Sometimes world collection implies a broadly represented collection even though there is no attempt to distribute samples. Conserved stocks are broad segments of germ plasm held in national and international seed storages for long-term conservation (conservation centers). These stocks duplicate working collections but are released only when the latter have been depleted. The flow of germ plasm is from holders of working collections to long-term storages. National seed storages accept all categories of germ plasm, have precise policies governing acceptance of seed, and attempt to provide the optimum temperature and humidity conditions to maintain seed viability for extended periods of time. In the United States the USDA’s National Seed Storage Laboratory, Fort Collins, Colorado, is a center for conserved stocks. A similar storage exists at the National Institute of Agricultural Sciences, Hiratsuka, Japan (Ito and Kumagai, 1969). FAO, in cooperation with the Turkish government has constructed a cold storage at Izmir, Turkey, to preserve the germ plasm collected throughout Turkey. Unlike the rather precise facilities which can be provided to protect reserves of seed-reproduced plants, working stocks of vegetatively propagated crops constitute our base of conserved materials. Because of the tremendous cost of holding vegetative stocks, duplication appears impractical. It is for this very reason that the loss or abandonment of these types of collections is so detrimental.

6

JOHN L. CREECH A N D LOUIS P. REITZ

I n contrast to the broad aspect of germ plasm, the term genetic stocks of crop plants, as defined by the Crop Science Society of America, is restricted to stocks of specific genes and gene combinations that have direct usefulness in genetic analysis. A characteristic of genetic stocks is that such materials frequently are maintained by individual workers. However, the Preservation of Genetic Stocks Committee, CSSA, is attempting to identify holders of genetic stocks and to encourage deposition of these stocks in the National Seed Storage Laboratory, Fort Collins, Colorado. A new encompassing germ plasm term was coined by the F A 0 Panel of Experts on Plant Exploration and Introduction (1970a). This is the genetic resources center. The purpose of delineating such centers is to provide for an umbrella-type organization to combine the objectives of long-term conservation (conservation center) and the propagation and distribution of plant materials held in one or more working collections. The essential requirements recommended by the F A 0 panel for the establishment and functioning of a genetic resources center include the following: A genetic resources center must provide for long-term conservation of seed and maintain vegetative collections. It should be operated by a professional staff with background and facilities for the propagation and distribution of germ plasm. These facilities do not need to be a physical part of the main center and one or more associated institutions with established collections could serve as subcenters. Because of the stringent quarantine safeguards necessary for international movement of plant materials, close collaboration with plant quarantine officials is essential. Some centers in countries out of the crop cultural range can serve as intermediate quarantine propagation stations in the manner that the Plant Introduction Station, Glenn Dale, Maryland, and Kew Gardens, England, do for coffee and cocoa, respectively. The center is responsible for organizing the increase of collections and arranging for the transfer of germ plasm from working collections to longterm storage. This will require methods for documenting and accumulating additional information. The center would be rzsponsible for providing data to a central information system at FAO, Rome. Ill.

O u r Needs for G e r m Plasm

Plants cover the land areas of the earth; some are found in the sea. In its totality, this embraces our heritage of germ plasm. Each organism owes its existence to the genes it contains which set in motion a train of events leading to its attained uniqueness. The value of germ plasm can only be equated with the magnitude of the benefits from plants to man’s total ex-

PLANT GERM PLASM N O W A N D FOR TOMORROW

7

istence and to the preservation of the environment in which he lives. I n recent years, man has realized that the latter engulfs the entire planet including our atmosphere. Most people do not regard germ plasm in such a broad setting, but think only of special needs for single, or a few, genes to utilize in reaching a momentary objective in plant breeding, or to find a new variant useful in achieving some particular goal. Yet, when the question is raised about what and how much we should be concerned, the list invariably grows and encompasses our entire flora. Even deleterious factors are sought as genetic markers or as a means to some positive goal. The world’s plants are the survivors of gene pools created by cross breeding, mutations, natural selection, or by other means. The germ plasm exists as recombinants, mostly in farmer’s seed in the case of cultivated crops; some exists in nature and some in living herbaria or collections. Under the dynamics of world change, the products of evolution and of plant breeding are quickly exploited over wide areas. One result seen repeatedly in cultivated crops is a dramatic change in the germ plasm comprising the cultivated species grown at the beginning and at t h e end of a single decade. This is now becoming applicable to every major agricultural country and in a more serious way, to developing nations. The recent highly successful transplantation of Mexico-derived wheat varieties to the Mideast and elsewhere totaling 20 million acres over a 5-year period is a good example of the extent of change. The United States, Mexico, Canada, and Australia may be cited where repeated replacement of contemporary wheat varieties by newer ones is an accepted pattern of agriculture. One thus has the option to discard or conserve the superseded varieties. Concern is often expressed that irreplaceable germ plasm is being lost. Of course, it is! The recent trend over large tracts of land whereby ancient varieties of local evolutionary development are being replaced by rather limited germ plasm, gives strong support to that concern. Land denuded by stripping off the timber or by overgrazing has erased irretrievable germ plasm. Further man-made improvement in crops through breeding will largely be traceable to genes extant in living herbaria or collections. Only at times of dire need do breeders supplement these by crash programs to collect breeding stocks among existing gene pools in the wild. More often they wait for, or hope to induce, the desired mutations. New crops are being sought to better serve man’s needs. Unless suitable germ plasm can be found which is amenable to the purpose and capable of manipulation to meet agronomic standards, these goals cannot be met. The range of worthwhile goals covers crops for medicinal purposes, industrial uses, pest repellents, and above all, nutritious foods. Research

8

JOHN L. CREECH A N D LOUIS P. REITZ

is being conducted on plants to find constituents for treatment and control of cancer; to discover new annual sources of fiber; to develop less hazardous insecticides; to extend the principle of biological resistance to more diseases and insect pests; and to provide new energy-trapping food plants to supplement those we have pushed almost to the limit. Established crops, such as sorghum, rice, wheat, maize, soybeans, and alfalfa, have been improved over the years by adding genes from alien sources to local or regional varieties. The objective has been to increase productivity, enhance stability, improve quality, and reconstruct plants to increase their physiological efficiency. Much work has gone into breeding for disease and insect resistance, and the need for new genes for this purpose is a continuing one. There is no better way than through genetic mechanisms to reduce losses from biological competition. Human population density is so great in certain areas and man’s dependence upon annual crop abundance so absolute that famine is axiomatic if we are faced with a major epiphytotic, if a new insect ravages the crops, or if planted crops are destroyed by other natural catastrophes. So, man’s dependence now on stable crops and his growing need for every greater volume of food production leaves little place for complacency about germ plasm both in the short and long views. Our need for germ plasm preservation has immediate and long-term aspects, and it varies considerably among the species. Some species are utilized in the wild form, vis., native grassland, timber, tundra, and some tree nut crops. For these to become extinct is conceivable since it is not feasible to preserve these materials with the same ease as for beans, oats, or clover. However, as we encroach on the wild plantings of forest species and grazing plants, and are faced with the reestablishment of cover on denuded areas, the same need for germ plasm exists as in the case of a food plant. Furthermore, a diversity of forms from which improved types for reestablishment may be developed approaches that heretofore thought about only in the case of cultivated crops. Wilderness areas and parks help to preserve such species. There is a constant relationship between the number of diverse genes available and the number of true-breeding recombinations which may theoretically be obtained. This is expressed by 2” in which n is the number of alleles. Ten alleles could be arranged in 2 ’ O or 1024 different truebreeding combinations or genotypes. Hence, one might have over 1000 items in a collection and be concerned with only 10 diverse alleles. By adding one new gene, the recombinations jump to 2048. Therefore, it is well to consider what the gene pool contains in contrast to the possible number of recombinants or genotypes. For various reasons, all recombinations are not obtained; some may not even be viable. Nearly all

PLANT GERM PLASM N O W A N D FOR TOMORROW

9

populations sampled will reveal the duplication over and over of most of the genes. One way to relate genes to populations is given in Fig. 1.

Species diversity

FIG. I . Relationship of gene base to species diversity. A small gene base can provide for considerable variability among populations that are derived from it.

IV.

W h e r e Germ Plasm Comes from

Germ plasm of crops is derived from three main sources. These are ( I ) the wild species and primitive forms of crops in primary centers of diversity, (2) plant migrants to secondary centers of culture where their diversity may be augmented, and (3) the unique products of plant breeding. The present-day theories of the origins of germ plasm are mostly refinements of Vavilov’s concept of the phytogeographic basis for plant exploration (Vavilov, 1950). While these modern interpretations, based on the ever-increasing knowledge of plant resources are significant, it is still Vavilov’s earlier concept that is employed in determining the gaps in our genetic resources, establishing the priorities for procuring wild and primitive crop progenitors, and conducting the necessary explorations to secure the material. In terms of cultivated plants we tend to think of the origins as those areas which contain the broadest array of genetic diversity. However, the concept is not always valid, cannot be irrevocably proved, and disallows multiple origins. Briefly summarized, Vavilov’s main centers of origin (now considered as centers of diversity) are listed below with the number of species of some degree of use to man and the approximate number of crops of considerable world importance contributed by each center. 1 . China- 136 species, 1 I crops 2. India- I17 species, 15 crops a. Indo-Malaysia-55 species, 4 crops 3. Middle Asia-42 species, 15 crops 4. Near East - 83 species, 20 crops 5. Mediterranean 84 species, 6 crops 6. Ethiopia-38 species, 15 crops 7. Mexico-Central America- 49 species, 9 crops

10

JOHN L. CREECH A N D LOUIS P. REITZ

8. South America (Peru, Ecuador, Bolivia)-45 species, 7 crops a. Chile-4 species, 1 crop b. Brazil, Paraguay - I3 species, 6 crops These are the primary centers from which the crop species were first moved for domestication. In view of the remarkable shifts of many crop species to distant lands for cultivation purposes, there has emerged the concept of secondary centers of diversity. In many respects, these secondary centers have become significant sources of germ plasm, especially in respect to different biological ecosystems. In primary centers of diversity the species is in competition with other natural elements of its environment, whereas in secondary centers new biological and physical stresses become selective factors. Primitive cultivars in these secondary centers are important segments of germ plasm because of man’s involvement in assuring their success although the age element is extremely brief in comparison to the natural evolvement of crop species in their primary centers of origin. While we regard the materials from primary and secondary centers as the main components of germ plasm, to these must be added the materials developed through highly advanced plant breeding techniques (Hanson, 1969). This source of germ plasm includes such significant contributions as induced polyploidy, mutations, and the combining of multiple traits into useful breeding lines not likely to be discovered either in progenitor species or primitive varieties. A simplified flow diagram of the origins of our germ plasm might be as depicted in Fig. 2. The most diverse component of our germ plasm is the contribution of the primary centers. In potato germ plasm held in the working collection Primary centerswild soecies of croDs and close relatives, immediate primitive cultivars I

I

,

Secondary centersprimative cultivors, land races with selective traits for new ecosystem stress

^

I

berm

Advanced breedina linescombined troits, controlled heterotic responses, induced mutations, apomictic lines, etc.

FIG.2. Sources of germ plasm relative to amount and diversity of contributions.

PLANT GERM PLASM N O W A N D FOR TOMORROW

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at Sturgeon Bay, Wisconsin, 97% of the introductions added since 1958 are wild collections or primitive types (Ross and Rowe, 1965). These are important sources of such traits as frost resistance (Ross and Rowe, 1969) and immunity to virus X (Solanum acaule Bitter), immunity to viruses A and Y ( S . stoloniferum Schlecth., S . chacoense Bitter), field resistance to late blight ( S . demissum Lindl.), and nematode resistance ( S . vernei Bitter & Wittm. ex Engl.). Recently, Radcliffe and Lauer (1966) screened 395 potato introductions involving 65 species, and found resistance to green peach and potato aphids in 6 species of limited distribution in Mexico. Thus, within the broad concepts of primary centers of diversity, microcenters yielding specific genetic traits are being identified. Contributions of secondary centers are apt to be less identifiable except when the germ plasm is evaluated in an organized manner. In the collection of pepper (Capsicum frutescens L.) screened at the Southern Regional Introduction Station, Experiment, Georgia (Sowell and Langford, I963), resistance to bacterial spot (Xanthomonas vesicatoria) was not found in accessions from South America, where C . frutescens is native. I t was located in introductions from India, where selection pressure was exerted on the host by the pathogen during the period of their association after both had been introduced into India. It is interesting to note that the varieties and selections of Cofea arabica L. which show the greatest degree of resistance to coffee rust (Hemileia vastatrix) races are descendants of a plant of variety K E N T which was discovered in a plantation at Mysore, India, in I9 I 1 . The rust had invaded India around 1870 and devastated most of the plantations. Although both Cofea arabica and the rust are native to northeastern Africa (Ethiopia), no particularly resistant types have been found among the collections from there. The contributions made by plant breeders and geneticists through the manipulation of germ plasm is often overlooked in relation to the quality of our germ plasm resources. Many of these research products would not likely survive in primary centers of germ plasm since they exert a neutral or negative influence on genetic continuity and are dependent on man’s intervention to realize their benefit. The new short wheats are a perfect example of the production of a germ plasm complex that includes photoperiodic insensitivity, shortened stature through the use of the introduction NORIN 10, broadly based disease resistance, and the ability to produce high yields with appropriate irrigation and fertilizer. In the wild, the character of short stature, so important to the new strains, might well be regarded by the plant collector as a deficiency and something not to be collected, or not even observed in a population of taller plants.

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JOHN L. CREECH A N D LOUIS P. REITZ

The H I G G I N S buffelgrass Pennisetum ciliare (L.) Link, may be cited as an example of an artificially produced crop variety developed by control and manipulation of apomixis (Anonymous, 1968). A single sexual plant (discovered in 1958) was used as a female parent in crosses with different biotypes of apomictic buffelgrass. Selected apomictic progeny from these crosses possessed combinations of characters (improved vegetative vigor, seed yield, and drought resistance) that had not been observed previously in collections of this species. Subsequent research has revealed that apomictic reproduction in buffelgrass is inherited like other genetically controlled characteristics, and can be manipulated. V.

Collecting and Assembling Germ Plasm

Collecting and assembling germ plasm has become a formidable task and of such a magnitude that no one individual can assume the responsibility for all of its aspects. Rather, private, state, regional, national, and international organizations need to act on a coordinated basis, if we are to collect and utilize effectively more than a fraction of the world’s genetic resources while they exist. This requires an organization and personal commitment to the principle of good management of germ plasm, a need that was recognized as early as 1898 by David Fairchild. He saw that plant introduction had special needs involving people and facilities for plant exploration, quarantine procedures, special propagation techniques, as well as distributing seed or plants and documenting the results achieved. It is interesting to note that the need to conserve germ plasm had not been judged to be essential. But this was in an era when there was rather free access to most of the world by the developed nations, and germ plasm did not appear to be threatened. The general philosophy expressed by Fairchild (1938) and the interest and enthusiasm developed by the team of scientists he assembled was to have a profound effect on American agriculture. Their efforts resulted in a long succession of plant explorations to centers of diversity. A system of documentation was devised and persists today in the form of the Plant Inventory. This is the published documentation of seeds and plants introduced by the U.S. Department of Agriculture. The first of the Federal Plant Introduction Stations was established, now represented by those at Chico, California; Miami, Florida; Savannah, Georgia; and Glenn Dale, Maryland (Hodge et al., 1956). It was in this era that individual plant explorers, N. E. Hansen, F. N. Meyer, P. H. Dorsett, H. L. Westover, C. R. Enlow, W. Popenoe, and scores of other scientists made their personal contributions to plant introduction (Ryerson, 1967). After World War I I, a committee of scientistladministrators headed by Director R. E. Buchanan, Iowa AES, recognized the need for organized

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Federal/State cooperation in the introduction, evaluation, and maintenance of “new crops.” No longer did the system of reliance on individual scientists to receive and evaluate germ plasm, often discarding what appeared nonessential, serve our national interests. The deliberations of this committee resulted in the system of regional plant introduction stations to serve the needs of scientists in regional associations of states. These stations are located at Agricultural Experiment Stations at Geneva, New York (Regional Project NE-9); Ames, Iowa (Regional Project NC7); Experiment, Georgia, (Regional Project S-9); and Pullman, Washington (Regional Project W-6) (Hodge and Erlanson, 1955). They also envisioned and caused the Potato Introduction Station, Sturgeon Bay, Wisconsin (IR-l), to be established in 1950 and the National Seed Storage Laboratory to be established at Fort Collins, Colorado, in 1958. There are two additional developments worthy of note here. In order to prevent the extinction of native strains of maize, The National Academy of Sciences - National Research Council formed a Committee on Preservation of Indigenous Strains of Maize (Clark, 1956). This Committee sponsored a project to collect, preserve, and study for future use as many varieties and pioneer corns as possible. The Committee, in cooperation with The Rockefeller Foundation, the Government of Brazil, and the USDA established seed centers in Mexico, Colombia, Brazil, and Maryland, USA. Over a 3-year period (195 1-54) some 12,000 variants of Indian corn were collected through cooperative efforts of collaborator scientists in the Caribbean area, Mexico, Central America, ColombianAndean area, Brazil-Eastern South America, the United States, and Canada. These materials have been in demand by plant breeders ever since their assemblage. The need to collect and evaluate ornamental plants on a sustained basis was recognized by The Longwood Foundation (Longwood Gardens), Kennett Square, Pennsylvania, in 1956. U p to this time exploration for ornamental plants had been supported by private institutions, but, with more restrictive quarantines and less private access to many parts of the world, there was need for a Federal program. The Longwood Foundation proposed ajoint project to the Agricultural Research Service to encourage the advancement of ornamental horticulture through the discovery and introduction of new or little-known plants of the world which would have potential value for research and ultimately, the people of the United States. Since 1956, funds from Longwood Gardens have supported 12 ornamental explorations to Europe, parts of the U.S.S.R., the Himalayas, most of the Far East, New Guinea, Brazil, and Australia. For the first time, the private sector and government had joined forces to support a sustained effort in ornamental plant exploration.

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JOHN L . CREECH A N D LOUIS P. REITZ

The principal means of assembling germ plasm are direct exploration, exchanges of plant material between scientists, and the transfer of increased stocks from existing working collections into more comprehensive ones. We are involved in assembling seed and vegetative germ plasm of hundreds of species and each has its own particular requirements for increase, evaluation, and conservation. A. SEEDGERMPLASM The exploration for, and introduction of, seed-reproduced crops involves direct collecting in the primary and secondary centers of diversity. Explorations are no longer conducted with the broad sweep of the earlier collectors, who considered the collecting of all crops encountered as their responsibility. Instead, we concentrate on collecting to improve the diversity of germ plasm for specific crops. The explorations are conducted in a systematic fashion by crop specialists. Most plant collecting explorations are of short duration, rarely exceeding four or five months, coinciding with the time of seed ripening for the species of primary interest as governed by altitudinal or latitudinal range. Working with efficiency, a well-equipped team of two collectors, familiar with the terrain, is unlikely to exceed an average of 10 collections daily or about 1000 samples for a trip. A striking conclusion by Bennett (1970) is the awareness that such a level of activity cannot possibly meet the needs to salvage genetic resources being depleted at an alarming rate. In order to improve, the situation requires the establishment of exploration priorities, international cooperation, trained personnel, and adequate funds to operate as the National Academy provided for maize. As a means of mounting a sustained effort in plant collecting, the F A 0 Panel of Experts on Plant Exploration and Introduction recommended that short-term practical training courses in plant collecting be given as well as support to university courses in the use and conservation of genetic materials; that personnel for training be drawn from developing as well as developed countries: and that individual governments consider ways to collect its indigenous germ plasm. In addition, the F A 0 offered to act as a clearinghouse for informing interested scientists of forthcoming explorations through the Plant Introduction Newsletter ( 1970b). The art of field collecting has also changed, and considerable attention is now paid to sampling techniques as well as population distribution. Field sampling procedures are now designed to review the fullest possible variability of the species. Collecting teams should therefore include broadly trained agronomists, geneticists, entomologists, and pathologists. It is essential that they document the greatest amount of useful data for the scientist making subsequent evaluations. Both random and directed

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sampling methods of collection, aimed at filling the gaps, are employed (see Fig. 2 ) and accurate documentation as to the character of sampling has become of increasing significance as a means of communication between the collector and the evaluator. In view of the complexity of modern field exploration, certain organizations, particularly FAO, are especially helpful in providing information about agricultural and geographical conditions in remote areas and often provide access to competent local collectors (FAO, 1969b). I n the United States, the New Crops Research Branch, Plant Science Research Division, Plant Industry Station, Beltsville, Maryland 20705, is capable of providing considerable basic information of this nature and provides collectors with its facilities for introduction, quarantine inspection, and accessioning. In return for such service, collectors are expected to share their collections with the USDA as a means of providing for the needs of other scientists. A most recent concept in collecting is the development of exploration centers in regions of crop diversity from which to conduct field operations. The Crops Research and Introduction Center, Izmir, Turkey, supported jointly by F A 0 and Turkey is the first active center of this nature (Schulz-Schaeffer, 1970). Here, the foreign collector can receive technical help and supplies as well as facilities for seed cleaning and preparation for shipment, and other facilities essential to success. Considerations are being given to a somewhat similar center for potato collecting in South America, supported cooperatively by several U.S. institutions. Such centers offer continuity of purpose, a means of recollecting by local staff members, and could become training centers as well as conservation centers.

B. VEGETATIVELYPROPAGATED GERMPLASM Collecting vegetatively propagated plants presents most of the problems of seed collecting explorations. I n addition, other difficulties are associated with transit survival, danger of insect and disease importation, and the high cost of propagating and developing vegetative collections. Because of these factors, many more vegetative collections have been lost as compared to seed introductions. Among the crops most frequently collected by vegetative means are bananas (Musa spp.), manioc (Manihot esculenta Grantz), pineapples (Ananas cornosus (L.) Merr.), potatoes (Solanurn spp.), sugarcane (Saccharurn oBcinarum L.), sweet potatoes (Ipornoea batatas (L.) Lam.), taro (Colocasia esculenta (L.) Schott), and yam (Dioscorea spp.); a vast array of deciduous and tropical fruit and nut crops, certain forage species (Cynodon, Digitaria, Andropogon, Brachiariu), and the perennial Arachis

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JOHN L . CREECH A N D LOUIS P. REITZ

species are maintained vegetatively. I n addition, many ornamentals are collected as bulbs, tubers, corms, cuttings, and grafting material. The international movement of vegetative stocks is complicated by quarantine regulations. The long periods of time required to grow populations, and the excessive cost of developing tree crop collections has discouraged intensive efforts with these crops. Meanwhile, the loss of wild stands of fruit tree species, often cut for fuel or razed to provide land for intensive cropping, and abandonment of orchards of old varieties accelerates. Recently, through the use of U.S. PL 480 funds in India, Poland, and Yugoslavia, it has been possible to collect and establish in-country collections of germ plasm. Yugoslavia has an excellent base of fruit and nut crop diversity with potentials for frost and drought resistance. The Agricultural College at Skopje is surveying the native fruit species of Macedonia and assembling these as a source of budwood and seeds for distribution. PL 480 funds permitted the collecting of seed stocks of small grains in Yugoslavia to search for resistance to the cereal leaf beetle. Plant exploration by local scientists with its opportunities for continuity has been one of the most enterprising results of the use of PL 480 currency. The USDA coffee and cocoa germ plasm collections illustrate an important aspect of a vegative collection in lieu of seed reserves. Coffee and cocoa seed is rather short lived and yet the time required to raise new seedlings to fruiting is several years. In addition, there are disease and insect problems that restrict the movement of these crops. In cooperation with USAID, varietal collections were assembled at the U.S. Plant Introduction Station, Miami, Florida, where, despite occasional frosts, both coffee and cocoa can be grown outdoors successfully. Neither crop is cultivated commercially and possible infection by coffee or cocoa pests is unlikely. These facts have made this an ideal extra-tropical isolation germ plasm collection center. Over the 15 years that the coffee collection has been developed, there has been a rather limited demand for material since the most serious disease, coffee leaf rust, had never been reported in the Western Hemisphere. I n 1970, coffee leaf rust was first reported from several locations in Brazil. Although the outbreak was restricted to the poorer producing regions where less than 10% of the production occurs, the disease is now a threat to production throughout the hemisphere and has caused producing countries to initiate programs to develop resistance combined with high yield and quality in Coffea arabica. The Miami collection with its safeguards plus the quarantine facilities at the U.S. Plant Introduction Station, Glenn Dale, Maryland, offers breeders a reliable source of germ plasm without the danger of introducing

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additional rust races or other diseases as might be the case if importations were made directly from Africa where important coffee types and the rust occur. In the case of sweet potato (Ipomoea bataras) (Yen, 1970), the building of a working collection at the Otara Vegetable Research Station, D.S.I.R., New Zealand, was developed over a period of seven years of collecting clonal material from seven American areas, Polynesia, and Melanesia. At the end of this period, 175 varieties were assembled, evaluated comparatively, and are available to sweet potato breeders. However, this collection may be abandoned unless efforts are successful to transfer the collection elsewhere. A similar effort is being conducted at the Federal Experiment Station, Mayaguez, Puerto Rico, where the true yam (Dioscorea spp.) is being assembled with USAID support. Yam varieties have been collected on farms, in markets, and from other stations in the Caribbean. The introductions undergo varietal identification and determination of tuber characteristics, disease screening, and quality observations. The ultimate objective is to establish a documented, disease-free working collection for use in the tropics as a source of breeding lines or to upgrade the quality of varieties now being grown. VI.

Evaluation, Increase, and Maintenance of Germ Plasm

Evaluation of germ plasm really begins with sample collection. Either some selectivity is exercised in choosing among plants from which collections are taken or a bulking of many source plants is utilized according to the plan, type of material available, and objective. When a random sample is taken, this implies that an appraisal of the mission’s objectives has been made whereby an effective use can be made of the material for later studies. Complete records about the collected items are essential and are a vital part of the evaluation. Generally, deficient plants, e.g., diseased plants, are rejected at the collecting site, but some valuable germ plasm may be unwittingly overlooked. Samples of adequate size often can be evaluated without an intermediate multiplication. Single fruits, seeds, panicles, etc., except for surface descriptive purposes, must be increased for further study. Quarantine restrictions must be considered and met when applicable. This may require a seed generation in detention, hence, the size of the original sample should be compatible with plans to meet quarantine needs and an increase for evaluation. Scions, cuttings, or other vegetative parts are subject to quarantine detention and propagation. Because this entails virus indexing procedures, it is essential that the collector be judicious in choice of the material. This

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JOHN L. CREECH A N D LOUIS P. REITZ

should be collected from individual specimens and not be a mixture from several trees of a variety. Otherwise, each propagating piece must be indexed because of the uneven and masked distribution of viruses. This is particularly applicable when samples are obtained from collections. Again, the documentation becomes extremely important in these followup operations of propagation, identification, and virus eradication. In the United States, quarantine and the initial increase of seed stocks frequently are combined in one operation. Small grains are grown in a detention nursery at Mesa, Arizona, where the growing crop is observed several times for evidence of seedborne diseases. The seed is treated before sowing with a disinfectant and all weed seeds, smut balls, etc., are screened out or removed by hand. Other crops, some requiring vegetative propagation, are handled in a comparable manner at the U.S. Plant Introduction Station, Glenn Dale, Maryland, and the Regional Plant Introduction Stations. These regional stations may increase seed introductions themselves or arrange for increase at other experiment stations in the region. The introductions are evaluated by teams of Federal/State agronomists, horticulturists, pathologists, and entomologists. Thus, when the seed is catalogued for general distribution, documentation relates to the collector’s notes and the observations made at the initial increase. As added information is accumulated through subsequent evaluation and use by crop specialists, this is provided to scientists requesting material. A portion of all collections is held at the regional station as working stock, and samples are also sent to the National Seed Storage Laboratory. To avoid unnecessary duplication of effort, the regional stations have developed crop priorities among themselves for multiplication and evaluation, and responsibility for working collections. A. SMALLGRAINCEREALS WORKING COLLECTIONS Wheat, oats, rice, barley, and other self-pollinated annual seed crops are relatively easy to handle in large numbers in a small space. Single plants, hills sown with perhaps 20 seeds, single or multiple rows spaced 30 to 60 cm apart and of any desired length (usually 1 or 2 meters) may be used to increase the seed of these crops. Simultaneously, many observations can be made for purposes of description and evaluation of the items. Evaluation at this stage must remain subordinate to multiplication of the seed, the primary purpose. Winter hardiness, specific disease reaction, yield, etc., are evaluated under optimum conditions to detect varietal differences. Obviously, extreme tests might eliminate many stocks which should be preserved for later tests of a different nature where they might prove to be excellent germ plasm.

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PLANT GERM PLASM NOW A N D FOR TOMORROW

Our method of handling accessions of wheat, oats, and barley, both new and old, is illustrated in Fig. 3 (Reitz and Craddock, 1969).

__ -- ------- c Decontamination - ------ - - - . -Accessioning - -Propagotion

in detention Mesa, Arizona

Maintenance

11 I Evaluation

Breeding

Other uses

I

FIG. 3. Flow chart outlining the steps in acquiring and maintaining germ plasm in the USDA collection of small grains.

The working collections are kept at Beltsville, Maryland, in a room held at about 50°F and 50% RH. The reserve location is the National Seed Storage Laboratory, Fort Collins, Colorado. One or two additional safety storage locations are maintained for each crop, but not all lines are at one geographical address. Since the call on our supplies by breeders and others who use the seed depletes most of the seed in four to six years, it is necessary to regrow accessions on a schedule of about 10,000 items annually. Mesa, Arizona, and Aberdeen, Idaho, have been satisfactory locations for this work because of favorable climates and irrigation facilities. Mesa accommodates nearly all types of cereals without regard to the peculiar growth requirements of some accessions. Mesa is sufficiently isolated from other grain areas to be safely used as a quarantine or detention center to intercept latent plant diseases that may have been

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JOHN L. CREECH A N D LOUIS P. REITZ

brought into the country when the seed was imported. Seedborne diseases such as viruses and smuts are examples. Seed in our collections is available to research workers of all kindspublic, private, domestic, and foreign. Evaluation studies include resistance to insects, disease-causing organisms, adverse environments, and production hazards. Nutritional and other unique genes of many kinds are sought. Occasionally, varieties are utilized for direct cultivation. The collections are replenished either when seed requests have diminished the supplies, or when viability begins to decline. Since only about 200 g of each item are held initially and some are depleted at a greater rate than others, the inventory of seed on hand becomes uneven. This tedious task has now been built into the data-processing machine program. The computer is programmed to print a list of the depleted items when inventories run low, and these items are returned to the field for multiplication the next year. All small grain collection items with descriptive data are entered on punch cards, then put on tape from which printouts are made. Coded information gives the genus, species, name or designation, accession number-Cereal Investigations (C.I.) and Plant Introduction (P.1.) - source of seed, origin of variety, kernel color, growth habit, spike or panicle characteristics such as density, awn, chaff color, pubescenes, etc., secondary type description if mixed when received, and general plant height. Such information is obtained routinely as the items are added to the collection and serves three functions: (1) it provides a history and basic description of each item, (2) it is a guide to authenticate items when being regrown to replenish the seed inventory, (3) it provides a basis for breeders to request certain types of major interest. There is need for germ plasm users to cooperate with the curator of a collection at this point in time since adequate evaluation for particular uses will involve special equipment, testing facilities, genetic analyses, etc. Data so derived, however, should be shared with the curator and part of them added to his total record. The latter is especially true when the entire collection is evaluated uniformly for some unique trait. Resistance to bunt, stem rust, sawfly, and cereal leaf beetle, as well as protein and lysine content have been determined for our entire wheat collection. Large segments have been evaluated for other resistances, agronomic value, and other characteristics. The chart (Reitz and Ward, 1958) (Fig. 4) illustrates how the curator and collection are intimately related to initial evaluations (central circle), less involved with programs where major responsibility rests with others (such as the International Rust Nursery), and remotely related to sustained breeding programs, and commercial production.

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Bulks comprised of compatible accessions are appealing provided equal competitive opportunity is maintained and evaluation procedures take this fully into account. However, if possible, when accessions are bulked,

Evaluation

FIG.4. Degrees of involvement of a collection, and its curator, are illustrated for wheat. The inner circles suggest that kinds of data the curator desires on all items. Once promising items are identified, these go into remote testing programs or into completely separated activities (peripheral arcs).

there needs to be a conserved collection of the original lines, developed prior to bulking; viz, stocks of the 12,000 primitive maize collections held as well as the 2000 bulked lines. Evaluation for one response is no guide to the usefulness of an item for some other purpose. Each purpose and case must be assessed independently although several evaluations may be obtained from one seeding. Another related problem is the difficulty of controlling extraneous influences. For example, a plant already defoliated by insects or a leaf blight cannot be evaluated for leaf rust reaction. This seems so obvious; yet it is a common weakness in evaluation programs.

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Procedures for handling the increase, maintenance, and evaluation outlined here are applicable to other self-pollinated crops such as beans, soybeans, self-pollinating grasses, and millets. Seed size, plant growth, the evaluation objective, and other factors alter specific procedures. Obstacles include specific requirements for photoperiod, vernalization, optimum soil and air temperature conditions, and protection during development. Much germ plasm is lost because these factors are inadequately met during the maintenance and replenishment phases. In some cases the evaluation is meaningless because soil-plant interactions or parasiteplant interactions were disregarded or not adequately assessed.

B. CROSS-POLLINATED SPECIES Rye, corn, sorghum, cotton, alfalfa, red clover, many turf and pasture grasses, fruit and forest trees, sugar beets, and other crops cross-pollinate to such a degree that the procedure outlined for small grains must be modified. Spatial isolation is recommended but becomes difficult or impossible to achieve with large numbers. Manual self pollination is effective in sorghum merely by placing a bag over the panicle during pollinating time. Bagged ears of corn may be pollinated with a bulk of that line’s own pollen but some inbreeding depression will occur. The latter would not directly affect the germ plasm resource unless it caused population drift by selectively causing some gene carriers to be depressed and lost. This problem is partially overcome by developing race groups, as has been done in corn and alfalfa, and maintaining the races in isolation. The use of border rows (which are discarded) to provide a pollen dilution gradient mitigates the contamination. Sorghum breedefs heretofore limited to sorghum varieties that flower under comparatively long daylengths such as those in the milo, kafir, and feterita groups, will soon share in a genetic bonanza. Under a Rockefellersponsored program in India and, more recently, an ARS-sponsored Public Law 480 grant, an extensive reservoir of sorghum stock, called the IS Collection, has been established by Indian scientists. The scientists assembled, characterized, and classified nearly 12,000 stocks from 44 countries. Because sorghum is a tropical crop and flowering is influenced by day length, many potentially valuable varieties do not flower under U.S. conditions. To offset this, an elite group of sorghums from the IS Collection is being used in the U.S. sorghum conversion program currently underway at the Federal Experiment Station, Mayaguez, Puerto Rico, and at Texas Agricultural Experiment Station, Lubbock. There, ARS and Texas geneticists are crossing exotic types with early dwarf varieties to recover desirable exotic characteristics and combine them with heights and

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maturities needed in the United States. From this conversion program, 63 new genetic lines were released to U S . breeders during 1970, and approximately 1000 elite items will eventually become available. Evaluation and maintenance of long-lived species is more difficult and time-consuming. Treatment to cause early flowering in perennial forms has made much progress in recent years thereby enabling breeders to obtain a seed generation at tolerable intervals. The perennial habit is an advantage, however, because one sowing or planting might persist forever, or until it is willfully destroyed. Opinons differ about the number of items comprising an adequate size of collection. These range from prime concern for the basic species, whether wild or under domestication, to thousands, even millions of individuals to represent the crop. The latter extreme imposes a heavy burden which virtually no institution can bear. The present collection of about 22,000 accessions of wheat in the USDA Collection and a like number of oats and barley combined requires the attention of one scientist and four assistants. This is a dynamic program of research evaluation as well as acquisition and maintenance. One difficulty regarding size is the basic concept about germ plasm. It is more than a bank of genes, but it need not embrace all the possible cross-combinations among genetic entities. Some germ plasm has merit because of the unique gene interactions represented; much of it is single-gene based (Ward, 1962). Every collection of any size quickly shows duplication of genes and phenotypes. For example, a half dozen awn types in wheat about covers the range we see; the same is true of most other morphological characteristics. Therefore, additions to our collection duplicate much of what we already have. I n our case, we are concerned with resistances, efficiency factors, physiologic capacity, and nutritional values. Selective additions are more significant than more items at random, especially if new geographically located gene pools can be sampled. The general situation is illustrated in Fig. 5 regarding successive samplings in the same gene pool. The assumptions are purely for illustrative purposes. It is evident that resampling leads to fewer and fewer new unique forms and a correspondingly larger number of duplicates. It has been conjectured that our barley collection of 12,000 items probably embraces a majority of the world’s barley genes. The conclusion is not that we have enough barley germ plasm, but that a concentrated effort should be redirected toward the missing portion, if definable. Those who propose that the base species are enough to retain would depend upon commercially available stocks, natural and induced mutations, and introgressive evolutionary forces to provide variability that might be needed later. The question was discussed in the 1940’s when

JOHN L. CREECH A N D LOUIS P. REITZ

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hybrid corn came into prominence whether any effort should be made to preserve the open-pollinated varieties of central U.S. Most of the genes resided in inbred lines, it was argued. Fortunately, a stubborn few corn

;'I

pq 000

I

15.000

I

Second

First

Third

Fourth

FIG. 5 . Four successive samplings of a population containing 10,000 unique forms. Ten thousand samples were taken each time. Assuming a duplication rate of 1/2, the four samplings would yield a total of 9375 unique forms on a descending frequency of 5000 from the first sample to 625 from the fourth sample.

breeders maintained O.P. corn, and on numerous occasions this has been the source of new and useful variation. For example, it is doubtful that any of our corn borer resistant lines would be available because essentially all of them were developed after 1940 from open-pollinated stocks. New varieties of limited pedigree sometimes sweep all others out of an extensive region, as indeed the new semidwarf wheats are doing in parts of Mexico, India, etc. This contributes to germ plasm losses. VII.

How G e r m Plasm is Used

Direct use has been the historical means of incorporating introduced germ plasm into agriculture throughout the world. Most of the crops grown in the United States originated elsewhere. Native Western Hemispheric crops - maize, common beans, peanuts, pumpkins, sweet potatoes, sunflowers, manioc, potatoes, rubber, and tobacco -found many homes in other continents. The geographical origin of plants has been

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discussed by Vavilov (1957), J. R. Harlan (196 I , 1966), Frankel and Bennett ( 1970), and many others. The dissemination of these crop species by man is an equally discussed subject. I n a symposium volume on Germ Plasm Resources (J. R. Harlan, 1961a; Cullinan, 1961; Weiss, 1961) it is clearly shown that origin, greatest variability, and greatest use of germ plasm may be in separate geographical areas, and that the use of germ plasm extends into all facets of molding the species subunits to fit a prevailing environment or to suit man’s subsistence and economic needs. The permutations are endless, it seems; simple generalizations become inadequate, and a full treatment of how germ plasm is used is both too tedious to set down and too detailed to gather. The range of plant variation is astounding, and yet, when one examines the pedigrees of varieties being grown commercially it is evident that only a small fraction of the available germ plasm has been incorporated. This means that ( I ) only a limited amount of the available germ plasm has been used successfully, ( 2 ) some of the germ plasm may be worthless, (3) pedigrees may not reveal the entire ancestry and may not be correct, (4)individual breeders tend to work within a relatively narrow range of material and inbreed rather extensively because local adaptation restricts merit of extreme genotypes, (5) all needs to be supplied by available germ plasm are not identified at one time and even the needs are not all recognized at once, and (6) biological systems are not static. We did not realize, for example, that resistance to the cereal leaf beetle was needed until the insect was introduced accidentally about 1962. How could anyone evaluate small grains for resistance? Higher protein and better balance for humans among the essential amino acids have recently come into prominence, and it is no suprise that variability has likewise been discovered in the germ plasm of several of these crops. Many evaluations and uses of germ plasm given in the paragraphs which follow are from progress reports by various Branches of the Plant Science Research Division, ARS, and from the annual and other reports from the four Federal/State Cooperative Regional Introduction Stations to their Technical Committees. A.

CEREALGRAINS 1 . Maize

Indian corn, or maize, quickly achieved world significance soon after the discovery of America and its early colonization and exploration. In fact, maize was so rapidly disseminated that arguments arose as to whether maize, in fact, did originate in Central America or whether it may have had an origin involving other continents. Certainly some of the maize forms outside America are strikingly unique, but they are logically

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explained by the merging of segments of germ plasm brought together under new stress environments. Much of the same thing happened to maize in North America in the evolution of varieties such as Reid Yellow dent, so highly productive in the Ohio and Mississippi Valleys (Jenkins, 1936, pp. 464-466). Valuable maize germ plasm has been found among introduced materials such as Zapalote Chico, P.I. 2 I74 13, a white dent corn recognized and used as a source of resistance to the corn earworm. This cultivar originated in southern Mexico but is easy to grow as far north as Minnesota because it is comparatively independent, or unaffected, by length of day. It is 8-10 rowed, short eared (about 5 inches) and has very dented kernels. P.I. 217407, or ‘Ladyfinger’ popcorn, has been widely used as a source of northern corn blight resistance, Helminthosporium turcicum. This introduction is a late maturing, prolific, high quality popcorn, very similar to the ancient popcorns of Peruvian graves. The high lysine germ plasm includes Opaque-2, a mutant form, and floury endosperm. A number of problems remain to be solved in corn improvement for which new germ plasm is sought. A higher level of resistance to stalk rots, resistance to other diseases, especially leaf blights, better male sterile cytoplasmic systems, and resistance to insects attacking the roots, stalks, and ears, to name only a few.

2 . Sorghum Sorghum is an ancient crop, but a highly successful immigrant in the United States. The crop in multiple forms has contributed immensely to agriculture in the southern, Central Plains, and southwestern States of the United States. Grain, silage, pasture, sirup, broom, and other types are grown. Much of the basic germ plasm in the United States was introduced 75- 100 years ago. Unknown processes, including natural crossing and mutations, resulted in an enriched germ plasm even as the crop was being grown by farmers. At least five distinct forms of milo appeared on farms during a 30-year period (Martin, 1936, p. 536). This evolution and cross breeding with kafir was the basis for developing types suited to combine harvesting. Numerous introductions have contributed to the improvement of sorghum for the production of grain, forage, and sirup. Within the sorghum genus perhaps the most valuable germ plasm yet introduced was contained in four accessions (P.I.’s 221569, 221570, 221572, and 221688) collected in Nigeria in 195 1. They produce grain with yellow endosperm and have higher levels of vitamin A than other sorghums. P.I. 221688 is the ‘Short Kaura’ variety grown in Nigeria, and the other three represent different seed lots of the variety ‘Kaura.’ All are too late for commercial

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plantings in this country but many sorghum hybrids released by both private and public breeders during the last 10 years contain germ plasm from these yellow endosperm sorghum introductions. In 1967, a U S D A sorghum exploration to Ethiopia was undertaken in cooperation with The Rockefeller Foundation. Materials collected from this highly successful venture plus other sorghum introductions received from India and elsewhere are increased and evaluated through the sorghum germ plasm conversion program at the Federal Experiment Station, Puerto Rico, and the Texas AES. New germ plasm is sought to provide better resistance to several diseases, especially stalk rots, and resistance to insects, notably a new strain of aphid in the Central and Southern Plains. Germ plasm to make sorghum adapted and productive in short season environments and where low temperatures preclude its production at present seem likely developments and would extend the range where the crop could be grown. Germ plasm sources and problems to be solved have recently been presented (Wall and Ross, 1970) in which sorghum of Asia, Africa, and the United States, are featured. Programs are being conceived whereby sorghum will play a greater role in agriculture of tropical America.

3 . Wheat Wheat has long been associated with man’s migrations and, because of its direct use as human food and wide adaptation, has been distributed worldwide. The story of wheat germ plasm in North America was recently reviewed (Reitz and Craddock, 1969). Many writings deal with the development, early history, germ plasm resources, and use of the crop (Clark, 1936). The success of plant introductions in the phenomenal development of modern wheat varieties is a singular achievement. In a crop where the varieties change completely in a span of a decade, a broad base of diversity is essential. Norin 10 (P.I. 156641), introduced from Japan in 1946, was the key to semidwarf wheat breeding in the Pacific Northwest and in Mexico (Reitz, 1970). Another plant introduction, P.I. 178383, illustrates the significance of maintaining accessions irrespective of the immediate evaluation. This is an accession of wheat collected from Turkey by J . R. Harlan in 1948. It has the appearance of a hard red type but its milling, starch, and baking properties are that of a soft red wheat. It has poor milling quality. P. I . 178383 is susceptible to leaf rust, has weak straw, and lacks winter hardiness. P.I. 178383 was early found to be highly resistant to stinking smut and was little regarded for any other use until 1960 when stripe rust suddenly

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JOHN L. CREECH A N D LOUIS P. REITZ

became epiphytotic and was devastating to wheat production in some areas of the Pacific Northwest. It is now known that P.I. 178383 has good resistance to four races of stripe rust (Puccinia striiformis), 35 races of common bunt (Tilletia caries, and T .foetida), and 10 races of dwarf bunt (Tilletia controversa), all of which occur in the Pacific Northwest. The accession also has usable tolerance to flag smut (Urocystis tritici) and snow mold (Fusarium and Typhula spp.). Thus P.I. 178383 (except for its bunt resistance) was neglected for a number of years following its introduction and later became one of the prominent breeding lines used in Montana, Idaho, Washington, and Oregon. I t is an excellent example of a single P.I. accession contributing multiple disease resistance. In addition to its disease resistance, P.I. 178383 has excellent seedling emergence. It is now used as the new “standard” for the comparison of emergence data in the Pacific Northwest. The final utilization of the remarkable characteristics of P.I. 178383 demonstrates the value of maintaining germ plasm even though tests for some lesser traits show it to be of little or no commercial value. This introduction is one parent in several varieties now in use on U.S. farms. Germ plasm.needs remain unfilled for a broad spectrum of resistance to all root and foot rots including snowmold, augmented resistance to streak, yellow dwarf, and soilborne mosaic viruses; there is a need for additional genes for rust resistance, mildew, Septoria, and numerous other diseases. The Hessian Fly has been partially controlled by use of resistance from many sources. In some cases control has been temporary because of the evolution of new virulent cultures of fungal and insect pests. 4 . Other Cereal Grains

The germ plasm requirements for barley, oats, rice, and rye have likewise been met to some extent by assessment and use of stocks from many countries. The variations used for each crop follow a pattern similar to that discussed for maize, sorghum, and wheat. The story is never complete because the beginnings of the species, the accumulated diversity from chromosome rearrangements, introgression from wild distantly related species, mutations from natural or man-induced causes must become known and be recounted. The germ plasm resources for these crops and how they have been used were recently reviewed by Reitz and Craddock (1969; see also H. V. Harlan and Martini, 1936; Stanton, 1936; J . W. Jones, 1936; Adair et al., 1966; Frankel and Bennett, 1970; Reid et al., 1968; Vavilov, 1957; Khush and Stebbins, 1961; B. D. Webb et al., 1968; Chandler, 1970). Higher nutritional quality as well as pro-

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cessing quality is being emphasized in recent work. The discovery of Hiproly (P.I. 60693) barley from Ethiopia in 1924, having high protein and lysine content, is exciting news (Munck et af., 1970).

B. GRASSA N D FORAGE Many introductions have contributed new cultivated species to the agriculture of the United States. Much of the early history of activity bringing species into the United States and of the variability conducive to breeding improved forms was discussed in the 1937 Yearbook of Agriculture (see especially McKee and Pieters, 1937; Vinall and Hein, 1937; Tysdal and Westover, 1937; Pieters and Hollowell, 1937). Direct introduction continues to be fruitful for U.S. agriculture but most improvement has come from the use of exotic forms in breeding programs. Commencing in the mid- 19303, an expanded program of forage crop improvement was initiated in the United States by public and more recently by private breeders with the result that the numbers of varieties have been greatly increased, regional and local adaptation more sharply defined, higher levels of productivity achieved, and some disease, insect, and nematode problems controlled. Recent interest has centered around expanded use of warm-season pasture grasses in the American tropics and southern warm-temperature regions of the United States. Many of the native grasses of South Africa (Digitaria, Hemarthria, Chloris, and Pennisetum) appear to have desired characteristics for this purpose. Oakes (1965; Oakes and Langford, 1967) has discussed some of the potentials of Digitaria for cold tolerance. This becomes a paramount limiting factor in attempting to extend the production range and increased yields to higher tropical elevations. Consequently, explorations for native grasses of South Africa are receiving high priority in the USDA plant collecting program. There are many worthy examples of forage legume and grass introductions which have contributed either as direct varieties or as parents in the development of other varieties. Annual ryegrasses, Lolium multijlorum Lam., collected in Uruguay in the 1950’s, have contributed resistance to crown rust in ryegrasses now grown in the south. Most important of these introductions are P.I. 193145, T.O. 1882, and P.I. 20 1980, separate introductions of a Uruguayan variety La Estanzuela 284, and two late maturing accessions, P.I. 194394 and 194395. A bromegrass, Bromus biebersteinii Roem. & Schult., P.I. 172390, collected in Turkey in 1949 was used by the USDA Soil Conservation Service and the Idaho AES to develop REGAR bromegrass, released in 1966. REGAR has excellent seedling vigor, develops numerous leaves and has a

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strong regrowth habit with early spring development and heavy forage production. Agropyron elongaturn (Host) Beauv., P.1. 98526, was collected in the Soviet Union in 1932. It illustrates an accession that was increased and distributed in its introduced state and by 1953 was grown on 114,000 acres in the United States and certified in Nebraska as ‘Nebraska 98526.’ Alfalfa introductions (Medicago spp.) are constantly under evaluation. Diseases, insect pests, and poor adaptation in certain regions are compelling reasons for breeders to continue the search for alfalfa germ plasm. Thus the recent outbreak of the eastern biotype of the alfalfa weevil threatened alfalfa’s position as a major forage plant in several States. Owing to the difficulty of maintaining alfalfa germ plasm as distinct entities, considerable research has been devoted to the development of broad gene pools as a means of concentrating resources in composite populations hoping to obtain new gene combinations and at the same time producing enough seed for use by breeders and continued conservation of the pool. Some of the most recent releases of alfalfa germ plasm find their origin among the earliest introduction of the USDA. TRAVOIS, released by the South Dakota AES in 1962, contains genes of three introductions, P.I.’s 24455, 28070, and 28071 collected in Russia by N. E. Hansen in 1908 and 19 10. These yellow-flowered alfalfas were perpetuated in nurseries in South Dakota and ultimately utilized in the natural hybrids out of which TRAVOIS was developed. The USDA released a broadly based alfalfa population, AWPX3, in 1968, as a source of resistance to various stages of the life cycle of the alfalfa weevil. The parentage includes 13 plant introductions collected in nine different countries between 1952 and 1960. This is a fine illustration of the variability which can be traced to a multitude of ecological regions. Stem nematodes are a serious alfalfa pest in areas of the southwestern United States where the successive culture of alfalfa crops creates a high nematode population and ultimate loss of the crop. Resistance to the nematode was found in an introduction, P.I. 141462 collected in Iran in 1940. When this resistance was transferred to commercial varieties, the savings represented millions of dollars to alfalfa growers. Bermudagrass, long frowned upon as a serious pest in cultivated fields, is the leading turf grass in the South. It is a highly variable species and several lawn types have been developed in recent years. Several of these improved varieties resulted in part or entirely from introductions of Bermudagrass.

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C. HORTICULTURAL CROPS The first 900 pages of the U.S. Department of Agriculture Yearbook for 1937 was devoted largely to variability and breeding opportunities with vegetables, fruit, nut, garden, and ornamental crops. Plant introductions have been and are used effectively in horticultural crop breeding. Scientists have turned to these germ plasm resources increasingly as specialization, mechanization, and decline of resistance in commercial varieties to diseases and insects become limiting production factors. The few examples used here are typical of the many benefits accrued from incorporating characters from seemingly undesirable species into cultivated ones. Virtually none of these is native to the continental United States although some are native to Latin America. Thus, U.S. industry is largely based on alien germ plasm. 1. Vegetable Crops

Common bean germ plasm of immense value has come from Mexico (Gentry, 1968). Resistance to Fusarium root rot, halo and common blight, and to two insects was found in some 5400 lines representing many local Indian varieties, but many of those have been only partially screened. Recently, demand for these accessions by scientists in foreign countries has created an additional drain on the working stocks held at the Regional Introduction Station, Pullman, Washington. Many of the beans are difficult to increase because of lack of adaptation. By growing the collection in the winter at the Federal Experiment Station, Mayaguez, Puerto Rico, we are able to produce two generations a year and overcome daylength problems. In cooperation with The Rockefeller Foundation, the Agricultural Research Service is now engaged in a germ plasm increase program of beans (Phaseolus) plus other edible legumes to provide breeding material for the general improvement of these important protein crops. In addition to the seasonal advantage, winter increase at the Federal Experiment Station permits staff pathologists to evaluate the collection for diseases and viruses not generally encountered in continental United States. One of the most important and useful cucumber introductions is P.1 220860, SHOGOIN, collected in Korea in 1948. This introduction is the source of the gynoecious character, which, when utilized in breeding lines and varieties, makes possible the large-scale production of hybrid cucumber seed. N o less than 18 other cucumber introductions show significant degrees of resistance to diseases. P.I. 2008 15, a cucumber collected in Burma in 1952, has been widely used as a source of bacterial wilt resistance in the United States and Canada. A single cucumber intro-

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duction collected in India, P.1. 197087, has contributed the anthracnose resistance contained in several varieties. In 1956, an attractive butterhead lettuce from Israel, P.1 21 1 1 18, RINAT HAKFAR, was evaluated at the Regional Introduction Station, Geneva, New York. Its main features were thick leaves, large heads, and exceeding slowness to bolt. From seed distributed by the Geneva, New York, Introduction Station, the Canada Department of Agriculture released a new variety BUTTERKING which extended the butterhead season by 6-10 days. In 1964, BUTTERKING won a bronze medal in the All-American trials. The continuing success in finding melon introductions with disease resistance is a remarkable credit to plant introduction. In 1937, a wild melon, P.I. 1241 1 1 , was collected in the hills of India. Subsequently, the winter melon industry was struck by a serious new race of powdery mildew. Published statements claim that the resistance found in P.1. 1241 1 I saved the $5 million melon crop for California. Over the succeeding years, cantaloupe varieties with powdery or downy mildew resistance from various P.I.’s have appeared in a number of states. Peas collected in their Mediterranean homeland and elsewhere in the Middle East have been essential in breeding for disease resistance. Three pea varieties released by the New York AES, Geneva, carry a dominant gene for resistance to pea enation mosaic virus found in a pea introduction from Iran, P.I. 140295. Scientists at the Washington AES have located 10 introductions of peas with extremely high resistance to a new race of wilt. As a wild plant, Pisum sativum L., appears on the decline and this is equally true of local varieties. Replacement by modern European varieties, eradication of “weed” species, and grazing threaten this essential germ plasm. Dr. Howard S. Gentry, USDA plant explorer, has conducted two explorations in 1969 and 1970 to the Mediterranean centers of Pisum diversity from Sicily to Ethiopia. Because there are many areas of Ethiopia where primitive agriculture is still practiced, there is a high degree of variability there. Over 170 seed samples have been collected and sent to the Regional Introduction Station, Geneva, New York, for increase. Both explorations received the support of FAO, Rome, through their offices in Turkey and Ethiopia. It is estimated that more than 100 tomato varieties carry wilt resistance tracing back to P.I. 79532, Lycopersicon pimpinellifolium (Jusl.) Mill., collected in Peru in 1929. This has saved growers millions of dollars every year. Among the more recent interests is that of locating tomato accessions capable of germinating in cold soil and setting fruit under low temperatures. Introductions from the U.S.S.R., P.l.’s 262929 and

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262934, have been reported by the Geneva, New York, Introduction Station as carrying these traits. Dwarf, determinate-flowering plant types are being introduced rapidly wherever mechanical harvesting of tomatoes is possible. The pioneering work of G. C. Hanna in California (Hanna, 1966; R. E. Webb, 1966; R. E. Webb and Bruce, 1968) led to the development of varieties adapted for machine harvesting combined with disease resistance. The variety SAN MARZANO introduced from Italy in 1930, was found to bear fruit tolerant to abuses of machine harvesters. It was crossed with earlymaturing varieties of determinate growth habit. Later, disease resistance was added. This development and subsequent progress has revolutionized the canning industry. Perhaps the most singular report on tomato germ plasm available appears in the North Central Regional Research Publication 172 (Skrdla ef al., 1968). Here, 2658 accessions are described as to horticultural characters and reaction to two major diseases, the leaf blight phase of early blight and tobacco mosaic virus. Plant introductions, genetic stocks, and breeding materials are included among the entries. 2. Fruit and Nut Crops

Introductions of fruit and nut tree crops are handled by the Federal Introduction Stations because of quarantine propagation and the time factors involved in evaluation and distribution. The apple, pear, peach, and many other fruit crops were introduced almost at once by early colonists who came to America (McCrory, 1958). Migrants, Indians, birds, and animals were involved in the widespread distribution of highly variable germ plasm. Depending upon species, this germ plasm provided superior chance seedlings or sports, later propagated by cuttings or grafts, from which whole orchards were established. Forty of the 55 American apple varieties listed by Magness in the 1937 Yearbook of Agriculture were developed from chance seedlings, and most of the remainder, while of unknown origin, presumably were from seedlings, also. Many of these and other newer varieties are triploid. New fruit varieties are bred by the usual scientific methods, often through consortiums of breeders in several State AES’s. New germ plasm in great diversity to help solve the limitations of production and marketing will continue to be sought. But the most disturbing fact is the decline of existing germ plasm in old collections. By 1842, there were about 1000 pear varieties known in the United States (Howlett, 1957). Many of the varieties that occupied an important place are no longer obtainable. In an effort to describe, evaluate, and conserve the early fruit introductions, several projects have been supported by the regional research programs. In the North Central States two regional

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bulletins on evaluation of fruit introductions (Howlett, 1957; McCrory, 1958) were published. In the Western region, support has been provided for pear collections in Oregon. An inter-regional project, 1R-2, has been established for the holding and distribution of virus-free stocks of desirable fruits. The repository program was begun in 1955 and includes over 600 Prunus clones and 90 Malus clones. New accessions are indexed at Prosser, Washington, before being placed in the isolation collection at Moxie, Washington. Clones are indexed annually and must remain virus-free for five years before they can be distributed. The development of distribution centers as IR-2, provides a source of authenticated, disease-free plant material and, in the long run, may replace the many collections of unknown health status from which grafting material is now distributed.

3. Ornamental Crops The arboretums and public gardens situated in every major city of the United States play a significant role in the introduction, evaluation, and maintenance of ornamental plants. These objectives have been pursued with vigor since Colonial days. But because of the increasing stringency of plant quarantines, the Federal Government has played an increasing role in the area of introduction. The public gardens are thus assuming a greater and perhaps more urgent role of adaptive evaluation as a result of increasing environmental stress on previously standard shade trees and garden plants. Numerous ornamentals have been selected, developed, and released by arboretums and botanic gardens, through the nursery trade and ultimately to the homeowner. The BRADFORD ornamental pear is an example of an introduction that has achieved notable success in recent years (Whitehouse et al., 1963). This variety was developed from seed introduced in 1918 from China as a potential source of disease resistance. The 100 pounds of seed of Pyrus calleryana Dcne., was one of the last important pieces of exploration work of Frank N. Meyer, who died in China shortly thereafter. In the early 1950’s one of the trees growing at the Glenn Dale Introduction Station was selected for street tree trial because of its handsome flower and foliage qualities. An experimental planting was developed in a newly constructed subdivision and observed over several years. The BRADFORD became an immediate success and has been called “the tree for all seasons” because of its beauty throughout the year, including bright red autumnal leaf coloring. In addition, it appears resistant to prevalent insects and is resistant to fire-blight. A second new ornamental of significance because it demonstrates the importance of evaluation and maintenance following introduction is the

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privet (Ligustrum vulgare L.) (Dodge et d., 1965). The Arnold Arboretum sent Dr. Edgar Anderson to the Balkans in 1934 to collect ornamentals among other plants. There he collected seed of a privet in the dry, barren hills near Sarajevo, Yugoslavia. The seed was sent to the USDA and assigned P.I. No. 107630. Plants were widely distributed in 1937. After only 2 years, observers in several rigorous climates including Cheyenne and Sheridan, Wyoming, and Sioux Falls, South Dakota, reported on the superior hardiness performance of this privet. Because of its sustained excellent hardiness rating during regional trials in the 1950's and its superiority over Amur River North privet, this introduction was named C HEYENNE by the USDA in 1965. I n this instance the collector deliberately selected his material from an area of severe cold, and subsequent trials bore out the validity of his selection. CHEYENNE

D. NEW CROPS New approaches and objectives in plant screeing and exploration are to procure germ plasm of wild species not previously considered for crop purposes (Q. Jones and Wolff, 1960; Creech, 1970b). The search is for species which are promising sources of industrial end products, such as fiber and pulp from annual species, unique industrial oils, gumlike products, waxes, pharmaceuticals, insecticides, and other products with specific chemical properties. This complex effort requires the cooperation of the chemist, economic botanist, agronomist, and economist. First, the literature about a potentially useful plant group is surveyed jointly by a botanist and a chemist. Collections are then obtained within the genera selected for consideration. For example, Vernonia anthefmintica (L.) Willd., a weed from India, is attractive on account of the unique epoxyacid in its seed oil, which may be useful for protective coatings, synthetic rubber and other industrial purposes (Berry et al., 1970). Unfortunately, the agronomic characteristics of this species need considerable improvement. To obtain a wider range of variation, and to determine the center of origin of the Vernonia species, explorations were conducted by the USDA in 1966 to Africa, where Vernonia anthefmintica appears to have originated. This species and its relatives were collected to clarify their taxonomic affinities as well as to obtain species with more useful characters, such as greater seed size and oil content, and improved plant habit. After this preliminary evaluation, a pilot plant stage to study the commercial utilization of the new crop was made. Thus the pattern of development for this entirely new crop follows that for established crops. The search for plant precursors of cortisone (Correll el al., 1953, represents the most successful venture into this field. It did not necessarily establish Dioscorea as a successful domesticated crop. However,

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this program, in which centers of species in Africa, Central and North America were explored, and the chemical analyses completed, established Dioscorea as the most promising source of steroids, displacing Strophanthus, Agave, Veratrum, Trillium, and Yucca. Further intense exploration for Dioscorea species decreased the field to Dioscorea composita Hemsl., D . floribunda Mart. & Gal., and D . spiculiflora Hemsl., out of scores of species sampled. Harvesting in the wilds of Mexico still provides the crude material for steroid intermediates. The effort to develop productive commercial plantings continues as the wild supply diminishes. Several potential new crops, unlike Dioscorea, will depend on successful establishment as cultivated crops for their utilization. Of these, the most promising are crambe (Crambe abyssinica Hochst. ex R. E. Fries) and kenaf (Hibiscus cannabinus L.). Crambe is the first new oilseed to be grown commercially as a direct result of the new crops program (White and Higgins, 1966). Crambe has been widely tested for adaptability and yield and was grown commercially for several years. The Indiana AES has an active program underway and has released the variety PROPHET, which was derived from the Swedish introduction, P.I. 247310, and the variety I N D Y , an introduction of Crambe hispanica L., P.I. 279346. Several thousand acres of crambe are now grown in Canada. Crambe seed is high in oil, and the oil contains about 60% of erucic acid, a fatty acid not available in other domestically produced oil seeds. The oil has superior properties in the lubrication of molds for continuous casting of steel. The oil may also be converted to a variety of promising products for industrial outlets, such as, coatings, molded plastics for gears, adhesives, extended objects, and films. The utility of kenaf as a pulp and papermaking raw material has been demonstrated by preliminary agronomic and utilization research. Extensive field testing needs to be conducted with emphasis in the Southeast (White et al., 1970). Excellent yields have been obtained in plot studies but several factors must be resolved. Susceptibility to root-knot nematodes is the major production problem; optimum fertilizer, varietal standardization and harvesting require additional research. The varieties EVERGLADES 71 and EVERGLADES 41, which evolved from P.1. 207883, are extensively used in experimental plantings. A Kenyan accession, P.I. 292207, which appears to be segregating for resistance to two rootknot nematode species, is included in the breeding program. Screening of kenaf germ plasm for nematode resistance is being done at Savannah and Tifton, Georgia, and breeding efforts are carried out at Savannah and Mayaguez, Puerto Rico. The Florida AES has embarked on a rather corn-

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prehensive breeding program, and from their experimental plantings, yarn and fabric have been made as well as paper. In addition, kenaf leaves, young stems, and growth tips contain rather high contents of crude protein. These by-products may be useful as commercial feed. The search for additional new crop leads continues. As of January 1969, some 8300 samples have been analyzed by the Northern Marketing and Nutrition Research Division, Peoria, Illinois, for oil and protein. A total of 1278 samples have been assessed for fiber potentials. From the broad botanical-utilization screening program, about 50 new seed lipid components have been discovered, are present in realistic percentages, and have unique characteristics to suggest practical utility. From these evaluations come the plant leads for preliminary agronomic investigations. These “new crops” represent a broad array of plant families and species, most of which are scarcely known except in taxonomic and related systematic research. VIII.

A.

Germ Plasm Collections

NUMBER OF ITEMS

In order to assess the strength of our existing genetic resources and to identify the needs for additional germ plasm, partial surveys of the extent of current collections have been made by FAO, The Rockefeller Foundation, and the Agricultural Research Service. In 1969 the Crop Ecology and Genetic Resources Branch, FAO, initiated a preliminary survey of world plant genetic resources. Holders of germ plasm provided rather simple information on species held, approximate number of samples, and conditions of storage. The inquiries, sent to about 500 individuals, revealed that there were some 2 million items held by the respondents. A view of the early returns of the survey (FAO, 1970b) is alarming in that only a small portion of this material (28.5%) is in special storage facilities. Furthermore, there is an obvious degree of duplication, although this in itself is not detrimental. It serves as a safeguard against losses which may result from storage conditions. The United States is a major contributor to this wealth of conserved germ plasm. The working stocks of the Agricultural Research Service, USDA, are estimated to be about 120,000 i.tems. Similarly, collections are held by State Agricultural Experiment Stations, the Soil Conservation Service, private institutions, and industry. In many of these collections, information is documented and retrieved by automatic data processing. Some collections, held by individual scientists, are not adequately documented nor are they brought to the attention of the general scientific community.

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The American Horticultural Society, through a grant from Longwood Foundation, has established and operates a Plant Records Center for the purpose of locating and documenting collections of woody ornamental plants in the United States. An excellent team approach to collecting the data has been devised whereby the Plant Records Center specialists arrange visits to each participating institution and retrieve the raw data in cooperation with the local staff. This principle could well apply to efforts on a large scale, dealing with the economic crops. Estimates of the extent of vegetative collections, except for those maintained in botanic gardens and arboretums, are more difficult to ascertain than seed collections. Consequently, many vegetative collections are abandoned without notice. Collections of some major crops are well documented; for example, an excellent sugarcane working collection of 1,420 lines of five species is maintained by the USDA at Canal Point, Florida. In the lesser crops, however, thousands of varieties are held in a casual manner, mostly by individual farmers. The true yams (Dioscorea), a most important crop of West Africa, could well benefit by efforts to assemble and document the variation in this crop. At present there is little attempt to identify holders of yams or assemble composite collections. Strict quarantine regulations control the movement of vegetative stocks and constant vegetative regeneration intensifies and spreads viruses. We scarcely know what increments of increase in yields might be achieved or improved varieties developed if a total examination of the yam could be undertaken. We are aware of the high cost of maintaining vegetative collections and little research has been directed toward itriproved techniques. In potatoes, however, conversion to true seed has been especially rewarding. Where applicable, meristem culture may be an answer to maintaining vegetative collections under the controlled conditions of growth chambers. The USDA has made surveys of the collections of fruits and nuts maintained by Federal and State Experiment Stations (Fisher, 1963a,b, 1964; Larson, 1961). The preliminary information indicated that of some 8600 clones reported, 44.6% were apples; 30% were stone fruits; 15.6% were pears; 4.5% were nuts; 5.3% were miscellaneous items. This survey did not include citrus, but a Florida survey of citrus collections around the world lists 70 collections in 40 countries, including 13 in the United States. Again, duplication reflects the complications of developing acceptable standards for vegetative collections. F A 0 held a conference on the propagation of tropical and subtropical fruits in 1969 (FAO, 1969a). The recommendations of this conference expressed the need to establish germ plasm collections of tropical fruit trees and to strengthen the interchange of information on the status of living collections. It also proposed

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collecting missions to areas where fruit tree germ plasm is being destroyed by monoclonal culture in the case of varieties, and as a result of elimination of forests in relation to wild species.

B.

LONG-TERM STORAGE CENTERS

1 . The National Seed Storage Laboratory The establishment of the National Seed Storage Laboratory by the U .S. Department of Agriculture in 1958 was a milestone in the conservation of germ plasm. This Laboratory is situated at Colorado State University, Fort Collins, Colorado. I t has the responsibility for long-term storage of our conserved stocks of seeds of crop and forestry plants. The basic Laboratory mission is to conserve important types of seed: document each accession; maintain them perpetually by the most effective control of viability and by rejuvenating the seed stocks; and publish periodic inventories of the seeds in storage. In addition to these activities, the Laboratory staff conducts investigations into the factors governing the long-term survival of seeds in storage and methods of storing the seeds. Unlike working collections, the NSSL does not distribute the stored seeds as long as they are available elsewhere in the United States. As specific seed samples in general working collections are no longer in demand, the NSSL will maintain them until there is a need for such collections again. Among the 78,000 seed lines in the NSSL, “world collections” outnumber all others. These are wheat, oats, barley, sorghum, soybeans, flax, tobacco, cotton, safflower, and sesame. Attempts are made to expand collections of obsolete commercial varieties. When Federal, State, and private breeders release new varieties or breeding lines, they are encouraged to deposit them promptly. The NSSL collection also includes genetic stocks, old open-pollinated lines, inbreds, plant introductions, differential hosts for pathogens, and virus indicators. Only seeds of high viability are placed in storage. When received, germination tests are run to determine the degree of viability. If the germination is satisfactory, the seeds are placed in one of the cold storage rooms where they remain for five years except where some lots may be borderline in viability. The latter are retested in two years, but five years is the standard interval. When viability of seed declines during storage it is necessary that the seeds be reincreased in such a manner that the genetic characteristics of the original seed will be retained. Reincrease work will be done under contract with a scientist with the special knowledge or in an area where

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JOHN L. CREECH A N D LOUIS P. RElTZ

the crop is adapted. All reincrease work will be done in isolation, or by sibbing or selfing according to the crop requirements. The value of the Laboratory will be realized more in the future than in the present. Requests for seeds of obsolete varieties have been filled, and as time progresses these kinds of requests will be increasingly evident. Collections which might be valueless when held under poor storage conditions in other places will be available at the Laboratory. In this respect, the Laboratory deserves much of the credit for rescuing the classical Blakeslee Duturu collection and other valuable genetic stocks. In the past, the working collections were reincreased every five years except where demand depletes stocks rapidly. By depositing small samples of the collections in the Laboratory, the increase interval can now be extended to 10 years with assurance that materials can be recovered from the NSSL. Under the provisions of the Plant Variety Protection Act, the NSSL could well serve in a new capacity. The Act requires that a viable sample of basic seed necessary for propagation of the variety will be deposited and replenished periodically in a public repository. This seed will serve as the reservoir for public use after the termination of the period of protection provided under the Act. The original policies under which the Laboratory operates were drawn up in 1959 by representatives of the Seed Trade, Commercial Plant Breeders, State Experiment Stations, and the Agricultural Research Service. Minor changes in policies were made in 196 I . The most important of these was a provision permitting a donor to deposit seed with a 5-year restriction on distribution as stated under Item f. The statement under Item j absolves the Laboratory of any responsibility for nomenclature, and Item n emphasizes the absence of Federal endorsement of any varietal material deposited in the Laboratory. The policies governing the NSSL are included below for the guidance of concerned scientists. a. The Laboratory is a Federal facility and all seed accepted for storage becomes Federal property. b. Only seed will be accepted for storage. c. Valuable seed stocks will be accepted by the Laboratory from Federal and State institutions, commercial seed interests, and private individuals. The basic criterion for acceptance is its potential use in plant breeding and genetic studies or fundamental biology. Information as to history and genetic composition and complexity is required for the retrieval of certain genotypes. d. Any bona fide research worker of the United States, its territories and possessions, may receive seed from collections stored at the Labora-

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tory subject to the restrictions in Item f. However, seed will not be provided by the Laboratory if available commercially or in working stocks of research agencies. The Laboratory will suggest sources of supply. e. The Laboratory will have no responsibility in relation to commitments with foreign countries. A11 requests from foreign sources will be sent to headquarters of the New Crops Research Branch, Beltsville, Maryland, where decisions in relation to foreign countries will be made. f. Both public and private donors of specific lots of valuable seed stocks or seed of new varieties, who wish to do so, may retain for a period not to exceed five years the exclusive right to withdraw or permit withdrawal of portions of such seed provided the optional restriction is clearly indicated at the time the seed lot or sample is deposited. No seed collection may be withdrawn in its entirety. After such time limit has expired, and on seed lots or samples deposited without this restriction, all seed deposited in the Laboratory shall be available to any bona fide research worker, whether public or private, of the United States, its territories, or possessions. g. The Laboratory will not hold bulk supplies or seasonal stocks: it is not a warehouse or seed distributing center. Rather, it is a germ plasm bank for valuable stocks to be held over the years for the use of research workers when needed. h. The Laboratory will issue periodic inventories of the stocks held in storage to inform research workers of material available. i. Only clean seed of reasonably high germination is acceptable for storage. If seed of low viability (below 60-65% germination) is received, it will be held on a tentative basis until the donor is able to provide replacement seed of higher viability (75% germination or better). j. N o charge will be made by the Laboratory for the service of furnishing seed. The Laboratory will use every care in keeping good records, but it is not responsible for errors which may occur in the original documentation. The varietal name supplied by the donor will be accepted by the Laboratory. k. When seed has been accepted officially, the Laboratory will be responsible for the increase of stocks if, during storage viability drops to a point where there is danger of loss of the accession or stocks have become depleted as a result of seed distribution. 1. The Laboratory will not assume responsibility for replenishment of stocks if the accessions received are sub-minimal in quantity or viability. However, if obsolete varieties are received not meeting the preceding acceptable standards, the Head of the Laboratory in consultation with the appropriate specialists in the Plant Science Research Division may make arrangements for increase.

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JOHN L. CREECH A N D LOUIS P. REITZ

m.The principal objective of the Laboratory is long-time holding of valuable seed, Research projects will be carried on at the Laboratory related to the Laboratory’s objective, i.e., physiological problems in seed viability and longevity. n. The acceptance of seed of a commercial variety by the Laboratory shall not be considered in any way a Federal endorsement as to the value of the variety. In addition to the above-revised policy, recommendations have been made as to what constitutes “valuable seed.” It is recognized that such a definition will vary greatly depending upon the significance attached to the present commercial value of the crop involved and the individual research worker’s evaluation whether he be a geneticist, horticulturist, agronomist, or pathologist. However, the following categories of crop seed will be accepted by the Laboratory: N e w Varieties: All newly released varieties, whether of private, public, or commercial origin, including reselections from varieties continuing in current use. Current Varieties: Varieties currently in use and under registration by respective crop group organizations, or otherwise documented as to specific origin and distinguishing characteristics. In this group would be included those varieties approaching obsolescence which have been superseded by new or currently popular varieties. Open-Pollinated Varieties: Stocks representing earlier varieties or types of specific crops which have been or will be replaced in the commercial field by hybrids. Inbred Lines: Parental lines of known genetic composition widely used in combination for hybrid production. Obsolescent Germ Plasm: Samples representing hold-over material from earlier research programs and of no immediate interest. Genetic Stocks: Includes materials of academic and genetic interests such as marker genes, mutants, translocations, monosomics, trisomics, and other chromosome aberrations. Replenishment of such stocks, if in a heterozygous state, will remain the obligation of the donor. With the latter type of stocks the Laboratory serves only as an insurance against loss. Plant Introductions: From Regional and Federal Introduction Stations or other agencies as seed is increased beyond “working stocks.” Differential Host Varieties: Used or being used as differential hosts for differentiating pathogenic races. Virus Indicator Plants: Used in indexing plant viruses. Physiologically Useful Species: Used in physiological studies or physiological assays. All inquires as to minimum quantities of seed required for specific

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crops, documentation, condition or quality, and other routine information should be addressed to the National Seed Storage Laboratory, USDA, Fort Collins, Colorado 8052 1. 2 . Other Storages National seed storages exist in a few other countries. A national center for conservation of germ plasm has been operating in Japan since 1966 at the National Institute of Agricultural Sciences, Hiratsuka, Kanagawa (Ito and Kumagai, 1969). Although the Hiratsuka storage has a similar responsibility as our Fort Collins storage for long-term preservation of seeds, it also serves as a distribution center for working stocks. This has resulted in some excellent research on containers for dual storageshipment purposes without having to disturb the seed during packaging. F A 0 and the Turkish Government established a Crop Research and Introduction Center at Izmir, Turkey, in 1964. A storage has been constructed to conserve the germ plasm native to Turkey and adjacent countries under optimum conditions of humidity and temperature (SchulzSchaeffer, 1970). Like the facility in Japan, this storage will serve for both long-term preservation of seed and distribution of working stocks. It also provides for exploration activities and other related aspects of the broad concept of a genetic resources center. Because of the support by FAO, the lzmir Center has taken on an international responsibility which might not endure should this support be discontinued. The International Rice Research Institute serves as an excellent example of a genetic resources center for a single crop. Founded in I962 at Los Banos, Laguna, Philippines (Chang, 1970; Chandler, 1970), lRRl is the effort of The Rockefeller Foundation, in cooperation with the Government of the Philippines, Ford Foundation, NSF, NIH, AID, and International Business Machines, Inc. This Institute has made spectacular progress in rice improvement. The germ plasm activities include preservation of primitive germ plasm and the development of an understanding of the complex system where there is a high frequency of outcrossing, low seed fertility, and other genetic factors combined with operating a storage where high temperature and high humidity prevail. The Institute holds over 900 wild forms of 38 entities as well as thousands of varieties of Oryza sativa L. As seed is increased these are transferred to the USNSSL as a backstop since the storage conditions are not considered truly adequate. Although the needs for long-term storage facilities for seed are recognized as essential, we are only on the threshold of this development. No one nation can hope to preserve all the species adequately. On the other hand, it is unrealistic to believe that every nation requires an expensive,

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JOHN L. CREECH A N D LOUIS P. REITZ

sophisticated seed storage. It falls on those nations with the greatest resources and stability to cooperate in such ventures. It is generally agreed that there is an urgent need to establish regional centers which will be concerned with long-term conservation of germ plasm in the Mediterranean, Western and Central Europe, and Scandinavia. There is also an awareness in the U.S.S.R. of the inadequacies of the current facilities for preserving the enormous number of collections (1 75,000) now held at the Vavilov All-Union Institute of Plant Industry, Leningrad (Brezhnev, 1970). It is an alarming fact that deficiencies exist all along the line in our efforts to establish stable centers to preserve germ plasm, and these will be compounded as efforts to collect germ plasm are emphasized. C. GAPS I N GERMPLASM One of the results of assessing the extent of our germ plasm collections is to identify gaps which can be closed by planned explorations that give priority to threatened materials. The sorghum germ plasm committee established by The Rockefeller Foundation in cooperation with the Crop Evolution Laboratory, University of Illinois, conducted a survey of collections and concluded that conspicuous gaps exist in wild and weedy forms of the genus and that many systematic collections have been lost due to lack of equipment and staff. There are incomplete collections of Chinese kaoliangs, Ethiopian and Sudanese varieties, primitive types from West Pakistan and other areas of Southeast Asia. Despite a major collection of sorghums in India, an absence of genetic barriers between the cultivated and wild forms, relatively few sorghum relatives have been used in breeding or are present in adequate variation in collections. As a consequence it is not known whether these species can be used successfully although they may be important sources of insect and disease resistance. But the threat to these resources by grazing and other agricultural pursuits continues unabated. A similar situation has been described for rice germ plasm. Although the present world collection consists of about 12,000 (Chandler, 1970) accessions representative of considerable varietal diversity, local races from such remote areas of northeast India across to northeast Thailand are deficient. Fortunately, through the use of PL 480 funds in India, an attempt is being made to systematically collect primitive and less important varieties in northeast India. Perhaps the greatest barrier to securing reserves of rice from some of these areas is the political and military conditions affecting these regions.

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Concern has also been expressed for the glaberrima (Oryza glaberrima subsp. stapfi (Roshev.) Chev.) cultivated in Africa as well as for the species which may be the clue to the evolution of this crop. Since this species appears as a weed as well, there is a deliberate erosion of it. With few sources of funds, such as PL 480, in the affected areas, collections from important areas of West Africa are unlikely. Realizing that some priorities for “rescue” operations to secure threatened germ plasm are necessary, the F A 0 Panel of Experts on Plant Exploration and Introduction ( I970a) recommended that the following are urgent projects. 1. The exploration and collection of primitive and wild wheats in Turkey, Iraq, Iran, Afghanistan, and West Pakistan because these resources are rapidly being displaced by introduced wheats. 2. The exploration and collection of glaberrima rices in West Africa as an important resource for future rice improvement. 3. The exploration and collection of native West African Dioscorea species which are being displaced by other root crops as well as subject to loss when propagating stocks have been used for food in times of stress. In reaching these priorities, the major concern has been for the rapidity with which agricultural development has proceeded and primitive crop varieties have declined. Germ plasm in those areas where subsistence agriculture has not changed drastically appears to be safe for the present as compared to regions where there has been a concerted effort by national and international groups to upgrade technology. Also some areas are much more accessible from the viewpoint of successive explorations. The series of explorations for primitive forms of beans (Phaseolus vulgaris L.) in Mexico, conducted by the USDA in 1966- 1967, resulted in a rich assortment of races which the local Indians selected and increased according to local environmental and ethnic demands. Fortunately, from the germ plasm aspect modern varieties have not made serious inroads in this traditional system of agriculture. In some parts of the world, decisions to require the growing of new varieties without a means of preserving the discarded ones has been detrimental to our germ plasm base.

IX.

Programs for the Future

We have now reached a time when serious consideration needs to be given to the direction our overall activities in germ plasm will take. The question is not so much what we can do, but whether the priorities that will be assigned by scientists and administrators to the conservation of germ plasm will meet the goals.

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In 1966, the National Academy of Sciences attempted to foresee the general trends of the plant sciences over the next decade. A section of the report (Anonymous, 1966) dealt with the future needs for basic research on the 15 food plants on which the world depends for its major sources of food energy. These are rice, wheat, corn, sorghum, and barley; sugarcane and sugar beet; common bean, peanut, and soybean; potato, sweet potato, and cassava; and banana and coconut. The report stressed the need to concentrate on basic biological characteristics of these principal food plants and to inventory and assess world resources of these and other plants which form the basis to today’s agriculture. It is interesting to note that much of the research accounting for our present agricultural abundance was conducted 25 or more years ago. We are in the era of research to meet the needs of the year 2000 and beyond. With new and menacing problems of the environment facing us, the need to accumulate as diverse a base of variability as possible becomes increasingly important. It has been made clear that these natural resources are not inexhaustible and the decline of primitive genetic resources continues unabated. Since U.S. agriculture is and will be dependent on the majority of these crops and others, it is to our national interests to be certain that the germ plasm we hold will fulfill the needs of future plant breeders. Among the specific programs for the future which are essential and which can be translated into programs for action are : (a) the development of plant resources information centers to cope with the expanding demand for expert information on the composition, use, and sources of plants beneficial to man; (b) the development of national and international clonal repositories to protect the dwindling resources of vegetatively propogated plants; (c) the development of more effective national and international surveys of holders of collections to make these genetic resources widely available; (d) the increased exchange of plant germ plasm among nations, and the initiation of such exchanges where they do not exist. A center, such as that recommended in recent conferences, to provide basic information on all kinds of economic plants is fundamental. In order to find out everything possible about crops as unique biological systems, a rich source of germ plasm is absolutely essential. While the National Academy of Sciences emphasized the 15 major crops, it is obvious that the need for germ plasm applies to basic inquiries into all plant species useful to man. Beyond the basic food crops, man’s needs for plants to provide adequate shelter, improved health, and aesthetic surroundings must be served.

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ACKNOWLEDGMENT The evaluations and use of germ plasm given as examples are largely from progress reports of the Plant Science Research Division and from annual and other reports o f the Coordinators of Regional Research Projects NE-9, Geneva, New York; NC-7, Ames, Iowa: S-9, Experiment, Georgia; W-6, Pullman, Washington; and IR- I , Sturgeon Bay, Wisconsin. REFERENCES Adair. C. R.. Atkins, J. G . . Beachell, H. M., Evatt, N. S., Everett, T. R., Green, V. E., Jr., Jodon, N. E., Johnston, T. H., Mikkelsen, D. S., Miller, M. D., Shaw, W. C., Smith, R. J., Jr., Thysell, J. R., and Webb, B. D. 1966. U . S . , Dep. Agr., Agr. Handb. 289, 1-124. Anonymous. 1966. “The Plant Sciences-Now and in the Coming Decade,” pp. 100-1 14. Nat. Acad. Sci., Washington, D.C. Anonymous. 1967. Annual report, 1966. Int. Rice Res. Inst., Los Banos, Philippines. Anonymous. 1968. Texas, Agr. Exp. Sta., Circ. L-731. Bennett, E. 1970. I n “Genetic Resources in Plants” (0.H. Frankel and E. Bennett, eds.), pp. 157- 178. Blackwell, Oxford. Berry, C. D., Lessman, K. J., White, G. A., and Earle, F. R. 1970. Crop. Sci. 10, 178-180. Brezhev, D. D. 1970. I n “Genetic Resources in Plants” (0.H. Frankel and E. Bennett, eds.), pp. 157- 178. Blackwell, Oxford. Chandler, R. F. 1970. “Catalog of Rice Cultivars and Breeding Lines (Oryza sativa L.) in the World Collection of the International Rice Research Institute.” Int. Rice Res. Inst., Los Banos, Laguna, Philippines. Chang, T . T. 1970. Sabrao Newsletter 2,59-64. Clark, J. A. 1936. Yearb. Agr. (US.Dep. Agr.) pp. 207-302. Clark, J. A. 1956. Econ. Bot. 10, 194-200. Correll, D. S., Schubert, B. G., Gentry, H. S., and Hawley, W. 0. 1955. Econ. But. 9,307375. Creech. J. L. 1963. Chemurgic Dig. 21,7-9. Creech, J. L. 1970a. Span. 13, I I 2- I I 4. Creech, J. L. 1970b. I n “Genetic Resources in Plants” (0.H. Frankel and E. Bennett. eds.). pp. 22 1-229. Blackwell. Oxford. Cullinan, F. P. 1961. I n “Germ Plasm Resources,” Publ. No. 66,pp. 91-102. Amer. Ass. Advance. Sci., Washington, D.C. Dodge, A. F., Ackerman, W. L., and Winters, H. F. 1965. Amer. Horf. Mag. 44,92-98. Fairchild, D. 1938. “The World Was My Garden.” Scribner’s, New York. FAO. 1967. “Report of the FAOllBP Technical Conference on the Exploration, Utilization, and Conservation of Plant Genetic Resources.” FAO, Rome, Italy. FAO. 1969a. “Report of the F A 0 Conference on Propagation of Tropical and Subtropical Fruits.” FAO, Rome, Italy. FAO. 1969b. “Report pf the Third Session of the F A 0 Panel of Experts on Plant Exploration and Introduction.” FAO, Rome, Italy. FAO. 1970a. “Report of the Fourth Session of the F A 0 Panel of Experts on Plant Exploration and Introduction.” FAO, Rome, Italy. FAO. I970b. “Plant Introduction Newsletter,” No. 23. FAO, Rome, Italy. Fisher. H. H. 1963a. U S . , Dep. Agr., A R S ARS 34-37-1, 1-324.

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Fisher, H. H. 1963b. US.,Dep. Agr., ARS ARS 34-37-2, 1-303. Fisher, H. H. 1964. U.S., Dep. Agr., ARS ARS 34-37-3, 1-292. Frankel, 0. H., and Bennett, E., eds. 1970. “Genetic Resources in Plants.” Blackwell, Oxford. Gentry, H. S. 1968. Econ. Bot. 23, 55-69. Hanna, G . C. 1966. In “Proceedings of the National Conference on Mechanization of Tomato Production,” pp. 9- 16. Nat. Canners Ass., Washington, D.C. Hanson, A. A. 1969. Proc. Int. Seed Test. Ass. 34,369-382. Harlan, H. V., and Martini, M. L. 1936. Yearb. Agr. (US.Dep. Agr.) pp. 303-346. Harlan, J. R. 1961a. I n “Germ Plasm Resources,” Publ. No. 66, pp. 3-19. Arner. Ass. Advance. Sci., Washington, D.C. Harland, J. R. 1966. In “Plant Breeding” (K. J. Frey, ed.), pp. 55-83. Iowa State Univ. Press, Ames. Hodge, W. H., and Erlanson, C. 0. 1955. Advan. Agron. 7,189-2 1 I . Hodge, W. H., Loomis, H. F., Joley, L. E., and Creech, J. L. 1956. Nut. Hort. Mag. pp. 86106. Howlett, F. S. 1957. Agr. Exp. Sta., Ohio, Res. Bull. 790, 1-131. Jenkins, M. T . 1936. Yearb. Agr. (US.Dep. Agr.) pp. 455-522. Ito, H., and Kumagai, K. 1969. Japan Agr. Res. Quart. 4,32-38. Jones, J. W. 1936. Yearb. Agr. (US.Dep. Agr.) pp. 415-454. Jones. Q., and Wolff. 1. A. 1960. Econ. Bot. 14,37-55. Khush, G. S., and Stebbins, G. L. 1961. Amer. J . Bor. 48,723-730. Lamon, R. E. 1961. In “Germ Plasm Resources,” Publ. No. 66, pp. 327-336. Amer. Ass. Advance. Sci., Washington, D.C. McCrory, S. A. 1958. South Dakota Agr. Exp. Sta., Bull. 471, 1-39. McKee, R., and Pieters, A. J. 1937. Yearb. Agr. (U.S. Dep. Agr.) pp. 999-1031. Magness, J. R. 1937. Yearb. Agr. ( U . S . Dep. Agr.) p. 604. Martin, J. H. 1936. Yearb. Agr. (US.Dep. Agr.) pp. 523-560. Munck, L., Karlson, K. E., Hagberg, W., and Eggum, B. 0. 1970. Science 168,985-987. Oakes, A. J. 1965. Trop. Agr. 42,323-331. Oakes, A. J.. and Langford, W. R. 1967. Agron. J . 59,387-388. Pieters, A. J., and Hollowell. E. A. 1937. Yearb. Agr. (US.Dep. Agr.) pp. 1190-1214. Radcliffe, E. B., and Lauer, F. I. 1966. Minnesota, Agr. Exp. Sra., Sta. Bull. 253, 1-23. 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. US., Dep. Agr., Agr. Handb. 338, I - 127. Reitz, L. P. 1970. Science 169, 952-955. Reitz, L. P., and Craddock, J. C. 1969. Econ. Bot. 23,315-323. Reitz, L. P., and Ward, D. J. 1958. In “First International Wheat Genetics Symposium,” pp. 143-159. Manitoba, Winnipeg, Canada. Ross, R. W., and Rowe, P. R. 1965. Wisconsin, Agr. Exp. Sta., Bull. 533, 1-73. Ross, R. W., and Rowe, P. R. 1969. Amer. Potato J . 46,5-13. Ryerson, K. A. 1967. In “Proceedings of the International Symposium on Plant Introduction,“ pp. 1- 19. Tegucigalpa, Honduras. Schulz-Schaeffer. J. 1970. Now 6, 8-9. Skrdla. W., Alexander, L. J., Oakes, G., and Dodge, A. F. 1968. Norfh Central Reg. Res. Bull. 172,l-1 10. Sowell, G., Jr., and Langford, W. R. 1963. Proc. Amer. Soc. Hort. Sci. 83,609-612. Stanton, T. R. 1936. Yearb. Agr. ( U . S . Dep. Agr.) pp. 347-414. Tysdal, H. M., and Westover, H. L. 1937. Yearb. Agr. (US.Dep. Agr.) pp. 1122-1 153.

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Vavilov, N. I. 1950. Chron. Bot. 13, 1-366. Vavilov, N. I. 1957. “World Resources in Cereals, Leguminous Seed Crops, and Flax and Their Utilization in Plant Breeding.” Acad. Sci. USSR, Moscow (transl. OTS 602 1127). Vinall, H. N., and Hein, M. A. 1937. Yearb. Agr. (U.S. Dep. Agr.) pp. 1032-1 102. Wall, J. S., and Ross, W. M. 1970. “Sorghum Production and Utilization.” Avi Publ., Westport, Connecticut. Ward, D. J. 1962. US.,Dep. Agr., Tech. Bull. 1276, 1 - 1 12. Webb, B. D., Bollich, C. N., Adair, C. R., and Johnston, T. H. 1968. Crop Sci. 8,361-365. Webb, R. E. 1966. In “Proceedings of the National Conference on the Mechanization of Tomato Production,” pp. 17-23. Nat. Canners Ass., Washington, D.C. Webb, R. E., and Bruce, W. M. 1968. Yearb. Agr. ( U . S . Dep.Agr.) pp. 103-107. Weiss, M. G. 1961. In “Germ Plasm Resources,” Publ. No. 66, pp. 103-1 16. Amer. Ass. Advance. Sci., Washington, D.C. White, G. A., and Higgins, J. J. 1966. US.,Dep. Agr., Prod. Res. Rep. 95, 1-20. While. G . A,. Cummins, D. G.. Whiteley. E. L., Fike, W . T., Greig, J. K., Martin, J. H , Killinger, G. B., Higgins, J. J., and Clark, T. F. 1970. US.,Dep. Agr., Prod. Res. Rep. 113, 1-38. Whitehouse, W. E., Creech, J. L., and Seaton, G. A. 1963.Amer. Horr. Mag. 42, 150-157. Yen, D. E. 1970. In “Genetic Resources in Plants” (0.H. Frankel and E. Bennett, eds.), pp. 341-350. Blackwell, Oxford.

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THE RELATION BETWEEN GEOMORPHOLOGY AND SOIL MORPHOLOGY AND GENESIS’ R. B. Daniels,

E. E. Gamble, and J. G. Cady

North Carolina Agricultural Experiment Station, Raleigh, North Carolina, a nd the Johns Hopkins University, Baltimore, Maryland

I. II. 111.

IV.

V.

Introduction .............. ......................................... Definition of Terms ........................................................... Evolution of Soil-Ge Criteria Used in Geo A. Surface Sequence, Depositional ........................ B. Surface Sequence, Erosional ................................................. C New Terminology .......................................................... Examples of Soil-Geomorphic Relations ............................. A. A Hillslope Study in Uniform Material .............. B. Australian Laterite and Solonetz ...................................................... C. New Mexico Desert-Argillic and Carbonate Horizons in Desert Soils .............. ............ ................ D. North Carolina Coastal ........................... ................ Summary ........... ...................................................... ..... References ...............................................................

I.

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s3 55 56 58 61 62 62 65 70 76 84 86

Introduction

Geomorphology is defined in the Glossary of Geology (Howell, 1957) as the “systematic examination of land forms and their interpretation as records of geologic history . . . .” Pedology is the science that studies the soils whose upper boundaries are the surface of the earth. A strong link should exist between these two sciences because they deal with parts of the same thing. Before World War 11 there was little conscious interchange of ideas between t h e two disciplines and even less application of the methods of one science to the solving of problems in the other. During World War 1 I , there was close collaboration among soil scientists and geologists in the Military Geology Unit of the U.S. Geological Survey. This started an interchange of ideas that has been increasing. During the ‘Paper No. 3367 of the Journal Series. A joint contribution from the Soil Conservation Service, USDA and the Department of Soil Science, North Carolina Agricultural Experiment Station, Raleigh, North Carolina.

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R. B. DANIELS, E. E. GAMBLE, A N D J . G . CADY

last twenty years there has been widespread effort to apply the concepts and knowledge of the stratigrapher and geomorphologist to problems of soil morphology and genesis. This report summarizes some of the progress made in recent years. Practically all work dealing with the distribution of soils on the earth’s surface employs some geomorphic concepts. In developing a short history of the interrelation between the two sciences, we will limit our review mainly to studies where geomorphic and allied approaches were used primarily to provide background information for soil genesis studies. This eliminates most studies of parent materials, of relations between distribution of glacial drift and soils, and of soils studied in relation to topography, slope, drainage, or erosion. It also eliminates most pure geomorphic studies, and we will not attempt to review the large volume of literature on buried soils. For those interested in the literature on buried soils, the papers by Thorp (1965), Morrison ( 1 968), and Ruhe (1968) are good places to begin. A paper by Hunt (1954) shows how stratigraphic principles can be used to determine the age of soils. We will define and illustrate the geomorphic criteria used in the various studies and define the terminology used. A limited number of studies that combine geomorphology and soil genesis work will be summarized. DEFINITION

OF

TERMS

Certain terms with precise meanings are used throughout the text. These and a few more general terms are defined as follows: Geomorphology. The science that studies the evolution of the earth’s surface. Geomorphologists are interested in how a surface evolved, what factor or factors were involved, and when these processes started and stopped. Stratigraphy. The science that studies the formation, composition, sequence, and correlation of rocks as parts of the earth’s crust (Howell, 1957). Land forms. “Features of the earth that together make up the land surface” (Ruhe, 1969). Weathering zones. Horizons or layers of rock or sediment altered from its original state, usually by subaerial weathering. Alteration may involve the loss of carbonate, weathering of minerals such as feldspar, and the removal or rearrangement of iron, and many other elements. The term “weathering zone” is used extensively by workers in the United States Midwest Pleistocene (Ruhe, 1954) and by Australian (Mulcahy, 1967; Northcote and Tucker, 1948) workers when describing laterite.

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Peneplain. A broadly undulating erosion surface that is almost a plain (“pene” meaning “almost”). Surface. A two-dimensional form that has length and width but no thickness. It may be a plane or it may be composed of compound curves. Geomorphic surface. A mappable feature that is “a portion of the landscape specifically defined in space and time” (Ruhe, 1969). The surface of the earth is made up of a large number of geomorphic surfaces. But there is the implication used throughout this paper that a geomorphic surface is something more than a part of the surface of the earth. It is a part that has been studied and mapped. A geomorphic surface may be depositional (formed by deposition of sediment) or erosional, or both. It may be a level plain, a straight slope, or may have a multicurvate or undulating configuration. It may be confined to one rock-type or sedimentary formation, or it may cut across several. A geomorphic surface may have formed in a short time throughout its extent, as in a lava flow or ash fall, or if erosional it may have taken a long time to develop. A geomorphic surface may be uplifed, lowered, faulted, or warped by tectonic movements, and it may be buried without being destroyed. But once a surface is eroded, it is destroyed because by definition it has no thickness. The erosion creates a new surface. To summarize, a geomorphic surface is a part of the surface of the land that has definite geographic boundaries and is formed by one or more agencies during a given time span. The time span may be relative or absolute. II.

Evolution of Soil-Geomorphic Concepts

Early workers in .soil genesis and classification used the classic ideas of geology and physiography to explain differences in soils and grouped soils on a geographic basis. But for a long time little attention was given to landscape age or to the origin of particular land surfaces. The distribution and genesis of laterite has intrigued geologists and soil scientists for years, and it is in the discussions of laterite that some individuals more or less pointed toward the relations between geomorphology and soils. Newbold ( 1 844), in discussing the laterite of southern India, said: “ I t is evident not only that it must have covered it (the peninsula) formerly to much greater extent than at present, but that it has since been much broken u p by the-subsequent denudation . . . . I t is impossible to compare these scattered and detached portions without imagining that the whole intervening country has once been covered with a great body of laterite, enormous masses of which have been removed by denudation” (quoted from Prescott and Pendleton, 1952). These and other comments of Newbold ( 1844, 1846) definitely pointed to the prob-

54

R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

ability that laterite in this area was the result of previous weathering and that it was much older than the soils on the later erosional and depositional surfaces. This is one of the first reports where specific parts of the landscape and allied soils were at least relatively dated. Woolnough ( I9 I8), in discussing the physiographic significance of laterite, stated, “If this view is correct (laterite formed under peneplain not plateau conditions), then the importance of laterite from a historic point of view is greatly enhanced. It owes its present position on the summit of the plateau to the uplift of the peneplain.” Davis ( 1920) believed that laterite formed in the old age of the peneplanation cycle. These statements point to the geologists’ belief that remnants of old landscapes are preserved. Soil scientists frequently have a physiographic bias when they discuss the soils of a region. This is illustrated by the publications of Marbut et al. ( 19 13) and Coffey ( I9 12) in which soils were discussed by physiographic regions such as “soils of the Piedmont Plateau Province, etc.” Yet Coffey and Marbut understood and used soil-landform relations. Marbut (1928), probably citing Fowler’s work (1927), talks about the Tifton series being on a very old land surface. Coffey apparently recognized that soils on stream terraces in Alabama were younger than those on the adjacent uplands and that they should be considered as another group. Milne ( I 935) in his original article on the Catena noted that the profiles changed along the traverse from the ridgecrest to the stream in accordance with topography and its influence on drainage. The present topography was in part influenced by that of times past. He discussed a complex of soils in Tanganyika and hinted that the red earths may be relict soils, especially when associated with calcareous black clays (Milne et af., 1935). Milne et al. recognized how landscape evolution can affect soils when they wrote, “The great plateaux lying behind the eastward-facing ranges carry material which was graded down during a long process of peneplanation, and which therefore may (a) retain characters impressed during its first weathering, (b) have acquired new ones as its profile developed under conditions of sluggish drainage, and (c) by undergoing a fresh adjustment to conditions of rejuvenated drainage following the elevation of the peneplain into plateaux.” Milne et af. were well aware that the history of the land surface had considerable influenc‘e on soil properties. Probably more important was the understanding that different parts of the landscape may have had different histories. The influence of various factors on soil development has been discussed by early writers (Glinka, 1963), but Milne et al. are among the first to clearly point out some of the multiple factors involved in soil-landscape relations. Since 1940 emphasis has been on the history of the landscape in rela-

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tion to soils. The Australian and African workers have been concerned with soils that could not have developed under the present climate. Numerous publications from Africa have dealt with the influence of previous weathering on soils (Nye, 1954, 1955; Spurr, 1954; Ollier, 1959; Radwanski and Ollier, 1959; Watson, 1964; Jongen, I96 1 : Maigninen, 1961; Maud, 1965). Similar work in Australia emphasized the fossil nature of laterite (Crocker, 194 I , 1946; Prescott, 1944; Stephens, 1946, 1949; Northcote, 1946; Playford, 1954; Blackburn and Leslie, 1958). After the initial work on the fossil character of laterite, many Australian workers paid increasing attention to minor modification of the landscape by erosion and deposition (Butler and Hutton, 1956; Hutton and Stephens, 1956; Van Dijk, 1958, 1959; Butler, 1958). This later work challenged several established soil-geomorphic concepts. Butler ( 1959) tested the geomorphic theory that large areas of t h e landscape had been stable against his evidence of episodic erosion and sedimentation. He developed the K-cycle concept from this work. Butler’s work was used and amplified by Van Dijk (1959), Walker, (1962, 1963), and Churchward (1963). Soil-geomorphic work in the United States in the 1950’s and early 1960’s was in regions where Quaternary deposits and complex erosionaldepositional surfaces make up a large part of the landscape (Daniels and Jordan, 1966; Gile, 1970; Hawley, 1965; Parsons and Balster, 1966; Parsons et al., 1970; Balster and Parsons, 1969; Ruhe, 1967, 1969). These studies emphasized the relations between geomorphic surface and soils, with the weight being placed on time relations based on radiocarbon chronology. A somewhat similar course was followed in Australia during the 1960’s where soil studies established a history of the profile based on its known geologic history (Mulcahy, 1960; McArthur and Bettenay, 1960; Wright, 1962, 1963; Bettenay and Hingston, 1964; Ward, 1966; Turton et al., 1962; Blackburn et al., 1967; Bettenay et al., 1964). Present work uses geomorphic data to develop ideas about how soils form. Soil scientists are trying to find out when a process starts and how fast it goes. With this greater interest in soil process, there has been an increase in the need for stratigraphic studies, pollen analysis, radiocarbon dating and many other kinds of information. Ill.

Criteria Used in Geomorphic Work

Most geomorphic work involves several other fields of geology, but one of the most used is stratigraphy, or the study of the sequence and correlation of rocks. The principle of superposition is used to determine

56

R. B. DANIELS, E. E. GAMBLE, A N D J. G. C A D Y

sedimentary and geomorphic surface sequence. This principle simply says that younger beds occur on top of older beds, providing they have not been overturned. In Fig. lA, bed 2 is younger than bed I because the A

B

Bed

2

Bed

I

-~

C

wu/ Bed

I

D

I

FIG. I . Generalized illustrations of typical sedimentary sequences. Relative ages of the beds can be determined by the principle of superposition, i.e., bed 2 is younger than bed 1.

younger bed always overlies the older. In Fig. 1B the topographically higher bed 2 is younger than bed 1 because it still overlies bed 1. Although the landscape form is the same in Fig. IB and IC, the topographically higher bed 2 in Fig. IC is the youngest because it overlies bed 1. The age of bed 3 in Fig. ID is questionable. Beds 3 and 4 are younger than bed 2, but bed 3 may be older than, equal to, or younger than bed 4. No greater refinement of dating beds 3 and 4 in relation to each other can be made with the available information. There are two types of geomorphic surfaces, depositional and erosional (Fig. 2). As their names imply, one is formed by deposition of sediments, and the other by erosion. On many landscapes, a surface can have depositional and erosional elements (Fig. 2B), and the two elements are considered as one surface. A. SURFACE S E Q U E N C E , DEPOSITIONAL Depositional surfaces are the same age as the immediately underlying sedimentary laminae. These surfaces do not necessarily have the same

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57

age throughout because sediment can be deposited on one part of a plain and not another. A depositional surface, however, should be restricted to one depositional episode and it must be shown that there have been no A Deposltional /Surface A

7 sed\JEros!on Bed

Surface

\

I

B

B Depositional Surface

A

Erosional Element,

Depositional Surface B

Element, Erosion

C

I

Bed

I

\t

FIG. 2. Generalized relations between geomorphic surfaces and sedimentary deposits. The principle of superposition can be used to determine the relative ages of sediments and surfaces. A geomorphic surface is younger than the youngest bed it truncates.

subsequent additions or removal. Depositional surfaces usually are dated by the age of the underlying beds that were formed somewhat earlier, but in the same depositional episode. For example, a depositional surface is late Miocene if it is at the top of a late Miocene formation, or it is amidPleistocene surface if the underlying beds are mid-Pleistocene. Stratigraphic superposition determines the relative ages of depositional surfaces, but in many instances the younger surfaces are topographically lower (see Fig. 3A). In eolian landscapes, the depositional surface may have a wide range in altitude (Fig. 3B). The relations shown in Fig. 3A are common in river valleys and in belted coastal plains where the highest depositional surfaces are the oldest and the lowest ones are the youngest. The relations in Fig. 3B are common in eolian landscapes whether the material is sand or parna (sand-sized clay aggregates). Figure 3B also illustrates that a surface may have a simple or a complicated two-dimensional shape.

58

R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

A.

OR M A R I N E

FLUVIAL

LANDSCAPES

Depositional Surface A , Bed

2\

Bed

I

J

b

B.

EOLIAN

e

Depositional Surface B

d 3

LANDSCAPES

-

Depositional

k Bed

d

3

I

FIG.3. Depositional surfaces; their age is determined by the age of the beds on which they occur. (A) Fluvial or marine landscapes. (B) Eolian landscapes.

B.

SURFACE S E Q U E N C E , EROSIONAL

Erosional surfaces are more complex than depositional surfaces in their distribution, relations to other surfaces, and dating. The following principles are very useful in determining the ages of erosional surfaces (Trowbridge, I92 I ; also see Ruhe, 1969). An erosional surface is younger than the youngest material it cuts, any structure it bevels, or any neighboring surface that stands at a higher level (Fig. 28). (There are some exceptions to the latter.) An erosional surface is older than valleys cut below it or deposits in that valley related to later alluviation, and it is older than any lower adjacent erosion surface. An erosional surface is the same age as the depositional surface it is graded to. The age of an erosional surface usually is determined in the field by observing what it slopes downward to and merges with in a smooth concave profile. In Fig. 2A, erosional surface B is younger than bed 2 and depositional surface A because it cuts, bevels, or truncates them. If the lower part of bed 2 were deposited 10,000 years ago, then depositional surface A is less than 10,000 years old. If depositional surface A is 8000 years old, then erosional surface B is less than 8000 years old. Figure 2B illustrates why an erosional surface is younger than a higher adjacent surface. Sur-

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59

face C truncates bed 3 and depositional surface B, therefore it is younger than either. Most landscapes consist of interfluves and valley slopes, and the relative ages assigned to erosional surfaces are based on relations of the slopes to alluvial fills. The alluvial fills are also good sources of material for radiocarbon dating. Figure 4 illustrates why radiocarbon dating is so Let us assume that bed 1 is Cretaceous and bed 2 is late Miocene. Deposit i o n o l Surface A

1

Surface B ,Erosional Element

010.000

60.000.000 yr

.

FiII,Bed

yr

3

14,000 yr

9,000 yr

FIG. 4. The age of a surface may be determined by its relation to other surfaces, sediments, and radiocarbon dates.

Because the erosional element of surface B’truncates bed 2, it is postMiocene, or younger than about 10 million years. The problem is that it could date from any time within this I0 million year period. Bed 3 is the alluvial fill associated with erosional surface B. The radiocarbon age of the base of the fill is 14,000 years. The subaerial element of erosional surface B, the sediment-air interface, is less than 14,000 years old because it slopes downward and grades to the top of bed 3, not to the base of bed 3. Another radiocarbon date near the top of bed 3 is 10,000 years. Thus, we now know by the relations shown in Fig. 4 that the erosional and depositional elements of surface B are less than 10,000 years old. But again we do not know how much less. If somewhere we can find datable material in beds younger than 3, then we can date surface B. If, for example, bed 4 is cut into bed 3 and has logs 9000 years old near its base, then we are justified in dating the erosional and depositional elements of surface B as being between 10,000 and 9000 years. We consider time zero of a geomorphic surface as the time when it was first exposed to subaerial weathering. On an erosional surface, this would be when erosion at that point stopped; on a marine depositional surface, it would be when the ocean withdrew and exposed the sediments to subaerial weathering. By this definition, the age of the geornorphic surface and the associated soil is the same. This definition may help overcome some of the confusion about soil-surface relations discussed by Moss ( I 968).

60

R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

Throughout the geomorphic literature there is considerable emphasis on a “stepped sequence of surfaces,” such as shown in Fig. 4. In most landscapes, profiles constructed along interfluves from the drainage divide to the stream will show a “stepped sequence” of levels. These levels are easy to see in the field. But stepped interfluve summits do not always represent remnants of erosional or depositional surfaces, especially if they are narrow and convex across the top when viewed in cross section. The interffuve summits may be related to the youngest erosion cycle, but their form and altitude may be related to resistance of the rock or position between streams. Each case must be proved; an accordance of altitudes of interfluve summits may suggest, but does not prove by itself, the existence of a remnental geomorphic surface. Erosion frequently produces a large discontinuity in ages of soils from one surface to the next. In Fig. 4, soils on depositional surface A are approximately 10,000,000 years old, but a short distance away on surface B the soils are 9,000 to 10,000 years old. While this is a true statement, it does not give all the history of a site on surface B. Soils formed under old depositional surfaces such as A in Fig. 3 may have solums 10-15 feet thick and an associated weathering zone, or zones, that may be tens of feet thick, especially under some of the Australian laterities (Wright, 1963). I n Fig, 5 , erosional surface B

7

Depositional Surface A B Hor

/////////////////y

U

01

m

-

a

m

‘Y

- --- -

I-------”

Unweathered Material

-8,

Bed I

FIG. 5 . Truncation of weathering zones by erosional surfaces. The soil properties are determined in part by the nature of the outcropping weathering zone.

truncates bed 2, its weathering zones, and the solum of the soil under surface A. It should be obvious that a soil under surface B at point u will have a solum that cannot be distinguished from one under surface A. In this case the solum was formed under surface A, but it was truncated during the formation of surface B. Progressively downslope from point u are soils formed in weathering zones I , 11, and 111 until at point c the

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61

solum apparently was formed in fresh materials. A soil formed at point b has developed in the last 9000 to 10,000 years from materials weathered during an earlier period. The chronological age of the solum is 9000 to 10,000 years, but its characteristics have been determined in part by earlier weathering. This outcropping of weathering zones occurs in Iowa (Ruhe et al., 1953, Australia (Northcote and Tucker, 1948), and Africa (Ollier, 1959). The outcrop pattern of weathering zones is very important when the distribution of soils is considered, and it is one of the major reasons why geomorphic surfaces and their associated soils do not have the same aerial distribution (Gamble et al., 1970). One may consider it more or less academic that point a of Fig. 5 is on a chronologically young surface - Why not consider it as part of surface A because the soils are the same? The reason is that the age of a geomorphic surface must be proved by geomorphic criteria, not soil criteria. That part of surface A above point a has been destroyed by erosion, and it no longer exists at this point, although its underlying weathering zones are intact. Truncation of soil horizons can be used as geomorphic evidence, but not the properties of these horizons. If soil criteria are used to prove the geomorphic surface then the geomorphic work cannot be used to prove the soil. The recognition, delineation, and dating of geomorphic surfaces in the detail required for soil-geomorphic relations involves considerable field work. The relation of surfaces to the underlying sediments, weathering zones, and to adjacent surfaces must be determined in a three-dimensional examination. Erosional surfaces require tracing in the field because most topographic maps have contour intervals too large to show the detail needed. The age of an erosional surface on a valley side is determined by what it grades to (or slopes down to and merges with in a smooth concave profile): its relative elevation or form has little meaning. An example of the detail needed is shown by some monadnocks rising above the Piedmont in North Carolina. From a distance the side of a monadnock appears to slope down to and merge with the Piedmont Peneplain. But when looked at in detail, most of the monadnock’s surface grades to the ephemeral streams on its sides and to the perennial streams at its base. The surface, therefore, is the same age as the streams, not the Piedmont Peneplain. This example illustrates why direct tracing in the field is necessary to determine the age of a surface and why younger erosion surfaces can locally rise above older surfaces. C. NEW TERMINOLOGY As more geomorphic-soil studies were made, a number of soil scientists became dissatisfied with some of the older concepts of geomorphic sur-

62

R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

faces. As a result, there have been several changes in nomenclature in a attempt to closely tie the geomorphic work to the soils (Butler, 1959; Don and Yaalon, 1968). Butler wrote ( 1959), “Their (geomorphologists) land surfaces, surfaces, or erosion surfaces are defined in terms of relative elevation, form and shape, or agency of formation, or in terms not involving soil criteria. Hence, it cannot be assumed that the definition of surfaces by either geologist or geomorphologist will bear any constant relationship to those defined by the pedologist.” He then proposed the term “groundsurface,” which was defined as “all those erosional and depositional surfaces and layers which have developed in a landscape during one interval of time and upon which a unit mantle of soils has developed.” Butler proposed the term “K cycle” to include the time interval from formation of the surface to its destruction by erosion or by deposition of other material. Detailed soil-geomorphic work has been done elsewhere using standard stratigraphic and geomorphic nomenclature (see Ruhe et al., 1966; Daniels and Jordan, 1966). If the geomorphic work is detailed and accurate, then the surfaces of interest to soil scientists and geomorphologists are the same. The authors believe that soil scientists should use the standard nomenclature of geologists so that all concerned with the subject can understand each other. IV.

Examples of Soil-Geomorphic Relations

There are numerous published soil-geomorphic studies. In this section we shall discuss some of these studies to illustrate the range and scope of the work. A. A HILLSLOPE STUDYI N UNIFORM MATERIAL Loess normally is a uniform material, and it should be ideally suited for studying the influence of various factors on soil formation. A cross section of an interfluve summit and adjacent valley slopes in Harrison County, Iowa (Daniels and Jordan, 1966) is shown in Fig. 6A. The material is Tazewell loess, and the sample sites of soils with slopes from I to 20% are shown. The traverse is from WNW to ENE. As would be expected from the study of Norton and Smith ( 1 930), some soil properties appear to be related to slope gradient. In the Iowa example, solum thickness and depth to carbonate decrease as slope gradient increases (Fig. 6B). There was no apparent difference in soil properties by aspect. With this much information available, a possible conclusion would be that the changes in soil properties shown in Fig. 6B are a true reflection of the effect of slope. The most probable explanation of this conclusion would

GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D GENESIS

63

be that steeper slopes result in less infiltration and more runoff, thus giving a drier site and less soil development per unit of time. A WNW

Lo

ENF

MI

M 5M \ 2 A

-60

\,

,

I 400

0

M4

I

800 Ft

B Solum Thickness

p e p f h t o Carbonate

y.88 6 - 3 4 6 x

n

20 0 20 Slope Gradient, P e r c e n t

FIG. 6. Hillslope study in Iowa. (A) Location of sampled profiles. ( B ) Relation between slope gradient and selected soil properties. (Idealized from Daniels and Jordan, 1966.)

How did geomorphic work improve the interpretation? First, through regional (Ruhe, 1969) and local stratigraphic studies it was found that the loess under broad flats or gently rounded summits has an upper noncalcareous or leached zone overlying calcareous loess. The distribution of these zones is shown in Fig. 7A. Local work, not illustrated, showed that this upper leached zone has about this same thickness under gently convex summits (as in Fig. 7A) or under level interfluves. This suggests that the centers of these gently rounded summits may be a depositional loess surface, and, if this is true, soil formation could date back approximately 15,000 years. The base of the leached loess is nearly level from the ridge crest to the steeper valley slope where it thins and curves downward, nearly paralleling the valley slope. This feature could be interpreted as a draping of the leached loess over calcareous loess. If this interpretation is made, it then follows that the landscape is the same age throughout. The curving downward of the thin leached loess under the valley slopes can also be interpreted as evidence that the valley slopes truncate the weathering zones of the loess. The small amount of leached loess on these slopes would then

64

R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

postdate the erosion of the slopes. Based upon this last interpretation, we now have probable differences in age between the sample sites on the ridge crest and valley sides, and also differences in slope gradient. But we need additional evidence to test these interpretations. A

,

Lo

0

I

400

I 800 Ft

6. Loess

1800 y r Mullenix

FIG. 7. Hillslope study in Iowa. (A) Location of sampled profiles in relation to loess weathering zones. (B) Relation of profiles to Hatcher Alluvium. (Idealized from Daniels and Jordan, 1966.)

Aerial work gives additional evidence. The slopes from M5 to M8 and M2 to M4 grade downward to the top of the Hatcher alluvium (Fig. 7B). The top of this alluvium is about 1800 years old. There is no evidence of a later deposit on the Hatcher where it stands above the Mullenix bed. The slopes that grade to the top of the Hatcher must therefore be about I800 years old. We now have a slightly different history for the soils sampled across this loess landscape than that provided by Fig. 6 alone. We have reason to suspect that profiles M3, M4, M6, M7, and M8 have formed from calcareous loess during the last 1800 years. Sites M5 and M2 were eroded 1800 years ago, but they formed partly in noncalcareous loess. Site MI may have been uneroded during the last 15,000 years; but if eroded 1800 years ago, very little material was removed because the noncalcareous loess is as thick here as under broader flats. Therefore, many

GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D GENESIS

65

of the characteristics of the soil at MI can date back to the end of loess deposition. The relations shown in Fig. 6B are the result of a combination of slope gradient, character of parent material, and length of weathering. Because climatic and vegetative changes are known to have taken place in Iowa during the last 15,000 years (Ruhe and Scholtes, 1956), weathering intensities also may have changed. If we want to evaluate the influence of slope on soil properties, only profiles M3, M4, M6, M7, and M8 could be used. To have much statistical significance, many more samples would be needed. The above study illustrates the generally complex history of even a relatively young landscape. Without knowledge of the erosional modification of the landscape, the worker would conclude that all, or many, of the differences in the soils are the effects of differences in moisture regime. But other interpretations are made when the stratigraphic and geomorphic work are considered. Maximum ages of the erosional and depositional elements of the landscape are established. Radiocarbon dating gives precise age differences, and pollen studies suggest that the climate has changed within the time span of soil formation. Thus the factors of time, slope, aspect, and parent material become controlled variables to be used in explaining the differences in soils. But there is still the further complication of climatic change that cannot be fully evaluated. A N D SOLONETZ B. AUSTRALIAN LATERITE

The Merredin area of western Australia is an excellent example of an old, deeply weathered landscape being modified by later erosion and deposition. The soils on the modern land surface and the processes currently operating are influenced by the total history of the area, not by just the most recent episodes. For example, the Merredin landscape has large areas of lateritic soils but receives only about 12 inches of rainfall annually. The detailed work discussed here was done by Bettenay ( I962), Bettenay and Hingston (1961, 1964), and Bettenay et al. ( 1 964). Part of this work was generalized later by Mulcahy ( I 967). The geomorphic evolution of the Merredin area is fairly well understood. It has not been affected by Pleistocene sea level changes because it stands above the nickpoints of erosion cycles initiated by uplift along the Darling Fault Scarp. From its position above the nickpoints, one would think that the area would be stable because the streams had not cut deep valleys. But detailed work has shown that minor erosion and deposition have modified the formerly extensive mid-to-late-Tertiary surface and weathering zones. These modifications are believed to be associated with climatic changes during the Pleistocene and Recent times.

66

R. B . DANIELS, E. E. GAMBLE, A N D J . G. CADY

During late Tertiary time, the entire area from the old plateau to the center of the shallow valleys probably had lateritic soils with thick weathering zones (Fig. 8A). Riverine activity in the valley stripped the

A.

NEW

I OLD

PLATEAU Breakaway

\

PLATEAU

Duricrust Yellow I

6.

Fic. 8. Soils and sediments in the Merredin area, Australia. (A) Relation of soils to topography and weathering zones. (Idealized from Bettenay and Hingston, 1964.) (B) Sediments to the lee of salt lakes, Horizontal hatchure is riverine deposit; vertical hatchure is colluvium. (From Bettenay, 1962.)

lateritic profile down to the pallid zone, resulting in an initial lowering of the valley floor. Contemporaneous erosion of the old plateau did not uniformly remove all of the preexisting profile, but in places left materials that later hardened to duricrust. Nearly level areas of the old plateau were deeply eroded in places which later were filled with sandy materials weathered from the laterite. These deposits are the sand plains, and they are considered to be relatively young because locally they are mixed with lake parna. Extensive colluvial deposits 4-5 feet thick overlie the pallid zone on the floors and sides of tributary valleys. The colluvium was derived from up-

GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D G E N E S I S

67

slope erosion of the duricrust, the pallid zone, or bedrock, depending on the amount of truncation. The colluvium merges or interfingers with relatively thin riverine deposits overlying the pallid zone. Extensive salt lakes or salinas occur on the valley floor. These are believed to be part of a river system that was active in Tertiary time. Uplift dismembered the rivers, and wind further modified them during postTertiary arid phases (Bettenay, 1962). Eastward, to the lee side, of the salt lakes are gypsum dunes, sand, silt or clay lunettes, and sheets of lake parna overlying riverine and colluvial deposits (Fig. 8B). Dunes of gypsum are being added to today by material crystallizing on the salt lake surface. Although the old plateau is still covered by several feet of material weathered duringTertiary time, there probably is none of the original Tertiary surface remaining (Mulcahy, 1967). The surfaces and the associated sediments are Pleistocene or later, but the effects of Tertiary weathering are still expressed in the soils and in the processes operating on that landscape. Some of the soils of the old plateau have formed in materials weathered during Tertiary, but exposed or reworked by post-Tertiary erosion. The duricrust has formed by drying of materials exposed by truncation of the laterite. Sandy deposits 15 or more feet thick formed by erosion of the laterite smooth out the irregularly eroded surface of the old plateau. These sandy soils are Yellow Earths (Fig. 8A) and have only trace amounts of Na, K, Ca, and Mg. The clay fraction is mostly kaolinite. Soils on colluvial materials and on parts of the riverine sediments are Brown Solonetz. In the B horizons, they have a clay maximum; and many have concentrations of carbonate. They have reasonable amounts of potassium. Near the old plateau, soils in preweathered materials have thin A horizons over acid mottled kaolinitic clays. Some soils in riverine and eolian sediments toward the centers of the valleys are affected by saline ground waters. On the lee sides of salt lakes are modern gypsum dunes, sandy lunettes with minimal soil development, and clayey lunettes, calcareous and saline, with no or very little soil development (Fig. 8B). In the sheets of lake parna, the soils are rich in carbonate, soluble salt, and acid-soluble potassium. Some of the potassium is from eolian alunite, but the greater part is from illite (Bettenay, 1962). Soils in the Merredin area are closely related to the weathering, erosional, and depositional history of their sites. Yet not all soil properties seem to be consistent with the stratigraphy or geomorphology. For example, the high calcium carbonate and potassium content of the soils in colluvium is not consistent with their being derived from weathered

68

R. B. DANIELS, E. E. GAMBLE, A N D J. G. CADY

granite or lateritic materials. Their topographic position makes it seem unlikely that ground water ever approached the surface and, if it did, the ground water in the pallid zone should be low in calcium and potassium. Most likely, small additions of parna to the colluvium are responsible for the high carbonate and potassium content (Bettenay and Hingston, 1964). Although these additions may explain the potassium and calcium content of soils in colluvium, it does not explain the original source of these elements because the plateau and the valley are underlain by the Tertiary pallid zone that is very low in alkali and alkaline earth metals. More detailed work by Bettenay et al. (1964) gave considerable additional information on the source, distribution, and relation of alkali and alkaline earth metals to the past history of the area. A cross section in the Belka Valley, part of the Merredin area, is shown in Fig. 9. The

FIG.9. Water movement in the Belka Valley, Western Australia. (From Bettenay et al., 1964.)

aquifer is the pallid zone resulting from Tertiary weathering of granite and gneiss. Overlying the aquifer in most places is a dense clayey aquiclude, which has above it sandy bodies and fine textured soils. Saline patches developed at seep spots in sandy materials after the area was cleared of native vegetation. The saline areas near the salt pans have been growing in size. These saline areas are the result of decreased transpiration and some increase in water entering the aquifer. Runoff has increased since clearing, but the runoff waters do not become saline until they flow across saline soils. The stream systems flow periodically, and the salinity values of the flow drops to less than 100 me/l if flow persists for some weeks (Hingston, cited by Mulcahy, 1967). The salt deposits in

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69

the lake areas therefore probably represent only a few years’ accumulation, and the net result of runoff is ultimately to remove salts from the system by way of the major drainage (Bettenay et al., 1964). Water analyses and water-table data from wells spaced across the landscape were used to interpret the origin of the salt (Fig. 9). From the intake area to the outlet, the salinity of the ground water increased in a regular manner from about 100 to about 800 me Cl-/l (Fig. 1 OA). The salts could not be concentrated by downward movement from soils because the aquiclude is relatively impermeable and the underlying aquifer is under pressure. I t is reasonable to assitme t h a t most of this concentration of salts is not from the aquifer because it is highly weathered material, low in salts. Bettenay et al. believe that the increase in salts is due to loss of water, ultimately as vapor, from the aquifer upward through the aquiclude by the combination of positive aquifer pressure and capillary action (Fig. 9). Toward the center of the valley the aquifer comes closer to the surface, and the whole soil is within the saturation zone of the now highly saline waters. Although upward movement is slow, it is by this process that salts accumulate. Eolian activity can then redistribute these salts across affected parts of the landscape. Bettenay et al. found that although the total salt content of the ground water increased from the intake to the outlet, the proportion of Na, K, Ca, Mg, and SO, decreased relative to chloride (Fig. IOA). This decrease in alkali and alkaline earths is associated with a decrease in pH from neutrality to less than 4 and an increase in aluminum and iron in solution (Fig. 10B). Apparently there is an exchange between the acid (aluminum) clays of the aquifer and the highly saline ground waters. Local rocks are either highly weathered or they are fresh granite. In either case they are not a good source for the salts in the area. Rainwater analyses indicate that the major source of salts in the Belka Valley is atmospheric accession of ocean salts and local or regional terrestrial sources. These salts enter the system in the rainwater, and they are concentrated locally by the mechanisms outlined above. Interpretations about the distribution of soils on the landscape and their physical and chemical properties are based largely on what is known about the stratigraphic and geomorphic history. Other factors such as salt content, its source, and how it gets to a specific part of the landscape are geochemical problems, but there is no clean-cut separation from soil chemistry. Interpretations of chemical data are modified by and partly depend upon stratigraphic and geomorphic data. Yet the stratigraphic and geomorphic data by themselves tell only part of the history of the area that is of interest to the soil scientist because they do not explain the source of salts nor their mode of accumulation.

70

E; K&

R. B. DANIELS,

E.

E. GAMBLE, A N D J . G. CADY

soor

A

/

-8

E400 \ E400 _I a, \ _I

E

Mg

Ca

400 Salinity ( M e CI-/Ltler)

0

Inlet

800

Outlet

160

r

B.

Aprox

I

E

Q

LW L

0

400

800

Salinity ( M e CI-/Liler)

Inlet

f

Outlet

FIG. 10. Changes in chemical composition of ground water, Belka Valley, Western Australia. (A) Relation between me of Na, Mg, SO,, Ca, and K per liter and salinity. (B) Relation between pH and salinity and Fe and Al concentration and salinity. (From Bettenay el al., 1964.)

c.

NEW MEXICODESERT-ARGILLIC A N D CALCIUM CARBONATE HORIZONSI N DESERTSOILS 1 . Geologic Setting

Ruhe, Gile, Hawley, and others have studied the land forms and soils near Las Cruces, New Mexico, for the purpose of “determining their origin within the physiographic history of the region” (Ruhe, 1967). The vegetation of the area is desert grassland (Humphrey, 1958). The annual precipitation at Las Cruces is 8-9 inches, but it increases to about 15 inches in the mountains (Ruhe, 1967; Gile et al., 1970). Most of the precipitation falls during the hot summer months: July has a mean temperature of 80°F (E. L. Hardy, 1941). The climate of the Las Cruces area is roughly similar to the Merredin area studied by Bettenay et al. (1964), but the geologic histories and soils are different. The Australian area is modified, highly weathered Tertiary peneplain, whereas the Las Cruces area is a tectonically controlled river

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71

valley and an internally drained basin area that dates its oldest surfaces and weathering from mid-Pleistocene (Ruhe, 1967). The stratigraphic-geomorphic history has been discussed by Ruhe ( 1962, 1964, 1967), Hawley ( 1963, Hawley and Kottlowski ( 1969), Hawley et al. (1 969), and Gile et al. ( 1970). The area in mid-Pleistocene time was composed of the internally drained Jornada del Mureto and the Mesilla Basins. Each basin had two major components: piedmont slopes and basin floors. The piedmont slopes include erosional surfaces and constructional alluvial-fan and coalescent-fan surfaces, and the basin floors include alluvial flats and playa-lake plains. Cutting of the present Rio Grande Valley system began in late mid-Pleistocene time. Development of graded valley-border surfaces related to episodes of valley-floor stability started with the emplacement of the Rio Grande. There was erosion and sedimentation in the internally drained basins and fan piedmont areas (Table I) at the same time the valley-border surfaces developed. This produced landscape areas that have been relatively stable for periods ranging from several thousands of years to several hundreds of thousands of years. But in contrast to the often highly weathered materials of the Australian area, the soils in southwestern New Mexico formed in relatively fresh unconsolidated debris derived from rhyolite, tuff, andesite, monzonite, limestone, shales, and sandstones (Ruhe, 1967; Gile and Grossman, 1968). The surficial basin-fill deposits in many areas consist of sediments derived from one rock type, and this provides excellent parent material control for soil studies. The climate apparently has had alternating episodes of moist and dry conditions from mid-Pleistocene to the present, although the record is sketchy. Ruhe (1967) accepted local and regional pollen studies and hydrologic reconstruction of pluvial lakes north of the area as evidence of a wetter environment more than 9500 years ago. Gile et al. (1970) cite faunal evidence for a significant lowering of life zones believed to be associated with past glaciation. R u h e ( 1962) believed that in the Las Cruces area the past pluvial environments should have resulted in greater vegetative cover, landscape stability, and soil formation. The interpluvial environments, as the present one, resulted in weaker vegetative cover and, in many areas, unstable landscapes and severe erosion. Reworking by wind and at least small additions of dust to old surfaces is a possibility, if past interpluvials were as dry as or drier than the present climate (see Gile, 1966a). The evidence cited by Ruhe ( 1967) and Gile et al. ( 1970) indicates that climate has not been stable from mid-Pleistocene to present. Neither the magnitude of these fluctuations nor their duration and distribution in time can be given detailed treatment. This part of the history of the area

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R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

TABLE I Geomorphic Surfaces and Soils in the Las Cruces Area" Major soils

Surface

Age and elevation ancestral Rio Grande above present flood-plain levels

Alluvial fan, piedmont, and apron Organ 1 100-4600 years

Issaks' Ranch Jornada I1

6400 years-latest Pleistocene Late Pleistocene

Jornada I

Mid-Pleistocene

Dona Ana

Mid-Pleistocene

Basins and scarplet surfaces Holocene and late Pleistocene Lake Tank Petts Tank La Mesa

Late Pleistocene M id-Pleistocene

Valley-border erosion surfaces Fort Seldon Group 1000-2600 years (43 ft) Fillmore Leasburg

7300 years-latest Pleistocene (65 ft)

Picacho

Late Pleistocene (70-90 ft)

Tortugas

Mid-late Pleisotcene (115-15Oft)

"From Ruhe (1967) and Gile er al. (1970).

Low carbonate parent materials

High carbonate parent materials

Haplustolls, Entisols, Camborthids, weak Haplargids Haplargids

Haplustolls, Entisols, weak Calciorthids

Haplargids, Paleargids, Calciorthids, Paleorthids Calciorthids, Paleorthids, Haplargids, Paleargids Paleargids, Calciustolls, Paleort hids

Calciorthids, Paleorthids

Torrerts, Haplargids Paleargids, Paleorthids, Haplargids

Entisols, Cam borthids Entisols. Camborthids, Haplargids, Calciorthids Haplargids, Paleargids, Calciorthids, Paleorthids -

Calciorthids -

Entisols Calciorthids

Calciorthids, Paleorthids

Calciorthids, Paleorthids

GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D GENESIS

73

would be valuable in soil genesis studies where one is concerned with rates of soil formation. Regardless of the magnitude of climatic fluctuation, apparently at no time since t h e Rio Grande Valley established its present course has the water table been close enough to the surface to influence the soils (Gile et al., 1970). This may be one of the major reasons why few saline soils occur in the area even though an abundance of sodium is in the parent rocks. 2 . Argillic Horizons Argillic horizons are of great interest to soil scientists because they are used as indicators of profile development. Horizons in the B position in the Las Cruces area range from raw alluvium to well expressed argillic horizons on the older surfaces (Gile, 1966b, 1970; Gile and Grossman, 1968; Gile ef al., 1970). Soils on historical (formed after the area was settled) surfaces show little or no evidence of soil formation. Soils on post Pleistocene-prehistoric surfaces have cambic horizons, and those on Pleistocene surfaces have argillic horizons. If the clay content is the same, argillic horizons are redder in soils on the older surfaces. Exceptions to these generalizations are found where soil fauna have destroyed these horizons and where they have been engulfed by carbonate (Gile et al., 1969). The morphology of the argillic horizon varies somewhat with texture. Many of the buried Pleistocene soils have prominent clay skins. But soils under the present surface with medium to fine textures do not have clay skins on ped faces although they are found in those parts of the argillic horizons that extend down pipes in the carbonate horizon. Evidence for clay illuviation in soils under the present surface is found in remnants of clay skins inside peds and in preferred orientation of clay around sand grains and pebbles. Apparently processes operating since late Pleistocene favored disruption of, or have not furnished stable sites for, clay skins. Gile and Grossman ( 1968) believe that the processes leading to clay skin disruption are carbonate accumulation, disruption by roots and fauna where the argillic horizon is close to the surface, and high-energy moisture changes involving montmorillonitic clay. Gile ( 1970) believes that silicate clay is currently accumulating in some soils. His belief is based on the fact that noncalcareous B horizons within the zone of wetting show evidence of clay illuviation. Gile et al. (1970) also show that 1339% of the dust presently falling in the Las Cruces area (0.1 kg/m2/yr) is clay-sized material. Thus there is considerable potential for adding clay-sized material to the surface of these soils. Given sufficient time, argillic horizons apparently could form even under present conditions. Prominent argillic horizons in soils in the Las Cruces area are thought

74

R. B . DANIELS, E. E. GAMBLE, A N D J . G . CADY

to have formed primarily during Pleistocene pluvials when more water was available for downward translocation of materials (Ruhe, 1967; Gile 1966b, 1970; Gile and Hawley, 1966; Gile and Grossman, 1968). The lower parts of these prominent argillic horizons are thought to be largely relict, but silicate clay presently is accumulating in their upper parts. The present apparently represents a period of low-intensity clay illuviation rather than a complete cessation of the process.

3. Calcium Carbonate Horizons Some of the more interesting work in the Las Cruces project has been done on calcium carbonate (lime)- its morphology, accumulation, and genesis. Gile et al. (1966) developed the concept of “stage of carbonate (lime) accumulation” that is applicable over wide areas (Fig. 11). The I

II

FIG. 1 I . Stages of calcium carbonate accumulation in gravelly soils near Las Cruces, New Mexico. The solid black areas are calcium carbonate. (From Gile et al., 1966.)

morphology resulting from lime accumulation in nongravelly soils is different from that in gravelly soils during the early stages, but later on they resemble each other. The various stages in both types of soils reflect an increase in the amount of lime accumulation and concurrent changes in morphology. In gravelly soils, the skeletal grains are coated with lime in the latter part of stage 111, and most of the pebble interstices are filled or plugged. At this stage, infiltration is markedly reduced and, with continued additions of lime, the horizon developes into stage IV. In stage IV, horizontal nearly pure calcium carbonate laminae overlie a lime plugged horizon. The laminar horizons, the tops of which look like poorly trowled concrete, vary considerably in thickness, and some show multiple layering. This laminar horizon has very low infiltration rates, high unconfined compressive strength, and high bulk density (Gile, 1961). It also is a barrier to roots (Gile e f al., 1966), and it physically forces the overlying material upward as the calcite crystallizes. Gile et al. believe that a plugged horizon (late stage 111) must develop

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75

before the laminar horizon can form. The numerous laminae suggest that the accumulation of the laminar horizon is a long-term process, and radiocarbon dates show that the laminae become younger upward (Gile et al., 1966). On the other hand, radiocarbon dates from a thick laminar horizon under the La Mesa surface suggest that some of these horizons can form quickly (Gile et al., 1970). Soils on all geomorphic surfaces except part of Lake Tank (Table I ) have some lime accumulation regardless of the rock type involved (Ruhe, 1967). Stage I is found in soils on the post-Pleistocene Fillmore surface and stage I 1 in soils on the Leasburg surface (> 7300 years to latest Pleistocene). Stages 111 and IV are found in soils on the late-Pleistocene Picacho and older surfaces (Gile et al., 1966). All sediments under old surfaces have thick horizons of lime accumulation. Ruhe ( I 967) believes that the lime in monzonitic and limestone sediments could be derived from the sediments themselves. But in rhyolitic gravels, these lime accumulations would require the decomposition of thick layers of the gravel. There is no evidence of decomposition of rhyolitic gravel. Therefore, other sources for the calcium must be sought where the sediments are dominated by rhyolite. Analyses of clay on a carbonate-free basis indicate that many calcic horizons also are zones of maximum clay (Gile, 1970; Gile et al., 1966; Ruhe, 1967). I t is suggested that the clay had to accumulate before being sealed and plugged by calcium carbonate because the permeability of these laminar or plugged horizons is almost nil. The above data is evidence that calcium carbonate engulfed part of former Bt horizons. Organic carbon sealed in a laminar calcium carbonate horizon from under the Picacho surface is 9550 years old. The underlying argillic horizon can be no younger than 9550 years because the overlying laminar calcium carbonate prevented further additions of clay. The last Wisconsin glacial period ended about 10,000 years ago. Ruhe suggests that the argillic horizon sealed under the laminar horizon is related to a wetter (pluvial) episode; and the lime deposition to a later drier (post pluvial) episode. Gile (1970) generally agrees with the time of argillic horizon engulfment, but he thinks that most of the lime of Recent age would have been emplaced in the lower part of the argillic horizon now developing above the laminar horizon rather than in the laminar horizon. Later radiocarbon data on organic carbon from laminar calcium carbonate horizons (stage IV, Fig. I 1) also suggest that the occluded organic matter is from pluvial periods. These pluvial periods were about 12,000 and 20,000 years ago. Dust traps in the study area collected about 0.1 kg/m2 per year (Gile et al., 1970), or about 1 cm of dust every 160 years. The dust added

76

R. B. DANIELS, E. E. GAMBLE, A N D J . G . CADY

about 0.2-0.4 g of CaCOa/m2/yr.Calcium is also brought in by precipitation, and Gile et al. estimated that about 2 g of CaCOJmz/yr is contributed to the soils from all atmospheric sources. They conclude that the major source of authigenic calcium carbonate is not from dry dust but from precipitation. Gile (1970) and Gile et al. ( I 966, 1970) generally accept the eolian origin for much of the calcium carbonate found in these soils. On the other hand, Ruhe ( 1 967) believes that pedogenic processes, eolian sources, groundwater and surface-water deposition may all have had a part in formation of a lime horizon in the Las Cruces area. Ruhe felt that it is not possible to separate the amount contributed by various processes. Later work shows that ground water probably has not been involved in lime deposition because the water table has always been 100 feet or more below the major surfaces (Gile et al., 1970). Some of the very intriguing questions raised by the Las Cruces work are: ( I ) What was the variation in calcium addition during pluvial periods? (2) What was the source area if dust was a transport vehicle during these pluvial periods? and (3) What would be the effect of pluvial periods on calcium carbonate morphology and placement in the profile? This work in the Las Cruces area again emphasizes that there are strong relations between geomorphic surfaces and soils. But it also shows that soils weathering for any length of time may have complex developmental histories. Evidence has been presented that pedogenic processes have either been discontinuous throughout time, or there has been considerable variation in intensity of process. This work shows that soil scientists should be cautious about conjectures regarding soil genesis based largely upon soil-profile characteristics. D. NORTHCAROLINA COASTALPLAIN 1 . Surficial Geology

The upper Coastal Plain near Raleigh, North Carolina, lies above an altitude of 275 feet. The upper Coastal Plain is a deeply dissected area with gently convex interfluves and a few narrow flats. These flats are remnants of pre-middle Coastal Plain depositional and erosional surfaces (Daniels et al., 1966),but they make up less than 10% of the area (Gamble et al., 1970). Average slope toward the ocean is 3-4 feet per mile across the remnants, but local slope gradients are near 1 foot per 100 feet (Daniels et al., 1970a). The Coats scarp,with a toe altitude of about 275 feet, marks the eastward limit of the upper Coastal Plain. The middle Coastal Plain.occurs as three stepped surfaces (Fig. 12) between the Coats and Surry scarps and has large areas of nearly level surface remaining. Regional slope to the east is 2-4 feet per mile and local slopes

GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D GENESIS

77

average less than 0.5 foot per 100 feet. These middle Coastal Plain surfaces are not absolutely flat but have a gentle swell and swale relief. UPPER COASTAL PLAIN

I

MIDDLE COASTAL P L A I N

FIG. 12. Idealized section of the Coastal Plain from west of the Coats Scarp to the Surry Scarp in North Carolina.

In the surficial sediments, quartz usually dominates the sand fraction, with minor amounts (< 10%) of feldspar and resistant heavy minerals. The clay fraction is largely kaolinite with less than 2 % mica. Textures range from clay to sand. The usual textural sequence is loamy sand to sandy loam in the lower beds grading upward into heavy sandy loam to sandy clay sediments at the surface. These sediments are 20-40 feet thick, and they usually overlie less permeable, more clayey, older formations. The surficial sediments are relatively thin compared to divide width in the middle Coastal Plain. This characteristic allows the lower beds to be saturated by water perched above the less permeable layer. The stream system usually trenches the surficial sediments and, in the upper Coastal Plain, cuts deeply into the underlying formations. This trenching allows the dissected edges of the surface to have deep water tables, but it may have little effect on water tables in the centers of broad divides such as those found in some areas of the middle Coastal Plain. The upper Coastal Plain surficial sediments are fluvial late Miocene to Pliocene deposits (Daniels et al., 1966; Daniels and Gamble, 1971). The middle Coastal Plain surficial sediments are fluvial Pliocene to possibly early Pleistocene deposits that may have some marine beds. The depositional and erosional surfaces in the upper Coastal Plain are late Miocene to Pliocene and have been weathering for about 10 million years. Surfaces in the middle Coastal Plain are Pliocene to possibly early Pleistocene age. The surfaces and the soils under them have been weathering

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R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

from 2 or 3 to about 8 million years. This is a long time for surfaces to exist without modification (Mulcahy, 1961), but a recent study (Daniels et al., I97 I ) indicates that they are stable. Part of the surface stability is related to the vegetational and climatic history. There seems to be no evidence that this area has had an arid or semiarid climate since the Miocene. Most evidence suggests a Pliocene climate similar to that present (Isphording, 1970). The climatic stability suggests that the vegetative cover has been nearly the same throughout the history of these geomorphic surfaces. Vegetation shifted to more northern types during the Pleistocene (Whitehead, 1963, 1964, 1969; Frey, 1953), but it was a matter of degree, because many pollen diagrams show mixtures of northern and southern species. The present climate in the Coastal Plain has warm summers and mild winters. The average July temperature is about 80°F and the January temperature about 45°F (A. V. Hardy et al., 1967). Precipitation is about 48 inches per year. 2 . Water Regimes The surficial deposits in the middle Coastal Plain are thin and the underlying formations are clayey and have low permeability. On wide divides this means that the water must move laterally above the underlying formation for long distances before the soils can drain after wet seasons. The upper Coastal Plain, on the other hand, is deeply dissected and the remnants of the original flats are narrow. The water table stands in the solum for only short periods because of this remnantal characteristic. Although the streams cut through the middle Coastal Plain surificial sediments, only the edges of the large flats are well drained. Water-table data from the Coharie surface near Newton Grove, North Carolina, allows us to partially reconstruct past water regimes. When the surfaces were formed, and before the stream system incised, the water table probably stood at or near the surface much of the year. The extent of the flats at that time is unknown, but it must have been miles between drainage systems. After the streams incised, the depth to the water table would be partially controlled by depth of incision and by the distance from the edge of the surface. Figure 13 shows the yearly water table regime of the Coharie surface at Newton Grove, North Carolina. All sites used are on the swells of the surface, and the stream system has cut through the surficial sediments so that additional stream incision without narrowing the divides will have little effect on water table levels. Sites farther than 0.37 mile from the surface edge are extrapolations of actual data obtained from sites closer to the edge (Daniels et al., 1 9 7 0 ~ ) . If the divide is 2 miles wide, the water table in the center of the divide

79

GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D GENESIS

is within 20 inches of the surface about half the time, and within 5 inches about 25% of the time. If the divide is as narrow as 0.2 mile, the water table drops so that the isopleth for 50% saturation (half the time) is about A

---__

-----___ ----------_

_----

0

I

l

01

02

l

,

1

1

06

04

1

,

I

08 Divide

B

/’

0

I

10

I

I

12

I

,

14

I

,

16

I

,

18

I

2.0

Width.Miles

C

,.-.,

01 03 Divide Width, Miies

05 Divide W i d t h , M i l e s

Fic. 13. Water table levels at Newton Grove, North Carolina: (A) 2-mile wide divide; (B) 0.5-mile wide divide; (C) 0.2-mile wide divide. The 25%. SO%, and 75% lines are saturation isopleths, or the level at which the soil is saturated 25, SO, or 75% of the time.

55 inches and the isopleth for 25% saturation is about 36 inches below the surface. The greatest change in water-table depth occurs when the divide is less than about 0.4 mile wide (Fig. 13). The change in water table per unit of divide width is small if the divides are from 2 to 0.4 mile wide. There is a close relation between soil morphology and water table levels. At Newton Grove, North Carolina, the B horizon at the dissected edge of the surface is a yellowish red (SYR 5/6) sandy clay (Daniels and Gamble, 1967). Soils with this color and texture form a discontinuous band about 0.05 mile wide around the edge of the surface and the water table seldom rises above 60 inches. Away from the yellowish red edge is a zone of soils with strong brown B horizons about 0.02 mile wide that,

80

R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

farther from the edge, is replaced by soils with yellowish brown B horizons. Several other soil properties have a progressive variation as the depth to the water table decreases across this sequence of soils. A2 horizons thin and their clay content increases (Fig. 14), and the clay and gibbsite

,A 2

Thickness

8 2 Clay C o n t e n t

‘A2

Clay Content

Lo

Gibbsite ,Content

--

Be H o r i z o n Thickness

20 60 I n c r e a s i n g Depth t o W a t e r Toble

FIG. 14. Generalized relations between selected soil properties and water table depth.

content of the B horizons decrease. The thickness of horizons with Be bodies (Daniels et al., 1968) increases to a maximum and then decreases. Only generalizations are given here, but these sequential changes have been discussed elsewhere (Daniels and Gamble, 1967; Daniels et al., 1967, 1968, 1970b, 1970~).It must be emphasized that these ordered patterns of change are on one geomorphic surface and in one nearly uniform parent material. The only differences that can be found are in the distance of the soil from the dissected edge of the surface, and the accompanying changes in the water table regime (Fig. 13). These morphological changes associated with the dry dissected edge of the surface are repeated on older and younger surfaces, and they are the rule rather than the exception. The B horizons on the dry edge are not always yellowish red, but they are brighter and may have redder hues than horizons away from the edge. This close connection between soil morphology, physical, and chemical properties, and water table levels seems to be a cause and effect relation because it is repeated at similar topographic positions over a wide area of the North Carolina Coastal Plain. In the middle Coastal Plain, dissection of the landscape determines the water table level. These soil-

GEOMORPHOLOGY A N D SOIL MORPHOLOGY A N D GENESIS

81

landscape associations are an example of how an external factor such as landscape dissection can be a control in soil morphology and genesis. There are several inferences about soil development that can be made from the relations between soil morphology and water-table levels. The first is that it would be possible for a soil on a remnant of a once broad divide to have had a water regime sometime in its history that was similar to that shown for each point in Fig. 13A. We do not imply that the bands of soils like those associated with the present dry edge will march across the landscape to the divide center. The water table regime associated with each soil will move across the landscape as dissection continues, but there may not be time or materials available to produce the soil patterns that we see now. If a broad divide could be narrowed at a uniform rate, the greatest change in water table, and possibly soil morphology, per unit of time would be where the divide has become less than 0.4 mile. This is where the water table starts to drop sharply. This suggests that when soils have been exposed to soil formation for long periods (2-6 million years in our example) their age is much less important than the internal environments. I n other words, soil formation is not necessarily a linear function of time (Daniels et al., 1970b). These relations also illustrate how soils on old stable surfaces may change when their environment changes. Processes, such as A2 horizon formation, may occur late in the history of the site in the center of the divide, yet the same process may have been active much earlier at other locations on the same surface. Thus it is necessary to know much more than how long a soil has been forming, because this information sets the time limits only. What we need to know is what has happened within these time limits.

3 . Soils with Plinthite Certain soils in the middle Coastal Plain and most of the soils in the upper Coastal Plain have a subsurface horizon that is strikingly mottled red, yellow, and gray. The red parts are iron concentrations. The pattern is reticulate with a horizontal orientation. Part or all of the red material will become hard if exposed to several cycles of wetting and drying. Other red iron concentrations with the same general appearance will not harden. The material that will harden is called plinthite, and the term will be used here to distinguish the material that will harden from the similar-appearing soft mottles that may be an incipient or earlier stage of the same process (Soil Survey Staff, 1960). Near Newton Grove, North Carolina, soils with less than 5 % plinthite make u p about 30% of the Coharie surface. The plinthite occurs 45 to 60 inches below the surface. I n the centers of the divide, these horizons are saturated with water 50-75% of the time (Fig. 13). The red mottles in

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R. B. DANIELS, E. E. GAMBLE, A N D J . G . CADY

these soils occupy 15-25% of the horizon, but only 3-5% of the horizon hardens upon exposure. This is incipient plinthite. Horizons with plinthite underlie about 5 5 % of the somewhat older Brandywine surface near Benson, North Carolina. Red mottles occupy about 25-30% of the horizon, and those that will harden make up about 15% of the total horizon. On the Brandywine surface, plinthite occurs in well and moderately well drained soils over large areas but is absent in some well drained soils near the dissected edge of the surface. Water perches for considerable periods above the horizontal platy plinthitic horizon. The true water table is below the plinthite horizon most of the year, as would be expected for a divide position less than 0.4 mile wide (Fig. 13). The divides in the Plain View surface of the upper Coastal Plain are about 0.2 mile wide, and plinthite makes up 25-30% of the plinthic horizons. Almost all red mottles harden upon exposure, and plinthite is under all of the Plain View surface in our study area. The true water table is always below 10 feet, yet water is held up in the plinthic horizon between 5 and 10 feet for several months each year. This perching is more a slowing down of water in the iron-rich zones than absolute impermeability as shown by the fact that all wells in plinthite will dry out during low rainfall periods. The distribution of soils with plinthite and the water table regimes associated with them at Newton Grove suggest that moderately high but fluctuating water tables are necessary to start plinthite formation. We believe that plinthite starts to form when a horizon is saturated 50-75 % of the time. During the initial stages of formation, this horizon does not perch water. When plinthite occupies about 10% of a horizon it perches water and keeps the horizon saturated for considerable periods. The plinthite horizon on the Brandywine surface has a water regime similar to that in the incipient horizon at Newton Grove, although the true water table is below 5 feet most of the year. Water regime of the soils on the Plain View surface is similar to that on the Brandywine except the saturation period of the plinthitic horizon is less. Plinthite occurs only on the local swells or high parts of the landscape on the Coharie and Brandywine surfaces. It fades and disappears as the soils become somewhat poorly drained. Thus, initial plinthite formation is a process in soils with somewhat restricted drainage. Its occurrence on the high parts of the landscape on slopes of 2-3 feet per mile almost precludes much lateral transfer of iron. If lateral transfer was the mechanism involved, then plinthite should occur in the low parts, not the high parts, of the landscape. Also if horizontal movement were active one should find a concentration gradient from weak to strong in the flow direction. None is found. Apparently, the concentration of iron is from within the

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83

pedon and not from outside sources. But more work needs to be done to find the source of iron. Is it brought from below as well as above, or is it segregated within the horizon? Plinthite occurs under a large part of the Brandywine surface except in the poorly drained soils. But it underlies all the higher older Plain View surface. The distribution of plinthite raises the question of whether or not it formed in former poorly drained soils on the Plain View surface after dissection lowered the water table and their drainage improved. For a poorly drained soil to develop into a well drained soil with plinthite would require considerable redistribution and possibly additions of iron. But our studies suggest that this does not happen because the configuration of the landscape and the mode of dissection make the preservation of poorly drained soils the exception rather than the rule. The gentle swell and swale landscape in the middle Coastal Plain is in reality a miniature drainage system with the swells forming the drainage divide and the swales forming the valleys and internally drained basins. After heavy rains, such as those accompanying hurricanes, runoff collects in the lows or swales. If the water is deep enough, it slowly moves from outlet to outlet until it connects with a drainage head. These drainage heads always end at or near a swale area of the undissected surface, suggesting that stream trenching and headward cutting is along the swales, or where the water collects. Thus, the poorly drained soils would be removed during landscape dissection, and the local swells or microdrainage divides would be the last to erode. Therefore, it is logical to assume that the soils with plinthite on the Plain View surface probably have been on the better drained parts of the landscape ever since plinthite formation started. They may never have been poorly drained. The increasing amount of plinthite from the Coharie to the Plain View surface is almost a textbook example of a soil geomorphic surface relation, i.e., the more strongly expressed soil properties occur in older surfaces. One interpretation of this type of data is that it is an age relation, or with increasing time there is increasing profile differentiation. We believe this interpretation is only partly true for several reasons. In the relation between plinthite and surfaces, one cannot assume a linear development of plinthite with time. I t does not necessarily follow that 10 times more plinthite will occur in a profile that has been weathering 10 times longer than another. Profiles on the Brandywine and Plain View surfaces have about the same amount of red mottling in the plinthitic horizon (20-30% of the mass), but they differ largely in the amount or percentage of mottles that will harden. On the Brandywine, about half the red mottles harden whereas all of them harden on the Plain View surface. The question is: when, in the development of plinthite, did all the

84

R. B. DANIELS, E. E. GAMBLE, A N D J . G . CADY

mottles on the Plain View surface become capable of hardening? Was it 10,000 years ago or 1,000,000 years ago? Profiles on the Plain View surface probably have reached the maximum degree of plinthite development possible under parent material and other controlling conditions. Additional time of weathering therefore will not change the degree of plinthite expression in these soils unless internal environments change so that plinthite can be destroyed. The increase in percentage of plinthitic soils from the younger to the older surfaces should not be interpreted as evidence of a constantly increasing area of soils with plinthite. There may be some increase in these soils during the initial stages of plinthite formation, from the Coharie to the Brandywine surface, for example. Plinthite is present under nearly all remnants of the Plain View surface, but its total area may be less because erosion may have removed plinthic as well as nonplinthic soils. Even though there is a relation between plinthite and surface (and it is partly a time function), one may not assume an age relation between a soil process and the geomorphic surface (Daniels et al., 1970b). The infrequent occurrence of plinthite on the younger Sunderland surface (Fig. 12) and its sporadic distribution on the Coharie are interpreted as evidence that plinthite formation did not start when the surface was first exposed to subaerial weathering. The Sunderland and Coharie surfaces may be 2 to 6 million years old, yet in that time they have developed essentially no plinthite, whereas the older Brandywine and Plain View surfaces have large amounts. Thus environmental conditions, some created by geomorphic processes, such as stream dissection, are more important in determining soil properties than a direct age sequence. V.

Summary

The studies reviewed represent a variety of relations between age and type of geomorphic surface and soils. The studies all show that conclusions about soil genesis based on conventional analysis and conventional consideration of present soil-forming factors usually are improved when geomorphic and stratigraphic information is added. It is a common practice to interpret a property as always indicating the same combination of factors. But in reality, a soil or other natural object can develop its features by a number of different possible routes. Knowledge about the history of a site, its relation to the surrounding landscape and especially the duration of its existence and exposure to various environments help clarify our understanding of the object we now see. Geomorphologists and pedologists have an overlapping interest in the same object. One studies the origin of the shape of the surface of the

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85

earth, the other studies the collection of natural bodies, soils, just beneath that surface. The geomorphic history of a site is also the history of the soil in that place. In addition to the shape of the land and its history, the origin of the material, past climates, water table regimes, outside additions such as dust and cyclic salt are also part of the geomorphic record. The pedologist studies soils in the field and laboratory to understand how their characteristics came to be and also to determine the importance of the characteristics - whether they are durable or transient. If he knows the history of the landscape in which his objects occur, in the way shown by the studies discussed here, he is in a position to interpret and decipher many things that might seem either too easily obvious or strange and anamalous. Since pedology is primarily a historical science, not an experimental one, solutions to its problems depend on having as much knowledge as possible about the natural variables that contribute to the resulting soil. The experiment has been run; we must interpret the results. The geomorphic data on process of development of the surface, its age and past climate and vegetation regimes provide far more control than is available in the properties of the soil itself and eliminates assumptions about the meaning of the direct observations. The studies discussed here are geomorphic in the main, but other fields of the earth and biological sciences are used. The contribution of geomorphology can and should be much more than a listing of the ages of surfaces and sediments (Wooldridge, 1949) because this is only the first step. If the concept that soil is the product of the interaction of the classical factors, these factors could well combine in different degrees to produce the same result on surfaces of different ages. One must avoid the trap involved in the easily made assumption that soils on old surfaces have passed through all the stages illustrated by what now exists on adjacent younger surfaces. This may be true, but it implies a continuity of factors in space and time-a very difficult hypothesis to prove. Frequently the assumption is made that rates of soil formation can be estimated by plotting some parameter as a function of time. This assumption may work in some areas where climate and other factors have been somewhat uniform across a sequence of surfaces. But most areas have had episodic fluctuations of soil-forming factors. The New Mexico and the Merredin, Australia, areas are examples. Thus the intensity of soil formation may vary greatly with time on one surface. The factor producing variations in intensity may be climatic as suggested for the New Mexico area, or it may be related to internal changes of soil environment, such as a drop in the water table, as suggested by work in North Carolina (Daniels et a/., 1970~). Geomorphic work is of maximum utility to the pedologist when it

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R. B. DANIELS, E. E. GAMBLE, A N D J . G. CADY

is used to develop a site history. Probably of greater importance, however, is that the pedologist may start asking new questions about morphology and genesis when such additional background material is available. REFERENCES

Balster, C. A,, and Parsons, R. B. 1969. Northwest Sci. 43, 1 16- I 19. Bettenay, E, 1962. J . Soil Sci. 13, lo- 17. Bettenay, E., and Hingston, F. J. 1961. CSIRO Austruliun Soils Lund Use Ser. No. 41. Bettenay, E., and Hingston, F. J. 1964. Australian J . Soil Res. 2, 173-186. Bettenay, E., Blackmore, A. V., and Hingston, F. J. 1964. Australian J . Soil Res. 2, 187210. Blackburn, G., and Leslie, T. I. 1958. CSIRO Australian Soil Publ. No. 12. Blackburn, G., Bond, R. D., and Clarke, A. R. P. 1967. CSIRO Australian Soil Publ. No. 24. Butler, B. E., 1958. CSIRO Australian Soil Publ. No. 10. Butler, B. E. 1959. CSIRO Australian Soil Publ. No. 14. Butler, B. E., and Hutton, J. T. 1956.AustralianJ. Agr. Res. 7,536-553. Churchward, H. M. 1963. Austrelian J . Soil Res. 1, 117-128. Coffey, G. N. 1912. US.Dep. Agr., Bur. Soil Bull. NO. 85. Crocker, R. L. 1941. Trans. Roy. Soc. South Australia 65, 103-107. Crocker, R. L. 1946. CSIRO Australian Bull. No. 193. Daniels, R, B., and Gamble, E. E. 1967. Geoderma 1, 117-124. Daniels, R. B., and Gamble, E. E. 1971. Univ. of Kentucky Press (in press). Daniels, R. B., and Jordan, R. H. 1966. U.S.Dep. Agr., Tech. Bull. 1348. Daniels, R. B., Gamble, E. E., Wheeler, W. H., and Nettelton, W. D. 1966. Southeast Geol. 7, 159-182. Daniels, R. B., Gamble, E. E., and Nelson, L. A. 1967. Soil Sci. 104,364-369. Daniels, R. B., Gamble, E. E., and Bartelli, L. J. 1968. Soil Sci. 106, 200-206. Daniels, R. B., Nelson, L. A., and Gamble, E. E. 1970a. Z. Geomorphol. [N.S.] 14, 175185. Daniels, R. B., Gamble, E. E., and Cady, J. G. 1970b. Soil Sci. SOC.Amer. Proc. 34,648653. Daniels, R. B., Gamble, E. E., and Nelson, L. A. 1 9 7 0 ~Agron. . Abstr. (abstr.). Daniels, R. B., Gamble, E. E., and Wheeler, W. H. 1971. Southeast Geol. (in press). Davis, W. M. 1920. Geol. Mag. 57,429-43 1 . Don. J., and Yaalon, D. H. 1968. Truns. Int. Congr. Soil Sci., 9th, Vol. 4, pp. 577-584. Fowler, E. D. 1927. Proc. Int. Congr. Soil Sci., 1st. Vol. 4, pp. 435-441. Frey, D. G. 1953. Ecul. Monogr. 23,289-3 13. Gamble, E. E., Daniels, R. B., and Nettleton, W. D. 1970. Soil Sci. Soc. Amer., Proc. 34, 276-28 1. Gile, L. H 1961. Soil Sci. SOC.Amer., Proc. 25,52-61. Gile, L. H. 1966a. Soil Sci. SOC.Amer., Proc. 30, 657-660. Gile, L. H. 1966b. Soil Sci. SOC.Amer., Proc. 30,773-781. Gile, L. H. 1970. Soil Sci. SOC.Amer., Proc. 34,465-472. Gile, L. H ,and Grossman, R. B. 1968. Soil Sci. 106,6-15. Gile, L. H., and Hawley, J. W. 1966. SoilSci. SOC.Amer., Pruc..30, 261-268. Gile, L. H., Peterson, F. F., and Grossman, R. B. 1966. Soil Sci. 101,347-360.

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Gile. L. H., Grossman. R. B., and Hawley, J. W. 1969. SoilSci. 108,273-282. Gile, L. H., Hawley, J. W., and Grossman. R. B. 1970. Guideb. Soil-Geomorphol. Field Con/:, 1970. Glinka, K. D. 1963. 4th ed. Israel Program Sci. Transl., Jerusalem. Hardy, A. V., Carney, C. B., and Marshall, H. V. 1967. North Carolina, Agr. Exp. Sta., Bull. 433. Hardy, E. L. 1941. US.Dep. Agr. Yearb. Agr.pp. 101 1-1024. Hawley, J. W. 1965. New Mexico Geol. Soc., Field Cont. Guideb. 16, Part 11, 188-198. Hawley, J. W., and Kottlowski, F. E. 1969. New Mexico, Bur. Mines Miner. Resour., Circ. 104, 89- I 15. Hawley, J. W., Kottlowski, F. E., Strain, W. S., Seager, W. R., King, W. E., and LeMone, D. V 1969. New Mexico, Bur. Mines Miner. Resour., Circ. 104,52-76. Howell, J. V. 1957. “Glossary of Geology and Related Sciences.” Amer. Geogr. Inst. Hunt, C . B. 1954. US.,Geol. Surv. Bull. 996C, 91-140. Hutton, J. T., and Stephens, C. G . 1956. J . Soil Sci. 7,255-267. Humphrey, R. R. 1958. Arizona, Agr. Exp. Sta., Bull. 299. Isphording, W. C . 1970. Amer. Ass. Petrol. Geol., Bull. 54,334-343. Jongen, P. 1961. Trans. Int. Congr. SoilSci., 7th 1960 Vol. 4, pp. 335-346. McArthur, W. M., and Bettenay, E. 1960. CSIRO Australian Soil Publ. No. 16. Maigninen, R. I96 I . Trans. I n t . Congr. Soil Sci.,7th, 1960 Vol. 4. pp. 17 1- 176. Marbut. C . F. 1928. “Soils, their Genesis, Classification and Development.” Mimeo. copy of lectures given at Graduate School, February to May, 1928. U S . Dep. Agr. Marbut, C . F., Bennett, H . H , Lapham, J. E., and Lapham, M. H. 1913. US.Dep. Agr., Bur. Soil Bull. No. 96. Maud, R. R. 1965. J . Soil Sci. 16,60-72. Milne, G. 1935. Soil Res. 4, 183-198. Milne, G., Beckley, V. A., Jones, G . H G., Martin, W. S., Griffith, G., and Raymond, L. W. 1935. Trans. I n t . Congr. Soil Sci.,3rd, 1935 Vol. 5, pp. 270-274. Morrison, R. B. 1968. I n “Means of Correlation of Quaternary Successions” (R. B. Morrison and H. E. Wright, Jr., eds.), pp. 1 - 1 13. Univ. of Utah Press, Salt Lake City. Moss, R. P. 1968. In “The Soil Resources of Tropical Africa” (R. P. Moss, ed.). pp. 29-60. Cambridge Univ. Press, London and N e w York. Mulcahy, M. J. 1960. J . Soil Sci. 11,206-225. Mulcahy, M. J. I96 I . Z . Ceomorphol. 5 , 2 I 1-225. Mulcahy, M. J. 1967. I n “Landform Studies from Australia and New Guinea” (J. M. Jennings and J. A. Mabbutt, eds.), pp. 21 1-230. Cambridge Univ. Press, London and N e w York. Newbold, T. J. 1844. J . Asiatic Soc. Bengal 13,984- 1004. Newbold, T. J . 1846. Roy. Asiatic Soc. 8, 277-240. Northcote, K. H. 1946. Trans. Roy. SOC.South Australia 70,294-296. Northcote, K. H., and Tucker, B. M. 1948. CSIRO Australian Bull. 233. Norton, E. A., and Smith, R. S. 1930. J . Amer. SOC. Agron. 22, 25 1-262. Nye, P. H. 1954. J . Soil Sci. 5,7-21. Nye, P. H . 1955.5. Soil Sci. 6 , 5 1 4 3 . Ollier, C . D. 1959.J. Soil Sci. 10, 137-140. Parsons, R. B., and Balster, C . A. 1966. Soil Sci. SOC.Amer., Proc. 34,485-49 I . Parsons, R. B., Balster, C. A,, and Ness, A. 0. 1970. Soil Sci. Soc. Amer., Proc. 34,485491. Playford, P. E. 1954. Australian J . Sci. 17, 1 I- 14. Prescott, J . A. 1944. CSIRO Australian Bull. 117.

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Prescott. J. A.. and Pendleton, R. L. 1952. Commonw. Bur. Soil Sci. Tech. Commun. 47. Radwanski, S. A., and Ollier, C. D. 1959. J. Soil Sci. 10, 149-168. Ruhe, R. V. 1954. Amer. Railway Eng. Ass., Bull. 514,639-645. Ruhe, R. V. 1962. J . Geol. 70, 151-167. Ruhe, R. V . 1964. Ann. Ass. Amer. Geogr. 54, 147-159. Ruhe, R. V. 1967. New Mexico, Bur. Mines Miner. Resour., Mem. 18. Ruhe, R. V. 1968. In “Loess and Related Eolian Deposits of the World” (C. B. Schultz and J. C. Frye, eds.), pp. 49-65. Univ. of Nebraska Press, Lincoln. Ruhe, R. V. 1969. “Quarternary Landscape in Iowa.” Iowa State Univ. Press, Ames. Ruhe, R. V., and Scholtes, W. H. 1956. Soil Sci. Soc. Amer., Proc. 20,264-273. Ruhe, R. V., Prill, R. C., and Riecken, F. F. 1955. Soil Sci. Soc. Amer., Proc. 19,345-347. Ruhe, R. V., Daniels, R. B.. and Cady, J. G. 1966. U . S . Dep. Agr., Tech. Bull. 1349. Soil Survey Staff. 1960. “Soil Classification, A Comprehensive System 7th Approximation.” US. Dep. Agr., Washington, D.C. Spurr, A. M. M 1954. Proc. Inter-Ayrican Soils Conf., 2nd, 1954 Vol. I , pp. 175-190. Stephens, C. 0 . 1946. CSlRO Australian Bull. 206. Stephens, C . G. 1949. J . Soil Sci. 1, 123-149. Thorpe, J. 1965. Soil Sci. 99, 1-8. Trowbridge, A. C. 1921. Stud. Natur. Hist. Iowa Univ. 9, 1-127. Turton, A. G., March, N. L , McKenzie, R. M., and Mulcahy, M. J. 1962. CSIRO Australian Soil Publ. No. 2. Van Dijk, D. C. 1958. CSIRO Australian Soil Publ. No. 1 I . Van Dijk, D. C. 1959. CSIRO Australian Soil Publ. No. 13. Walker, P. H . 1962. J . Soil Sci. 12, 167-177. Walker, P. H 1963. Australian J . Soil Res. 1, 223-230. Ward, W. T. 1966. CSIRO Australian Soil Publ. No. 23. Watson, J. P. 1964. J . Soil Sci. 15, 238-257. Whitehead, D. R. 1963. Ecology 44,403-406. Whitehead, D. R. 1964. Ecology 45,767. Whitehead, D. R. 1969. Southeast Geol. 10, 1-16. Wooldridge, S. W. 1949. J. Soil Sci. 1 , 3 1-34. Woolnough, W. G . I9 18. Geol. Mag. 55,385-393. Wright, R. L. 1962. J . Roy. SOC. Western Australia 45, 5 1-64. Wright, R. L. 1963.J. Geol. Soc. Australia 10, 151-163.

FACTORS AFFECTING ROOT EXUDATION M. G . Hale, C. 1. Foy, and F. J. Shay Department of Plant Pathology and Physiology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia

I. Introduction ..................................................................................... 11. History ............................................ ....... ................. 111. Sources of Exudate and Pattern of Root ................................

IV. V. VI. VII. VIII.

1x.

Interactions of Organic Nitrogen Sources and Exudation ......................... Effects o n Carbon and Nitrogen Balance in Plants ................................. Foliarly Applied Compounds and Root Exudation .................................. Root Exudation-Mineral Nutrient-Microbial Interactions . Effects of Environment on Root Exudation ........................................... Summary ........................................................ References .....................................................................................

89 92 93 95

95 97 101

I03 I07 I07

I. Introduction

Absorption and desorption of substances extremely diverse in molecular size and in physicochemical and biological properties occur at the root surface. Substances (other than water) which are released from plant surfaces have been termed exudates by many investigators regardless of whether their appearance on the surface is the result of passive or active transport. In regions of the plant other than the root, exudation may occur from special structures called glands, but in roots no glands have ever been demonstrated. Possible sources of metabolites in exudates include intact living cells, moribund cells, or injured cells and tissues still attached to the root and the apoplast. At least one investigator has included sloughed cells and tissue in the term exudate (Rovira, 1969b). A large body of published work on exudation has been done by microbiologists and plant pathologists who were mainly concerned with exudates as a source of nutrients or growth factors for microorganisms and the attraction of microorganisms to roots. The role that root exudation plays in the physiology and life cycle of the plant itself and the mechanisms of exudation have been neglected. Our purpose is to bring together the body of information pertaining to the quantitative and physiological aspects of root exudation and to point out how the development of techniques for axenic culture of whole plants 89

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may aid this kind of research. In these two aspects this report differs significantly from that of Rovira (1969a). Some of the terminology pertaining to the absorption of ions and root exudation is given in Table I. The scientific names of plants referred to in the text by common name are listed in Table 11. TABLE I Concepts or Definitions of Terms Used in Reference to Root Exudation and Interactions of Roots with the Surrounding Medium Term Accumulation

Active transport

Absorption

Adsorption Apoplast Axenic Carriers

Excretion

Exudation

Exudates, root Free space (or “outer space”)

Concept or definition and literature reference Increase in concentration of a substance, usually both ions of a salt, in the vacuoles of cells as a result of an expenditure of energy by the cells. [Sutcliffe (1962) includes movement of ions against a concentration gradient and the passive movement resulting from establishment of Donnan equalibrium.] The process whereby an ion is moved against an electrochemcal potential gradient and is therefore dependent on a decrease in free energy in some metabolic process (Briggs et al., 1961, p. 131). A general term used for the entry of a substance into any plant cell or plant part by any mechanism. Desorption is the reverse process. Ions or molecules held by polar linkages to charged groups of cellular structures, and thus available for exchange. The continuum of nonliving cell wall material that surrounds and contains the symplast (Crafts, 1961, p. 142). Germfree, absence of other organisms. Compounds with which ions combine chemically in a labile form, and are transported across a membrane, after which the ions are released (Sutcliffe, 1962, pp. 40-46). Elimination of useless superfluous or harmful substances which may reach the exterior of the plant, or which may be stored in nonfunctional tissue. Exudation of applied pesticides may be excretion but the term is more applicable to animals than to plants. The appearance on a plant surface of substances from inside the plant whether as a result of passive movement or secretion. Frequently the pathway to the surface is established through wounds. Those substances which are released into the surrounding medium by healthy and intact plant roots (Rovira, 1969a). Defined as that part of a tissue or organ into and through which the solute and solvent from the external solution move readily. The volume of free space may vary slightly with solute and solvent but usually is around 10% (Briggs et al., 1961, p. 74; Devlin, 1969, pp. 238-239).

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FACTORS AFFECTING ROOT EXUDATION

TABLE I (continued) Concept or definition and literature reference

Term Leaching

Leakage as a result of the flow of solvent or dilute solution surrounding the organ (Tukey, 1966). Efflux by purely physical means (diffusion and exchange). May occur from symplast to the apoplast or from plant organ into the surrounding medium, or from vacuoles into cytoplasm (Sutcliffe. 1962, p. 27). Absorption of substances previously released or desorbed. That part of the rhizophere adjacent to the root surface. The external surfaces of the plant roots together with any closely adhering particles of soil or debris (Clark, 1949). That sone of soil in which the microflora is hfluenced by plant roots. I t is a poorly defined zone of soil in which one finds microbiological gradients from the root surface into the soil (Rovira, I965a). A component of the exosphere (Scott, 1969).

Leakage

Resorption Khizoplane

Rhizosphere

Secretion

Efflux by mechanisms involving metabolic energy (active transport). May result in loss to plant surface or into cell vacuoles (Levitt, 1969, p. 85). The continuum of interconnected protoplasts of the plant (Crafts, 1961, p. 142).

Symplast

TABLE I 1 Common Name, Scientific Name, and Reference for Plants Mentioned by Common Name in the Text

~

Alfalfa Apple Barley

Bean

Beet Broad bean Chrysanthemum Corn Cotton Cucumber Flax Oats

Reference

Scientific name

Common name _

_

_

_

~

Medicago sativum L. Pyrus malus L. Hordeum distichon L Hordeum vulgare L. C.V.C A M P A N A C.V. MARIS BADGER Phaseolus vulgaris L

Beta vulgaris L. Vicia faha L. Chrysanthemum sp. Zea mays L. Gossypium sp. Cucumis sativus L. Linum usitatissimum L. C.V. BISON & NOVELTY Avena sativa L.

Richter et al. (1968) Head (1964) Vancura (1964) Hiatt and Lowe (1967) Barber and Loughman ( 1967) Miller and Schmidt (1965a). Foy and Hurtt ( 1967), Schroth et al. (1966) MacDonald ( I 967) Pearson and Parkinson ( 196 I ) Woltz (1963) Morre et al. ( I 967) Schroth et al. ( I 966) Vancura ( I 967) West (1939) Schroth and Hildebrand ( 1964)

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M. G. HALE, C. L. FOY, A N D F. J . SHAY

TABLE I I (continued) ~~

Common name

Scientific name

Orchardgrass Pea

Dactylis glomerata L. Pisum sativum L.

Peanut P halarisgrass, Canarygrass Pine

Arachis hypogaea L. Phalaris caroliniensis L.

Potato Ragi, finger millet

Solanum tuberosum L. Eleusine coracana Gaertn.

Rattlebox Red clover

Crotalaria medicaginea Trifolium pratense L.

Rice Sicklepod Sorghum

Oryzae sativa L. Cassia tora L. Sorghum vulgare Pers.

Strawberry Subterranean clover Sunnhemp

Fragarin virginiana L. Trifolium subterraneum L. Crotalaria juncea L.

Timothy Tobacco

Phleum pratense L. Nicotiana tabacum L. Nicotiana rustica L. Lycopersicon esculentum

Tomato

Wheat

Pinus radiata, Pinus strobus L.

Triticum aestivum L. C.V.FEDERATION 41 Triticum vulgare C.V.CABO

Reference Couch and Bloom (1960) Ayers and Thornton ( I 968), Kerr ( I964), Schroth e f al. (1966) Hale (1968) Rovira (1959) Bowen (1968, 1969a,b) Slankis et al. (1964), Street ( I 966) O’Brien and Prentice ( I 930) Balasubramanian and Rangaswami (1969) Sullia ( 1 968) Bowen and Rovira ( 1 966), Couch and Bloom (1960) Ramchandra-Reddy (1968a) Sullia ( I 968) Balasubramanian and Rangaswami ( 1969) Hussain and McKeen (1963) Rovira ( I 959) Balasubramanian and Rangaswami (1969) Couch and Bloom ( 1960) Steinberg (1950) Steinberg (1952) Bowen and Rovira ( I 966), Subba Rao et a / . (1961). Rovira (1959) Ayers and Thornton ( I 968) Bowen and Rovira ( I 966)

II. History

As early as the nineteenth century the French botanist, DeCandolle (1832) ascribed an important role in the “soil sickness” problem to excretions from roots. The work that has ensued since then has been amply reviewed (Bonner, 1950; Borner, 1960; Evanari, 1961 ; Garb, 196 1 ; Grodzinsky, 1962; Loehwing, 1937; Lyon and Wilson, 1921; Rovira, I969a; Santovich, 1965; Schroth and Hildebrand, 1964; Street, 1966; Woods, 1960). Comprehensive treatment of the literature is beyond the

FACTORS AFFECTING ROOT EXUDATION

93

scope of the present discussion but some papers of historic interest are worthy of mention. Four such papers have been reviewed by Rovira (1965b): Knudson ( I 920) concluded that sucrose in the nutrient solution was absorbed by the roots of axenic plants, hydrolyzed and exuded by the roots as reducing sugars; Lyon and Wilson ( 1 92 1 ) found that nitrogencontaining organic compounds were released into sterile rooting medium; Cranner (1 922) showed that roots of seedlings and of mature plants released phosphatides; and O’Brien and Prentice ( 1 930) presented the first conclusive evidence of stimulation of specific organisms by root exudates when they showed that the cysts of potato eelworm (Heterodera Rostochiensis) were caused to hatch in the presence of root washings of potato, but not of some other plants. The evidence that some organisms in the rhizosphere are dependent upon roots for growth factors was demonstrated by West ( 1 939). Thiamine and biotin were found to be released from flax roots in amounts of 0.33 pg of thiamine and 0.06-0.08 pg of biotin in 1 week from five plants. It has been established subsequently that most of the metabolites found within plants may also be found outside of plants under various experimental conditions. Axenic culture techniques and continuous harvesting of exudate samples have revealed that there is an endogenous rhythm of exudation in cereal plants (Dubrov and Bulygina, 1967) and alfalfa (Richter et al., 1968). The rhythm was exhibited for amino acids and a yellow pigment. Compounds applied to foliage, or their metabolites, also may appear or reappear in the rooting medium (Blackman, 1956, 1958; Blackman et al., 1958; Crafts, 1961; Foy and Hurtt, 1967; Foy and Yamaguchi, 1965; Hurtt and Foy, 1965a; Klein, 1968; Levi, 1968; Linder et al., 1958, 1964; Mitchell et al., 1959; Preston et al., 1954; RamchandraReddy, 1968a,b; Sullia, 1968). These include such things as mineral nutrients, growth regulators, and pesticides. Ill. Sources of Exudate and Pattern of Root Exudation

There are several well documented examples of exudation from special structures. These include guttation from hydathodes as a result of root pressure; secretion from glands, such as those in nectaries of flowers and in salt glands found in some halophytes. N o glands have been demonstrated in roots of plants although formation of droplets containing a highly hydrated hexose polysaccharide have been observed at the tips of corn roots (Morre et al., 1967) and apple roots (Head, 1964). Mollenhauer ( 1967) has concluded that all terrestrial or epiphytic roots have some secretory activity from root cap cells.

94

M. G . HALE, C. L. FOY, A N D F. J. SHAY

Many of the substances identified as root exudates are probably released as a result of injury by lateral or adventitious roots as they grow from their internal site of origin to the outside, by injury from cultural practices, or by injury from attacking organisms. Ayers and Thornton ( 1 968) discussed the possibility of injury causing exudation because, when they moved a root across filter paper, greater quantities of amino acids were released than if the root was undisturbed on the paper. Agitation with sand in the nutrient solution bathing the roots also caused an increase in amino acids exuded. McDougall ( 1968) was able to demonstrate that when wheat roots were deliberately cut or crushed considerable exudation occurred from the injured site. Some substances may originate from sloughed root cap, epidermal, and cortical cells. Visual examination of peanut roots growing in nutrient solution in a sterile environment revealed quantities of sloughed material clinging to the root axis and to the root cap (G. J. Griffin, M. G. Hale, and F. J. Shay, unpublished observations, 1969). Slight agitation caused quantities of this material to floc to the bottom of the container. Microscopic examination revealed that masses of root cap cells, recognizable because of the conical shape of the mass, and sheets of cortical cells make up the bulk of the material with few single cells present. Other masses of cells originate at the site of eruption of lateral roots. In 1919 Knudson made similar observations on corn and pea seedlings and found that such cells remained alive as long as 40 days after sloughing. He estimated the total weight would be about 20 mg per 42-day-old plant. Over the growth period of a root the quantity of organic matter released into the rhizosphere as sloughed cells and tissue probably plays an important role in microbial succession in root colonization. The qualitative and quantitative amounts of soluble nutrients released into the rooting medium from sloughed material are still not known. It is not clear what proportion of exudates may be the result of leaching from the apoplast of the root and what proportion may result from exchange reactions with inorganic nutrient ions (Hiatt and Lowe, 1967). Burstrom ( 1965) has suggested that modes of exudation from various sources may yield different groups of compounds. Loss from the apoplast may yield compounds of low molecular weight, whereas secretion from the vacuoles and cytoplasm may result in compounds representing the entire cell contents. The source of pressures or gradients which might cause exudation are largely unknown although their existence and involvement in absorption is well established. The polysaccharide exuded by root cap cells is probably the result of the activity of Golgi bodies and a positive turgor pressure (Morre ef al., 1967). Gradients of efflux of ions occur along roots (Bowen, 1968). Efflux of

FACTORS AFFECTING ROOT EXUDATION

95

chloride ions in the apical 2-3 cm in 24 hours was approximately 20% of that originally present in the apex of the root but was only 8.2% in a region 6 to 8 cm from the apex. A distribution pattern for efflux of I4C along roots was different. McDougall ( 1968) found that I4C was released at a fairly uniform level along the root of 5- to 6-day-old wheat plants except at the base of the root (about 8 cm from the tip) where large amounts were exuded. The compounds contained no ninhydrin-reacting substances, On the other hand, broad bean roots were found to exude amino acids from a region centered about 28 mm from the root apex (Pearson and Parkinson, 1961). Exocellular enzymes also are exuded. Chang and Bandurski ( 1964) used two methods to study root exudation from 4- to 5-day-old corn seedlings. In one method the seedlings, substrate, and cofactors were placed in the same test tubes, and enzyme activity was measured for a time. Total activity of free enzymes and those on the surface of the root yielded invertase, cellobiase, adenosine triphosphatase, pyrophosphatase, ribonuclease, and deoxyribonuclease. In method two, an aliquot of the solution bathing the roots was removed from the presence of the roots and substrate plus cofactors added. Only free, exuded enzymes were measured by this method and yielded invertase, ribonuclease, and deoxyribonuclease. N o attempt was made to ascertain the distribution pattern along the root and the number of enzymes found was limited by the assays used. IV. Interactions of Organic Nitrogen Sources and Exudation

Resorption of exudates or absorption of metabolites from organisms living on exudates from roots may affect the growth of plants. The effects of amino acids have been studied in this respect. Steinberg (1950) was able to show that amino acids in the rooting medium could produce the symptoms of frenching of tobacco and associated release of these amino acids by microorganisms in the soil with appearance of disease symptoms (Steinberg, 1952). A similar relationship has been shown for chrysanthemums (Woltz, 1963). Axenic culture of plants has been used to prove that amino acids can be absorbed from soil (Miller and Schmidt, I965b). The sources of nitrogen that can be used by higher plants and the interactions between microorganisms and plant nutrition have been reviewed by Barber ( 1968). V. Effects on Carbon and Nitrogen Balance in Plants

Attempts to measure productivity based on increases in dry weight need to account for the photosynthate lost through the roots just as ex-

96

M. G. HALE, C. L. FOY, A N D F. J . SHAY

cretion of photoassimilated organic compounds must be given attention in studies of aquatic angiosperms and algae (Wetzel, 1969). Applications of 14C02to the aerial portion of the plant and subsequent detection of 14C have shown that significant quantities of carbon compounds leave the roots in forms other than COr (McDougall and Rovira, 1965; McDougall, 1968; Slankis et al., 1964). 14C appeared in the rooting medium in 4-5 hours after application to seedling wheat plants. It has also been demonstrated that labeled carbon moves out of the roots of one plant and into the roots of an adjacent plant labeling all parts of the plant within 21 hours (Ivanov et al., 1963). Rovira ( 1969b) has chosen to differentiate between diffusible exudates and nondiffusible exudates, the latter being sloughed cells and mucilaginous material. The nondiffusible material is not collected in most root exudate studies, and the contribution of the plant root to soil is underestimated to a considerable degree. Amounts of material lost through the roots under natural conditions are unknown largely because of the difficulty of measuring loss. Under experimental conditions it has been demonstrated that even slight agitation of the root system increased the amount of amino acids released into the nutrient solution. The maximum amount of ninhydrin-reactive compounds measured was 24 pg per 15 wheat seedlings after 14 days in the culture solution (Ayers and Thornton, 1968). This yield was obtained with agitation of the roots by swirling the nutrient solution, containing a small amount of sand, against the roots. Although undisturbed roots of wheat yielded no amino acids, those of peas did. Slightly more than 33 pg of amino-N per 5 undisturbed pea seedlings was released after 14 days in the culture solution. Also those plants of both species which grew in sand released more amino acids than did those which grew in nutrient solutions. The greater release was attributed to injury of the roots by the sand. Richter and co-workers ( 1 968) were able to establish a system whereby they could continuously harvest the nutrient solution without disturbance of the root system. Average daily yields of 0.24 pmole of amino-N per 7 alfalfa seedlings over a period of 57 days were obtained. They were able to show that the loss fluctuated in a rhythmic pattern for each of several amino acids and that the respiratory poison, dinitrophenol, decreased the loss of some amino acids but not others. This is one of the few attempts to correlate exudation with root metabolism. Vancura (1964) obtained 0.4-0.5 mg dry weight of exudate from roots of barley seedlings. This amounted to 7-10% of the dry weight of the tops and was the result of exposing roots to water stress and then relieving the stress.

97

FACTORS AFFECTING ROOT EXUDATION

Manorik and Belima (1969) believe that the best way to express the amount of exudate for comparisons between species and between experiments is on the basis of amount of exudate per unit area of absorbing root surface (Table 111). Such an expression would eliminate errors caused by differences in growth rate and nutritional status of the plant. TABLE 111 Micrograms of Amino Nitrogen in Root Exudates of Peas and Corn" Per gram of roots Variant

Per plant

Fresh

Dry

Above ground part, fresh

Peas Corn Peas :corn ratio

6.8 I 3.86 1.76

9.90 3.40 2.9 1

7 1.84 24.78 2.89

5.76 2.48 2.32

Per square decimeter of absorbing surface of roots 2 I .07 2.24 9.40

OData from Manorik and Belima 1969, Plenum, N e w York, by permission.

Measuring the absorbing root surface area, however, might be difficult. The expression micrograms lost per square decimeter is useful only for the diffusible or soluble exudate, and not necessarily for the nondiffusible exudate and sloughed cells. The amount lost per plant is a more readily obtainable figure. Any expression must also include a time unit. Some comparisons are made in Table IV by recalculating the data of several investigators into the amount lost per plant per week. Since the examples used are for seedlings of about the same age, such comparisons seem valid. Quantitative data of this kind are quite meager although there are data relating to semiquantitative analyses such as size of spots on chromatograms and relative effects on microbial populations in the rhizosphere. There is evidence which indicates that amounts of exudates occurring into soil may be greater than those occurring into nutrient solution (Table V), but the difficulties of removing roots without injury with the increased loss from wounds make direct comparisons questionable. It is evident that measurable losses of soluble organic material occur from roots and more quantitative data are needed from a variety of experimental conditions before the principles of root exudation can be fully elucidated. VI. Foliarly Applied Compounds and Root Exudation

Herbicides and other growth regulators have been observed to differ markedly with respect to rate of uptake and subsequent translocation,

W

00

TABLE I V Amounts of Amino Nitrogen, Sugars, and Total Substances Lost from Seedling Roots of Various Crop Species"

Species

Compound or group

Amount

Amount recalculated to pg/plant/week

24 pg/15 plants/l4 days 33 pg/15 plants/l4 days 0.29 pmole/72 plants/day 2.54 @/plant/ 15 days 3.16 pg/plant/ 15 days 1.72 pg/plant/15 days 1.20 pg/plant/30 days 0.104 pnole/plant/l4 days 1.7 to 3. I mg/plant/24 days

0.8 1 3.30 0.37 0.22 0.28 0.15 0.05 0.73 60- 104b

-

Reference

Amino N Wheat Peas Alfalfa Sorghum Sunnhemp Ragi Tomato Pinus radiata Phaseolus vulgaris

Ayers and Thornton (1968) Ayers and Thornton ( 1 968) Richter et al. ( 1968) Balasubramanian and Rangaswami Balasubramanian and Rangaswami Balasubramanian and Rangaswami Balasubramanian and Rangaswami Bowen (1968) Miller and Schmidt (1965b)

(1969) ( I 969) (1969) (1969)

Sugars Sorghum Sunnhemp Ragi Tomato Peanut

82 pg/plant/15 days 68 pglplantll5 days 42 pg/plant/l5 days 32 pg/plant/30 days 3.8 pglplantlweek

38.3 31.7 19.6 1.46 3.80

Balasubramanian Balasubramanian Balasubramanian Balasubramanian Hale ( I 968)

and and and and

Rangaswami Rangaswami Rangaswami Rangaswami

Total organic substances Barley Peanut

0.5 mg/plant/ I0 days 0.54 mg/plant/l88 days

350' 21

Vancura ( 1 964) Hale (1968)

"Grown in nutrient solution except as noted. "Plant grown in sterile soil and soil extracted for analysis; fertilized with KNOI. Some root injury on removal from soil. =Plants grown in sand, allowed to dry down and then watered.

( 1969)

(1969) ( 1969) ( 1969)

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FACTORS AFFECTING ROOT EXUDATION

TABLE V Comparison of Amino Acids Found in Autoclaved Soil before and after Growing Beans in I t for 24 days"," Concentration in soil after growth of Phaseolus vulgaris C.V. BLACK VALENTINE

(pg per 250 g dry soil)

Amino acid

Concentration in autoclaved soil

1"

2

3 479.3 464.4 76.2

Aspartic Threonine Serine Glutamic acid Glycine Alanine Valine Leucine Tyrosine Phenylalanine

232.9 405.5 105.5 -

377.4 249.5 137.2 I 14.6 70.8 468.2 136.2 185.8

379.8 225. I 156.8 69. I 169.4 182.9 933.9 273.3 131.1 597.7

139.1 135.0 186.0 704.0 427.6 409.0

Summation

743.9

1739.7

31 19.1

3020.6

"Data from Miller and Schmidt 1965a, Williams & Wilkins, Baltimore, Maryland, with permission. *Anoka soil with 36 mg K N O , added to each container. All roots were removed before extracting the soil with ammonium acetate. Since sterility of the root system and the rooting medium was maintained, the additional amino acids could come only from the bean plants. 'Plant number.

both into and out of roots, as revealed by autoradioaugraphy, isotope counting, and bioassay (Crafts, 1964; Foy and Yamaguchi, 1965). Similar differences in mobility patterns among compounds were observed after foliar treatments. Certain substances, e.g., substituted urea and s-triazine derivatives, apparently move in the apoplast, whereas others, e.g., 2,4-dichlorophenoxyacetic acid (2,4-D), have a stronger affinity for the symplasm and are phloem-mobile. Some compounds are known to be translocated not only from the shoots into roots, but out of roots into the culture medium. Accumulation and perhaps active secretion of certain of these substances are suspected. The loss from roots of trans-cinnamic acid (Bonner and Galston, 1944) is a classical example of the release of a naturally occurring growth regulator by plant roots. a-Methoxyphenylacetic acid (MOPA) was apparently the first exogenous compound reported as being excreted from roots (Preston et al., 1954). Subsequently, five other exogenous growth

100

M. G . HALE, C. L. FOY, A N D F. J. SHAY

regulators were reported to be exuded from roots (Linder et al., 1958; Mitchell et al., 1959). More recently, the excretion of dicamba ( 2 methoxy-3,6-dichlorobenzoic acid) was reported by Linder et al. ( 1964) and the excretion of the important herbicidal derivative of picolinic acid, picloram (4-amino-3,6-trichloropicolinicacid), was reported by Hurtt and Foy ( 1 965a,b). Thirty-one compounds were examined by Foy and Hurtt ( 1 967) with respect to their ability to be excreted from the roots of bean plants following foliar application. From this series of compounds picloram, dicamba, and 2,3,6-trichlorobenzoic acid emerged as three of the most potent from the standpoint of injuring untreated plants growing in close proximity to the treated plants. The transfer of herbicide from treated to adjoining untreated plants via the respective root systems was demonstrated in soil, sand, and nutrient solution. Symptoms of herbicide injury were consistently observed on untreated plants when about 2 pg of either picloram or dicamba were applied to the corresponding adjacent plants. Picloram and dicamba were absorbed, translocated, and excreted, regardless of whether they were applied by leaf dipping, spraying, drop application, or application through a severed petiole. No detectable dicamba was released into nutrient solution from the stems of plants whose roots had been excised before application of the herbicide. In comparable studies, small amounts of picloram leaked out of the stems of treated plants but the quantities were small compared with those released by plants with intact root systems. Neither herbicide was released from plants whose roots had been steamed before herbicide application. The total amount of dicamba or picloram excreted into nutrient solution by the roots of intact plants over a 4-day interval was 10-15% of the amount applied as a foliar application (Hurtt and Foy, 1965a). Autoradiographs (dicamba-14C) and bioassay data indicated that neither herbicide was excreted when the phloem was girdled by steam before herbicide treatment. Both herbicides were excreted under aerobic conditions, but dicamba was not excreted by plants whose roots were grown under anaerobic conditions obtained by aerating the nutrient solution with nitrogen. The substitution of oxygen for air as a source of aeration did not increase the amount of dicamba excreted. Picloram, in contrast, was excreted under nitrogen aeration, and the substitution of air or oxygen for nitrogen did increase the amount of herbicide excreted (Hurtt and Foy, 1965b). Ramchandra-Reddy ( 1968a,b) applied antibiotics, trace elements, and metal chelates to foliage and concluded that changes in the rhizosphere populations depended upon the nature and concentration of substances used and the season of growth. Sullia (1968) applied 100 ppm each of gibberellic acid and indole-3-acetic acid to foliage of sickle pod and rattle-

FACTORS AFFECTING ROOT EXUDATION

101

box. There was an increase in total number of fungi observed but no change in the species present in the rhizosphere. Balasubramanian and Rangaswami ( 1969) observed that generally foliar applications of a 0. I % solution of nitrogen in the form of N a N 0 3 increased the concentrations of amino acids exuded by sorghum, sunnhemp, ragi, and tomato but applications of P as Na2HP04reduced the concentration. The results on sugars exuded were the reverse. N applications reduced total sugars exuded while P applications increased the sugar concentrations. There were also some changes in the kinds of amino acids exuded as a result of treatment. Considerable significance can be attached to the alteration of root exudates by foliar applications as a possible means of influencing rhizosphere populations of microorganisms and thus, perhaps, controlling root diseases of plants (Rovira, 1969a). Study of root exudation or excretion of organic compounds, particularly endogenous and exogenous plant growth-regulating substances, and their subsequent fate has been neglected. More consideration needs to be given to the role of root-colonizing microorganisms. VII. Root Exudation -Mineral Nutrient- Microbial Interactions

The effects of microorganisms on mineral nutrient availability are varied and depend upon plant species, age, microbial population, and the particular conditions of the experiment being conducted. Care must be exercised in interpreting experimental results from studies that do not use soil for the rooting medium and that deal with unnatural microbial populations. The incidence of microorganisms capable of dissolving organic phosphates is higher in rhizosphere soil than in nonrhizosphere soil (Greaves and Webley, 1965; Sperber, 1957). Bowen and Rovira (1966) demonstrated that in short-term uptake studies nonsterile clover and tomato plants took up 45% and 85% more phosphate than did sterile plants. Similar results for barley have been reported (Barber and Loughman, 1967) and for pine (Pinus radiata) (Bowen, I969b). The increased availability of phosphate caused by microorganisms is reflected by higher levels of nucleic acids, phospholipids, and phosphoproteins in the nonsterile plants. A greater loss of phosphate from nonsterile plants was noted when the plants were transferred to a phosphate-free solution (Bowen and Rovira, 1966; Barber and Loughman, 1967). A possible explanation is that the phosphate was released from the microorganisms at the root surface or that the microorganisms migrated into the ambient solution. Plant-microbial interactions affecting nutrient availability and/or trans-

102

M. G . HALE, C. L. FOY, A N D F. J . SHAY

location have been reported for several elements other than phosphorus. Sulfur translocation to the shoot of tomato plants infected with Fusarium and Trichoderma spp. was reduced 16-46% in the infected plants (Subba Rao et al., 1961). This may have been caused by either reduced translocation of sulfur as a result of infection, a reduction in the availability of the element, or a reduction in its absorption. Calcium and rubidium uptake and translocation in the roots and shoots of clover seedlings were reduced when previously sterile plants were inoculated with suspensions of rhizosphere microorganisms (Trolldenier and Marckwordt, 1962). Microorganisms also influenced the absorption of sodium and chloride ions by beet discs and the effects were shown to be comparable to those caused by low concentrations of growth depressants. It was suggested that the microorganisms released compounds which influenced the metabolism of the beet root cells (MacDonald, 1967). The interaction of plant roots and microorganisms may also be complicated by the presence of root exudates. Exudates may serve as a microbial substrate and/or they may play a direct role in liberating nutrients from the soil. For example, quinic and glutamic acid exuded from the roots of lucerne and clover have been shown to release phosphate from calcium, iron, and aluminum phosphates (Barber, 1968). The availability of mineral nutrients has been shown to affect root exudation quantitatively and qualitatively. Rovira ( 1959) found that varying the concentration of calcium from 5 X IW4 to 5 x lo-* M i n the rooting medium had little effect on amino acid loss from the roots of tomato, subterranean clover, and phalarisgrass. However, the lowest concentration of calcium used by Rovira was within the range of adequacy established for most plants (Bowen, 1969a). Therefore, the effect of calcium deficiency on exudation remains unknown. Quantitative and qualitative differences in the loss of amides and amino acids from sterile pine seedlings when grown under conditions of nitrogen deficiency, phosphate deficiency, and nutrient sufficiency were reported by Bowen ( I 969b) (Table VI). In the exudate collected from 2- to 4-week-old seedlings, the amido-amino nitrogen was 104.5 X mde/plant when grown in complete nutrient solution, and the plants grown in phosphate-deficient molelplant (Bowen, 1969b). The solution yielded a total of 248.5 x quantitative effect of nutrient deficiency on the exudation of individual amino acids and amides was variable, as may be seen in Table VI. The complexity of the plant-microbial exudate interactions and their effects on nutrient availability must be understood when one investigates the mechanisms of ion uptake; however, these interactions are usually overlooked. The review by Laties (1 969) emphasized a dual mechanism of ion uptake. One mechanism is prevalent at low ion concentrations and

FACTORS AFFECTING ROOT EXUDATION

103

TABLE VI Exudation of Amides and Amino Acids (Moles X IO-!'/Plant) from Roots of Pinus radiata Seedlings, 2 to 4 Weeks"." Nutrient solution

Amino acid or amide

Complete

Asparagine Glutamine" A-Aminobutyric acid u-Alanine Aspartic acid Glutamic acid Glycine Leucine Serine Threonine Valine Total amino nitrogen

10.9 23.6 5.2 I .6 4.4 6.0 7.3 3 .O 4.8 I .4 I .8 104.5

Phosphate deficient 32.5 52.0 13.8 2.8 9.6 19.7 14.0 5.6 8.0 2.0 4.0 248.5

Nitrogen deficient 3 .O 2.8 I .o 1.2 2.0 2.0 3.4 1.8 2.0 0. I 25. I

"Data from Bowen ( I969a). "Roots were of similar length in all treatments. 'Some arginine was also present, but only in small amount.

affects the accumulation of ions in the cytoplasm, and the other mechanism is operative at high ion concentrations and affects the movement of ions across the tonoplast. However, most of the experiments leading to these conclusions were conducted under nonaxenic conditions, and it has been shown that microorganisms affect both the uptake and translocation of inorganic ions. Barber (1968) suggested that the effects of microorganisms on nutrient availability would be greatest at low ion concentrations. Microorganisms have been found to inhabit a mucilaginous layer which covers some roots (Jenny and Grossenbacker, 1963; Brams, 1969) and as a result may play a role in absorption and root exudation. Most studies of the mechanisms of ion uptake employ solutionculture grown roots. A mucigel layer, if present under these conditions, may support a microbial population different from that of roots grown in soil and, hence, an erroneous understanding of absorption may result. VIII. Effects of Environment on Root Exudation

Definitive investigations of effects of environmental factors on root exudation are relatively few. There is some qualitative value in examining situations in which indirect evidence involving the rhizosphere effect

104

M. G. HALE, C. L. FOY, A N D F. J . SHAY

has been reported. These studies, however, have not resulted in precise quantitative data of the kinds and amounts of exudates released under differing conditions. They show only that changes in environment of the plant affect microorganisms in the vicinity of the root. It would be helpful to know and understand how temperature, light intensity and soil moisture affect the exudation pattern of various crop plants. It is to be expected that light and temperature, as they affect photosynthesis and translocation, would have a profound effect on the amounts and kinds of exudates released. From the limited information available it is difficult or impossible to develop concepts about effects of the variables on exudation because of lack of uniformity of conditions, age, species of plant and methods of analysis from investigator to investigator. Schroth and Hildebrand (1 964) reported that each of four investigators who studied the exudation of amino acids from oats reported different results. Ayers and Thornton (1968) stated that there are “widely differing techniques that have been used to grow plants for studies of root exudation, varying from simple culture of seedlings on filter paper or in culture tubes, to elaborate systems using sand or soil as the rooting medium. In some cases, no distinction is made between materials emanating from roots and seeds or other portions of the plant. Others exclude seed exudates by special absorbents. Likewise, collection techniques have varied in the use of a mineral solution or distilled water rinses, with the roots intact in the rooting medium or after they are mechanically removed from the soil, sometimes with the aid of a sieve and bristled brush.” It is not strange that a systematic study of environmental effects on exudation has not yet been undertaken. There are many difficulties to overcome before plants can be cultured under controlled environmental conditions and under the axenic conditions necessary to eliminate complications created by the presence of other organisms. Procedures must be available for harvesting exudates in large numbers of samples and large amounts, keeping them sterile until analysis and analyzing them quantitatively. Few investigators have access to all necessary facilities and techniques. Then too, the justification of such research may be questioned as there arises the difficulty of applying such knowledge and techniques to natural conditions and interactions that occur in soil. Soil moisture stress is known to influence quantitaitve and qualitative exudation of organic compounds from plant roots. Using methods which placed plants under water stress, Vancura ( I 964) was able to recover 0.4-0.5 mg of organic compounds from the rooting medium of seedling wheat and barley plants after 10 days. This amount was 7-10% of the top dry weight. The exudates were analyzed chromatographically in

FACTORS AFFECTING ROOT EXUDATION

I05

several fractions which included amino acids, sugars, growth regulators, and phenols. It is not clear, however, how much of this material may have come from the seed. Root exudates were collected from plants which had been allowed to wilt and were then watered. One hour after watering, the pots were leached and the leachate was analyzed. The amino nitrogen was appreciably greater in the leachate of pots in which plants had been allowed to wilt than in the leachate from pots in which wilting did not occur (Katznelson et al., 1954). Ivanov et al. (1964) tried to duplicate these conditions in studying movement of I4Cbetween plants. Movement was greater with drying and wetting than without. Also, labeled carbon from donor plants whose tops were exposed to "CO, was absorbed by receptor plants not exposed to I4CO2growing in the same container. The amount transferred was greater when the soil was allowed to dry from field capacity to 35% moisture content than when the moisture content was maintained at field capacity. Soil moisture stress has been shown also to increase the amount of sugar released by pea seeds (Kerr, 1964). Another example of indirect evidence that soil moisture stress affects root exudation is that of Couch and Bloom (1960). Fourteen plant species, representing 4 families were grown under irrigation cycles that produced stresses at semiconstant saturation capacity (SC), field capacity (FC), permanent wilting percentage (PWP), and cycles SC -+ PWP + SC and FC + PWP + FC. Non-amino acid fractions of the root exudates extracted from rooting media of cyclic SC -+ PWP + SC soil moisture regimes produced significant reductions in percentage egg hatch of Meloidogyne incognita. Greatest inhibition of egg hatch was obtained with collections from orchardgrass, timothy, and red clover in which plants had been grown under cyclic FC + PWP,+ FC patterns. Similar fractions from exudates collected from plants of the same species grown at semiconstant SC, FC, and PWP did not have as great an effect. The relationship of soil moisture stress, root exudates, and nematode behavior needs further elucidation. The effect of temperature on the exudation of various compounds has been investigated. From roots of strawberry, Hussain and McKeen (1963) found that at 5"- 10°C greater amounts of amino acids were exuded than at higher temperatures. Schroth et al. (1966) found that a higher rate of exudation from cotton and bean occurred at 37°C but that the exudation from peas decreased at this temperature. The highest rate of exudation from peas occurred at 27°C. Vancura (1967) found that the amount exuded within a certain period increased with an increase in temperature from 8" to 28°C although, in the case of sugars, the amounts of some individual sugars decreased at the higher temperatures. The exudation

106

M. G . HALE, C. L. FOY, A N D F. J. SHAY

pattern varied not only quantitatively but also qualitatively after a “cold shock” when temperature was dropped to 5°C for 3 days. Such differences in release of exudates might be explained by the effect of temperature on permeability of the cellular membranes or by effects on cellular metabolism. Lower metabolic energy at lower temperatures may allow substances to leak out of cells. The pattern of amino acids exuded may vary with temperature, light intensity, age of plant, and species (Rovira, 1959). For example, tomato and canarygrass roots exuded more amino acids in general than subterranean clover. Glutamic acid was abundant in exudates of tomato and canarygrass but not as abundant from tomato and clover. The concentration of serine, glutamic acid, and a-alanine exuded from clover decreased with reduced light intensity. In shaded tomato there was a decrease in aspartic acid, glutamic acid, phenylalanine, and leucine but an increase in serine and asparagine. In general, an increase in the amount of exudate occurred with an increase in temperature, but the relative proportions of the amino acids changed. The effect of age of plant on exudation is described in Table VII. TABLE VII Effects of Age of Plant on Micrograms of Amino-N and Sugars Exuded per Plant per Week for Four Crop Plants“ 1st to 15th day

3 1st to 45th day

16th to 30th day

Crop plant

Amino-N

Sugars

Amino-N

Sugars

Amino-N

Sugars

Sorghum Sunnhemp Ragi

0.22 0.28 0.15

38.3 31.7 19.6

0.19 0.38 0.10

44.8 22.4 16.8

0. I4 0.18 0.09

27.1 19.6 14.0

3rd to 10th day

I Ith to 18th day

21st to 28th day

29th to 34th day

5 1st to 57th day

Alfalfa (amino-N only) 0.46

0.29

0.33

0.33

0.6 I

“Recalculated from original data of Balasubramanian and Rangaswami ( I 969) for sorghum, sunnhemp, and ragi and from data of Richter e? al. ( I 968) for alfalfa.

Lack of oxygen favors anaerobic respiration which converts pyruvic acid formed during glycolysis into ethanol. Grineva ( 1 963) found that both corn and sunflower released ethanol into the rooting medium under low oxygen tensions and the rate of glycolysis increased. Anaerobic conditions also seemed to enhance excretion of mineral and organic

FACTORS AFFECTING ROOT EXUDATION

107

substances (Grineva, I96 1). Ayers and Thornton ( 1968) discovered that the gaseous atmosphere to which roots might be exposed had an effect on the quantity of amino acids released from pea roots. More ninhydrin active material was released under conditions of “soil-air” (i.e., air enriched to 0.5% COs) than with other gas mixtures. For example, the yield was 28.4 pg/plant for “soil-air” aeration compared to less than 6 pg/plant for the 2% O2 gas mixture and for the 10% COr gas mixture. Lundegardh and Stenlid ( I 944) reported that hydrogen ion concentration had little or no effect on the loss of organic compounds from roots. However, it has been found (Jacobson et al., 1950) that hydrogen ion concentration does have an effect on the exchange of inorganic ions. Blackman ( 1 956) found the uptake of 2,4-D to be highly dependent on the pH of the solution. However, the exudation of 2,4-D was unaffected by external pH. This factor has not been thoroughly investigated with regard to exudation of organic ions or compounds from roots. IX. Summary

Exudation from roots of organic substances is affected by a variety of factors including soil water stress, temperature, light intensity, age and species of plant, mineral nutrition, soil microorganisms, degree of anaerobiosis, and foliar application of chemicals. Compounds exuded, such as amino acids and carbohydrates, are involved in the ecological succession of microorganisms colonizing roots and in interactions with adjacent plants. The implications in control of plant root diseases, in control of weeds, and in mineral nutrition are as yet unknown. Development of new techniques and simplified systems is needed to establish cause and effect relationships and interactions in the soil-microbial-plant root ecosystem. ACKNOWLEDGMENTS We thank Sue A. Tolin and L. I . Miller for reading the original manuscript and for their useful suggestions. REFERENCES Ayers, W. A., and Thornton, R. H. 1968. Plant Soil 28, 193-207. Balasubramanian, A., and Rangaswami, G . 1969. Plant Soil 30, 210-220. Barber, D. A . 1968. Annu. Rev. Plant Physiol. 19,7 1-88. Barber, D. A., and Loughman, B. C. 1967. J. Exp. Bot. 18, 170-176. Blackman, G . E. 1956. I n “The Chemistry and Mode of Action of Growth Substances” (R. L. Wain and F. W. Wightman, eds.), pp. 253-259. Butterworth, London. 4/h / / J / . Co/igr. P l t i ~ ~ Prorwt., t 1957. Blackman. G . F.. l95X. PI.(JC.. Blackman, G . E., Sen, G., Birch, W. R., and Powell, R. G. 1958. J. Exp. Bot. 10,33-54.

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Bonner, J. 1950. Bot. Rev. 16,51-65. Bonner, J., and Galston, A. W. 1944. Bor. Gaz. 105, 185-198. Borner, H. 1960. Bot. Rev. 26,393-424. Bowen, G . D. 1968. Nature (London) 218,686-687. Bowen, G . D. I969a. PIanr Soil 30, 139- I4 1. Bowen, G. D. 1969b. Australian J. Biol. Sci. 22, 1125-1 135. Bowen, G. D., and Rovira, A. D. 1966. Nature (London) 211,665-666. Brams, E. 1969. Planr Soil 30, 105-108. Briggs, G. E., Hope, A. B., and Robertson, R. N. 1961. “Electrolytes and Plant Cells” Davis, Philadelphia, Pennsylvania. Burstrom, H. G. 1965. In “Ecology of Soil-Borne Plant Pathogens” (K. F. Baker and W. C. Snyder, eds.), pp. 154-169. Univ. of California Press, Berkeley. Chang, C. W., and Bandurski, R. S. 1964. Plant Physiol. 39,60-64. Clark, F. E. 1949. A d i m . Agron. 1, 242-288. Couch, H. B., and Bloom, J. R. 1960. Phyropathology 50,319-321. Crafts, A. S. 1961. “Translocation in Plants.” Holt, New York. Crafts, A. S. 1964. In “The Physiology and Biochemistry of Herbicides” (L. J. Audus, ed.), pp. 75-1 10. Academic Press, New York. Cranner, B. H. 1922. Meld. Norg. Landbrukshoeisk. 5, 1-160. DeCandolle, A. P. 1832 Physiol. V e g . 3, 1474-1475. Devlin, R. M. 1969. “Plant Physiology,” 2nd ed. Van Nostrand-Reinhold, Princeton, New Jersey. Dubrov, A. D., and Bulygina, E. V. 1967. Fiziol. Rust. 14, 247-263. Evanari, M. 1961. In “Handbuch der Pflanzenphysiologie” (W. Ruhland, ed.), Vol. 16, pp. 69 1-736. Springer-Verlag, Berlin and New York. Foy. C. L., and Hurtt, W. 1967. Proc. W e e d S o c . Amer. p. 40. (abstr.). Foy, C. L., and Yamaguchi, S. 1965. Absorption Translocarion Org. Subst. Plants, Symp., 1964, pp. 3-28. Garb, 0. 1961. Bot. Rev. 27,422-443. Greaves, M. P., and Webley, D. M. 1965. J. Appl. Bacteriol. 28,454-465. Grineva, G . M. 1961. Fiziol. Rust. 8,686-691. Grineva, G . M. 1963. Fiziol. Rust. 10,432-440. Grodzinsky, A. M. 1962. Ukr. Bor. Zh. 19, 3-20. Hale, M. G. 1968. Bull. Ass. Southeast. Biol. 15, 39. Head, G. C. 1964. Ann. Bot. (London) [N.S.] 28,495-498. Hiatt, A. J., and Lowe, R. H. 1967. Plant Physiol. 42, 1731-1736. Hurtt, W., and Foy, C. L. 1965a. Proc. Northeast. W e e d Contr. Con$ 19, 602. Hurtt, W., and Foy, C. L. 1965b. Plant Physiol. 40, Suppl., xlviii. Hussain, S. S., and McKeen, W. E. 1963. Phytoparhology 53, 541-545. Ivanov, V. P., Yakobsin, G. A., and Voinov, M. I 1963. Kukuruza 8,34-35. Ivanov, V P., Yakobsin, G. A., and Fomenko, B. S. 1964. Fiziol. Rust. 11, 631-637. Jacobson, L., Overstreet, R., King, H. M., and Handley, R. A. 1950. Plant Physiol. 25, 639-647. Jenny, H., and Grossenbacker, K. 1963. Soil Sci. SOC.Amer., Proc. 27,273-277. Katznelson, H., Rouatt, J. W., and Payne, T. M. B. 1954.Nature (London) 174,l 110-1 I I I . Kerr, A. 1964. Australian J . Biol. Sci. 17, 676-685. Klein, L. K. 1968. I n t . A t . Energy Agency, Proc. pp. 39 1-402. Knudson, L. 19 19. Amer. J. Bot. 6, 309-3 10. Knudson, L. 1920. Amer. J. Bor. 7, 371-379. Laties, G. W. 1969. Annu. Rev. Plant Physiol. 20, 89- I 16.

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Levi, E. 1968. Naturwissenschafren 55,42. Levitt, J. 1969. “Introduction to Plant Physiology.” Mosby, St. Louis, Missouri. Linder, P. J., Craig, J. C., Cooper, F. E., and Mitchell, J. W. 1958. J . A g r . Food C h e m . 6, 356- 357. Linder, P. J., Mitchell, J. W., and Freeman, G. D. 1964. J. A g r . Food Chem. 12,437-438. Loehwing, W. F. 1937. Bot. R e v . 3, 195-239. Lundegardh, H., and Stenlid, G . 1944. A r k . Bot. 31, 1-27. Lyon, T. L., and Wilson. J. K. 1921. Cornell Univ., A g r . Exp. Sta., M e m . 40, 1-44. MacDonald, 1. R. 1967. Ann. Bot. (London) [N.S.] 31, 163-172. McDougall, B. 1968. Trans. Int. Congr. Soil Sci. 9th pp. 647-655. McDougall, B., and Rovira, A. D. 1965. Nature (London) 207, 1104-1 105. Manorik, A. V., and Belima, N. 1. 1969. Fiziol. Rust. 16, 358-364. Miller, R. H., and Schmidt, E. L. 1965a. Soil Sci. 100, 267-273. Miller, R. H., and Schmidt, E. L. 1965b. Soil Sci. 100, 323-330. Mitchell, J. W., Smale, B. C., and Preston, W. H., Jr. 1959. J . A g r . Food C h e m . 7, 841843. Mollenhauer, H. H. 1967. A m e r . J. Bot. 54, 1249- 1259. Morre, D. J., Jones, D. D., and Mollenhauer, H. H. 1967. Planta 74, 286-301. O’Brien, D . G., and Prentice, E. G. 1930. Scot. J. A g r . 13, 391-396. Pearson, R.,and Parkinson, D. I96 I . Plant Soil 13,39 1-396. Preston, W. H.. Jr.. Mitchell, J . W., and Reeve, W. 1954. Science 119,437-438. Ramchandra-Reddy, T. K. I968a. Plant Soil 24, 102- I 13. Ramchandra-Reddy, T. K. 1968b. Plant Soil 24, 1 14-1 18. Richter, M., Wilms, W., and Sheffer. F. 1968. Plant Physiol. 43, 1747-1754. Rovira, A. D. 1959. Plant Soil 11, 53-64. Rovira, A. D. 1965a. Annu. R e v . Microbiol. 10, 242. Rovira, A. D. 1965b. In “Ecology of Soil-borne Plant Pathogens” (K. F. Baker and W. Snyder, eds.), pp. 170- 186. Univ. of California Press, Berkeley. Rovira, A. D. 1969a. Bor. R e v . 35, 35-57. Rovira, A. D. I969b. Australian J. Biol. Sci. 22, 1285- 1290. Santovich, S. A. 1965. Fiziol. Rust. 12, 837-846. Schroth, M. N., and Hildebrand, D. C. 1964. Annu. R e v . Phytopathol. 2, 10-132. Schroth, M. N., Weinhold, A. R., and Hayman, D. S. 1966. C a n . J . Bot. 44, 1429-1432. Scott, G. D. 1969. “Plant Symbiosis.” St. Martin’s Press, New York. Slankis, V., Runeckles, V. C., and Krotkov, G. 1964. Physiol. Plant. 17, 301-313. Sperber, J. I. 1957. Nature (London) 180,994-995. Steinberg, R. A. 1950. Bull. Torrey Bot. Club 77, 38-44. Steinberg, R. A. 1952. Plant Physiol. 27, 302-308. Street, H. E. 1966. Annu. R e v . Plant Physiol. 17, 315-344. Subba Rao, N. S., Bidwell, R. G. S., and Bailey, L. D. 1961. C a n . J . Bot. 39, 1759-1764. Sullia, S. B. 1968. Plant Soil 24, 292-298. Sutcliffe, J. F. 1962. “Mineral Salts Absorption in Plants.” Pergamon, Oxford. Trolldenier, G., and Marckwordt, U. 1962. Arch. Mikrobiol. 43, 148-15 I. Tukey, H. B., Jr. 1966. Bull. Torrey Bot. Club 93, 385-401. Vancura, V. 1964. Plant Soil 21,23 1-248. Vancura, V. 1967. Plant Soil 27,319-328. West, P. M. 1939. Nature (London) 144, 1050-1051. Wetzel, R. G. 1969. BioScience 19, 539-542. Woltz, S. 1963. Plant Physiol. 38,93-99. Woods, F. W. 1960. Bot. R e v . 26,546-569.

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NATURE, EXTENT, AND VARIATION OF PLANT RESPONSE TO AIR POLLUTANTS H. E. Heggestad and W. W. Heck Agricultural Research Service, U. S. Department of Agriculture, Beltsville, Maryland, and Environmental Protection Agency, North Carolina State University, Raleigh, North Carolina

I.

Ill

Introduction

B. Nature and Extent of .................. C. Meteorology ...................................................................... D. Economic Considerations ................................................. 11. Nature of Plant Response ...............................

......................... A. Geographic .....................

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

A. Genetic Factors .............................

Ill I I3 I I4

I15 1 I6

I I6 I17 I20 I20 121 121 I22 I22 125 131

133

V.

E. Time-Concentration-Injury Relations F. Mechanism of Action of Pollutants ............................ Discussion ....................................................................... References ..............

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

I.

A.

I35 137 I39 I40 141

Introduction

HISTORICAL PERSPECTIVE

Investigations of air pollution injury to vegetation began near the middle of the nineteenth century. A. Stockhart and J. von Schroeder of Germany studied the effects of sulfur dioxide and fluorine (0%1907). Von Schroeder and Reuss ( 1 883) described injury symptoms caused by sulfur dioxide and other pollutants. Injury from leaking illuminating gas mains also was an early problem. Ethylene was identified as the toxicant Ill

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H . E. HEGGESTAD AND W. W. HECK

in the illuminating gas (Neliubov, 1901). Reviews of the early German literature are available (Haselhof and Lindau, 1903; Ost, 1907). Historical information on air pollution injury to vegetation in the United States is found in several reviews (Crocker, 1948; Katz, 1949; Thomas, I95 1 , 196 1). The first reports were accounts of sulfur dioxide injury to plant life (Widtsoe, 1903; Haywood, 1905). In the early episodes, sulfur dioxide emissions caused complete destruction of vegetation over large areas, for example, Ducktown, Tennessee (Seigworth, 1943) and Trail, British Columbia (National Research Council of Canada, 1939). More recently, severe losses occurred also around Sudbury, Ontario (Linzon, 1958). Complete loss of vegetation may be avoided in the future, but interest in the problem has continued, primarily because of the increased number of large power plants which burn sulfur-containing fuels and emit high concentrations of sulfur oxides (Wood, 1968). The use of very tall stacks tends to reduce the frequency and duration of high ground-level concentrations, since dispersal is over a greater area. Research on fluoride as an air pollutant in the United States was initiated about 1940 (Zimmerman and Hitchcock, 1946; Leone et al., 1948; V. L. Miller et al., 1948). Fluoride accumulates in leaves and directly injures many species of plants. Other plants, such as alfalfa and several grass species, may accumulate large amounts of fluoride from very low air concentrations, resulting in severe injury to animals which ingest the forage. Injury to vegetation by photochemical pollutants (oxidants) was first observed about 1944 in a small area of Los Angeles County (Middleton et al., 1950). The injury was characterized as glazing, silvering, and bronzing of lower leaf surfaces of broadleaf plants. Similar injury was produced in the laboratory by exposure to reaction products of ozone and unsaturated hydrocarbons (Haagen-Smit et al., 1952). Later, peroxyacyl nitrates (PANS) were shown to be the primary cause of the undersurface injury (Stephens et al., 1961). Ozone was first found to be phytotoxic from studies involving electric currents (Knight and Priestly, 19 14). The first laboratory study involving ozone and plants was conducted about twenty years later (Homan, 1937). It was not until 1958, however, that ozone injury to field-grown plants was identified (Richards et al., 1958). They determined that ozone caused “grape stipple,” an injury on the upper leaf surface of grapes grown in the Los Angeles area. Subsequently, ozone was implicated as the cause of “weather fleck” of tobacco (Heggestad and Middleton, I959), emergence tip burn of white pine (Berry and Ripperton, 1963), and chlorotic needle mottle of ponderosa pine (P. R. Miller et al., 1963). Now, ozone injury to vegetation is more common than injury from any other pollutant (Rich,

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1964; Heggestad, 1969). Recent reviews of the literature on effects of major air pollutants on crop plants are available (Brandt and Heck, 1968; Heggestad, 1968; Jacobson and Hill, 1970; Webster, 1967). B.

NATUREA N D EXTENTOF A I R POLLUTANTS

Phytotoxicants in the atmosphere may be grouped into two categories: ( 1 ) primary pollutants emitted from combustion sources or industrial

processes, and (2) secondary pollutants produced by chemical reactions in the atmosphere. Primary pollutants of major concern to agriculture are sulfur dioxide, ethylene, fluoride, nitrogen dioxide, and pesticides. They are emitted primarily from point sources and usually affect agriculture in a localized region. Dilution and dispersion of the pollutants from these sources is normally effective in limiting detectable injury to a radius of a few miles. Injury has extended as much as 30 miles downwind from a major source. Since significant amounts of ethylene and nitric oxide are emitted in automobile exhaust, they are more widely dispersed than most primary pollutants. The nitric oxide is converted to nitrogen dioxide, which is phytotoxic and participates in photochemical reactions. Secondary pollutants, i.e., ozone, PAN, and nitrogen dioxide are formed in the atmosphere. They are more widespread than the primary pollutants and may occur in phytotoxic concentrations over an extensive area of a State or over several States. I n the eastern United States, these pollutants may be in higher concentrations to the north and east of urban centers because the air movement tends to be from the south-southwest when pollutants are high (Wanta and Heggestad, 1959). Because it takes time for ozone to be formed by action of sunlight on products of fuel combustion, the concentration of ozone may be higher several miles downwind of the city (Wanta er al., 196 I ) . Many factors, however, determine the ozone and PAN content of the air (Haagen-Smit and Wayne, 1968). The most common phytotoxic air pollutants in the United States are ozone, sulfur dioxide, fluorides, peroxyacyl nitrates, ethylene, nitrogen dioxide, pesticides, chlorine, heavy metals, acid aerosols, ammonia, aldehydes, hydrogen chloride, hydrogen sulfide, and particulates, such as cement dust. Ozone and sulfur dioxide are widely distributed. In this country, ozone seems to be causing more plant damage than any other air pollutant; but on a worldwide basis, there is evidence that sulfur dioxide is more injurious than ozone. Sources of phytotoxic air pollutants were reviewed recently (Wood, 1968). Sulfur dioxide is emitted primarily from combustion of coal and other petroleum products, smelting and refining of ores, and the manufacture and utilization of sulfuric acid. Fluorides originate primarily from aluminum and other metal reduction processes, manufacture of phos-

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HEGGESTAD A N D W. W. HECK

phate fertilizer, brick and pottery plants, and steel manufacturing. Ozone and PAN are formed by photochemical reactions. Additional sources of ozone may be stratospheric ozone which is brought to the earth’s surface (Wanta et al., 1961; Davis and Dean, 1966), ozone formed in electric storms, and by electrical discharges. Nitrogen oxides originate from high temperature combustion of fuels, such as gasoline in motor vehicles. Efforts are presently underway to reduce emissions of contaminants from motor vehicles. Hydrocarbons, carbon monoxide, and nitrogen oxides are the primary targets. There has been little progress to date in controlling the nitrogen oxides. C. METEOROLOGY The atmosphere is the medium in which air pollutants are transferred from a source. Air pollution episodes are closely associated with stagnating air over a region. The role of meteorology in air pollution has been the subject of many investigations, and a large body of literature exists. A recent book (Stern, 1968) has four chapters devoted to different aspects of the phenomenon, including Meteorology and Air Pollution, Atmospheric Dispersion of Stack Effluents, Air Pollution Climatology, and Meteorological Management of Air Pollution. The growing problem of urban air pollution with its multiple sources of pollutants is receiving increased attention. According to Pack ( I 964), from one year to another pollution emissions tend to stay constant, and the meteorology of diffusion varies, but over a period of several years, it is the meteorology that is relatively stable, and the pollution sources that vary. Stagnating anticyclones, or warm highs, in the eastern United States, occur most frequently in the southeast, centering around Georgia and South Carolina (Hosler, 196 1) Significant meteorological parameters during some high-ozone days at Washington, D.C., were determined; they include: relatively high air temperatures and solar radiation, low relative humidity, surface wind direction from a southerly quadrant, slow wind speeds (< 8 miles per hour) at the surface and near the top of the convective layer, and depth of convective layer ranging from 200 to 4700 feet (Wanta et al., 1961). In the western United States, stagnating conditions occur frequently over the southwest, especially southern California and Arizona, and over the Great Basin of Utah. Topographic barriers, such as those around the Los Angeles Basin, further slow the flow of air in and out of the area. Pack ( 1964), commenting on the worldwide meteorological situation favoring the accumulation of pollutants, says: “The semipermanent inversion is a feature of west coasts of continents throughout the world. Africa, the Siberian Peninsula, South America, and the southwestern coast of the

PLANT RESPONSE TO AIR POLLUTANTS

1 I5

United States all have this typical vertical turbulence lid created by subsidence associated with the semipermanent high-pressure areas of the eastern subtropical oceans.”

D. ECONOMIC CONSIDERATIONS Guderian et al. (1960) make a distinction between the terms injury and damage, which is useful in a discussion of the economic impact of air pollutants on agricultural receptors. Injury is defined as any identifiable and measurable response of a plant to air pollution. Damage is a n y identifiable and measurable adverse effect upon the desired or intended use of the plant (or upon the derived product of the plant). Necrotic lesions produced by pollutants is injury, but the assessment of damage depends on the extent to which yield, or use of the plant, is reduced. The initial identification of injury also requires judgment, since injury patterns are not always unique to the pollutant and may be caused by disease, nutrition, insects, or environmental and management factors. Some of the metabolic changes that occur with low pollutant concentrations also may result in damage (economic loss). Visible injury must be evaluated to determine whether damage actually occurred. A pollutant that injures the leaves of a leafy crop before harvest may not affect yield, but the appearance of the leaf may make it unmarketable. The result is complete loss of the crop. I t is fairly easy to relate effects to this kind of damage, but very difficult to evaluate the effects on growth, development, survival, or use of plants when visible injury is absent. We may compare growth of plants in filtered and unfiltered air; but extrapolation to field conditions is tenuous. Several attempts have been made to assess air pollution damage to agriculture; all require major judgmental decisions by the investigator who collects the data. Landau and Brandt ( 1 970) suggest that this limits the degree of applicability of the survey. They belleve that the success of surveys conducted by the Statistical Reporting Service, U.S. Department of Agriculture, is based on the collection of data which require a minimum of subjective decisions. To evaluate air pollution damage, methods that require the fewest possible decisions are likely to produce the best estimates of loss. A group of trained observers was used in a California survey (Middleton and Paulus, 1956) involving crops of economic importance in the state. These observers underwent special training which, in addition to public motivation, affected their results. They reported all they saw on a field-by-field basis, but may have missed some injury and damage. No attempt was made to judge reduced growth or yield. An excellent record of the distribution of plant injury from air pollutants was obtained.

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A somewhat similar survey was reported from the State of Pennsylvania where an intensive training and surveillance program was initiated during the 1969 growing season. First-year reports from this survey give an estimate of $ I 1.5 million loss for the State (Lacasse el al., 1970). Similar training sessions and surveys are being planned for other States in an effort to develop a nationwide estimate of economic losses. These surveys assess only the visible injury to affected vegetation; consequently, they suffer the major deficiency of ignoring growth and yield effects. A second type of study was initiated in 1969 to develop a model from which dollar values could be calculated (H M. Benedict, Stanford Research Institute, personal communication). The model made use of known effects of pollutants on various crop species from laboratory and field exposures. It also made use of data from atmospheric chemistry and the amount of secondary pollutants produced from given concentrations of primary pollutants; and the reported levels of pollutants which cause injury to crops. The researchers used hydrocarbon values from over I00 statistical reporting areas within the United States. On the basis of these hydrocarbon values and related oxidant data, they developed injury and damage estimates for specific crops in the statistical reporting areas. The approach, by its very nature, uses many subjective assumptions and relates only to visible injury symptoms. Research information is not available to make an accurate assessment of the overall impact of air pollution on the agricultural economy. The survey by Benedict projected about $100 million losses to vegetation. Gross estimates in the past have run between $500 and $1000 million annually. When we project preliminary greenhouse and field data which relate to reduced growth and yield, and take into account effects on ornamentals, wildlife, and esthetic values, we believe that these gross estimates may be too low. II.

N a t u r e of Plant Response

A. TYPESOF INJURY The visible symptoms of injury to plants attributable to air pollutants can be placed into three broad categories: acute injury, chronic injury, and physiological effects. (As discussed under Section I, D, not all injury results in damage.) Acute injury is manifested by cell collapse with subsequent development of identifiable necrotic patterns. Symptoms result from short exposures (measured in hours) to varying concentrations of the pollutant, and usually appear within 24 hours after exposure. In some cases, the injury may be intercostal and show only on the upper or lower leaf surfaces. If large amounts of the pollutant are absorbed, there may be

PLANT RESPONSE TO AIR POLLUTANTS

I I7

complete loss of some leaves, and even death of plants. Each pollutant tends to produce a characteristic pattern of acute injury. Chronic injury results from intermittent exposures, over long periods, to low concentrations of the gas. I t results in chlorotic or other pigmented patterns in leaf tissues, and may be accompanied by an increase in leaf drop. At times, injury may be severe and even develop classical necrotic patterns, as in the marginal necrosis produced by fluoride. Chronic injury patterns are often highly characteristic, but by no means specific for each pollutant. Diseases, insects, nutritional imbalances, low temperature, drought, and other factors can produce leaf patterns similar to those induced by air pollutants. Chronic injury may appear as early senescence in leaves of many sensitive species and thus avoid recognition by the uninformed field observer. Physiological effects include growth alterations, reduced yields, and changes in the quality of plant products. They also include transitory metabolic disturbances which may not be measurable in terms of growth or yield. Some of these effects have been measured under laboratory conditions and include changes in respiratory or photosynthetic rates, in transpiration, and in rates of enzymatic processes. Comparison of growth of plants in filtered and unfiltered air, or exposure of plants to low levels of pollutants under controlled conditions for long periods of time has provided information on reduced growth and yield, as well as information on symptoms of chronic injury. Ethylene can cause epinasty of leaves; it can reduce growth and cause flower and leaf abscission, without visible injury (Heck and Pires, 1962). There is also evidence that oxidants such as ozone can reduce growth of certain crops: for example, citrus (Thompson and Taylor, 1969), radish (Tingey et al., 1969a), tobacco (Reinert et al., 1969), and carnations (Feder and Campbell, 1968). With species such as citrus, yields may be reduced even though there is very little visual evidence of injury to leaves. A reduction in percent germination of pollen and in the growth in length of pollen tubes has been reported on tobacco by ozone (Feder, 1968) and on sweet cherry by fluoride (T. Facteau, Oregon State University, personal communication). These effects could be classified under the general category of physiological effects. B.

DESCRIPTION OF INJURY

TO

AGRONOMIC SPECIES

1 . Ozone

On most herbaceous plants, ozone induces small necrotic spots on the upper surface of fully expanded leaves. Palisade cells are first to be

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visibly injured. On grains and grasses which lack palisade tissue, injury develops in the mesophyll and appears on both leaf surfaces. On all plants, the individual small lesions are interveinal and tend to be irregular in shape. Bifacial necrosis occurs when lesions are large. Chlorotic mottling and increased pigmentation are frequently associated with the injury. Older leaves may become prematurely senescent and drop (Ledbetter et al., 1959; Hill et al., 1970) On tobacco and some other plants, leaves exhibit wilting or have an oily appearance on days of high ozone concentration. The next morning, water-soaked lesions are a common first symptom of injury on field-grown tobacco plants. Necrotic lesions are frequently more numerous along small veins. They usually appear dark at first, but they change to a light gray or tan fleck as the tissue dies. If the plants are nitrogen deficient, the lesions may remain dark. When leaves overlap or are folded, there may be no injury on the portions of leaves that were covered. On soybeans, after fumigation with ozone, one observes dark lesions on the older and more chlorotic leaves, whereas lesions may be dark or light on younger, green leaves. Ozone injury to alfalfa results in variable symptoms. Various necrotic and chlorotic patterns develop. Frequently, the injury is concentrated along veins. On small grains and forage grasses, some of the injury may appear as interveinal streaks. The outer mesophyll cells adjacent to the vascular bundle sheath and cells overlying small vascular strands without bundle sheath extensions are frequently those most readily injured by ozone (Hill et al., 196 1). On some species of grass, especially if plants are grown with high nitrogen, the lesions are reddish-brown rather than tan or gray. Symptoms of ozone injury may vary considerably between different species and even between plants of the same variety. However, at least some leaves are likely to show the described symptoms. 2. PAN

PAN causes an undersurface leaf injury described as glazing, silvering, and bronzing. Usually only a few rapidly expanding leaves are injured after an episode. The injury is at the apex of the youngest susceptible leaf, as a transverse band on an intermediate leaf, and at the base of the older susceptible leaf (0. C. Taylor e f al., 1960; 0. C. Taylor and MacLean, 1970). The two primary leaves of Pinto bean are uniformly sensitive, so that banding does not occur. Growth of young tissue in the injured area may be suppressed so that leaves of petunia and other plants develop a pinched appearance as they mature. Leaves of monocotyledons develop the most distinct transverse bands (Juhren et al., 1957). AIthough glazing and bronzing are usually confined to the lower leaf surface,

PLANT RESPONSE TO AIR POLLUTANTS

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symptoms have developed on the upper surface of tobacco, petunia, and tomato exposed to PAN in controlled fumigations.

3. Sulfur Dioxide Acute sulfur dioxide injury is usually bifacial and interveinal with relatively large collapsed areas surrounding the larger veins which remain green. The injury is usually ivory in color, whereas with chronic injury, the brown and red colors are more common. Because of parallel veins, leaves of monocotyledons may show necrotic streaks. The injury is usually more severe near leaf tips and along the blade where the leaf bends. As with ozone, the young, fully expanded leaves are the most sensitive to sulfur dioxide. The youngest leaves are resistant. The acute markings of sulfur dioxide on alfalfa are easily confused with those caused by ozone. Plants exposed to low concentrations of sulfur dioxide for long periods of time may show elevated sulfur content in the leaves and may have a general chlorotic appearance (Barrett and Benedict, 1970; van Haut and Stratmann, 1970). 4 . Fluoride The predominant symptom of fluoride injury to most plants is necrosis of leaf tips and margins. The lesions may be gray or light green at first, but later they become reddish-brown or tan. There is usually a sharp line of demarcation between healthy and diseased tissue. Sometimes there is a narrow red transitional area. Some plants may have premature abscission of leaves if the injury is severe. Fluoride may cause a chlorotic symptom expression in leaves of citrus. The chlorosis extends from the margin to the areas between larger veins (Treshow and Pack, 1970). Fluoride injury on corn consists of a chlorotic flecking predominantly along the leaf margins and extending to the leaf tip. When injury is severe, the entire leaf may be chlorotic (Hitchcock er al., 1963). The chlorotic tissue may become necrotic if injury is hvere. Injury symptoms on sorghum are similar to those on corn. Diagnosis of fluoride injury is aided by leaf analysis. Injured leaves of sensitive species may have 20 to 100 ppm fluoride, whereas tolerant plant species, such as cotton, may contain 4000 ppm without injury (Jacobson er a/., 1966). 5 . Nitrogen Dioxide Information on the nature of injury by nitrogen dioxide has been provided by 0. C. Taylor and MacLean (1970). Acute injury by nitrogen dioxide closely resembles symptoms produced by sulfur dioxide. The injury is most likely to be associated with accidental releases of the toxi-

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cant. Glater ( I 970) stated that ambient levels of nitrogen dioxide may be responsible for some of the chronic injury to vegetation prevalent in the Los Angeles Basin. She believes that injury from nitrogen oxides is replacing the old PAN-type. However, the type of injury reported is similar to what we have seen from ozone exposures and high oxidant levels in Eastern urban areas. 0. C. Taylor and Eaton (1966) did not find that nitrogen dioxide, at low concentrations for several days, would produce the type of injury reported by Glater ( I 970). They reported an increase in chlorophyll in the exposed plants. The responses reported by Glater ( 1 970) are probably more related to ozone than the nitrogen oxides, but her suggestion that PAN-type of injury is decreasing is probably correct. As discussed in Section IV, B, 7, there is evidence that nitrogen dioxide and other pollutants, such as sulfur dioxide, may produce additive injury.

6 . Other Pollutants Injuries by minor pollutants have been described by Heck et al. ( 1 970), who reviewed information on effects of the following: unsaturated

hydrocarbons (as ethylene), pesticides (especially the volatile herbicides), chlorine, ammonia, hydrogen chloride, mercury, particulates, hydrogen sulfide, and carbon monoxide. The review mentions those concentrations that cause injury, and it also discusses the relative sensitivity of some plant species to specific pollutants. Ill.

A.

Extent of Response

GEOGRAPHIC

Growers of special crops have had to movc out of high pollution areas for example, orchid growers from the Los Angeles and San Francisco areas (Middleton, 1964). The continuous problem with air pollution on cigar-wrapper tobacco in the Connecticut Valley has increased the cost of production, and to some extent, it has caused growers to either discontinue or reduce the acreage of the crop. Air pollution has reduced the production of certain vegetable crops near large urban centers, such as New York, Philadelphia, and Los Angeles. Agriculture near industries that emit fluorides and sulfur compounds has been either changed or eliminated. In some cases, the industries find it less expensive to purchase the land than to deal with the original owners on crop losses or alleged losses. Air quality standards for the protection of agriculture may need to be developed. Considerable information is available on concentrations of the various pollutants that cause significant injury. The quality of the air that is needed will depend on the type of vegetation desired in each area. In

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the future, more consideration will have to be given to the best use of land because certain pollution sources and certain kinds of agricultural uses are not compatible. B. SEASONAL Air pollution episodes tend to cause most injury when crops are either in the seedling to young stage, or as they approach maturity. Levels of photochemical air pollutants are usually highest in midsummer when temperatures are high. The frequency of low level inversions that favor accumulation of pollutants is greatest in the fall. By that time, in Northern latitudes, most crops are harvested, but truck crops and fall-seeded crops are vulnerable in southern areas, especially in California. There is evidence that the greatest injury to peach fruit from fluorides occurs in the spring when fruit is in the developmental stage. This may be true of both citrus and sweet cherry. By contrast, tobacco, lettuce, and spinach crops have been injured severely just prior to harvest by photochemical air pollutants. A recent study of white pine indicates that leaves of certain sensitive trees may be injured by exposure to only 0.05 ppm sulfur dioxide for an hour (Costonis, 1970). The leaves, however, must be in a certain developmental stage; consequently, they are most vulnerable for only a few days in late spring or early summer, depending on the geographic location. C.

FUTURETRENDS

The increased population and demands of people everywhere for higher standards of living seem to assure a continuing air pollution problem involving vegetation. Although emissions from specific sources, including the automobile, may be reduced, the increased number of units may result in as much pollution. Greater efforts are underway to reduce pollutants from automobiles by the mid- 1970’s (Council of Environmental Quality, 1970). Projections have been made for pollutant emissions to the year 2000 (Wood, 1968). Total emissions from transportation of all types may triple. Much attention is being given to desulfurization of coal and other fuels, and scrubbing sulfur dioxide from stack gases. These efforts may be successful ; however, the increased pollutant emission from oil- and coalfired generating stations were projected to double from 1960 to 1980. A study of air basins in Pennsylvania (Wood, 1968) showed a large increase in the size of the area with potential vegetation damage from powergenerating stations. The possibility of interactions involving sulfur dioxide, ozone, and nitrogen oxides increases the possibility of vegetation

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injury especially in areas with several coal-fired electric power-generating stations. Unless a new type of power plant is developed for motor vehicles, our major problems of air pollution on vegetation will be with photochemical air pollutants. At present, the entire east coast of the United States, from Washington to Boston, tends to have about the same level of oxidant air pollution. IV.

Variation in Response as Related to Other Factors

Many factors influence the sensitivity of plants to air pollutants. In most cases, our understanding of the importance of any given factor on a specific variety or species of plant is fragmentary or preliminary in nature. Additional work is essential before the relative importance of these factors can be adequately interpreted. The response of a given species or variety of plant to a specific air pollutant cannot be predetermined on the basis of the known response of related plants to the same pollutant. Neither can the response to a pollutant be predetermined by the known response of a plant to similar doses of a different pollutant. Before we can predict how a plant variety will respond to a specific pollution insult, we must have knowledge about the influence of many interrelated factors. FACTORS A. GENETIC

Present knowledge concerning the influence of genetic variability on plant response to pollutants is confined to general field observations, and to research to determine varietal response in chambers under controlled conditions. Let us discuss the information in relation to two general areas of interest: first, the variable response within species and the basic genetic makeup that might account for this variability; second, the potential for increasing tolerance of plants to pollutants by breeding studies. I . Response of Species

Much genetic variability exists between and within species as regards susceptibility to air pollutants. However, susceptibility to one air pollutant may not mean susceptibility to another pollutant, as evidenced by the inverse susceptibility of some plants to fluoride and sulfur dioxide. Species variability has been recorded in numerous genera and families (Jacobson and Hill, 1970); and major varietal differences have been shown in such species as oat (Sechler and Davis, I964), potato and oat (Brennan et al., 19641, petunia (Feder et al., 1969a), forage legumes (Brennan et al., 1969), turfgrasses (Brennan and Halisky, I970), tobacco (Heggestad et

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al., 1964; Macdowell et al., 1963; Menser, 1966, 1969; Menser and Hodges, 1970), onion (Engle and Gabelman, 1966), tomato and radish (Reinert et al., 1969), soybean (Tingey et al., 1969b), lettuce (Reinert et al., 1970), corn (Cameron et al., 1970), alfalfa (Howell et al., 1971), and white pine (Berry and Hepting, 1964). Varietal variations have been most extensively studied in the species Nicotiana tabacum L. Heggestad et al. ( 1964) compared the response of six tobacco varieties to various oxidants or oxidant mixtures. Injury varied, depending on the toxicant and variety used. Menser ( 1966) found that cigar-wrapper varieties of tobacco were more sensitive than five flue-cured tobacco varieties, including White Gold. Macdowell et al. (1963) reported White Gold to be the most susceptible of 32 tobacco varieties tested. R. A. Reinert (personal communication) reported that several burley tobacco varieties were less sensitive than the cigarwrapper variety BeLW3. Haas (1970) reported that an oxidant induced bronzing of a uniform stand of white bean (Phaseolus vulgaris L.) did not develop uniformly through the stand. He believes that field testing in a breeding program will be difficult because of high within-line variability in disease incidence. However, it is known that selection for increased tolerance within lines of cigar-wrapper tobacco has been very productive. White pine (Pinus strobus L.) shows variable sensitivity to many pollutants; about 30% of the individuals are injured more or less severely by one or more of the major pollutants: ozone, sulfur dioxide, or fluoride. Within a given seed population, some trees are sensitive to more than one pollutant, others to a single pollutant, and some to none of the pollutants (Berry and Hepting, 1964). A chlorotic dwarf syndrome of white pine has been related to the general problem of air pollution in the eastern United States (Dochinger and Seliskar, 1970). This disease also affects about 30% of the pine. Dochinger et al. (1970) report that 0.05 ppm of sulfur dioxide or ozone will occasionally produce slight tip burn, chlorotic mottle, or both, on chlorotic dwarf sensitive clones of white pine. Slight to severe needle mottle and slight tip burn were routinely produced when the sensitive pine were exposed 8 hours per day for several days to a mixture of these pollutants, each at the same concentration (0.05 ppm). The pollutant concentrations used occurred fairly often in the chlorotic dwarf area of Ohio. One of the most interesting studies of varietal susceptibility to ozone involved experiments with onion (Engle and Gabelman, 1966). A single dominant gene pair controlled the resistance response. The trait regulated the sensitivity of the guard cells to ozone. The stomata of the resistant variety closed after exposure to ozone and prevented injury. They reopened soon after the exposure terminated. The stomata of the susceptible

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variety remained open upon exposure to ozone, and injury occurred. The inheritance of plant resistance to pollutants requires further investigation. Some studies reflect the effect of fluoride and ozone on reproductive structures. Mohamed ( 1 968) reported an increase in genetic aberrations in progeny of tomato whose parents were exposed to fluoride. T. Facteau, Oregon State University (personal communication), found a reduction in percentage of germination of sweet cherry pollen, and also in the rate of elongation of germinating pollen, as a result of exposure to hydrogen fluoride. He also found a reduction in fruit set following exposure to fluoride during bloom. Ozone reduced the germination of tobacco pollen and the length of pollen tubes (Feder, 1968). The relative susceptibility of pollen to ozone was correlated with the susceptibility of parental varieties and species (Feder and Sullivan, 1969). Field observations in California showed a reduction in fruit set in corn in areas where severe injury to corn leaves had occurred from ambient oxidant pollution (Cameron et al., 1970). These observations lend support to the possibility of direct effects of pollutants on plant reproductive structures. 2 . Breeding Studies The above studies clearly indicate that considerable genetic variability in pollutant sensitivity exists within varieties of any given species. Because plant breeders normally select plants and breeding lines with highest yield and least injury regardless of cause, this natural selection has, no doubt, increased the tolerance of some native and crop species to pollutants. Because air pollution is increasing and controls are not yet available to greatly reduce pollution, there is a need to identify the most resistant plant material and to develop more resistant varieties, especially of sensitive species commonly grown in the more heavily polluted areas of the United States. Breeding studies were initiated about 15 years ago in the Connecticut Valley to reduce weather fleck injury to wrapper tobacco. Use of the more sensitive varieties was discontinued, and the development of resistant varieties encouraged. Except for tobacco, no definitive breeding programs to increase resistance to air pollutants have been developed. This research is underway in the United States, primarily in Connecticut, Maryland, and Florida. Breeding studies are in progress also on tobacco in Ontario, Canada (Povilaitis, 1967). Researchers concerned with other crops are beginning to discuss the development of such programs. The varietal studies previously listed under response of species (Section IV, A, I), identify possible sources of more resistant genetic material for use in breeding programs. This is an area where additional research is needed.

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B. CLIMATIC FACTORS The effects of climatic factors on the expression of pollutant injury to sensitive plants has been studied, primarily under laboratory conditions. Many current reports are incomplete or have studied only one or two factors without controlling others. Contradictions in results have occasionally been noted: The effects of climatic variables on the sensitivity of plants to specific pollutants must be understood, if field injury to plants is to be adequately interpreted. Environmental conditions prior to, during, and after exposure to air pollutants may alter plant response. A given set of conditions for only 1-5 days prior to exposure may increase or decrease the injury. Conditions during exposure can be extremely critical. Studies are needed also to determine possible interactions between conditions prior to and during exposure. Conditions after exposure are important, but they are probably less so than those before and during exposure. 1 . Light Quality

The quality of light received by a plant prior to exposure may affect sensitivity. Numerous reports suggest a different sensitivity between plants grown outdoors, in greenhouses, and under growth chamber conditions. Since it is impossible to control outside variables and greenhouse variables are only partially controlled, it is highly speculative to suggest that the foregoing variations in sensitivity are due to light quality. Plants grown in greenhouses are usually more sensitive to air pollutants than those grown in growth chambers. Pinto bean is sensitive to PAN only when there is light prior to, during, and after exposure to PAN (0.C. Taylor et al., 1961). The presence of a photoreactive system within the plant was suggested. Critical studies involving light of different wavelengths revealed injury to bean by PAN was maximal at 420 and 480 nm, and it was several times greater than at 640 nm (Dugger et al., 1963a). The authors suggested that the carotenoid pigments, rather than the chlorophylls, were responsive. Later, Dugger and Ting ( 1 968) found that a two-light reaction system at 660 and 700 nrn controlled the response of the plant to PAN. Plants were more sensitive under 660 nm than under 700 nm.

2. Light Duration (Photoperiod) A given duration of light in a 24-hour period is known to exert a controlling effect on certain aspects of plant development. Juhren et al. ( 1957) reported that an 8-hour photoperiod produced greater oxidant sensitivity in annual bluegrass than a 16-hour photoperiod, regardless of the temper-

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atures during growth. Heck and Dunning ( 1 967) found that Pinto bean and tobacco were much more sensitive to ozone when grown under an 8-hour photoperiod, as did Menser ( I 962) and Macdowall ( I 965) when using tobacco of different ages as well as different photoperiods.

3. Light Intensity Pinto bean was more sensitive to ozone when grown under a light intensity of 900 ft-c than when grown under 2200 ft-c, but the responses to PAN were reversed (Dugger et al., 1963b). Pinto bean and tobacco grown under an 8-hour photoperiod and 2000 ft-c, as opposed to 3000 ft-c, showed a similar response to ozone (Heck and Dunning, 1967). They found that sensitivity to ozone was reduced more by changing from an 8- to a 16-hour photoperiod than by increasing light intensity from 2000 to 3000 ft-C. Early work with sulfur dioxide (Setterstrom and Zimmerman, I939), and later studies with products of photochemical oxidants (Heck et al., 1965; Juhren et al., 1957) indicate a positive correlation between injury and increasing light intensity up to at least 3000 ft-c during exposure. It has been suggested that sensitivity might increase with increasing light intensity up to full sunlight with some pollutants o r for specific plants. Hull and Went ( 1952) reported that plants exposed in the dark were less sensitive to ozonated hexene than plants exposed in the light. Koritz and Went ( 1 953) found that tomato plants, exposed in the dark to low levels of ozonated hexene, showed no reduction in growth, but a definite growth reduction occurred when exposed in the light. According to Juhren et al. (1957), an exposure light intensity between 300 and 400 ft-c is a threshold level for the production of oxidant injury. This intensity of light was also about the threshold required for stomata1 opening. The literature suggests that light is essential during exposure of sensitive plants to pollutants for injury to occur. Nitrogen dioxide may be an exception, since two recent reports have indicated greater sensitivity during night or low light exposures than in daytime exposures (0.C. Taylor, 1968; van Haut and Stratmann, 1967). Under summertime stresses of low soil moisture and high light intensity, tobacco was a more sensitive monitoring plant under 50% shade than in full sunlight (Heck et al., 1969). German investigators have suggested that night exposures of sensitive plants to low levels of sulfur dioxide may predispose plants to chronic sulfur dioxide injury (van Haut, 1961; Zahn, 1963). When pollution is low, injury may increase with increasing light intensity to the maximum light available. Stomata1 opening seems to correlate with injury at lower light intensities, but light

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intensity has an effect on plant response over and above its effect on stomatal opening. 4 . Temperature

Hull and Went (1952) grew plants at constant temperatures of 30", 17", or 3 ° C for I or 8 days prior to exposure to ozonated gasoline at 26°C. Injury after either the I - or 8-day temperature pretreatment was directly related to increased temperature. The temperature effect was much greater when plants were grown for 8 days at the three temperatures than when grown only 1 day. Kendrick et al. (1953) reported that injury was greater to spinach, romaine lettuce, and endive grown for 7 days at 24°C than when grown at 13°C prior to exposure to ozonated hexene. Lettuce grown fewer than 4 days at 13°C acquired no tolerance to the oxidants. Middleton (1956) found the same pattern with lettuce grown at temperatures of 24"and 13°C for periods of 0-9 days. There was a progressive decrease in sensitivity to ozonated hexene as the plants were grown at 13°C for 0-9 days before exposure. The most extensive work on the effects of growth temperatures on the sensitivity of plants to oxidants was reported by Juhren et al. (1957). Five diurnal temperature cycles were used in their studies. Sensitivity of the plants varied with age and with the temperature conditions under which they were grown. Some plants were sensitive at a very young age, while others were not sensitive until the initiation of flowers. This study illustrates the interaction of plant age with temperature conditions during growth on the relative sensitivity of annual bluegrass to the oxidant pollutants. When plants were changed from warm to hot conditions, they lost sensitivity within 3 days. The reverse change increased sensitivity. Reversals in sensitivity, due to temperature, may correlate with changes in stomatal functioning. Macdowall ( 1 965) exposed tobacco to ozone after 3 days of preconditioning at 2 day and 3 night temperatures. Sensitivity was increased by low day and high night temperatures. Heck et al. ( 1965) reported an increased sensitivity of plants to ozone, at time of exposure, as the temperature in the greenhouse increased. In subsequent growth chamber studies, plants were exposed to 4 temperature conditions under uniform light intensity. An inverse relation between sensitivity to ozone and temperature was found for both Pinto bean and tobacco. These results were confirmed by Cantwell (1968), who used a sensitive tobacco variety and close control over humidity and light intensity. Menser ( 1 962) found that tobacco was more sensitive at 15°C and 95% humidity than at 32°C and 50% humidity. Hull and Went ( 1952) found a positive correlation between temperature

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and severity of injury after exposure when temperatures varied from 3" to 36°C. This corresponds to our observations on the importance of water stress after exposure for development of maximum injury to plants. 5 . Humidity

Humidity also exerts an effect on the sensitivity of plants to pollutants. Menser (1962) showed an increase in sensitivity of tobacco to ozone exposed at either 15" and 32"C, as the humidity was raised from 50 to 95%. He found that injury generally increased with increasing humidity. Hull and Went (1952) reported that injury increased as humidity at the time of exposure increased from 5 5 to 90%. They found no effect of postexposure humidity variations on injury development. Heggestad et al. (1964) suggested that the variations in humidity between the arid West and the humid East could explain the greater sensitivity noted in reported research on the East coast. A positive correlation of injury with humidity during growth could be interpreted as response of membranes. An effect at the time of exposure, however, could be better explained on the basis of stomatal function. Thomas and Hendricks ( I 956) reported at 90% loss of sensitivity when the humidity was varied from 100% to essentially 0 at time of exposure, with a direct relation between sensitivity and humidity. More recent work from several laboratories has substantiated the thesis that plants grown and exposed under high humidity conditions are more sensitive than those grown and exposed under low humidity conditions (Otto and Daines, 1969; Wilhour, 1970). Recent work in the laboratory of Heck and associates has shown an interaction between humidity and light during growth of Pinto bean. They found that growth humidities of 60% and 80% had no effect on sensitivity when light intensity was maintained at 4000 ft-c (46% and 44% injury, respectively), but produced a marked effect when plants were grown at 2000 ft-c (66% and 79% injury, respectively). According to Macdowall (1966), dew did not increase injury to plants from oxidant pollution. Hull and Went (1952) reported similar results. Costonis and Sinclair (1969), however, found injury to white pine consistently greater when moisture was actually on the needles. Leone and Brennan ( I 969) reported varying results with tobacco, cucumber, and begonia exposed to ozone, but their results generally suggest that at low humidities moisture on the leaves increased sensitivity unless the ozone concentration is too high. Their data suggest that stomatal opening is involved. Evidently free moisture may play a significant role under certain conditions.

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6. Carbon Dioxide The carbon dioxide concentration within the leaf may be a controlling factor in stomata1 action. Thus, the variation in carbon dioxide concentration could exert an effect on plant sensitivity to air pollutants. Heck and Dunning (1967) found that tobacco plants exposed to 500 ppm of added carbon dioxide, immediately before and during exposure to ozone, were less sensitive than were control plants. Exposure of Pinto bean in the same fashion had no significant effect on sensitivity. The high variability in carbon dioxide concentrations in both greenhouse and growth chamber areas suggests a need to further investigate the importance of this variable in altering plant response to pollutants. The effect of carbon dioxide concentrations prior to exposure has not been investigated. If results are substantiated, the added use of carbon dioxide in many greenhouse management practices could result in the protection of plants from oxidant injury.

7. Pollutant Interactions One of the obstacles to understanding the effects of pollutants on plants is the lack of information about the possible interactions (additive, antagonistic, or synergistic) due to mixtures of pollutants in the atmosphere. This possibility was first explored in the early 1950’s when sulfur dioxide was injected into an exposure chamber, together with the reaction products of ozone-gasoline mixtures (Haagen-Smit et al., 1952). They suggested some possible antagonistic responses. Heck (1964) obtained no interactions between the hydrocarbon gases tested, or between the hydrocarbon gases and products of irradiated mixtures of nitrogen dioxide and propylene. The first positive interaction was reported by Menser and Heggestad (1966), who worked with the ozone-sensitive Bet-W3 variety of tobacco. They found that a 4-hour exposure to 0.05 ppm of ozone and 0.25 ppm of sulfur dioxide caused severe injury, but the same levels of pollutants were not independently injurious to tobacco. These results have been substantiated in the laboratory of Heck and associates with other plant species. They found injury to Bet-W3 occurring with 0.03 ppm of ozone, plus 0.1 ppm of sulfur dioxide. Similarly, an interaction was found between nitrogen dioxide and sulfur dioxide, using Bel-W3 tobacco. Severe injury occurred during a 4-hour exposure to mixtures of 0.1 ppm of nitrogen dioxide and 0.1 ppm of sulfur dioxide. By contrast, the plants were only slightly injured by 0.75 ppm of sulfur dioxide, or 2 ppm of NO2 during 4-hour exposure periods.

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A n interaction was reported (Dunning et al., 1970) between nitrogen dioxide and sulfur dioxide on 6 crop plants. Injury was found in 4-hour exposures using mixtures of the gases in the concentration range of 5 to 25 pphm for each gas. Injury with the single gases did not occur below 50 pphm for sulfur dioxide or below 200 pphm for nitrogen dioxide. Injury developed as chlorotic or necrotic upper surface fleck or as pigmented lesions instead of the interveinal bifacial necrosis commonly found with the single gas exposures. Sensitivity of the 6 species followed the general order of soybean, radish, tobacco, Pinto bean, oat, and tomato. The work with white pine and its response to sulfur dioxide and ozone using mixtures of 5pphm of each gas is another example of pollutant interactions which can markedly influence our concepts of pollutant concentrations which cause plant injury (Dochinger et a/., 1970). These results also help explain some of the unsolved plant injury syndromes.

8. Meteorological

Considerable information on factors influencing pollutant injury has come from laboratory and greenhouse investigations. Before a pollutant complex can be completely understood, laboratory results must be interpreted in relation to field factors. Several studies report attempts to relate meteorological variables to plant injury. The most thorough studies of meteorological conditions and associated plant response have been reported in Canada, where correlation of plant injury with oxidant dose was attempted by using ambient oxidant levels for one summer (Macdowall et al., 1964; Mukammal, 1965). No correlation was found until an empirical relationship (the coefficient of evaporation), involving evapotranspiration, was developed. When dose was corrected for this relationship, dose and injury were related in a linear fashion. Although dose and injury are not linear over a wide range in concentration of ozone (Heck et al., 1966), the Canadian workers, using the above empirical relationship, were able to predict fleck attacks with fair success. The relative importance of such factors as wind speed and barometric pressure has seemed insignificant in relation to the primary factors already discussed. Some studies conducted in exposure chambers, however, indicate that air movement may have a significant effect on pollutant uptake. Under ambient conditions, it may be impossible to separate these factors from the other factors. 9. Diurnal Effects

The time of day during which exposure takes place is important when one is considering controlled exposures over short periods, such as relatively short fumigations to high (ambient) levels of pollutants. Plants are

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generally more sensitive in mid to late morning and early afternoon, Under some conditions, for example if moisture stress develops, there may be a loss of sensitivity at midday. This time-of-day effect on sensitivity to air pollutants is related to the total environmental interaction on the physiology of the plant.

C. EDAPHIC FACTORS Soil moisture is known to affect the sensitivity of plants to air pollutants. Some work on nutritional interactions has been reported, and preliminary observations can be made as to the effects of temperature, aeration, and salinity.

1 . Soil Moisture Numerous studies have shown that plants grown under drought conditions are less susceptible to air pollutants than when grown under moist conditions. Oertli (1958) grew plants in I , 2, 4,and 8 strength nutrient solutions corresponding to an osmotic stress of 0.75 to 6.0 atmospheres and in sand cultures under moisture stress of 0.3 and 0.8 atmospheres. He found increased resistance to oxidant injury with both increasing osmotic stress (salinity) and soil moisture stress. Hull and Went (1952) found plants less sensitive to ozonated hexene when water was withheld within 3-5 days before exposure. The plants were completely resistant when water was withheld long enough for them to be slightly wilted. Middleton (1956) confirmed these results, and suggested that some protection from oxidant injury might be obtained on irrigated lands by withholding water during periods of expected pollution. Seidman et al. ( I 965) found that petunia, Pinto bean, and tobacco were completely protected from irradiated auto exhaust when the plants were close to wilting. Koritz and Went (1 953) found no growth reduction if plants were under water stress when exposed to ozonated hexene. G. S. Taylor et al. ( 1960) have reported protection from ambient oxidant in field-grown tobacco during drought periods. They found that recently irrigated plants were more sensitive than unirrigated plants, even when adequate moisture was available. When tobacco plants were grown under dry conditions for 6 weeks before exposure to ozone, the plants developed drought characteristics and were less sensitive to ozone, even if well-watered several hours prior to exposure (Macdowall, 1965). T h e plants showed stomata1 opening only in the morning hours; however, the watered plants had well-opened stomata except for some midday closure. This study suggests that mois-

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ture stress can change the physiological state of the plants so their tolerance to ozone is increased.

2 . Nutrition Various studies involving nutrition and plant sensitivity to oxidanttype pollutants have yielded results that are not in agreement. Middleton ( 1 956) found spinach and lettuce more sensitive to ozonated hexene when grown in soil to which the equivalent of 45 Ib/A of nitrogen had been added. He also found increased sensitivity in barley and oats grown on an enriched nitrogen soil. Brewer et al. ( 196 I ) reported similar results with mangels and with spinach exposed to ozone. They also reported an interaction between potassium and phosphorus, which needs to be further explored. Some investigators have reported a decreasing sensitivity of plants at low nitrogen levels; increasing sensitivity with optimum nitrogen: and decreasing sensitivity with higher nitrogen levels (Leone et al., 1966: Menser and Hodges, 1967). Both groups attempted to correlate injury with leaf total nitrogen, but a critical review of their work indicates that nutrient levels of nitrogen give a better correlation with injury than leaf levels. In a conflicting report, Macdowall (1965) found a reduced sensitivity even at medium nutrient nitrogen levels. He did not report leaf levels of nitrogen. Lee (1966) correlated sensitivity to ozone with the amount of soluble nitrogen in the plant. There is, no doubt, a real effect of soil nitrogen level on the sensitivity of plants to pollutants. The effect is indirect, perhaps by altering cellular metabolism to increase or decrease sensitivity. There may be an interaction between nitrogen and other elements. but the nature of this interaction is unknown. 3. Other Soil Factors Research has not related pollution injury to soil temperature: however, a positive correlation does exist between soil temperature and both water uptake and transpiration. This suggests a possible correlation between soil temperature and plant sensitivity to pollutants. Stolzy et al. ( I96 I , 1964) subjected the roots of tomato plants to partial pressures of oxygen from 0 to 152 mm Hg for 40 hours before exposure to PAN and ozone. They found a reduced sensitivity at partial pressures below 10 mm. This reduction correlated well with reduced water uptake and plant vigor. At pressures above 10 mm, differences in injury were not significant. Plants grown in heavy clay soils are less sensitive to ozone than those grown in a light soil mix (Heck and Dunning, 1967). Although oxygen tensions were not determined, low oxygen tensions in the heavy soil may have been one of the reasons for reduced sensitivity.

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Any soil factor that adversely affects plant-water relationships also reduces water uptake, favors drought conditions within the plants, and may cause stomata1 closure. These conditions would increase resistance of plants to air pollutants.

D. OTHERFACTORS The interaction between pollutants and various biological agents has received little study. Field observations suggest that sulfur dioxide reduced the incidence of several pathogenic leaf and needle fungi, including species of Melampsora, Pucciniastrum, Coleosporium, Cronartium, and Diplocarpon (Linzon, 1958; Scheffer and Hedgcock, 1955; Saunders, 1966). The report by Yarwood and Middleton (1954) showed that areas of Pinto bean and sunflower leaves around rust pustules were less sensitive to ozonated hexene than healthy leaves. Recent work with a bacterial infection of kidney bean has shown a similar response (Kerr and Reinert, 1968), while the development of oat crown rust infection was reduced by exposure to ozone (Heagle, 1970. Manning et al. ( 1969,1970) reported that ozone injury prior to inoculation of plants with Bofrytis cinera increases infection to potato and geranium. Treshow et al. (1967) reported that fluoride stimulated tobacco mosaic virus induced lesions on bean. Studies of interactions with pollutants and various plant diseases have produced interesting results, indicating the value of more studies of this nature. In California, oxidants predispose ponderosa pine to secondary attack by bark beetles (Stark et af., 1968). High insect populations on some pollution-sensitive tree species in the East may be due to the reduced resistance of these species to insect attack because of the effects of pollutants. The interactions of pollutants and insects may produce early senescence and leaf fall as noted in specific species. Observations such as these need to be explored more fully in well-designed experiments. The increasing prevalence of the oxidant syndrome throughout agricultural areas, especially in the vicinities of large metropolitan centers, has stimulated interest in developing protectant sprays which will prevent or reduce the severity of injury to sensitive crops. Antioxidant sprays have been used with varying success, but no practical means of application have been found (Jones, 1963; Ordin et al., 1962; Seidman et al., 1965; G. S. Taylor and Rich, 1962; Walker, 1967; Silber, 1964). Several carbamate-containing and other fungicides also have reduced oxidant injury to bean and tobacco (Kendrick ef al., 1962; Walker, 1967; G . S. Taylor, 1970). By contrast, P. W. Miller and Taylor (1970) found several nematocides increased the sensitivity of tobacco to oxidants. Certain sprays could be recommended for use; however, there are four

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general weaknesses in any suggested spray program: the frequency of spraying needed for continued resistance; the cost; the possibility of undesirable residues; and the inability to predict high oxidant days accurately. No reliable chemical treatment to protect plants from oxidants has been developed. However, lime sprays have long been recommended during the formation of the peach fruit as a protectant against soft suture in peach fruit caused by fluoride. Heck and co-workers have noted a seasonal effect from exposure of plants to ozone which has been especially pronounced in Pinto bean. Injury in plants, whether grown and exposed in greenhouses or growth chambers, is low during the winter months, increases during early spring, and is fairly uniform from May until late October. This variation may be related to stornatal opening, since Seidman and Riggan (1968) have reported a similar yearly cycling of stornatal opening in Pinto bean. They suggest that in Pinto bean this is related to a yearly rhythm (clock) which is set within the embryo at the time of seed formation. The physiological age of leaf tissue (maturity) plays a role in the response to pollutants. Juhren et al. ( 1 957) found, with oxidant pollutants, that the most sensitive age in annual bluegrass varied with temperature conditions during growth. Middleton ( 1 956) found that Pinto bean primary leaves were initially insensitive to ozonated hexene and increased in sensitivity up to 14 days of age, where they remained uniformly sensitive for 21 days under the growth conditions used. Dugger et al. ( 1 963b) reported that the youngest leaves of Pinto bean were more sensitive to PAN, while the older leaves were more sensitive to ozone. As might be expected from field observations on fleck development, repeated fumigations of tobacco with ozone injured the lower, mature leaves first. Later fumigations increased the number of injured leaves higher on the plant (Heggestad et al., 1964). Ting and Dugger (1968) found cotton leaves to be most sensitive to ozone when they reached about two-thirds of their full expansion. In general, younger leaf tissues appear to be more sensitive to PAN and some of the ambient oxidant pollutants, while recently matured tissues seem to be most sensitive to ozone and most of the other pollutants. In mature plants, the oldest leaves are less sensitive, and young, newly expanding leaves are insensitive except to PAN and to extremely high doses of other pollutants. Hydrogen sulfide, however, is known to affect the youngest leaves and the growing point first, while the mature leaves are quite insensitive. The effect of environmental preconditioning on sensitivity patterns has not been determined. There is some evidence that a low-level night pretreatment of plants with sulfur dioxide will increase injury following an acute dose the fol-

PLANT RESPONSE TO AIR POLLUTANTS

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lowing day (Section IV, B, 3). By contrast, oxidant or ozone injury may be reduced by pretreatment with the pollutant (Engle and Gabelman, 1966; Koritz and Went, 1953). In the sensitive onion variety, this was linked to stornatal action which prevented further entrance of ozone. Macdowall (1965) found either an increase or decrease in sensitivity by a pretreatment, depending on the ozone concentration. A. S. Heagle (personnal communication) has found with tobacco in field studies that previous exposure to subthreshold levels of ambient oxidant increased the amount of injury following exposure to a higher level of oxidant. Heck and Dunning ( 1 967) found that plants were more sensitive when given a specific dose of ozone in 1 hour than when this same dose was divided into 2 half-hour exposures, with variable intervals between exposures. This reduction in injury could result from stomatal closure after the initial exposure; partial recovery from incipient injury or to the ability of the tissue to remove some of the ozone reaction products with partial recovery of the removal system before the second exposure. When tobacco plants were exposed to ozone over a period of 4-5 days by using two 0.5- to 4-hr exposures each day, the injury was cumulative and more severe on plants that received the shortest (0.5 or 1 hour) exposures (Heck and Dunning, 1967). There were indications that the early exposures tended to sensitize the tobacco to additional ozone exposures. Because of the variable results with studies of this kind, no conclusions are possible. Effects of long-term, low-level exposures also are not adequately understood: but reports suggest that several protective devices may be operative. Stomata1 closure has been definitely established as one device (Hill and Littlefield, 1969), but some data point to biochemical protection (Dugger and Ting, 1970), at least in certain plants.

E. TIME-CONCENTRATION-INJURY RELATIONS A knowledge of the interrelations of time and concentration as they affect injury to plants is essential for an understanding of pollutant effects. These relations have been inadequately studied. There are few data in the literature relative to the effect of time-concentration relationships on the production of chronic injury, or in the reduction of growth, yield, or quality of plant material. There is also a dearth of information concerning the relationship of time and concentration on acute injury from pollutants or mixtures of pollutants, except for ozone and sulfur dioxide. The acute effects of ozone and sulfur dioxide at various concentrations and times have received sufficient study to permit preliminary time-concentration curves to be constructed for several sensitivity groupings of plants. One of the first dose (time-concentration) relations for plants was

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reported by O’Gara (1922) for sulfur dioxide. He was concerned only with the acute type of injury which developed over a relatively short period of time. He related concentration (c) and time of exposure (t) as

The parameters a and b are dependent on the species and variety of plant and the degree of injury. Concentration was measured in parts per million (ppm) and time in hours. O’Gara’s equation can be rearranged to c = b/t

+a

The plot of c vs. l/r is a straight line. The parameter a is the intercept for l / t = 0 or when t is infinitely large. This intercept could be considered the threshold concentration for injury. The O’Gara equation is a mathematical form which fits experimental data obtained from exposures limited in time. Guderian et al. ( 1 960) do not believe that the O’Gara equation fits their observations and suggest an exponential relationship to best describe their data: t = K e - f l ( C - ”where ) K is the vegetation life time (hours), a is a biological complex factor, and r is the injury threshold. These parameters vary with species and degree of injury. In the middle time range, both equations give a reasonable fit to available data. The exponential form probably fits over a wider range of time. Both these equations relate a given time and concentration to a specific percentage injury and are capable of developing only a two-dimensional model; both require a threshold injury value before they can be solved. An expression of the degree of injury produced as time and concentration vary is needed in describing injury. Heck et al. (1966) presented this information graphically for Pinto bean and Bel-W3 tobacco exposed to ozone. Mathematical surfaces of this type can make apparent the frequently steep slope in the injury versus concentration, or injury versus time planes. The steepness of these slopes gives a relative measure of the degree of variability to be expected in data collected under greenhouse and field conditions. Other reports also stress the importance of both time and concentration (Menser and Hodges, 1968; Ting and Dugger, 1968). Heck and colleagues have recently developed a linear model from experimental exposures of a group of plants to sulfur dioxide, ozone, and nitrogen dioxide which treats injury as a dependent variable with both time and concentration as independent variables. A companion

PLANT RESPONSE TO AIR POLLUTANTS

I37

model has also been developed, with concentration as the dependent variable, and injury and time as the independent variables. These curves permit the development of either 2-dimensional or surface response curves and delete the necessity of developing a threshold concentration before the equations can be solved. A field investigator can use these equations to predict the amount of injury to be expected from a given pollutant concentration over a limited period, or to predict a pollutant concentration that could be in the atmosphere for a limited period that would produce zero or slight injury to a given variety or species of plant. The models show that a given dose does not give constant injury. The foregoing relationships provide an insight into what may happen under a given set of circumstances. These relationships are probably universal and could be derived for any toxicant producing a definite acute-type of tissue collapse. Relationships of this type permit the assumption that as long as a certain concentration is not exceeded for a given period of time, no acute injury will occur. They do not indicate the severity of injury at higher concentrations or for longer time periods. The value of extending any of these relationships beyond the available experimental data upon which they are based is questionable. None of the experimental data presented provide any more than suggestions of occurrences in the field. The data cover only single timeconcentration relationships under standard conditions. No consideration is given to fluctuations in concentration in a given interval or the effect of repeated fumigations over either several days or even several hours in one day. Further, most of the available data are from short-time exposures; that is, short in relation to the growing season. To extrapolate any of the presentations to long periods would give results of very questionable validity. Zahn (1963) has reported on some problems of this complex type. Certainly, in the case of sulfur dioxide, the problem of chronic injury begins to appear with time. A number of investigators have reported the time-concentration effects of ozone on various species of plants. Table I summarizes some of the threshold levels ( 5 % ) derived from time-concentration results with ozone, and Table I1 presents similar information for sulfur dioxide. These tables suggest the times and concentrations necessary to produce injury in sensitive, intermediate, and resistant plants at the threshold level of injury. OF ACTION OF F. MECHANISM

POLLUTANTS

The various factors affecting the response of vegetation to air pollutants must be mediated through stomata1 control, through other internal factors that affect cellular responses, or a combination of these. The importance

I38

H . E. HEGGESTAD A N D W. W. HECK

of stomatal control is recognized with ozone-resistant onion (Engle and Gabelman, 1966) and is a generally accepted requirement. TABLE 1 Projected Ozone Concentrations that Will Produce, for Short-Term Exposures, Threshold Injury to Vegetation Grown under Sensitive Conditions" Concentrations (pphm) producing injury in three susceptibility groups of plants Time (hr)

0.5 1.o 2.0

4.0 8.0

Sensitive

Intermediate

15-30 10-2s 7-20 5-15 3-10

25-60 20-40 15-30 10-25 8-20

Resistant 50 35 3 2s 3 20

3 3

3

IS

('The values in this table were developed from a subjective evaluation of injury reported in many papers where both time and concentration were considered. TABLE I I Projected Sulfur Dioxide Concentrations that Will Produce, for Short-Term Exposures, Threshold Injury to Vegetation Grown under Sensitive Conditions" ~

Concentration (ppni) producing in.ji1r-y in three susceptibility groups of plants Time (hr)

Sensitive

Intermediate

0.5

1 . 0 -5.0

I .o 2.0

4.0-I2

0.5 -4.0 0.25-3.0 0.1 -2.0 0.05- 1 .o

4.0 8.0

3 .o- I0 2 .o-7.5 I .o-s 0.s -2. s

Resistant 3

3 3 3 3

10 8 6 4 2

"The values in this table were developed from a subjective evaluation of injury reported in many papers where both time and concentration were considered.

Perhaps the best direct evidence for controlling mechanisms other than stomatal aperture is that involving the photochemical complex of air pollutants, since they affect different but specific tissue on the same plant. The reaction of each pollutant within the leaf tissue to produce injury is, no doubt, a biochemically mediated response. This is suggested by studies with irradiated auto exhaust (Hindawi er al., 1965). Three toxicants were identified in the mixture by their differential response to tobacco leaf tissue. Studies on the influence of light on the sensitivity

PLANT RESPONSE TO AIR POLLUTANTS

I39

to ozone and PAN (Dugger et al., 1963b) led to several studies on the influence of carbohydrate metabolism. This research and that on the influence of enzymes, cellular components, membrane permeability, and stomata were recently reviewed by Dugger and Ting ( 1 970). Considerable information is available on physiological and biochemical changes induced by ozone and PAN. These authors concluded, however, that the actual mechanism of oxidant damage to plant tissue remains unanswered. V. Discussion

To fully understand air pollution problems on vegetation, we must be aware of the many factors that determine plant response to air pollutants. Similar concentrations of pollutants in air may result in very different amounts of injury, depending on species grown, physiology of the plant, and stage of growth, among others. Injured, sensitive plants are usually the first warning of reduced air quality. The possibility of air pollution injury to vegetation from a point source, such as an industry, is much easier to understand than injury due to multiple sources of pollution. A significant part of this problem is that action of sunlight on combustion products, such as nitrogen dioxide and hydrocarbons, results in the formation of some very phytotoxic secondary pollutants, such as ozone and PAN. The motor vehicle is a major source of these combustion products. Ozone is now rated by many as the most important pollutant affecting vegetation. Because ozone is a normal component of the atmosphere, and there have been suggestions in the past that it is healthful, some people have difficulty thinking of ozone as an air pollutant. The situation is further confused because instrumentation is not generally available to specifically measure ozone; that is, with most instrumentation, the values tend to reflect the total oxidizing nature of air. These values are best referred to as total oxidants. However, when oxidants are high, as during air pollution episodes, 90% or more of the oxidant is ozone. We recognize that pollution sources change very little from day to day; however, only on certain days is the meteorology favorable for the pollutants to accumulate near t h e earth’s surface. Frequently, air pollution problems on vegetation are identified because of the culture of some varieties of plants which happen to be very sensitive to specific pollutants. We also know that air pollution losses would be much higher if plant breeders were not continuing to develop adapted, high-yielding varieties. Placing selection pressure on maximum yield and the avoidance of leaf injury has increased the tolerance of some varieties to air pollutants even without knowledge of phytotoxic pollutants in the

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area. Limited varietal testing in the presence of controlled levels of pollutants confirms the availability of much genetic material of potential value in breeding programs. The organized breeding efforts with cigarwrapper tobacco to avoid weather fleck (ozone injury) made it possible to continue successful culture of this crop. The development of agronomic and horticultural varieties with tolerance to air pollutants should be as feasible, as improving disease resistance in plants or increasing their tolerance to cold temperatures. Of course, efforts to control pollution at its source must be continued. Sharp increases in concentrations of pollutants will reduce the yields and quality of even the most tolerant varieties. Also, many of the pollutants that affect vegetation are injurious to the health of animals and people. Some species of plants, however, are extremely sensitive to pollutants. Except for such pollutants as carbon monoxide and some of the heavy metals, it is much easier to demonstrate an effect on plants than on animals and humans. Injuries from air pollutants may resemble injuries caused by insects, plant diseases, nutrient imbalance, and such stress factors as cold, heat, and deficient moisture. Field evaluation may require the specialized knowledge of scientists in several disciplines. When fluorides are suspected, analysis of leaf tissue is helpful, but for most pollutants, analytical techniques are not available to identify the pollutant or pollutants involved. Air sampling may yield significant information, but it must be done over a period of several weeks and with sufficient accuracy. In the case of fluorides, concentrations in air must be detected at levels less than a part per billion. Biological indicators are of some value, depending on the pollutant and indicator plants used. Some of the problems associated with identifying air pollution injury are discussed by Weinstein and McCune ( 1 970). The book that contains this chapter has five chapters by other authors, dealing with various air pollutants. A total of 120 colored plates were published as an aid to recognizing injury by different air pollutants on different species of plants (Jacobson and Hill, 1970). VI. Summary

The major pollutants have been identified, and the nature and extent of air pollution problems discussed. The symptoms of injury caused by these pollutants, especially on crop plants, have been described. Air pollution problems have increased because of multiple sources and mixtures of pollutants. There is increased concern about chronic injury and reduced growth attributed to air pollutants, such as photochemical oxidants and sulfur oxides. Response to pollutants may be altered by many factors, such as genetic, environmental, cultural conditions, time-con-

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centration relationships, and the presence of mixtures of pollutants. The identification and use of tolerant varieties, including resistant varieties developed by breeding, will help reduce losses and assure maximum agricultural production. REFERENCES Barrett, T . W., and Benedict, H. M. 1970.I n “Recognition of Air Pollution Injury to Vegetation: A Pictorial Atlas” (J. S. Jacobson and A. C. Hill, eds.), pp. C I-C 17.Air Pollut. Contr. Ass., Pittsburgh, Pennsylvania. Berry, C. R., and Hepting, G. H. 1964. Forest Sci. 10,2-13. Berry, C. R., and Ripperton, L. A. 1963.Phytopathology 53,552-557. Brandt, C. S.,and Heck, W. W. 1968. In “Air Pollution” (A. C. Stern, ed.), 2nd ed., Vol. I , pp. 401-433.Academic Press, New York. Brennan, E. G., and Halisky, P. M. 1970.Phytopathology 60,1544-1546. Brennan, E. G., Leone, 1. A., and Daines, R. H. 1964.Plant Dis. R e p . 48,923-924. Brennan, E. G., Leone, 1. A., and Halisky. P. M. 1969.Phytopathology 59, 1458-1459. Brewer, R. F., Guillemet, F. B., and Creveling, R. K. 1961.S o i l S c i . 92,298-301. Cameron, J. W.,Johnson, H., Jr., Taylor, 0. C., and Otto, H. W. 1970.HortScience 5, 2 17-2 19. Cantwell. A. M. 1968.Plunt Dis. R e p . 52,957-960. Costonis. A. C. 1970.Phytopathology 60,994-999. Costonis, A. C., and Sinclair, W. A. 1969.Phytoputhology 59,1566-1574. Council of Environmental Quality ( 1970).“Environmental Quality,” I st Annu. Rep. (transmitted to the Congress). Crocker. W. 1948.I n “Growth of Plants,” pp. 139- I7 I , Reinhold, New York. Davis, D. R., and Dean, C. E. 1966.Mon. Weuther R e v . 94, 179-182. Dochinger, L. S.,and Seliskar, C. E. 1970.Forest Sci. 16,46-55. Dochinger, L. S.,Bender, F. W., Fox, F. L., and Heck, W. W. 1970. Nature (London) 225,476. Dugger, W. M., Jr., and Ting, I. P. 1968.Phytopathology 58, 1102-1 107. Dugger. W.M..Jr.. and Ting, I. P. 1970. Annu. R e v . Plant Physiol. 21,215-234. Dugger, W. M.,Jr., Taylor, 0. C., Klein, W. H.. and Shropshire, W., Jr. 1963a. Nature (London) 198,75-76. Dugger, W. M., Jr., Taylor, 0. C., Thompson, C. R., and Cardiff, E. A. I963b.J. Air Pollut. Contr. A s s o c . 13,423-428. Dunning, J. A., Tingey. D. T., and Reinert, R. A. 1970.HortScience 5,333. Engle, R. L., and Gabelman, W. H. 1966.Proc. A m e r . Soc. Hort. Sci. 89,423-430. Feder, W. A. 1968.Science 160,1172. Feder, W.A., and Campbell, F. J. 1968.Phytoputhology 58, 1038-1039. Feder, W.A,, and Sullivan, F. 1969.Phytoputhology 59,399. Feder, W. A., Fox. F. L., Heck, W. W., and Campbell, F. J. 1969a. Plant D i s . R e p . 53, 506-5 10. Feder, W. A., Sullivan, F., and Perkins, I. 1969b.Phytopathology 59, 1026. Glater, R. A. 1970. Rep. No. 70-17.School of Eng. Appl. Sci., University of California, Los Angeles, California. Guderian, R., van Haut, H., and Stratmann, H. 1960. Z. Pjanzenkr. Pjanzenschutz 67, 257-264.

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Povilaitis. B. 1967. Can. J . Genet. Cytol. 9, 327-334. Reinert, R. A,, Tingey, D. T., and Carter, H. B. 1969. HortScience 4, 189. Reinert, R. A., Tingey, D. T., and Carter, H. B. 1970. HortScience 5, 334. Rich, S. 1964. Annu. Rev. Phytopathol. 2, 253-266. Richards, B. L., Middleton, J. T., and Hewitt, W. B. 1958. Agron. J . 50, 559-561. Saunders, P. J. W. 1966. Ann. Appl. Biol. 58, 103- 114. Scheffer, T. C., and Hedgcock, G. G. 1955. US.,Dep. Agr., Tech. Bull. 1117, 1-49. Sechler, D., Davis, D. R. 1964. Plant Dis. Rep. 48,9 19-922. Seidman, G., and Riggan, W. 9. 1968. Nature (London) 217,684-685. Siedman, G . , Hindawi, 1. J., and Heck, W. W. 1965. J . Air Pollut. Contr. Ass. 15,168-170. Seigworth, K. J. 1943. Amer. Forests 49, 521 and 558. Setterstrom, C., and Zimrnerman, P. W. 1939. Contrib. Boyce Thompson Inst. 10, 155- 18 I . Silber, G. 1964. Tobacco Sci. 8,93-95. Stark, R. W., Miller, P. R., Cobb, F. W., Jr., Wood, D. L., and Parameter, J. R., Jr. 1968. Hilgardia 39, 121-126. Stephens, E. R., Darley, E. F., Taylor, 0. C., and Scott, W. E. 196 I . Int. J . Air Waterfollut. 4,79- 100. Stern, A. C., ed. 1968. “Air Pollution and Its Effects,’’ 2nd ed., Vol. I I . Academic Press, New York. Stolzy, L. H., Taylor, 0.C., Letey, J., and Szuszkiewicz, T. E. I96 I . SoilSci. 91, I5 I - 155. Stolzy, L. H., Taylor, 0. C., Dugger, W. M., Jr., and Mersereau, J. D. 1964. Soil Sci. Sue. Amer., Proc. 28, 305-308. Taylor, G. S. 1970. Phytopathology 60,578. Taylor, G . S., and Rich, S. 1962. Science 135,928. Taylor, G . S., DeRoo. H G.. and Waggoner, P. E. 1960. Tobacco Sci. 4,62-68. Taylor, 0. C. 1968. J. Occup. Med. 10,485-499. Taylor, 0. C.,and Eaton, P. M. 1966. Planrfhysiol. 41, 132-135. Taylor, 0. C., and MacLean, D. C. 1970. I n “Recognition of Air Pollution Injury to Vegetation: A Pictorial Atlas” (J. S. Jacobson and A. C. Hill, eds.), pp. El-E14. Air Pollut. Contr. Ass., Pittsburgh, Pennsylvania. Taylor, 0. C., Stephens, E. R., Darley, E. F., and Cardiff, E. A. 1960. Proc. Amer. Soc. Hort. Sci. 75,435-444. Taylor, 0 .C., Duggar, W. M., Jr., Cardiff, E. A., and Darley, E. F. 1961, Nature (London) 192,8 14-8 16. Thomas, M. D. 1951. Annu. Rev. Plant Physiol. 2, 293-322. Thomas, M. D. 1961. I n “Air Pollution,” World Health Organ., Monogr. Ser. No. 46. pp. 233-278, Columbia Univ. Press, New York. Thomas, M. D., and Hendricks, R. H. 1956. In “Air Pollution Handbook” (P. L. Magill, F. R. Holden, and C. Ackley, eds.), McGraw-Hill, New York. Sect. 9, pp. 144. Thompson, C. R., and Taylor. 0. C. 1969. Environ. Sci. Technol. 3,934-940. Ting. I . P., and Duggar, W. M., Jr. 1968. J. Air Pollut. Contr. Ass. 18, 8 10-8 13. Tingey, D. T., Heck, W. W., and Reinert, R. A. 1969a. HortScience 4, 189. Tingey, D T., Reinert, R. A., and Carter, H B. 1969b. Agron. Abstr. 61, 34. Treshow, M., and Pack, M. R. 1970. I n “Recognition of Air Pollution Injury to Vegetation: A Pictorial Atlas” (J. S. Jacobson and A. C. Hill, eds.) pp. D 1-D17. Air Pollut. Contr. Ass., Pittsburgh, Pennsylvania. Treshow, M., Dean, G., and Harner, F. M. 1967. Phytopathology 57,756-758. van Haut, H. 1961. Staub 21,52-56.

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van Haut, H., and Stratmann, H. 1967. Schrifenr. Landesanst. Immissions- Bodennutzungsschurz Landes Nordrheim- Westfalen, Essen 7 , 50-70. van Haut, H . , and Stratmann, H. 1970. “Farbtafelatlas iiber Schwefel-dioxidwirkungen an Pflanzen.” Verlag W. Girardet, Essen, Germany. von Schroeder, J., and Reuss. C. 1883. “Die Beschadigung der Vegetation Durch Rauch und Die Oberharzer Hiittenrauchschaden.” Parey, Berlin. Walker, E. K. 1967. Can. J . Planf Sci. 47,99- 108. Wanta, R. C , and Heggestad, H. E. 1959. Science 130, 103-104. Wanta, R. C., Moreland, W. B., and Heggestad, H. E. 1961. Mon. Wearher Rev. 89,289296. Webster, C. C. 1967. Publication of the Agricultural Research Council, Ministry of Agriculture and Fisheries, Great Britain, pp. 1-53. Weinstein, L. H.. and McCune, D. C. 1970. In “Recognition of Air Pollution Injury to Vegetation: A Pictorial Atlas” (J. S. Jacobson and A. C. Hill. eds.) pp. G 1434. Air Pollut. Contr. Ass., Pittsburgh, Pennsylvania. Widtsoe, J. A. 1903. Utah, Agr. Exp. Sta., Bull. 88, 149-179. Wilhour, R . G . 1970. Phyropathology 60,579. Wood, F. A. 1968. Phytopathology 58, 1075- 1084. Yarwood, C. E., and Middleton, J. T. 1954. Plant Physiol. 29,393-395. Zahn, R. 1963. Staub 23,343-352. Zimrnerman, P. W., and Hitchcock, A. E. 1946. Amer. J . Bor. 33, Suppl., 233.

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BEHAVIOR OF PESTICIDES IN SOILS Charles S. Helling, Philip C. Kearney, and Martin Alexander Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland, a n d Department of Agronomy, Cornell University, Ithaca, N ew York

1. Introduction ................................................................... 11. Processes Affecting Pesticides in Soils ...................................................

A. Physicochemical ....................................................... B. Microbial Metabolism .......................................... 111. Effect of Pesticides on Soil Community ................................. 1V. Implications .................. ...................................... A. Persistence ........................................................................ B. Bioactivity and Uptake ...................................... V. Summary .............. ............................................ References ............

I.

I47 148 I48 181 208 216 216 219 227 229

Introduction

The behavior of pesticides in soils has been the subject of research long before pollution became a byword. Early workers had regard for side effects, such as phytotoxicity from arsenic accumulation, but most research was related to the efficacy of soil-incorporated pesticides. The important, first studies of soil metabolism of 2,4-D’ and its analogs, in the mid- 1940’s, demonstrated broader concern for the fate of pesticides, including their effect on the soil microbial population. In recognition that soil is the ultimate sink for most widely used pesticides, and given the impetus of recent public awareness of the quality of our environment, the past two decades have marked much progress in the understanding of the fate and behavior of pesticides in soils. A strong case for the continued use or precipitate abandonment of agricultural pesticides is inappropriate here. I t is reasonable, however, to note the vitally important role pesticides have assumed in increasing the quantity and quality of our foodstuffs, timber, and ornamental plants; in improving animal health; and in combating certain diseases transmitted to man.

’ Chemical designations of pesticides mentioned in the text appear in Table IV. I47

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CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

One must similarly evaluate the hazards of pesticides to man and other components of the ecosystem. Entry of pesticides into aquatic systems and their subsequent biomagnification into higher members of the food chain has been of special concern among conservationists. DDT, in particular, has been singled out; it is readily absorbed and accumulated by organisms and their predators, apparently because the insecticide is both lipophilic and inherently persistent. Similar trends may occur in the soil, sometimes with inadvertent harm to wildlife. Emphasis on the behavior of pesticides in soils is likely to increase in the future. Newer compounds may be tailor-made or specially formulated, not only for high biological activity and selectivity, but also to achieve desired characteristics of soil adsorption, movement, and persistence. This approach should lessen the required pesticide dosages. At the same time, a more detailed knowledge of the fate of pesticides is being required for their registration. This includes their metabolites, most of which (fortunately) appear to be innocuous and/or short-lived. Investigations of the physicochemical and biological properties of pesticide metabolites are, as yet, few. Recent attention has focused on the herbicide 2,4,5-T because of its reported teratogenic effects. An outgrowth of this has been examination of the behavior in soils of certain impurities in the formulated herbicide. Mercury pollution of waters in Japan, Sweden, Canada, and the United States has been of great concern recently. Although agricultural use is relatively small? a quantitative balance should be made of mercury originating in organomercury fungicides. Because of these concerns and other accusations brought against organic pesticides, there is a critical need to understand the reactions of these compounds in the soil environment. The present review attempts to summarize much of the significant literature which has contributed to our basic understanding of pesticides in soils. These are usually given as generalizations, with specific citations chiefly reserved for the recent advances amplifying this knowledge. The reader is also referred to a number of excellent reviews covering specific topics pertinent to our title subject: these are listed where appropriate in the following review. II.

Processes Affecting Pesticides in Soils

A. PHYSICOCHEMICAL Of the processes influencing the fate and behavior of pesticides in soil, adsorption is the most significant. The relative availability of a pesticide 2Agricultural consumption of mercury was 204,000 Ib, or 3.4%, of total 1969 mercury consumption in the United States (Anonymous, 1970).

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149

may influence physical distribution, biological activity, and even its susceptibility to microbial metabolism. References to the effect of adsorption thus appear in several sections of this review. 1 . Adsorption

Adsorption of pesticides is the subject of a recent thorough review (Bailey and White, 1970). Similarly, Greenland ( I 970) and Mortland ( 1970) reviewed clay-organic complexes, including some pesticides. The present review will therefore be a synopsis of the soil and pesticide characteristics influencing adsorption with emphasis on recent literature. a. Methodology. Adsorption in soils is usually described empirically by either the Langmuir equation ( I ) or the Freundlich equation (2),

_ x --KibC m

l+bC

where xlm is the amount ( x ) adsorbed per unit amount of adsorbent ( m ) ; K I (adsorption maximum), b (related to adsorption energy), K , and n are constants; and C is the equilibrium solution concentration. Langmuir constants are evaluated, when appropriate, by a double reciprocal plot of mlx vs. C-I. If linear, the intercept is K1-' and the slope (bK1)-l. The Freundlich isotherm, the most commonly used model, is solved graphically by plotting log xlm vs. log C , yielding a straight line of slope Iln. Adsorption of ureas, triazines (Bailey et af., 1968; Hance, 1969a), lindane (Lotse et af., 1968; Mills and Biggar, 1969b), and disulfoton (GrahamBryce, 1967) corresponded to Eq. (2); amitrole adsorption, to Eq. (1) (Nearpass, 1969, 1970a,b). The technique of pesticide adsorption was examined from the standpoint of precision. Green and Yamane ( 1 970) suggested increasing the soil :solution ratio if statistical analysis indicated that AC, the concentration change, was too small. However, Grover and Hance (1970) found adsorption to vary widely as the soil:solution ratio was altered. The Freundlich K values for linuron decreased from 12.3 to 2.7 as ratios increased from I : 10 to 4: 1 . Although the latter more nearly represents field conditions, most pesticide adsorption studies are conducted as slurries, i.e., an adsorbent: solution ratio < 1 : 1. b. Soil Characteristics. The quantity and type of clay and organic matter, their surface area, the soil structure, water content and quality,

I50

CHARLES s. HELLING, P H I L I Pc . K E A R N E Y , A N D MARTIN ALEXANDER

temperature, and pH are all factors that may affect the distribution of pesticides between soil particles and surrounding water or air. Bailey and White ( 1 970) emphasized the surface charge characteristics of the adsorbent. Weed and Weber ( 1 968) attributed preferential adsorption of diquat over paraquat on vermiculite (high charge density) to the estimated charge center separation on the organic cations-3.5 for diquat and 7.0 A for paraquat. Steric factors were less important on montmorillonite (low charge density), where paraquat was preferentially adsorbed. Similarly, on montmorillonite the pyridinium ion was adsorbed in a planar configuration, whereas on vermiculite the pyridinium ring was forced into a perpendicular orientation (Serratosa, 1966). The competitive adsorption of diquat and paraquat has been used to estimate surface charge density of clays (Philen e l al., 1970). The total charge and surface area of soil components are also highly significant in terms of pesticide adsorption. Both generally decrease in the series organic matter > vermiculite > montmorillonite > illite > chlorite > kaolinite (Bailey and White, 1964). Charge in the preceding series was considered as cation-exchange capacity. Allophanic clays may have high surface area (Aomine and Otsuka, 1968), and these and other oxides and hydroxides may develop positive charges at neutral to low pH values. The influence of noncrystalline hydrous oxide, which may occur as clay coatings, has received surprisingly little attention in pesticide adsorption studies. The existence of an anion exchange capacity in soils should have most effect on organic acids. Thus, increased adsorption of picloram and 2,4,5-T was associated with Fe content in soils (Hamaker ef al., 1966). In like manner, amiben, dicamba, and 2,4-D were adsorbed by kaolinite but not by montmorillonite, illite, or vermiculite (Bailey el al., 1968; Burnside and Lavy, 1966). On the other hand, a comparable weight of montmorillonite adsorbed ca. 20 times more paraquat from solution than did kaolinite (Calderbank and Tomlinson, 1968). No adsorption of atrazine or simazine was detected with kaolinite, but increasing adsorption occurred on beidellite, illite, and montmorillonite (Talbert and Fletchall, 1965). Much recent research on adsorption of pesticides to clays has utilized diquat or paraquat. Since these herbicides are not soil-incorporated, their use perhaps reflects the ease of using cations in exchange studies. Knight and Tomlinson ( 1 967) and Tucker el al. ( 1967) distinguished between the relatively unavailable bipyridylium herbicide (“Strong Adsorption Capacity” or “tightly bound”) and that more loosely held. The former required reflux with 18 N H2S04for complete removal, whereas the latter was desorbed by saturated N H4CI solution. The unavailable herbicide seems associated with clay, as peroxidized soil had only a slightly re-

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151

duced strong adsorption capacity (Calderbank and Tomlinson, 1968). The herbicides are more weakly adsorbed on organic matter (Radaelli and Fusi, 1968; Tucker et al., 1967). Diquat and paraquat have been adsorbed to 100% of the cation-exchange capacity of kaolinite and montmorillonite clays, while adsorption to vermiculites generally ranged from 30% to 90% (Dixon et al., 1970; Weber et al., 1965; Weed and Weber, 1969). Adsorption was more complete on Na+-saturated vermiculite than with Ca"- or Mg'f-saturated clay. Low levels of adsorbed paraquat made montmorillonite nonexpanding; despite this, it was self-exchangeable with 14C-labeledparaquat in solution but apparently not with inorganic salts (Knight and Denny, 1970). Others, however, have shown BaZf,Ca", or Al"+ capable of removing 5- 10% adsorbed herbicide on montmorillonite, ca. 50% on vermiculite, and 80% on kaolinite (Weber and Weed, 1968; Weed and Weber, 1969) Dixon et al. (1970), using K+, desorbed 2344% diquat from several montmorillonites, 59% in a nontronite, and up to 98% in vermiculites. Increased desorption among vermiculites was correlated with increased cation-exchange capacity, probably because high charge densities became unfavorable for diquat retention. Mechanisms of pesticide-clay bonding have been investigated mainly by interpretation of infrared spectra, sometimes coupled with X-ray diffraction analysis. An exception was the extensive study of Bailey et af. ( 1968), using only adsorption isotherms on montmorillonite. Water on air-dry montmorillonite is more acidic than normal water and can donate a proton to bases such as amines and amides (common functional groups in many pesticides), and to ionized acids such as 2,4-D and amiben. This may occur several pH units above the pK, of the molecule (Harter and Ahlrichs, 1969: Mortland, 1968: Russell et af., 1968b). Amitrole is protonated on the montmorillonite surface and is apparently held by cation exchange and proton association (Nearpass, 1970a; Russell et al., 1968a). The herbicide is completely exchangeable with other cations. Amitrole forms coordination complexes with Cu"- or Ni'+-montmorillonite (Russell er al., I968a). Carbaryl is also adsorbed by protonation and coordination mechanisms, depending on the exchangeable cation (Payne and Bailey, 1969). Other pesticides, not protonated at normal soil pH's, may adsorb via hydrogen bonding or direct ion-dipole interactions. Carbonyl groups as in EPTC (Mortland and Meggitt, 1966), malathion (B. T. Bowman et a/., 1970; MacNamara, 1968), linuron (MacNamara, I968), ureas (Farmer and Ahlrichs, 1969), and 2,4-D ( K u o et al., 1969) participate in such bonding. The interactions occur between the organic molecule and hydrated water; bonding strength is likely to increase with increased exchangeable cation valence and decreased hydration status. Extensive

I52

CHARLES s. H E L L I N G , P H I L I Pc . KEARNEY, A N D MARTIN ALEXANDER

reviews of the mechanisms of adsorption have been published by Bailey and White ( I970), Mortland ( I970), and Greenland ( 1965). Adsorption on various clays is most often compared on a weight basis, i.e., x / m (Eqs. 1 and 2). Thus Ca-kaolinite and Ca-montmorillonite adsorbed 2.70 and 10.3 mg/g, respectively, of y B H C (Mills and Biggar, I969a). On a surface area basis, however, kaolinite adsorbed far more: 0.18 vs. 0.0127 mg/m2. y B H C was therefore thought to compete more effectively with water on kaolinite’s hydroxy surfaces than on the oxygen surfaces of montmorillonite. Although the mineral fraction is most influential in adsorption of organic cations such as diquat, paraquat, or phenylmercuric acetate (Aomine and Inoue, 1967), soil organic matter is undoubtedly of much more general importance in governing pesticide adsorption in soils. Goring (1967) cited 41 references attesting to the significance of organic matter, and many recent papers could be added. For example, 90% of the variability of lindane (Adams and Li, 1971) or simazine (J. D. H. Williams, 1968b) adsorption was accounted for by soil organic matter content. A humic acid adsorbed ca. 70 times more linuron and malathion than did K+montmorillionite in comparable experimental conditions; the difference was much wider with other clays and saturating cations (MacNamara and Toth, 1970). Qualitative differences among soil clays with respect to pesticide adsorption are well documented. Organic matter, in contrast, is usually considered invarient in its properties. Triazine adsorption onto 17 organic (> 6% C) soils seemed to corroborate this, with differences arising chiefly from the extent of decomposition of added plant residues (A. Walker and Crawford, 1968). Fibrous peat and muck soils differed in their adsorptivity of several herbicides (Doherty and Warren, 1969), again reflecting different stages of decomposition. Lambert (1 968) has of soil organic matter, variable distinguished the “active fraction” among soils, as being an improved predictor of adsorption of neutral pesticides. Adsorption is seen solely as the distribution of pesticides between water and soil organic matter; adsorption on soils is thus sometimes expressed as the quantity sorbed per unit weight of organic matter (Briggs, 1969; Furmidge and Osgerby, 1967; Hamaker et al., 1966). Two approaches in studying pesticide-organic matter interactions have been isolation of natural clay-organ0 complexes and addition of model organic adsorbents to clays. I t is clear in both instances that the association of clay and organic matter reduces the adsorption capacity of the individual components (Hance, I969a; Radke, 1967). Alkyl groups have been suggested by Hance as being adsorptive components of soil organic matter. Fats, waxes, cellulose, nucleic acid, etc., contributed little to atrazine adsorption, but humic acid, lignin, and quinalizarin were all

(a)

BEHAVIOR OF PESTICIDES IN SOILS

I53

highly sorptive (Dunigan, 1967). Adsorption to soil organic matter may be diffusion-controlled, as is characteristic of porous adsorbents (Dunigan, 1967; Calderbank and Tomlinson, 1968; Leenheer and Ahlrichs, 1970; Schwartz, 1967). Desorption from organic matter is frequently slower than to clays and in some cases, sorption is at least partially irreversible. Chemical reactions could cause this (see Section 11, A, 4), although very strong adsorption onto the macromolecular organic matter is most likely. The importance of soil pH as a factor affecting pesticide adsorption depends largely on the pesticide itself. That is, acids such as 2,4-D and picloram may be positively adsorbed on montmorillonite below pH 3-4 but negatively adsorbed (as anions) at pH 6-7. Weak bases are protonated at low pH; e.g., triazine adsorption onto montmorillonite was pHdependent while phenylurea adsorption was not, in the range pH 4-8 (Hance, I969a). Phenylmercuric acetate adsorption onto montrnorillonite, allophane, and kaolinite was remarkably pH-dependent (Inoue and Aomine, 1969). Maximum adsorption occurred at pH 6, since in acid solution hydronium ions competed with the pesticide cation, whereas at higher pH's the ionization constant of phenylmercuric hydroxide ( I .3 x lo-'") was very much less than that of phenylmercuric acetate (1.5 X lo-"). A related aspect to soil pH is the exchangeable cation balance. Nearpass (1967) found a decline of atrazine and simazine adsorption to soil as base saturation increased, although there was no apparent difference among cations (Na, K, Mg, Ca). Hance ( I969a), however, found that triazine adsorption to montrnorillonite at low pH occurred more readily in the order Na > Ca > Mg, which he attributed to ease of cation displace men t . The effect of electrolytes in the adsorption solution is unclear. It appears that at normal pH's, dilute salts slightly increase adsorption while concentrated solutions sharply increase adsorption. When the adsorbed species is an organic cation, competition with the inorganic ion is observed (Frissel, I96 1 ; Fusi and Corsi, 1969; Gilmour and Coleman, 197 1 ; Hance, I969a; Malquori et al., 1967; Nearpass, 1970a,b). Increased temperature, in general, leads to decreased adsorption as physical adsorption is characteristically an exothermic process. Ionexchange mechanisms are temperature independent, as with diquat adsorption (C. I . Harris and Warren, 1964). Mills and Biggar (1969b) found decreased adsorption of lindane, or y-BHC, on various adsorbents as a function of temperature (Fig. 1). Temperature changes affect solute solubility as well as the energy relations of the adsorption reaction. By plotting x / m (Eqs. I and 2) versus reduced concentration, C / C , (where C is the solute concentration and C , is the solute solubility at a specified

I54

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

temperature); Mills and Biggar demonstrated an increase in lindane adsorption at higher temperatures. The adsorption process, indicated in Fig. 1 as being exothermic, is at least partially so because of a solubility-

50.0

Legend - Ca-Staten peaty muck Ca-Venodo clay

10.0

-3.

Q

5.0

0

F

\

I .o 0.5

0.I 0.001

I

0.005 0.01

0.05

0.1

0.5

1.0

5.0 10.0

C (,ug/ml)

FIG. 1. Adsorption of lindane from water onto various adsorbents at four temperatures (platted using the Freundlich equation). From Mills and Biggar (1969b) by permission of Soil Science Society of America Proceedings.

temperature interaction. The importance of organic matter is clearly seen when comparing a muck soil, a montmorillonitic clay soil, and montmorillonite (Fig. 1). At least one family of pesticides, the thiocarbamates, show decreased solubility with increased temperature (Freed et a f . , 1967), perhaps explaining their unusual adsorption behavior (Freed, 1966). c. Pesticide Characteristics. Examination of a pesticide’s structure and some physicochemical properties often permits estimation of its adsorption behavior. As adapted from Bailey and White (1970), those include: (i) overall chemical character and configuration; (ii) acidity or basicity (denoted by pK, or pK,,); (iii) solubility in water; (iv) electronic effects (charge distribution, polarizability); and (v) molecular size. The classification is somewhat arbitrary and interrelated, but it should help isolate the important pesticide characteristics affecting adsorption. One

BEHAVIOR OF PESTICIDES IN SOILS

I55

might add properties such as vapor pressure and thermodynamic constants as well. The chemical character is largely determined by the number, type, and relative position of functional groups. Adsorption is characteristically increased with functional groups such as RaN+-, -CONHz, - OH, -NHCOR, -NHz, -OCOR, and -NHR. Amino groups are especially important as they may protonate, depending on their pKb, and thus adsorb as cations. Both amino and carbonyl groups may participate in hydrogen bonding, an important mechanism of pesticide adsorption. Results from 52 related N-phenylcarbamates, acetanilides, and anilines suggested that hydrogen bonding between the imino hydrogen and the absorbent’s carbonyl oxygen (using nylon or cellulose triacetate) was the preferred adsorption mechanism (Ward and Upchurch, 1965). Introduction of double bonds increases adsorption affinity, especially if conjugated. The position of substituents may permit coordination with transition metal ions, either stabilizing adsorption or promoting decomposition, as with amitrole (Russell el al., 1968a) or diazinon (Mortland and Raman, 1967). Several workers have attempted to correlate molecular structure and adsorption to soils. Lambert ( 1967) found that the parachor, an approximation of molar volume, of various phenylsulfones and phenylureas correlated very well with K,., a distribution coefficient between soil and water. He also criticized the use of the Freundlich K unless I/n = I (Eq. 2). Lambert’s treatment assumed a nonionized molecule with relatively little hydrogen bonding. Hance ( I 969b) incorporated both parachor and a term to correct for hydrogen bonding. His empirically derived equation for 29 aromatic herbicides on two soils was: log K

= 0.0067

( P - 44N) - 0.65

(3)

where K is the Freundlich constant, P is parachor. and N is the number of proton or electron donating sites on the pesticide which could participate in hydrogen bonding. Functional group contributions to P were published by Quayle (1953). Diuron was assigned a value of N = 3 because it contains two amino groups (secondary and tertiary) and one carbonyl group. Equation (3) probably is not valid for soils and pesticides in which adsorption to clay is the dominant process. Briggs (1969) found that both Lambert’s ( I 967) parachor and Hance’s ( I969b) “parachor-45N” equations were unsatisfactory predictors of phenylurea adsorption, accounting for only 7.5% and 24.6% of variability in sorption. These equations were better predictors of alkyl-N-phenylcarbamate behavior. Briggs obtained much better correlation (75.5%)

I56

CHARLES s. H E L L I N G , PHILIP c. KEARNEY, A N D MARTIN ALEXANDER

of adsorption with chemical structure when he described the molecule in terms of Hammett (a)and Hansch (T) constants, both free energy related. In contrast to parachor, they distinguish among positional isomers on the benzene ring. For nonionic compounds without long alkyl chain, ring deactivation was suggested as the factor controlling adsorption. The dissociation constant of a compound indicates whether it can be protonated in aqueous solution. Within the normal pH range of soil this applies principally to loss of H + by acids and gain of H+ by nitrogen atoms. Frissel ( I 96 1) found negative adsorption of acids such as 2,4-D and 2,4,5-T at pH values above their pK,. Even phenols (dinoseb and DNOC) were negatively adsorbed at pH > 7. Protonation and adsorption of s-triazines to soil and its components was directly related to triazine basicity (Brown and White, 1969; Weber, 1966, 1970; Weber et al., 1969b). Weber er al. include an extensive review of s-triazine adsorption in their paper. With respect to substituents on the number 2 carbon, the decreasing order of basicity is hydroxy > methoxy > methylthio > chloro. Adsorption also increases with increasing size of the alkylamine group. Maximum adsorption of individual triazines seems to occur near their pK,. Thus triazines are more strongly absorbed at lower soil pH. At pH 2 pK, 2, adsorption of basic compounds is assumed due to van der Waals forces. Weber er al. found that the order of adsorption onto soil organic matter was tetraetatone = prometryne = hydroxypropazine > trietatone > prometone > simetone > propazine. The order of adsorption by montmorillonite depended on the exchangeable cation (Hance, 1969a). Water solubility is sometimes considered an approximate indicator of adsorption, i.e., lower solubility is related to greater adsorption. Bailey et al. (1968) concluded instead that, within a chemically homologous series, the extent of adsorption was directly related to or governed by water solubility. Their adsorbate was rather specific, however: Namontmorillonite for triazines and H-montmorillonite for phenylureas. It is far more common to find the reverse trend within a limited number of comparisons (e.g., diuron is more strongly adsorbed and less soluble than monuron), or to find no definite relationship between solubility and soil adsorption of many compounds. Water solubility did account for 60% of the total variation in adsorption of 52 carbamates, acetanilides, and anilines to model adsorbates (an inverse relation) (Ward and Upchurch, 1965). Another consideration with respect to solubility is that pH may affect it: with decreasing pH, s-triazines are more soluble (Ward and Weber, 1968) whereas ionized carboxylic acids revert to the lesssoluble free acid. Electronic effects on pesticide adsorption include charge distribution

+

BEHAVIOR OF PESTICIDES IN SOILS

157

in ionic compounds, polarity, and polarizability. Previously we cited (Section 11, A, 1, b) the more compact loci of charges on diquat as explaining its preferential adsorption over paraquat on vermiculite, a highcharge clay (Weed and Weber, 1968). One measure of polarity is the existence of a dipole moment. In y-BHC, three chlorine atoms are in the axial configuration and three are equatorial; its dipole moment is 2.84 debyes. Another isomer of the hexachlorocyclohexane, P-BHC, has all equatorial chlorine atoms; it is thus centrosymmetric and has no dipole moment. This difference in polarity was thought by Mills and Biggar ( 1 969b) to explain greater adsorption of y-BHC on silica gel, since a dipole-dipole interaction was possible. However on muck and clay soils and on montmorillonite P-BHC is more adsorbed, in part because its higher solution fugacity provides a greater “escape tendency” for PBHC. There is a trend for nonpolar molecules to be adsorbed more strongly by nonpolar adsorbents. Thus pesticides such as DDT are associated more closely with organic matter than with crystalline clays, which possess high charge fields and to which water molecules are effective competitors of adsorption sites. Increasing molecular size leads to greater adsorption, when comparing homologous nonionic adsorbates on nonionic adsorbents (Traub’s rule). In confirmation, increased N-aliphatic chain length or additional aryl substitution in urea herbicides led to greater soil adsorption (Hance, 1965). As molecular size increases, additional water molecules are displaced from the adsorbent surface, resulting in a favorable entropy gain. Besides this effect, the larger molecule has more points of contact for van der Waals or hydrogen bonding. In summary, although much is understood about adsorption mechanisms, especially at layer silicate surfaces, prediction of pesticide adsorption is largely empirical. For most pesticides, soil organic matter content remains the best predictor of adsorption, with pH and clay content sometimes relevant.

2 . Movement The physical transport of pesticides occurs within and through the soil, away from the soil surface, and along the soil surface. The processes are leaching, volatilization, and runoff. Pesticide movement in soils has recently been reviewed (Helling, 1970), so the following discussion will deal primarily with current research. a . Leaching. Movement of solutes in the water phase consists of two components - molecular diffusion and mass transfer. Hartley’s ( 1960) calculations indicate diffusion is probably significant for only a few centimeters distance. This is governed by factors such as the inherent diffusion

I58

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

coefficient of the molecule, soil structure characteristics, soil water content, and adsorptivity of the pesticide to soil. Diffusion occurs in both soil water and air and the relative importance of each depends in part on the solubility and vapor pressure of a pesticide. Goring (1967) suggested that chemicals with water:air ratios (i.e., the weights of chemical in equal volumes of water and air) under I x lo4 will diffuse primarily through air; those over 3 x lo4,primarily through water. By this measure, chloroneb, DDT, EPTC, lindane, CDEC, trifluralin, and the common fumigants should diffuse mainly in soil air; s-triazines, monuron, diuron, and phenylmercuric acetate, in soil water; and CDAA, diazinon, and parathion, intermediate between air and water. Apart from fumigants, relatively few studies of pesticide movement have dealt directly with diffusion. In soils, the apparent diffusion coefficient of nonvolatile compounds increases rapidly with increased moisture since the water path becomes less tortuous. For example, the diffusion coefficients (D) of three s-triazines, also averaged across eight soils, were 0.26 X lopx and 1.83 X lop8 cm2/sec at 0.5 and 1.0 field capacity, respectively (Lavy, 1970). For the insecticide dimethoate, D was 3 I3 1 X 1 O-x cm2/secat 10% volumetric moisture content and I4 I x at 43% (Graham-Bryce, 1969). In contrast, diffusion of the more cmz/sec at 41 % HzO) strongly adsorbed disulfoton was less (2.83 x and did not change greatly as the soil dried, indicating that vapor phase diffusion was an important path. In either case, transport in soils is very slow. In the wettest soil, the root mean square displacement [(2Dt)”’] of the diffusing molecules was up to 2.5 and 0.3 cm per month for dimethoate and disulfoton. That is, 3 1.73% of the molecules will have moved farther than these values in time t. Graham-Bryce ( I 969) derived an equation showing how soil factors affect pesticide diffusion:

where DI, is the diffusion coefficient in free solution (usually 3-6 x lop6 cm2/sec in HzO); V,, is the fraction of soil occupied by the liquid phase; f i . is the tortuosity factor for a soil; b is the slope of the adsorption isotherm, if linear; and p is the bulk density. Thus, increased adsorption should reduce diffusion. This inverse relationship was observed with propazine and prometryne by A. Walker and Crawford ( 1970), who also used Eq. (4). Factors normally correlated with increased adsorption, e.g., organic matter, have been correlated with increased diffusion of triazines (Lavy, 1970), but this presumably reflects a significant effect on VIAand

BEHAVIOR OF PESTICIDES I N SOILS

I59

h,.Reducing soil pH increases triazine adsorption (Section 11, A, I , b) and decreases its diffusion (Lavy, 1970). Lavy also found the diffusivity to be atrazine > simazine > propazine, and Walker and Crawford reported propazine > prometryne. This is the same order as their overall relative mobility in soils (Helling and Turner, 1968). Diffusion coefficients ranged from I5 X 1 O-x cm2/sec for propazine in a sandy soil to 0.3 1 x cm2/sec for prometryne in organic soil (A. Walker and Crawford, 1970). In the first example, diffusion beyond I cm of 10% of an applied dose would require about 2 weeks. Other recent experiments of liquid phase diffusion have dealt with 2,4-D (Lindstrom et al., 1968), D D T and D D E (Lopez Gonzalez and Valenzuela Calahorro, 1968a,b), and various herbicides (H. D. Scott and Phillips, 1970). Leaching of pesticides is usually synonomous with mass transfer, although diffusion occurs simultaneously. If soil is considered as a chromatographic column, pesticide applied near the surface may move downward as a band. This band becomes diffuse due to diffusion and hydrodynamic dispersion processes, the latter related to nonuniform pore size distribution in the soil. Adsorption to soil components controls the distance of leaching and the maximum pesticide concentration. Increasing adsorption imparts greater skewing or “tailing” to the concentration profile. Slow rates of desorption also cause tailing if the percolation rate is too great. Helling ( 1970) summarized the techniques used in pesticide mobility evaluation. These include field and laboratory methods. In the former category are residue analysis with depth and lysimeter experiments. Among laboratory methods are soil columns and soil thin-layer chromatography (soil TLC). Soil columns have been most commonly used; soil TLC is a recent innovation (Helling and Turner, 1968). Miscible displacement experiments, in which one solution replaces another in a soil column while leaching at a known rate, are especially useful in evaluating the influence of flow rate. The technique has been used with atrazine (Elrick ef al., 1966; Green et al., 1968; Snelling et al., 1969), lindane (Kay and Elrick, 1967), picloram (Chang et al., 1970), fluometuron, and diuron (Davidson and Santelmann, 1968; Davidson et al., 1968). Green e l af.found flow rate unimportant in saturated columns while slightly increasing atrazine mobility in unsaturated soil. Nonequilibrium conditions causing increased movement apparently prevailed at higher (2-2.4 cm/hr) elution rates with lindane and picloram. Restriction of atrazine movement was correlated with soil organic matter, surface area, and cation-exchange capacity (Snelling et al., 1969). These three soil parameters are normally correlated with one another, however, and organic matter may actually be the only significant factor.

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CHARLES S. HELLING, PHILIP C . KEARNEY, A N D MARTIN ALEXANDER

Soil TLC is less convenient than miscible displacement for studying flow rate effects, but it is highly suited for screening and classifying pesticides on the basis of their mobility (Helling, 1971b; Helling and Turner, 1968; Rhodes et af., 1970) and for evaluating soil parameters influencing movement (Helling, 197 Ic). The method is based on the leaching of pesticides applied to thin (usually 500-2000 p) soil layers on glass plates. When radioactive compounds are used, movement is easily assessed by autoradiography. Recent development of bioassays (Chapman et af., 1970; Helling and Kaufrnan, 1970) has extended its scope. Helling ( 1 97 I a) described physical details of the technique per se. Mathematical prediction of pesticide movement is based on chromatographic theory. Usually, adsorption equilibria are treated as instantaneous reactions. The model of Oddson et al. ( 1970) was more realistic, containing a kinetics term. Some recent equations have included diffusion and pesticide degradation terms (Davidson et al., 1968; King and McCarty, 1968; Lindstrom et af., 1967). Among the obstacles to prediction of pesticide movement by mathematical models is hysteresis of the adsorption. It is not generally accounted for, and its effect is that more pesticide remains near the soil surface than anticipated. D. T. Smith and Meggitt (1970a) did assume little or no desorption of pyrazon, as seen in Eq. (5):

where L is the maximum depth of movement, Xis the amount of pesticide applied to soil surface (A), xlm is the amount adsorbed (see Eqs. 1 and 2), and p is the soil bulk density. Their simple expression gave approximate agreement with field results. McCarty and King ( 1966) clearly demonstrated the influence of degradation on pesticide movement (Fig. 2 ) . Total radioactivity (T-3) was recovered only slightly faster than parathion-32P (P-3) in autoclaved soil, indicating that very little chemical degradation had occurred. These curves are representative of parathion movement without the influence of degradation. In natural soil (T-2, P-2) the amount of parathion leaching through the soil column diminishes. Microbial degradation was confirmed when using enriched soil, i.e., soil which had developed an adaptive microbial population by repeated prior treatment with parathion. Almost no parathion emerged from this soil (P-1), but recovery of 32P-labeled metabolite(s) was complete (T-1). Talbert et af. (1 970) also prevented the rapid hydrolysis of chloramben’s methyl ester by leaching in autoclaved soil. When it was incubated 48 hours in natural soil before leaching, both mobile (acid) and immobile (ester) components were found.

BEHAVIOR OF PESTICIDES I N SOILS

161

Pesticide mobility in soils is influenced by both soil and pesticide factors. These are documented in previous reviews (Bailey and White, 1970; Edwards, 1966; Goring, 1967; Helling, 1970). I n brief, the following observations seem to be generally true. I

Water eluted

(cm)

FIG. 2. Elution of parathion-:?T (P) and total radioactivity (T) through 15-cm columns of Hugo gravelly sandy loam. The soil was enriched (l),natural (2), or autoclaved (3).After McCarty and King (1966).

Adsorption to soil colloids most affects leaching. Soil organic matter is correlated more closely to retention against leaching than is clay for nearly all compounds, the organic cations diquat and paraquat being exceptions. Pesticides are more readily leached in light- than in heavytextured soils, reflecting the typically higher clay and organic matter contents and higher field capacity of heavy soils. Field capacity is often negatively correlated with pesticide mobility. A given quantity of water, from rainfall or irrigation, will penetrate farther in soils of low field mosture capacity; this term is also correlated with the adsorptive organic matter and clay components and thus the relationship is complex. I n relatively acidic soils, the reduced pH may restrict leaching (by increased adsorption) of triazines and organic acids. Depth of penetration will increase as the applied water increases. The effect of initial soil moisture content and water flux is unclear. It is important to remember that mass transfer of pesticides occurs upward, in drying soils, and laterally, from wetter to drier soil, as well as downward. Molecular characteristics are important inasmuch as they affect adsorption (Section 11, A, 1, c). Esterification of acidic herbicides such as chloramben, 2,4-D, and dicamba increases adsorption and greatly reduces

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CHARLES s. HELLING, P H I L I Pc. KEARNEY, A N D MARTIN ALEXANDER

mobility. Conversion to the free acid usually occurs readily in soils, so mobility behavior characteristic of the ester may be transient in the field. Further microbial degradation will restrict the depth and quantity of pesticide leached, as shown earlier with parathion (Fig. 2). Solubility has sometimes been directly correlated with pesticide movement, as with thiocarbamate herbicides, but the correlation does not appear to be of general validity. Solubility does limit the maximum concentration in the soil water phase (adsorption normally further reduces this value). Mobility is greater for higher pesticide applications; in part, this may reflect analytical limits of detection. To avoid an unwieldy compilation of mobility references, we have attempted to consolidate the literature. Table I thus is based on many references; those cited contain at least four pesticides which were directly compared. Of the 82 entries in Table I, 40 occurred in a single publication (Helling, I97 1 b). The model for relative movement is mass transfer in an “average” soil. Vapor phase movement does, however, influence ranking of some rather immobile pesticides. If the compounds in Table I are representative of most pesticides (apart from fumigants) likely to reach the soil, then: (i) pesticides are generally of intermediate to low mobility; although (ii) acidic compounds are relatively mobile; (iii) phenylureas and s-triazines tend to be in mobility class 2 or 3; and (iv) chlorinated hydrocarbon insecticides are usually least mobile, preceded somewhat by organophosphate insecticides. Recently, residue data from several long-term field studies were published. Two IS-year experiments used insecticides. Plots in Nash and Woolson’s report ( 1968) were sprayed, cropped, and cultivated for 3 years, then left idle. All insecticides, but especially lindane (y-BHC) and isodrin, were relatively depleted in the surface 7.5 cm, perhaps indicating surface volatilization. Lindane and isodrin also had the highest concentrations below 30 cm, again suggesting greater mobility than the other chlorinated hydrocarbons. In the second insecticide experiment (Voerman and Besemer, 1970), dieldrin, lindane, DDT, and parathion were applied several times every year. Maximum residues were always in the 0- I0 cm zone. Parathion disappeared within 6 months after the last application, so only traces were found in the sandy soil. The more persistent DDT and dieldrin moved to 30-40 cm at lower rates and 50-60 cm at high rates. Lindane did not occur below 10-20 cm. Fryer and Kirkland ( I 970) could not detect simazine below 0-2 inches after six annual applications at I .5 Ib/acre; residues from higher (4 Ib/acre) semiannual applications were mainly in this surface zone. Linuron showed movement to 2-4 inches, with some possible residues in the 4-6 inch layer.

I63

BEHAVIOR OF PESTICIDES I N SOILS

These three examples seem to show that degradation, volatilization, and possibly plant uptake may alter the expected mobility patterns in a longterm field situation. TABLE 1 Relative Mobility of Pesticides in Soils" Mobility Class"

5

4

3

2

I

TCA" Dalapon 2,3,6-TB A Tricamba Dicamba Chloramben

Picloram Fenac Pyrichlor MCPA Amitrole 2,4-D Dinoseb B ro macil

Propachlor Fenuron Prometone Naptalam 2,4,5-T Terbacil Propham Fluometuron Norea Diphenamid Thionazin Endothall Monuron Atratone WL 19805 Atrazine Simazine lpazine Alachlor Ametryne Propazine Trietazine

Siduron Bensulide Prometryne Terbutryn Propanil Diuron Linuron Pyrazon Molinate EPTC Chlorthiamid Dichlobenil Vernolate Pebulate C hlorpropham Azinphosmethyl Diazinon

Neburon Chloroxuron DCPA Lindane Phorate Parathion Disulfoton Diquat Chlorphenamidine Dichlormate Ethion Zineb Nitralin C-6989 ACNQ Morestan Isodrin Benomyl Dieldrin Chloroneb Paraquat Trifluralin Benefin Heptachlor Endrin AIdrin Chlordane Toxaphene DDT

"From data of Gray and Weierich (1968b). C. I. Harris (1967b, 1969). Helling (1971b), Helling and Turner (1968). Koren et al. (1969). Nash and Woolson (1968), Rhodes et al. ( 1970). and many other references. I' Class 5 compounds (very mobile) to Class 1 compounds (immobile) are in the scheme of Helling and Turner (1968). Within each class, pesticides are ranked in estimated decreasing order of mobility. ' Names of herbicides are set in normal type: insecticides, fungicides, and acaricides in italics.

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CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

When a mobile pesticide (Class 4 or 5 in Table I) is also moderately persistent, residue analyses have detected the compound deep in the soil profile. Picloram applied at low rates leached out of the upper zone in 12-18 months in sandy soils (Bovey et al., 1969). In Puerto Rico it was detected to 45-5 1 inches after only 3 months. Similarly, more picloram was found at 2-3 feet than nearer the surface of a Nebraska sandy loam 10 months after treatment (Scifres et al., 1969). Here as with other compounds, movement was apparently greatest when picloram was fall-applied rather than spring-applied. b. Volatilization. By vapor phase movement certain pesticides may be distributed throughout the soil profile and eventually lost via surface evaporation. Volatilization is dependent on inherent chemical characteristics (especially vapor pressure), soil texture, soil water content, soil adsorptivity, and temperature. Soil pH is also important for ionizable compounds: liming reduced volatilization losses of dinoseb (Barrons el al., 1953) and KN3 (Parochetti and Warren, 1970). Fumigants such as methyl bromide (vapor pressure = 1380 mm/20"C) are extreme examples of volatile toxicants. Movement of several fumigants has been detected to at least 245 cm (O'Bannon and Tomerlin, 1968). However, many herbicides also exhibit significant vapor phase movement, e.g., EPTC, pebulate, CDEC, CDAA, propham, chlorpropham, dichlobenil, and trifluralin. Much current research interest centers around volatilization of insecticides, especially the persistent chlorinated hydrocarbons such as dieldrin, endrin, and heptachlor. By comparison, vapor pressures of this group are only lop4to lo-' mm Hg (Edwards, 1966), while those of the above herbicides are lo-' to mm Hg. Determination of pesticide vapor pressure was discussed recently (Hamaker and Kerlinger, 1969). As with leaching, several generalizations can be made about pesticide volatilization within and from soils. Volatilization is increased by higher temperature and lower clay or organic matter content. Volatilization losses are usually greater from moist than dry soil; gaseous diffusion within soil, however, becomes negligible as pores become water-saturated. Surface loss is decreased by soil incorporation, compaction, or sealing (as with plastic films). Hartley (1 969) isolated two distinct effects of water on volatilization of pesticides. Wick evaporation depends on the evaporation of water from the soil surface. Thus, as water evaporates there is a bulk flow from lower capillaries to replace this loss, and therefore mass transfer upward of the pesticide. When the soil surface dries, this mechanism of indirect acceleration by water largely breaks down. The second mechanism Hartley cited was adsorption displacement. Water is a more efficient competi-

BEHAVIOR OF PESTICIDES I N SOILS

165

tor than many pesticides for adsorption sites, especially clay surfaces, and wetting the soil desorbs and activates compounds such as EPTC. In the second mechanism, loss of water is not required for substantial pesticide volatilization. This was shown experimentally with dieldrin (W. F. Spencer and Cliath, 1969; W. F. Spencer et al., 1969). Vapor density was unaffected by water content until it (water) decreased to an amount equivalent to a surface monolayer; vapor density than approached zero on further drying. Dieldrin vapor pressure was apparently unaffected by water, so “codistillation” is unlikely. Soil reduces volatilization of low dieldrin concentrations (10 ppm) but does not greatly affect higher levels (100 ppm). Loss of D D T and lindane is also greatly reduced when soils dry to less than a monolayer of water (Guenzi and Beard, 1970). At low insecticide concentrations, relative loss of lindane :dieldrin : D D T was 1 7 : 5 : 1 (Igue et al., 1969). Ehlers el al. (1969a,b) described the overall diffusion of lindane in soils. At 10% water content in Gila silt loam, diffusion occurred equally in vapor and “nonvapor” phases, whereas at near saturation, movement was entirely in the “nonvapor” phase. Maximum lindane diffusion occurred at 3% water content, decreasing to zero at 1 % water and to a lower steady state at > 5 % water. Decreasing bulk density or increasing temperature increased diffusion. On the basis of diffusion measurements, Farmer and Jensen (1970) predicted that up to 20% of a 1.12 kg/ha dieldrin application, incorporated to 15 cm, could be volatilized per year from a silt loam in equilibrium with air at 75% relative humidity. Approximately 75% of the fungicide PCNB which was lost after 10 months had been volatilized (Caseley, 1968). These results and atmospheric analyses of endrin and DDT (Willis et al., 1969a,b) after soil treatment suggest that volatilization may be an important process of pesticide loss. c. Runoff. Lateral movement of a pesticide across the soil surface is enhanced by steep topography, low soil permeability, and intense and/or prolonged precipitation. Factors conducive to wind or water erosion are important since pesticides most likely to be removed from bare soil are those that are not mobile. That is, leaching protects a pesticide from runoff but an immobile compound remains adsorbed at the surface, where erosion occurs. Where vegetative cover existed, mobile pesticides such as dicamba,.picloram, and 2,4,5-T were seen in the initial runoff. Four months later, however, losses were reduced to < 1 % of the first values (Trichell et al., 1968). Formulation of 2,4-D as the amine salt greatly reduced runoff when compared to esters of the herbicide (Barnett et al., 1967). The order of lateral movement for one group of herbicides was isocil > diuron > simazine > monuron (Upchurch et al., 1968).

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CHARLES s. HELLING, P H I L I P c . KEARNEY, A N D MARTIN ALEXANDER

Lateral movement of DDT from spot-treated soil did not exceed 10 inches (V. K. Smith, 1968). Dieldrin applied to a watershed at 5 Ib/acre yielded an average runoff concentration of 0. I ppb; runoff from adjacent untreated land was 0.03 ppb (Anonymous, 1969). Toxaphene and D D T concentrations were < 1 ppb. Hindin et al. (1966) measured runoff of DDT, ethion, and diazinon insecticides from a coarse silt loam, low in organic matter. The plot was corn-cropped and regularly irrigated; generally, 25-40% of applied water was returned as runoff. Under these conditions less than 0.01% of pesticide applied was recovered in runoff water plus silt. Most. of the loss (ca. 60%) occurred after the first irrigation. Long-range wind transport of pesticide-contaminated dust from Texas to Ohio has been shown (Cohen and Pinkerton, 1966). More typical results are probably those of Menges (1964), in which movement of treated soil reduced weed control and caused injury to adjacent nontreated crops. External contamination by dust may also be a source of pesticide residues in plants, as with sodium arsenite-treated Plainfield sand (Jacobs et al., I970a). Most pesticide runoff is short range. On cultivated lands, stream contamination by pesticide runoff seems unlikely unless soil erosion is itself a problem. Some runoff from rangeland occurs with chemicals such as picloram. 3 . Photodecomposition

The practical significance of photodecomposition, or degradation by the direct influence of light, as a process affecting pesticides in soils is certainly less clear than adsorption, movement, chemical reactions, or metabolism. It can occur only at the soil surface; therefore, only those compounds not soil-incorporated or those which have moved to the surface during drying will be degraded. Several pertinent reviews on pesticide photodecomposition have appeared. Crosby and Li ( t 969) discussed theory, methodology, and herbicide degradation; more recently, the photochemistry of halogenated herbicides was reviewed (Plimmer, 197 I). Photodecomposition of pesticides in general is included elsewhere (Crosby, 1969b; Kearney et af., 1969~). Most research deals with reactions occurring in solutions, often organic rather than aqueous. Furthermore, ultraviolet lamps are normally used as energy sources, despite almost no radiation of this frequency actually reaching the earth’s surface. Crosby and Li ( 1 969) discussed the difficulty of conducting experiments in sunlight under natural environmental conditions. Contamination, variable light intensity, and vola-

BEHAVIOR OF PESTICIDES IN SOILS

I67

tilization are only a few of the problems. Since photodecomposition does occur under the less energetic sunlight, sensitizers have been suggested as occurring in soil. These substances resemble catalysts in that they are light-activated, then transmitting this energy to the pesticide before returning to ground state. Riboflavin and ferric salts are known sensitizers. Logical goals in future pesticide photodecomposition research would seem to be establishment of the quantitative significance of photo degradation, evaluation of the soil parameters influencing photodegradation, and understanding the photochemical mechanisms at the soil surface. a. Herbicides. Many herbicides contain halogen atoms. A common photochemical reaction is sequential loss of these substituents. Plimmer ( 1 97 I ) suggested the ease of ortho-chlorine displacement from substituted aromatic rings was CO,H > OCH, > CH,; for para-substituents, OCHs > COzH = CHs; and for rneta-substituents, CHa > OCH, > C0,H. In aqueous solution, t h e position is often hydroxylated. Thus 2,4-D irradiation produces 4-chloro-2-hydroxyphenoxyaceticacid and some 2-chloro4-hydroxyphenoxyacetic acid. Fission of the ether linkage also occurs, however, and 2,4-dichlorophenol and 4-chlorocatechol were isolated. Aqueous solutions of monuron, linuron, and metobromuron were degraded to para-hydroxy analogs (and other products) in sunlight. Picloram was degraded with loss of two chlorine atoms by a presumed free radical mechanism (Hall et al., 1 968). Several chloro-s-triazines were converted by irradiation at 253.7 nm in water, to corresponding hydroxytriazines (Pape and Zabik, 1970). Atrazine, simazine, and propazine irradiated in methanol gave, respectively, atratone, simetone, and prometone. With methylthio-s-triazine analogs, in solution or in the solid state (Plimmer et al., I969), hydrogen replaced the leaving group. Reductive dechlorination also occurs for chloramben (yielding 3-amino5-chlorobenzoic acid and other products) and pentachlorophenol. Further conversion of phenols often produces colored polymeric products, such as in photolysis of chloramben, 2.4-D, and ioxynil. When chloramben was surface-applied to moist Lakeland sandy loam, solar illumination reduced its bioactivity by I I - 14% after 7.5 hours. Since no loss occurred in dry soil, and volatilization was considered unimportant, lsensee et al. ( I 969) concluded that water movement toward the surface kept the mobile chloramben in an exposed position. Conversion of the herbicide to Nbenzoylchloramben prevented its photodegradation. Phenylureas are oxidized to N-methylurea or urea derivatives upon irradiation. Formyl intermediates in the stepwise oxidization of monuron have been isolated (Tang and Crosby, 1969). Degradation, from dilute aqueous solution in sunlight, amounted to < 6% in 14 days. The parent aniline has been isolated from monuron and from the phe-

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CHARLES s. HELLING, PHILIP c. KEARNEY, A N D MARTIN ALEXANDER

nylcarbamate propham. In the latter case, phenyl isocyanate also forms and can react with aniline to yield sym-diphenylurea. Irradiation of solid C-6989, an aromatic ether, by ultraviolet light caused ether cleavage, nitro reduction, and deamination (of an amino photolysis product) reactions yielding at least eight products (Eastin, 1970). Degradation under phytotron lighting was similar, although slower. Sunlight rapidly degraded diquat adsorbed on silica gel to 1,2,3,4detrahydro- 1-oxopyrido[ 1,2-a] -5-pyrazinium salt and picolinamide (A. E. Smith and Grove, 1969). In solution, picolinic acid and other minor products formed as well. Calderbank (1968), while reviewing the photochemistry of bipyridylium herbicides, cites an interesting case of adsorption-modified photodecomposition. Paraquat is only slowly degraded in sunlight while in aqueous solution; degradation is observed on surfaces. however, and may be related to an increase in,,,A (256 + 275 nm) when adsorbed on clay minerals. 4-Carboxy- 1-methylpyridinium salt is a prime photodegradation product of paraquat. Loss of trifluralin bioactivity from soil surfaces has sometimes been attributed to photodecomposition. Photolysis does occur in organic solvents under ultraviolet irradiation (summarized by Probst and Tepe, 1969). However, in recent work Hein and Parochetti (1 970) found no loss in activity of trifluralin, benefin, or nitralin, surface-applied to moist Lakeland loamy sand, if the containers were covered by quartz plates during sunlamp irradiation. Without the plates, substantial volatilization of trifluralin and benefin occurred; the authors thus concluded photodecomposition was not an important mode of loss. b. Insecticides. Solid D D T slowly degrades in sunlight to DDE, T D E (DDD), p,p’-dichlorobenzophenone,and other products. Products are similar in methanol or with the insecticide methoxychlor, but rates are faster. Plimmeref al.(1970~) have suggested D D T photolysis in methanol involves the formation of peroxy and alkoxy radicals, in the presence of oxygen. Whether in the presence or absence of oxygen, photolysis of DDT or DDE yielded many identifiable products. Solid aldrin yields its epoxide, dieldrin, in exposure to sunlight. These CI

Photoaldrin

CI

Photodieldrin

169

BEHAVIOR OF PESTICIDES IN SOILS

two cyclodiene insecticides are also converted to photoaldrin and photodieldrin, respectively. Photodieldrin is approximately twice as toxic as dieldrin to insects and mice. Other related insecticides photolyzed by sunlight include chlordene, endrin, heptachlor, and isodrin. Formation of ketoendrin (Rosen et al.,. 1966) and 1,8-exo-9,1I , 1 1-pentachloropen(I) (Zabik et al., 1970) from tacyclo-(6.2.1. 13~6.02~7.04~10)-dodecan-5-one endrin is shown below: c1

Emirin

CI

Ketotendrin

n

(I)

Endrin is photolyzed to other products as well. It should be noted that ketoendrin and a related aldehyde also form spontaneously, according to Asai et al. (1969), on some air-dry soils (see Section 11, A, 4, b). Many carbamate insecticides including carbaryl, Matacilm, Zectranm, BanoP, and Mesurolm undergo photodecomposition (Menzie, 1969). The methylmercapto group of MesuroP is oxidized to the sulfoxide and sulfone. The sec-amino groups of Zectranm and MataciP are dealkylated with production of formamido derivatives as well. Carbaryl is converted to I-naphthol. A common photoconversion among thiophosphates is oxidation of sulfur in alkyl side chains to sulfoxides (as with demeton) or sulfones. Parathion is oxidized by sunlight to paraoxon and isomerized to S-alkyl or S-aryl analogs. Solid diazinon exposed to ultraviolet irradiation produced a hydroxylated isopropyl derivative, also found on leaves exposed to sunlight (Pardue et al., 1970). In sunlight, the acaricide chlorphenamidine degraded to N-formyl-4chloro-o-toluidine and lesser products in water and on silica gel (Knowles and Sen Gupta, 1969); hydrolysis to the toluidine may be chemical. c. Fungicides. Dexon solutions in water rapidly decolorize in sunlight, then become very dark (Hills and Leach, 1962). The suggested reactions involve photochemical reduction of the diazonium group with loss of Nz, oxidation, and ultimately polymerization. Aqueous solutions of chloranil are unstable unless stored in darkness. By comparison, dichlone is more stable in solution and on foliage. Burchfield ( 1967) related to this dichlone’s lower oxidation potential. Mercury, in organomercury fungicides, may undergo photoreduction depending on the compound and conditions of photolysis (Menzie, 1969, p. 241).

170

CHARLES

s.

HELLING, P H I L I P c . KEARNEY, A N D MARTIN ALEXANDER

4 . Chemical Reaction

Recognition of nonbiological processes altering pesticide structure in soils is sometimes clear, as with hydrolytically unstable molecules. More often, however, evidence for chemical reaction occurring in the field is speculative or even overlooked. The latter arises because many workers tacitly assume that restricted degradation in “sterilized” soil proves the degradation process to be microbial. Kaufman et al. ( 1968) discredited this generalization while demonstrating chemical degradation of amitrole by a mechanism inactivated by steam sterilization. Chemical reactions of pesticides may occur independently of soil or they may be soil-catalyzed; an attempt is made to categorize representative reactions in the following sections. When reaction rate is pH dependent, this differentiation becomes arbitrary since pH near clay surfaces is markedly lower than in the bulk solution. a. Reactions Not Catalyzed by Soil. The most prevalent nonenzymatic reactions in soils are hydrolysis, oxidation, and isomerization. This, of course, neglects ionization and formation of salts, which are functions of the pH and ion status in the soil solution. O’Brien (1967) reviewed the principals governing nonenzymatic reactions of organophosphate insecticides. Organophosphates characteristically undergo alkaline hydrolysis. Thus, substituents on the pesticide which render the phosphorus atom more positive also increase its susceptibility to nucleophilic attack by OH-. Beside the inductive effect, field and resonance effects contribute to the chemical stability (and biological activity) of a pesticide. These effects are seen in comparing the half-lives of several organophosphates at pH 8 and 25°C: TEPP, 3.04 days; paraoxon, 925 days; and parathion, 8460 days. Paraoxon, an oxidation product of parathion, is more labile

w TEPP

Pd I’d0 XO Il

than its precursor because =S is replaced by the more electronegative =O. Even slower hydrolysis in acidic conditions (Peck, 1948) suggests that chemical degradation of parathion in soil is probably minor. Isomerization in the organophosphates is represented by the conversion of sulfur from thiono (= S) to thiolo (- S -), as in parathion to Sethyl parathion (Woodcock and Stringer, 195 1). The reaction took place at elevated temperatures and so its significance in soil systems is not known. Alkaline conditions favor hydrolysis of binapacryl (a fungicide) to

171

BEHAVIOR OF PESTICIDES IN SOILS

Binapacryl

Dinoseb

dinoseb (a fungicide/insecticide/herbicide). Hydrolysis of fenoflurazole is sufficiently rapid so that it is considered unstable in the spray tank after OH

I

CI

+ CI

Fenotlurazole

+

H

L4

4 hours dilution with water (E. Y. Spencer, 1968). A similar hydrolysis of benomyl readily occurs by nucleophilic attack, producing an imidazole (11), which Kilgore and White (1970) surmise may be the fungicidally active component. Solutions of benomyl are hydrolyzed within 4 days

O&\NHC~ H, Benomyl

(C. A. Peterson and Edgington, 1969). Another fungicide, captan, has a half-life in solution of only 2.5 hours at pH 7.0 (Burchfield and Schectman, 1958). Stability increased at lower pH’s. The half-life in a moist silt loam soil was 3-4 days (Burchfield, 1959). Proximpham, a new phenylcarbamate herbicide, has a half-life in neutral aqueous solution of 13 days (Jumar and Griinzel, 1968). I t decomposes by two pathways, a first-order reaction in acidic or neutral solutions, and a second-order reaction in basic media. Decomposition in soils occurs by both chemical and microbial processes, with a half-life of 7-10 days.

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CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

I’roximplwin

(acid or neutral)

(base)

In the presence of acidic soils, sesone (Carroll, 1952; Vlitos, 1952, 1953) and 2,4-DEP (Sheets and Danielson, 1960) are hydrolyzed to a common intermediate, 2,4-dichlorophenoxyethanol(III), which in turn can be biologically oxidized to the herbicide 2,4-D (Audus, 1952). Above pH 5 . 5 , the hydrolysis of sesone occurred only by microbial processes.

?,4-DEP

EPTC is hydrolyzed by water at 20°C in a first-order reaction yielding ethyl mercaptan, COz, and dipropylamine. Another thiocarbamate herbicide, cycloate, was also hydrolyzed in autoclaved soil. Microbial metabolism’is likely the more important process in soils, however (Gray and Weierich, 1968a; Sheets, 1959). Rapid release of the toxic methyl isothiocyanate from soils treated with dazomet (Mylone@)or metham (VapamB) is well known (Gray, 1962; Lloyd, 1962; Munnecke el al., 1962; Munnecke and Martin, 1964; Drescher and Otto, 1968). The apparent catalysis of dazoment by clays may reflect a buffering effect (Munnecke et al., 1967). In soil and buffered

BEHAVIOR OF PESTICIDES IN SOILS

173

aqueous solution, decomposition of dazomet is most rapid near neutrality, and is increased by greater soil moisture and temperature. Dazomet, in acidic solution, decomposes slowly in the cold to CSz, methylamine, and formaldehyde. In base, CS2 is absent and sulfur occurs chiefly as sulfide. An aqueous neutral solution becomes turbid with elemental sulfur after 1-2 days, producing methyl isothiocyanate, methylamine, and formaldehyde as well. Drescher and Otto ( 1968) observed formation of the isothiocyanate within 15-20 minutes after mixing dazomet with a moist compost soil. The fungicide was degraded within 4 hours at 20°C. N , N ' Dimethylthiourea is also formed by reaction of methyl isothiocyanate and methylamine, a reaction which occurs in metham solutions as well (Gray and Streim, 1962). Methylthiourea was sometimes detected, arising from reaction of methyl isothiocyanate with soil NH,. Drescher and Otto also isolated, from a sandy soil in which dazomet hydrolyzed slowly, (IV). The nona triazine, 1,3,5-trimethylhexahydro-s-triazine-2-thione persistent and biologically inactive product apparently is synthesized by

Dazonir t CH,NH,

combination of other dazomet breakdown products. Oxygen is apparently required for decomposition of metham to methyl isothiocyanate (Turner and Corden, 1963) explaining why this reaction was increased with decreasing soil moisture, permitting better aeration. Decomposition is essentially complete in 1 hour in the presence of montmorillonite, vermiculite, or peatmoss, yet only 6- 14% complete in calcite, talc, sand, and cellulose powder paper (Gray, 1962). Loss was rapid in a high clay soil. At relatively low pH's there is a shift to slower nonoxidative decomposition similar to that observed with nabam (Ludwig and Thorn, 1958). Dilute aqueous nabam solutions are unstable upon exposure to air; its reactions are summarized in a general review of the chemistry of dithiocarbamate fungicides (Ludwig and Thorn, 1960). For field applications, nabam is therefore converted to more stable metal complexes such as zineb (Zn) and maneb (Mn). The kinetics of acid hydrolysis and thermodynamic properties of the ethyl analog of metham, SDDC (sodium diethyldithiocarbamate), were determined in DzO (Dale and Fishbein, 1970). SDDC degrades to CS, and diethylamine at pH 7.3, and this

174

CHARLES s. H E L L I N G , PHILIP c . KEARNEY, A N D MARTIN ALEXANDER

reaction was followed using NMR. At pD 4.8, half-life is 0.5 minute at 28"C, increasing to 57 minutes at pD 6.8. Chloral hydrate, a herbicide used to control couch grass and wild oats, decomposes in water to HCI, C 0 2 , and formaldehyde. In soil it is converted to another herbicide, TCA, within a few days (Schutte and Stephan, 1969). High adsorption to an alkaline clay (pH 9) was thought to be related to alkaline decomposition (Schutte and Stephan, 1968). Chloral hydrate undergoes conversion to CHCl3 in aqueous alkaline solution. Oxidation is a chemical reaction often modifying S-containing pesticides. The dimethyldithiocarbamate ion is oxidized to tetramethylthiuram disulfide (thiram) by FeS+at pH s 3: 2 (CHn)xN-C(S)S-

- ?e-

(CH:j),N-C(S)S-SC(S)-N(CH,),

Carboxin, a systemic fungicide, is converted (ca. 20% in 7 days in autoclaved soil) to its sulfoxide without further reaction (Chin et al., 1970); in solution the reaction is acid catalyzed. Bayer 25 141, an organophosphorus insecticide, oxidized slowly in air to the sulfone, when exposed on glass or cotton leaf surfaces (Benjamini et al., 1959). Some isomerization to the S-ethyl analog and oxidation of this to a sulfone also occurred. Nonenzymatic conversion of P = S to P = 0 has been demonstrated with dimethoate (Dauterman et al., 1960). b. Reactions Catalyzed by Soils. Investigations of the occurrence and nature of soil-catalyzed pesticide degradation have often been concentrated on the clay fraction. The general subject of clay-organic complexes, including clay catalysis reactions, has recently been summarized by Mortland ( 1970). The ability of certain clays to catalyze reactions seems to be related to their strongly acidic nature. In montmorillonite, for example, the protondonating ability was correlated with the nature of the exchangeable ion as well as the basicity of various nitrogenous bases (Mortland, 1968). When residual water is relatively highly dissociated, as on dehydrated clay, conversion of amines to NH,+ may occur. The reaction with urea, for example, proceeded at 20°C in Cug+-montmorillonitebut was not seen with alkali or alkaline earth saturated clays (Mortland, 1966). Aliphatic and aromatic amine-substituted montmorillonites degraded to N H4+and, presumably, to alcohols and phenols at 250°C (Chaussidon and Calvet, 1965). There was no evidence of this reaction occurring at room temperature. Ethyl acetate hydrolysis and sucrose inversion were catalyzed by H-saturated clays (McAuliffe and Coleman, 1955). The reactions were always greater in the presence of clays than with an equivalent amount of acid alone. When boiled with vermiculite, montmorillonite, or halloysite,

BEHAVIOR OF PESTICIDES IN SOILS

175

glycerol is catalytically degraded to carbonaceous products. G. F. Walker ( 1967) assumes two silicate surfaces must be in simultaneous contact with the molecule; small, highly charged cations (H, AI, Mg) in interlayer positions enhance the effect. The oxidation of benzidine to benzidineblue, a radical cation, characteristically imparts a blue color to montmorillonite. Solomon et a f . (1968a) showed this reaction to occur at aluminum atoms exposed on crystal edges and at transition metal ions in their higher valency state. Lewis acid sites were also significant in transformation of other leuco dyes, in polymerization of unsaturated organic compounds (Solomon et al., 1968b), and in the rearrangement of the insecticide ronnel to 0-methyl S-methyl 0-(2,4,5-trichlorophenyl) phosphorothioate on clays preheated to 950°C (Rosenfield and Van Valkenburg, 1965). In all cases, the ability of the solvent to compete successfully for reactive sites governs the ultimate reaction. The reactions cited in the preceding paragraph sometimes occurred only at elevated temperatures or in nonaqueous solvents. They serve as a guide, however, to some mechanisms which may affect chemical alteration of pesticide molecules in the natural environment. Early investigations of pesticide breakdown dealt with the effect of “inert” clay diluents on the stability of formulated insecticides. Fleck and Haller (1 945) demonstrated the catalytic effect of kaolinite, montmorillonite, some talcs, FeCls, AICls, and CrCI3on conversion of DDT to DDE at 1 15- 120°C. Van Valkenburg ( 1969) has traced subsequent work on the compatibility of clays with pesticides. Evaluation of clays is based in part on their surface acidity, usually measured by observing color changes in adsorbed Hammett indicators (Walling, 1950; Benesi, 1956). Acid clays such as attapulgite (pK, < I ) rapidly degraded heptachlor; by incorporating oxygen-containing chemicals such as diethylene glycol, both surface pK, and insecticide stability were markedly increased (Malina et al., 1956). Glycols were also used to stabilize solid formulations of the acaricide aramite (Yaffe, 1958). Malathion is relatively stable in neutral or moderately acidic media, and can be formulated on dry mildly alkaline surfaces. In the presence of moisture, however, base-catalyzed hydrolysis is rapid even near neutrality (Yost and Frederick, 1959). The degradation rate of malathion of various carriers was of the order attapulgite %- kaolinite > talcs and pyrophyllite. Ronnel underwent substantial hydrolysis to 2,4,5-trichlorophenoI when incubated at 50°C on montmorillonite, especially if AI- or Fe-saturated (Rosenfield and Van Valkenburg, 1965). When free water was removed by prior heating to 300”C, the hydrolysis was accelerated, presumably because effective acidity and surface area are both increased. Aqueous suspensions of dichlone on attapulgite clay slowly became deep red in color with ap-

176

CHARLES s. HELLING, P H I L I P c. KEARNEY, A N D MARTIN ALEXANDER

parent formation of 2-hydroxy-3-chloro- 1,4-naphthoquinone (Burchfield, 1967). Fowkes et al. ( 1960) noted significant decomposition of chlordane, toxaphene, heptachlor, DDT, dieldrin, and endrin on acidic diluents, such as kaolinite and attapulgite. Dieldrin was degraded much more rapidly on kaolinite substituted with H or Al”+than with N a + or Ca”. They indicated that on degradation of epoxidized compounds (dieldrin and endrin), the epoxy group is apparently replaced by a carbonyl group. Endrin, for example, formed a ketone of unchanged molecular weight. Organic bases were effective stabilizers. Downs et al. (195 I ) used the procedure of Fleck and Haller (1945) to evaluate DDT stability on adobe soil surfaces. Susceptibility to thermal degradation at 130°C corresponded inversely to its persistence in the field: e.g., a soil which degraded 90% of the DDT in 3 hours also inactivated the insecticide within 3-6 months in normal use conditions. Iron oxides in soil appear to catalyze the reaction (Downs et al., I95 I ; Birrell, 1963). In addition to DDE, Birrell found 4,4’-dichlorobenzil after heating DDT at 112°C in a nitrogen atmosphere. The latter occurred only when iron oxides, especially goethite or hematite, were present. Thermal degradation of DDT was also promoted by allophanic soils or clays, presumably by their amorphous alumina; degradation may be retarded by organic matter in soil. High iron and aluminum content in soils favored adsorption of DDT, dieldrin, and y B H C (Press, 1959), a fact probably not unrelated to the preceding observations on DDT reactivity. p,p’-DDT conversion to DDE during diffusion experiments with montmorillonite or vermiculite clays seemed to occur preferentially on newly exposed clay (Lopez-Gonzales and Valenzuela-Calahorro, 1970). If, however, the diffusion coefficient of DDE (formed first in the treated clay) is larger than that of DDT, there would also be a relative enrichment of D D E in the untreated clay column. Although the aforementioned reactions have generally been associated with clays, Crosby (1969a) alluded to an interesting role of organic matter in pesticide transformations. He noted the in vitro reduction of D D T to TDE (DDD) in the presence of reduced porphyrins, compounds which, along with a demonstrably high free radical content, are also present in soils. One pathway of heptachlor loss in soils is through chemical conversion to 1-hydroxychlordene. Partial reaction had occurred in water at 26.5”C after 20 hours (M. C . Bowman et al., 1964). Conversion was essentially complete at 45°C within 24 hours in a series of dry, low organic matter soils (M. C. Bowman et al., 1965a). However, the reaction did not occur on two soils of much higher organic matter content; these two soils also inhibited the catalytic degradation of isobenzan (TelodrinB) and endosul+

BEHAVIOR OF PESTICIDES IN SOILS

177

fan. Only the soil containing 19% organic matter prevented total loss of endrin. Since moisture decreased degradation of the insecticide, the role of soil organic matter may simply be to increase water held in the soil. Alternately, it may block reactive clay sites. I-Hydroxychlordene has since been found in heptachlor-treated field (M. C. Bowmanet al., 1965b; Carter and Stringer, 1970; Duffy and Wong, 1967) and greenhouse (Beall and Nash, 1969) soils. Rapid formation of I-hydroxychlordene from heptachlor in their dust formulation makes the evaluation of the soil's role rather difficult (M. C. Bowman et al., 1965b). The heptachlor component of chlordane was completely converted to the stable 1 -hydroxychlordene within 30 days of exposure to water (Bevenue and Yeo, I969a,b). Soil microorganisms can then convert 1 -hydroxychlordene to I-hydroxy-2,3epoxychlordene (Miles et al., 1969). Degradation of endrin in soils may be very rapid. Asai et al. (1 969) reported that, after 45 hours at 25"C, 7 of 10 soils showed complete absence of endrin and formation of two isomers, an aldehyde (4,5,6,7,8,8hexachlorohexahydro-4,7- methano- 3,5,6- methenoindan- 1 -carboxaldehyde) and a ketone [ 1,8,9,10,I 1,ll-hexachloropentacycIo(6.2.1.13,60.2J04~10)-dodecan-5-one].In 16 hours, Huerohuer sandy loam degraded 90% and 65% of applied endrin while stored at 25°C and 3"C, respectively. The samples were stored in sealed glass containers so volatilization was not a factor. N o endrin loss occurred in soils containing 20% water. These results not only suggest that chemical degradation of endrin may occur naturally in dry soils, but they also serve clear warning that improper sample preparation may produce chemical artifacts. Fate of the organophosphate insecticides in soils has received less attention than that of the chlorinated hydrocarbons. Chemically organophosphates are less stable in water and soil. The rates of malathion (Konrad el al., 19691, Ciodrins (Konrad and Chesters, 1969), and diazinon (Konrad et al., 1967) degradation were directly related to their adsorption by soil and were first-order reactions. Malathion and Ciodrin@are base-hydrolyzed whereas diazinon, in contrast to most organophosphate insecticides, is acid-hydrolyzed. Soil catalysis was more than a pH effect: e.g., sterile Poygon sic1 (pH 7.2) degraded 99% of added malathion in 2 days, whereas only 25% degraded in 7 days in aqueous solution ( p H 9). Konrad and co-workers suggested chemical degradation in soils preceeds as shown, with cleavage first in the a position, then at b (see p. 178). Hydrolysis at a appears to yield a malathion half-ester first, based on experiments with enrichment cultures (Tiedje and Alexander, 1967). The alpha form of malathion, 0,O-dimethyl S-( l-carboxy-2carbethoxy)ethyl phosphorodithioate, has been the only half-ester identified from biological systems, in this case, rat urine (Chen et al., 1969).

178

CHARLES

s. HELLING, PHILIPc . KEARNEY, AND MARTIN ALEXANDER

b

b

U

U

Ciodrin@ Malathion

Diazinon

Diazinon was degraded equally in autoclaved and nonautoclaved soils (Getzin, 1968). Degradation increased at lower pH, higher temperature, and higher soil moisture. In sterilized soils, disappearance was rapid in an acidic clay pH (4.7) but very slow in other clay (pH 6.6) and clay loam (pH 7.6) soils (Sethunathan and MacRae, 1969). Initial hydrolysis in solution cultures of soil microorganisms also appeared to be chemical (Gunner, 1967). Imidan, a broad-spectrum insecticidelacaricide, was rapidly hydrolyzed in two moist soils (Menn et al., 1965). The times required for 50% hydrolysis in autoclaved and nonautoclaved Sorrento sandy loam (pH 7.2) were, respectively, 4.5 and 3 days. Under the same conditions, Santa Cruz loam (pH 5.1) required 12 and 8 days. Thus, either metabolism compliments chemical breakdown or sterilization has somehow retarded the dominant chemical hydrolysis pathway. In dilute aqueous solution (pH 7.0), the base-catalyzed hydrolysis is 50% complete in < 12 days. Getzin and Rosefield (1968) isolated a heat-labile soil organic matter fraction which catalyzed malathion degradation. This substance, corresponding approximately to humic acid, may explain the markedly faster loss of malathion, dichlorvos, Ciodrina, and mevinphos in gammairradiated soils as compared to autoclaved soils. In the studies previously described (Konrad and Chesters, 1969; Konrad et al., 1969), soil sterilization was also by irradiation. Dimethoate, parathion, and G S 13005 were apparently unaffected by the heat-labile substance. There exists yet another mechanism of pesticide degradation in soils which may be influenced by soil sterilization techniques. The reaction with free radicals in soils was considered by Kaufman et al. ( 1 968) and Plimmer et al. ( 1 967) to be responsible for amitrole degradation. Electron

BEHAVIOR OF PESTICIDES IN SOILS

179

paramagnetic resonance measurements have also indicated the existence of free radicals in soils (Steelink and Tollen, 1967). Free radical content may be reduced by autoclaving but increased by gamma-irradiation. Thus an alternate explanation of Getzin and Rosefield's results ( 1968) would be creation of more highly reactive free radicals during soil sterilization, a sufficient number of which remain to decompose malathion and other insecticides. They would be destroyed at high temperatures and therefore appear "heat-labile." Malathion (Konrad et al., 1969) and Ciodrin@ (Konrad and Chesters, 1969) degradation may also have been promoted by the free radical process. Some metallic ions, Cu2+ in particular, catalyze the nonenzymatic hydrolysis of organophosphates (Mortland and Raman, 1967). Mortland and Raman found the ease of Cu2+-catalyzedhydrolysis to be Dunban@ > diazinon > ronnel B ZytronB. They postulated the two most active molecules underwent coordination with Cu2+,as shown with Dursbanm:

The strength of Cu-exchanger bonding was very important in that Cumontmorillonites were quite active in insecticide hydrolysis while Cusaturated beidellite, nontronite, and vermiculite were rather ineffective and Cu-organic soil was without hydrolytic activity. Formetanate, a new acaricide, is rapidly decomposed in alkaline soil (pH 8.0) to rn-formaminophenyl-N-methylcarbamate,m-formaminophenol, and rn-aminophenol (Arurkar and Knowles, 1970). Since these were also predominant after formetanate was incubated 4 hours with Tris-HCI buffer (pH 7.4), the decomposition in soil is likely chemical as well. Soil may, however, reduce the rate of hydrolysis. Transformation of a new herbicide RH-3 15 (Kerb@)occurred first by cyclization, then by subsequent hydrolysis as shown (see p. 180) (Yih et al., 1970). Reaction rate increased greatly as soil temperature was increased from 5" to 37"C, perhaps explaining RH-3 15's superior performance in cool weather in the field. It also varied widely among soils. In aqueous solution the cyclization is acid- or base-catalyzed while the hydrolysis reaction is only acid-catalyzed. cis- and trans- 1,3-DichIoropropene, nematicides, are hydrolyzed up to 3-fold faster in moist soil than in solution. The products are the corre-

180

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

sponding 3-chloroalkyl alcohols (Castro and Belser, 1966). In the field, degradation may be slower since the compounds persisted at least 8 months in slightly acidic soils (I. H. Williams, 1968a).

One of the newer herbicides, WL 9385, is reduced by a zero-order reaction to its 2-amino analog (V) in soils or clay (Barnsley and Gabbott, 1966). Very little conversion occurs on air-dry soil. Besides the relatively persistent 2-amino product, small amounts of 2,4-diamino-64-

butylamino-s-triazine (VI) and other products occurred, presumably from microbial activity (Beynon and Wright, 1969). The chemical hydrolysis in soils of atrazine and other chloro-striazine herbicides was first reported by Armstrocg et al. (1967) and C. I. Harris ( 1967a). Conversion to their nonphytotoxic 2-hydroxy-s-triazines represents a detoxication mechanism. Acid and alkaline hydrolysis of chloro-s-triazines was known in solution (Gysin and Kniisli, 1960; Horrobin, 1963); Armstrong et al. demonstrated increased atrazine hydrolysis as soil pH decreased. The mechanism of soil catalysis appears directly related to the extent of atrazine adsorption (Armstrong and Chesters, 1968), perhaps by carboxyl groups in soil organic matter. Protonation of or hydrogen bond formation to a ring nitrogen in the triazines should facilitate nucleophilic displacement of the chlorine atom.

BEHAVIOR OF PESTICIDES IN SOILS

181

Thompson ( 1968) noted that adsorption of 2-chloro-s-triazines onto Hhumic acid was accompanied by hydrolysis at 7 0 T , but little occurred at room temperature. This is somewhat surprising since cation exchange resins caused hydrolysis of both chloro- (Armstrong and Chesters, 1968) and methoxy-s-triazines (Weber et al., I968b). Increased atrazine degradation as a function of soil temperature has been frequently seen (McCormick and Hiltbold, 1966; Hance, 1967; Obien and Green, 1969; Roeth et al., 1969). Based on spectroscopic evidence, montmorillonite clay caused the protonation and subsequent hydrolysis of chloro-striazines (Russell er al., 1968b; Brown and White, 1969). The resulting hydroxytriazine was thought adsorbed as a ring-N-protonated, keto tautomer. Hance ( 1969c) extrapolated chemical hydrolysis data obtained at 95°C and estimated half-lives of 5.2, 10.7,3.2, and 6.3 years, respectively, for atrazine, chlorpropham, diuron, and linuron at 20°C. Hydrolysis increased as the soil : solution ratio increased, suggesting that leaching and other processes which increased pesticide dispersion would also increase their rate of chemical degradation. Other recent studies (Obien and Green, 1969; Roeth et al., 1969) indicate atrazine loss is much more rapid than Hance’s estimate, but the herbicide presumably was subject to biological attack as well. In addition to hydrolysis, triazines readily undergo other nucleophilic substitions in normal chemical systems and these may be overlooked reactions in soils. For example, dyrene reacted with more than 60 amino acids, peptides, and related high-molecular weight compounds (Burchfield and Storrs, 1957, 1958). Reactions with thiols or amino groups may involve only their ionized forms; reaction rates were thus high near the pK of a reacting group. Similarly reactive functional groups probably occur in soil organic matter, perhaps contributing to “irreversible” adsorption of triazines. Although the extent of adsorption was directly related to atrazine hydrolysis (Armstrong and Chesters, 1968), an opposite relationship apparently exists with dichlobenil (Briggs and Dawson, 1970). The rate of dichlobenil hydrolysis to 2,6-dichlorobenzamide was inversely related to its partition coefficient, so that higher soil organic matter content protects the dichlobenil from decomposition. They believe the slow reaction to be chemical, whereas others (Verloop and Nimmo, 1970) ascribe it to microbial metabolism.

B. MICROBIAL METABOLISM Microbial metabolism represents a major route of degradation for many pesticides. The factors tnat render a pesticide molecule biodegradable

182

CHARLES

s. HELLING, PHILIPc . KEARNEY, A N D MARTIN ALEXANDER

are not well understood. Slightly soluble, highly chlorinated pesticides are generally most recalcitrant to microbial attack. The chlorinated hydrocarbon insecticides fall into this category. Introduction of polar groups such as OH, NH2, : N-C(O)-, COO-, NO2, and others, common to many pesticides, often affords microbial systems a site of attack. The rate of the degradation reaction is further modified by steric and electronic factors on neighboring atoms. Catalysts facilitating these reactions are induced and constitutive microbial enzymes. Some microbes metabolize certain compounds only in the presence of other energy sources, and the process of cometabolism is thus recognized as an important mechanism for certain pesticides. The ultimate objective of the organisms degrading these pesticides is to obtain usable energy (- AF) for other life processes. The initial reactions of many pesticides often require an expenditure of energy from the standpoint of the microbe. Only when the pesticide is fragmented to compounds that can be channeled into oxidative cycles, e.g., the Krebs cycle, does the organism derive any useful energy. Whereas the mechanisms by which microbes degrade pesticides are still under intensive study, the climatic and edaphic factors favoring metabolism are well understood. Warm soil temperatures, adequate moisture and the presence of organic matter generally promote microbial activity and, consequently, metabolism of pesticides. Moisture levels often play an important role in governing both rate and direction of microbial metabolism. Reduction of nitro groups and displacement of C1 by H represent alternate reactions which may be encountered under anaerobic conditions. These reactions are also usually more rapid than the oxidative pathways occurring in aerobic conditions. Where appropriate, the microorganisms, major metabolites, and edaphic factors pertinent to the metabolism of many pesticides are spelled out in the subsequent sections. 1 . Insecticides

The major thrust of metabolic work conducted on insecticides has been in insects, plants, animals, and to lesser extent, soils. Lichtenstein at Wisconsin has probably been the pioneer in soil-insecticide metabolic research. In recent years, the field has rapidly expanded due to environmental pressures and the need to accumulate residue information for registration purposes. Much of the present environmental controversy centers around DDT. This life-giving compound to millions of people in malaria ridden regions of the world has the unfortunate capacity to move from the intended site of application and accumulate in biota. Most biological systems cannot cope with the molecule, and so it progresses, es-

183

BEHAVIOR OF PESTICIDES I N SOILS

sentially undegraded, into higher members of most food chains. In contrast the organophosphorous and methyl carbamate insecticides are degraded fairly rapidly in soils, in part by chemical reactions. Most metabolic studies with D D T and the cyclodiene insecticides are highly selective, since these insecticides degrade very slowly in nature. Rates of degradation under laboratory conditions are therefore unrealistic when these same compounds are known to persist for several years in soils. a. DDT. Although D D T is the insecticide most widely studied in the environment from a residue standpoint, the exact route by which it is fully degraded in soils is still obscure. Studies with microbial systems have shown only partial degradation with most of the systems involved. Partial degradation in this context is defined to mean the transformation of one organic compound to another and not the complete conversion to inorganic end products. The two partial degradation products of D D T most frequently detected in the environment are D D D (TDE) and DDE:

Q

CI

CHCCI,

ci

Q

c1

Q

c=cCI,

CH-CHCII

ci

a' p , p'-DDT

Ct

DDE

DDD

The degradation product of DDT most frequently encountered in soils is DDE. It forms by dehydrohalogenation of DDT and is mediated by an enzyme system described in great detail (Lipke and Kearns, 1960). Studies with deuterated DDT show that D D D and DDE are not sequental metabolites in the same pathway, but arise independently from DDT (Plimmer el al., 1968). In soils, D D T is rapidly converted to D D D under anaerobic conditions and very slowly to DDE under aerobic conditions. Guenzi and Beard (1968) compared the disappearance of DDT in Pawnee silt loam samples incubated anaerobically and aerobically. After 12 weeks, < 1% of the applied DDT was recovered in anaerobic soils amended with alfalfa, and only D D D plus trace amounts of six other degradation products were detected. After 6 months 0.f aerobic incubations 75% of the D D T was recovered and a maximum of 4% DDE plus a trace amount of D D D was detected during the incubation period.

184

CHARLES s. HELLING, P H I L I PC . KEARNEY, A N D M A R T I N ALEXANDER

Bacteria and certain fungi are highly effective in converting DDT to DDD, especially under anaerobic conditions. D. W. Hill and McCarty (1967) conducted an extensive study on the anaerobic degradation of selected chlorinated hydrocarbon pesticides by sewage sludge. Active cultures of anaerobic methane-producing and sulfate-reducing bacteria rapidly converted DDT to DDD when injected into anaerobic sludge held at 35°C. Under aerobic conditions, DDT persisted unchanged. Subsequent degradation of DDD at a concentration of I ppm followed characteristic first-order kinetics with a half-life of about 4 days. When DDT was injected into the same anaerobic culture daily at 1 ppm for 57 consecutive days, DDT was converted to DDD in a period of 2 days and was not detected thereafter. Larger doses of DDT ( I 00 ppm) injected into the same sludge resulted in a slower degradation of the DDD. Several bacteria have been isolated from animal systems which can rapidly convert DDT to DDD including Proteus vulgaris from DDTresistant mice (Barker and Morrison, 1965); Escherichia coli and Aerobacter aerogenes from the intestines of rats (Mendel and Walton, 1966); and Serratia marcescPns, E. coli, and an unidentified strain from the excrement of flies (Stenersen, 1965). Chacko and his associates (1966) were the first to demonstrate the ability of certain aerobic soil fungi, Nocardia eryrhropolis and five species of streptomyces, to convert DDT to DDD. The maximum conversion to DDD by these systems was about 25% in 6 days, and occurred only during the active growth phase of the organisms. An extensive list of microorganisms metabolizing DDT to DDD and in some cases DDE, is shown in Table 11. TABLE I 1 Microorganisms Metabolizing DDT to DDD" Achromohactrr sp. Aerobuctrr ac~rojirties Agrohacterirrtn /rrmq/ucietu Bacillus cereus Bacillus cereus var. mycoides Bacillus subtilis Clostridium pasteurianum Clostridiuni prrjiingens Corynebacterium miclrixanense Escherichia coli Erwinia amylovoru Erwinia ananas Erwinia carotovora Erwinia chrysanthenii

" After Menzie ( I 969).

Kurthia zopB Pseudomonas aeruginosa Pseudomonas juorescens Pseudomonas glycinea Pseudomonas marginalis Pseudomonas morsprunorun Pseudomonas syringae Pseudomonas tabaci Streptococcus bovis Streptococcus durans Sfreprococcus faeculis Streptococcus ,fuecium Streptococcus liquefaciens Streptococcus zymogenes

BEHAVIOR OF PESTICIDES IN SOILS

185

The mechanism of reductive dechlorination of DDT to D D D has been studied in a number of isolated systems. Wedemeyer ( 1966) working with a cell-free system from A . aerogenes obtained about 70% conversion to DDD. The addition of carbon monoxide or 0.001 M cyanide completely inhibited the conversion to DDD. Consequently, Wedemeyer suggested that reduced cytochrome oxidase was probably the cellular agent responsible for reductive dechlorination. I t should be pointed out, however, that nonbiological processes are also apparently important in the reductive dechlorination of DDT. Ecobichon and Saschenbrecker ( 1967) showed that heparinized chicken blood containing DDT was slowly converted to DDE and D D D within I2 weeks even though the samples were sealed and stored at -20°C. Plasma samples containing D D T showed no evidence of degradation under identical conditions. They concluded that tissues and microorganisms which contained large quantities of reduced coenzymes, porphyrins. and other metalloproteins could carry out these steps by simple redox reactions. Dilute solutions of iron porphyrins exposed to DDT at room temperature are rapidly oxidized. This observation lead Castro (1964) to suggest that DDT may interact with an iron center in the respiratory chain and consequently might be one mechanism of toxicity in susceptible species. Miskus et cil. (1965) have also investigated the role of reduced porphyrins in the conversion of DDT to DDD. Addition of sodium dithionite to a solution of hemoglobin containing DDT-14C resulted in a conversion of 60-75% of the insecticide to D D D at room temperature. Evidence supporting enzymatic reductive dechlorination of DDT has recently been presented by A. L. French and Hoopingarner ( 1970). Membrane fractions obtained by lysozyme treatment of E . coli cells in the presence of exogenous FAD (flavin adenine dinucleotide) produced substantial amounts of DDD. The cytoplasmic factor alone or in the presence of boiled membrane fraction was completely inactive. The addition of NAD (nicotinamide adenine dinucleotide), NADP (nicotinamide adenine dinucleotide phosphate), ADP (adenosine diphosphate), inorganic phosphate or the Krebs cycle intermediates, malate and pyruvate. did not enhance D D D production over the membrane fraction alone. With this system, reductive dechlorination was dependent on reduction of FAD and occurred only under anaerobic conditions. A large number of metabolites of D D T have been detected in mammals and insects exposed to DDT. Typical of some of the schemes proposed for subsequent metabolism of DDT, Wedemeyer (1967) working with whole cells or cell-free extracts of A . aerogenes has proposed the following pathway for the oxidation of D D T to 4,4’-dichlorobenzophenone (DBP), where R is the 4-chlorophenyl group:

186

CHARLES s. HELLING, P H I L I Pc . KEARNEY, AND MARTIN ALEXANDER

DDA

DBP

Only recently, however, have any attempts been made to study the subsequent metabolism of intermediate products resulting from D D T metabolism. Focht and Alexander ( 1970) have examined ring cleavage of metabolites known to be generated from D D T as well as structural analogs by a Hydrogenomonas sp. isolated from sewage. Diphenylmethane, benzhydrol, and p-chlorobenzhydral were utilized for growth of the organism, but DDT and DBP could not sustain growth. Metabolism of diphenylmethane led to aromatic ring cleavage and the production of phenylacetic acid. Two structural features that inhibited metabolism of the D D T analogs by the Hydrogenomonas sp. were para-chlorine substitution on the phenyl rings and substitution of a carbonyl or trichloromethyl group on the carbon atom binding the two phenyl groups. The rapid disappearance of DDT under anaerobic conditions has prompted several investigators to suggest that flooding DDT-contaminated soils might be a feasible means of decontaminating soils with high residue levels (Guenzi and Beard, 1967; Kearney et al., 1969d). Although investigations suggest this approach to removing residual D D T from field soils has some merit, the feasibility and exact mechanism by which loss occurs is still not well understood. The use of specific soil fungi to degrade DDT residues in soils has also met with little success (Anderson et al., 1970). Mucor alternans partially metabolized DDT, within 2-4 days in shake cultures, to three hexane-soluble and two watersoluble products. These products could not be identified as any known metabolites of DDT, including DDD, DDE, DBP, bis@-chloropheny1)acetic acid (DDA), or several others. Addition of M . alternans spores to DDT-contaminated silt loam resulted in loss of this capacity of the fungus to degrade DDT. b. Cyclodienes. The cyclodiene insecticides, including aldrin, chlordane, endrin, dieldrin, and heptachlor, are generally recognized, along with DDT, as the most persistent organic pesticides in the environment. In soils, these insecticides are dissipated slowly by a number of processes including microbial metabolism. Owing to a number of factors, however, microorganisms indigenous to most soils cannot adapt their enzyme systems to rapidly transform the cyclodiene insecticides. Consequently, most pathways show “partial degradation” routes, similar to the pathway outlined for DDT.

BEHAVIOR OF PESTICIDES IN SOILS

I87

Aldrin is oxidized to dieldrin in soils (Menzie, 1969). Both the parent compound and the epoxide are insecticidal; consequently, the biological activity of aldrin persists, in part, by formation of dieldrin. Epoxidation is mediated by soil microorganisms as indicated by Lichtenstein and Schulz ( I 960), who worked with sterile and nonsterile soils and found that aldrin was converted to dieldrin substantially only in nonsterile soils. Subsequently, Lichtenstein et al. (1963) showed that the conversion of aldrin to dieldrin in soil was inhibited by the additions of synergists at relatively high rates, and that inhibition paralleled a decrease in microorganism population. Detailed studies on the elucidation of specific microorganisms involved in the conversion of aldrin to dieldrin have been reported by Tu et al. (1968). Most of the 92 pure cultures screened for aldrin-degrading activity showed some capacity for converting aldrin to dieldrin. Trichoderma spp. were the most active fungi effecting epoxidation. In addition, several Trichoderma spp. appeared to metabolize the dieldrin to other products. Among the other fungi examined, Fusarium and Peniciflium were effective converters of aldrin to dieldrin. Actinomycetes were also effective converters. The most active isolate, Fusarium sp., oxidized about 9.2% of the added dieldrin during the 6-week incubation period. It is possible to lose both aldrin and dieldrin from sterile nutrient agar in petri dishes (Lichtenstein et al., 1968). Loss occurred by volatilization (see Section 11, A, 2, b) and amounted to about half of the added aldrin during the first day of incubation. Dieldrin volatilized more slowly and at a constant rate. Disappearance was considerably retarded by bacterial or fungal growth on the agar plates. A number of partially degraded metabolites of dieldrin have been isolated and tentatively identified from culture solutions of a Pseudomonas sp. and from soils previously amended with the insecticide (Matsumura et al., 1968). The major metabolites reported were aldrin and a number of ketonic structures, an aldehyde, and an acidic compound formed by loss of a carbon from the ring to which the epoxide function was formerly attached. A proposed dieldrin degradation pathway carried out by soil microorganisms is shown in Fig. 3. Heptachlor is converted to heptachlor epoxide in soils (Barthel et al., 1960; Gannon and Bigger, 1958; Lichtenstein and Schulz, 1960; Murphy and Barthel, 1960; A. T. S. Wilkinson et al., 1964; Young and Rawlins, 1958). Although it was assumed that soil microorganisms were responsible for the conversion of heptachlor to its epoxide in soil, only recently have the causative organisms been isolated and identified. Thirty-five of 47 fungi and 26 of 45 bacteria and actinomycetes isolated from soil produced the epoxide (Miles et al., 1969). Conversion to heptachlor epoxide was

CHARLES s. HELLING, P H I L I P c. KEARNEY, AND MARTIN ALEXANDER

188

produced by cultures of Rhizopus, Fusarium, Pencillium, Trichoderma, Nocardia, Streptomyces, Bacillus, and Micromonospora. Heptachlor is chemically hydrolyzed to 1-hydroxychlordene (Section 11, A, 4, b), which

&

CI

CI

CI

&c

CI

2 OH

FIG.3. Dieldrin metabolism by soil microorganisms, according to Matsumura et al. (1968).

is subsequently epoxidized to 1 -hydroxy-2,3-epoxychlordene(VII) by microbial activity. Bacterial dechlorination of heptachlor produces chlordene, which also undergoes microbial epoxidation to form the corresponding chlordene epoxide (VIII). Pathways showing epoxidation, hydrolysis, and reduction of heptachlor are shown in Fig. 4.

BEHAVIOR OF PESTICIDES IN SOILS

I89

Residue studies suggest that 1-hydroxychlordene may be a more prevalent metabolite than heptachlor epoxide in certain soil types (Carter and Stringer, 1970). Extracts of a Quincy loamy fine sand from Oregon 3

&OH

.o

h &OH

CI

CI

a

CI

CI

CI

(VII)

I -Hydroxychlordene

& & ___t

CI Cl

CI

CI

c1

CI

Heptachlor Heptachlor epoxide

-

CI

CI

a

a Chlordene

(VIII)

FIG.4. Heptachlor metabolism and chemical degradation in soils, according to Miles et al. ( 1969).

years after application of technical heptachlor contained about 60% of the insecticide as I -hydroxychlordene. Negligible amounts of l-hydroxychlordene, however, Were detected in Lebanon silt loam from Missouri, Cataula loamy sand from South Carolina, Makalopa clay from Hawaii, and Lakeland sand from Florida. By comparison, heptachlor epoxide was

190

CHARLES s. HELLING, PHILIP c . KEARNEY, AND MARTIN ALEXANDER

detected less frequently and generally in lower concentrations than the 1-hydroxychlordene in these same soils. c. Lindane. Lindane is the gamma isomer of hexachlorocyclohexane (y-BHC). In general, lindane is less persistent than DDT or the clorinated cyclodiene insecticides. The conversion of lindane to y-pentachlorocyclohexene by dehydrochlorination in moist soil was attributed to soil microorganisms (Yule et al., 1967). The bacteria Clostridium sporogenes and Escherichia coli, produce trace amounts of benzene and chlorobenzene from lindane (Allan, 1955). Further fragmentation and even ring cleavage of lindane was suggested from C o n studies in submerged soils (MacRae et al., 1969). Anaerobic metabolism of lindane by a Clostridium sp. produced a metabolite that could not be identified as y-pentachlorocyclohexene (Sethunathan et al., 1969). Reductive dechlorination, in which one chlorine is replaced by a hydrogen atom, was proposed as the reaction mechanism. The product of the reaction, however, is still under investigation. The conversion of lindane to other isomers of hexachlorocyclohexane has been reported under submerged conditions (Newland et al., 1969). They estimated that 15% of the y-BHC was converted to the a-BHC under aerobic conditions, whereas 90% of the added yBHC was converted to the alpha and delta isomers under anaerobic conditions in simulated lake impoundments, after incubation for 88 days. Volatilization, especially in the anaerobic impoundment, was a major source of loss. Recent experiments in four Philippine rice soils (Yoshida and Castro, 1970) confirm the rapid disappearance of lindane under flooded conditions. Degradation was most rapid in Casiguran sandy loam, where none of the parent insecticide could be detected after 1 month. Increased temperature and organic matter enhanced degradation; molecular oxygen, nitrate, and manganic oxide retarded lindane degradation. d . Organophosphates. Biological and nonbiological reactions are important in the degradation of phosphate insecticides in soils. Diazinon, parathion, phorate, and thionazin (ZinophosB) are used to control soilborne insects. Most organophosphorus insecticides are degraded fairly rapidly in soils, but the rates are significantly influenced by soil temperature, moisture content, and acidity. For example, Getzin (1 968) examined the persistence of diazinon and thionazin as a function of three temperatures, four soil moisture levels, and four pH levels in sterile and nonsterile Sultan silt loam. Higher temperatures and soil moisture levels accelerated decomposition of both insecticides. Thionazin degradation was faster in nonautoclaved soil than in autoclaved soil, while diazinon degradation was essentially independent of sterility. An increase in soil pH of 4.3 to 8.1 enhanced the biological breakdown of thionazin, ap-

BEHAVIOR OF PESTICIDES IN SOILS

191

parently by providing a suitable environment for microorganisms metabolizing this insecticide. Increasing soil acidity accelerated the nonbiological degradation of diazinon. Other investigators (C. R. Harris and Lichtenstein, 196 1 ; Lichtenstein and Schulz, 1964; Corey, 1965; Menn et al., 1965; Whitney, 1967) have all shown that higher soil temperature and moisture levels enhance the insecticidal loss either by accelerated microbial activity, chemical degradation mechanisms, or volatilization. Soil microorganisms have been implicated in the degradation of several organophosphorus insecticides. In probably the first studies on phosphate insecticide metabolism by isolated soil microorganisms, Ahmed and Casida (1958) examined the rates of degradation of several dialkyl phenylphosphates and phosphorothioates, dimefox, schradan, and phorate plus its sulfinyl and sulfonyl analogs by the yeast Torulopsis utilis, the alga Chlorella pyrenoidosa, and the bacteria Pseudomonas Jluorescens and Thiobacillus thiooxidans. The rate of hydrolysis, by Torulopsis and Chlorefla, was phorate > phorate sulfoxide P phorate sulfone. In addition, both organisms readily oxidized phorate to its respective sulfoxide (IX), but slowly converted this product to the phosphorothioate sulfoxide (X), with little or no formation of the sulfide or sulfone. Pseudomonas and Thiobacillus did not oxidize phorate, but hydrolyzed the compound. The various pathways involved in phorate metabolism are below: (Cz H,O)z P(S)SCH2SC2Hs

H/ (CIHSO)~P//S ‘OH

+

P h \

HSCHzSCzH,

(CzH*O)zP(O)SCHzS(O)C,H,

(XI

(Cz HSO)zP(SWHzS(O)CzHs

/

(Cz HsO)P(S)SCHz S(O)zC2HS

(XI)

In soil, phorate is oxidized to its sulfoxide (IX) and sulfone (XI) (Getzin and Chapman, 1960; Bache and Lisk, 1966; Lichtenstein, 1966). The oxidation products of phorate have been identified in Dunkirk sandy loam and Lordstown silt loam in a study to determine the reason for increased toxicity in phorate-treated soils with time (Dewey and Parker, 1965). None of the oxidative products were sufficiently toxic to account for the observed increase in toxicity in the assay organisms, Drosophila melanogaster and Musca dornestica. The persistence and degradation of phorate and its five oxidative analogs have been determined by Getzin and Shanks ( 1 970). All were rapidly oxidized to their respective sulfoxides and sulfones in Sultan silt loam. The unique reduction of phorate sulfoxide back to phorate in soil was first reported in this investigation.

192

CHARLES s. HELLING, PHILIP c . KEARNEY, A N D MARTIN ALEXANDER

Degradation of parathion was either (i) by hydrolysis to p-nitrophenol and diethylthiophosphoric acid, or (ii) by reduction to its amino form, depending on population of soil microorganisms (Lichtenstein and Schulz, 1964). Yeasts were reportedly responsible for the reduction of parathion in soil to aminoparathion. Bacteria apparently had no effect. Malathion was rapidly metabolized by a soil fungus, Trichoderma viride, and a bacterium, Pseudomonous sp., isolated from Ohio soils which had received heavy application of the insecticide (Matsumura and Boush, 1966). From these, soluble esterase enzymes were isolated which could hydrolyze malathion to the carboxylic acid derivative(s). In addition to the strong carboxylesterase activity of these microorganisms, some variants of T . viride exhibited high demethylation activity, suggesting that two pathways are involved in malathion metabolism. It should be noted that there is good evidence that hydrolysis of some of these same phosphate insecticides takes place by nonenzymatic reaction in solution cultures of isolated soil microorganisms (Section 11, A, 4,b). Malathion and diazinon, specifically, appear to degrade in this manner. Species of Pseudomonas, Arthrobacter, and Streptomyces isolated from diazinon enrichment cultures apparently attack the products of hydrolysis rather than the intact diazinon (Gunner, 1967). In sandy loam soil, dimethoate has a half-life of about 2 days when rainfall occurs after application, whereas the half-life is about 4 days under drought conditions (Bohn, 1964). The phosphate insecticide TemikB, CH3SC(CH&CH = NOC(0)NHCH3, has approximate halflives of 9, 7, and 12 days in Houston clay, Norwood silty clay loam, and Lakeland fine sand (Coppedge et al., 1967). The major product recovered from these soils after 12 weeks was the Temik sulfoxide. Oxidation of the sulfoxide to the sulfone was slow, and the overall degradation of TemikB in soils was found to be slower than in the cotton plant. The route of degradation of TemikB in soils, however, appears to be similar to the pathway in plants. Chlorfenvinphos metabolism has been examined in four soils maintained at 22°C for 4 months (Beynon and Wright, 1967). The proposed metabolic pathway for chlorfenvinphos is shown in Fig. 5. Extraction and separation of the chlorfenvinpho~-'~C by thin-layer chromatography implicated the following metabolites: desethyl chlorfenvinphos (XII), 1,2-diol 2,4-dichlorophenacyl chloride (XIII), 2,4-dichlorophenylethane(XIV), 2,4-dichlorophenyloxirane (XV), 1-(2,4-dichlorophenyl)ethanol1-01 (XVI), and 2,4-dichloroacetophenone(XVII). In high organic matter soils, the 2,4-dichlorophenacyl chloride accumulated to a maximum of 0.1 1 ppm after I5 weeks from an initial application of 8 lb/acre (Beynon et al., 1966).

193

BEHAVIOR OF PESTICIDES IN SOILS

O\

HCCl 0 F-O-P(OC2H5)l II

,CHIC1

F‘

I

CI

CI

HCCl

It

0

II

C-O-P-OC,H5

Q”w (XII) CI

Chlorfenvinfos

Cl

\

\

\

(XVI)

FIG.S. Chlorfenvinphos metabolism in soils, according to Beynon and Wright (1967).

2. Herbicides

A vast amount of research has been conducted on the metabolism of organic herbicides in soils. There are probably several reasons for the greater emphasis on the soil metabolism of weed killers. First, many preemergence herbicides exert their phytotoxic effect on the germinating weed, and consequently are applied directly to soils. The performance of these materials depends on their interaction with the soil environment.

194

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

Thus much early effort was directed toward learning how rapidly herbicides dissipate from soils and what role microbes play in this process. To overcome losses from volatility and photodecomposition on the soil surface, many herbicides are directly incorporated into soils to extend their selective action. Again it became important to know whether microbial metabolism negated any advantage gained from soil incorporation. I t is also reasonable to suppose that much early weed research work was conducted by agronomists, and their associations with soil scientists fostered more intensive research on herbicides in soils than that given insecticides. which classically have been the domain of the entomologist. Regardless of the direct or indirect reasons for the emphasis of this research, it is quite clear that the herbicides have received major attention from scientists engaged in metabolic research. An organized examination of insecticide metabolism is relatively simple, because the major insecticides can be classified under three major headings; in contrast, the herbicides are less easily grouped. At present, there are approximately I27 registered herbicides that fall into a number of chemical classes. Exhaustive treatment of these I3 or more categories is beyond the scope of this review and has recently been summarized in book form (Kearney and Kaufman, 1969). Consequently only important metabolites and recent advances are dealt with in this section of the text. a. Phenoxyafkanoic Acids. The phenoxy herbicides are probably the most thoroughly studied biocides in the soil environment. This important class of herbicides includes the well-known compounds 2,4-D, 2,4,5-T, MCPA, silvex, 2,4-DB and the lesser known members dichlorprop, sesone, 2,4-DEP, erbon, and others. A rather extensive list of organisms has been compiled which have been identified as metabolizing various chlorinated members of the phenoxyacetic acid family (Loos, 1969) and include species of Pseudomonas, Achromobacter, Flavobacterium, Corynebacterium, Arthrobucter, and Sporocytophaga. The list includes 14 bacterial species and 2 actinomycetes, some with the capacity to degrade more than one specific phenoxy herbicide. 2,4-D was metabolized by every organism described because it could be used as the substrate in the enrichment media. The major metabolic reactions associated with phenoxyalkanoic acids are shown in Figs. 6 and 7. Encompassed in these schemes are most of the significant reactions associated with microbial metabolism of both the intact and cleaved ring compounds. The major reactions include: (i) beta oxidation of the long-chain aliphatic acid moiety; (ii) ring hydroxylation; (iii) cleavage of the ether linkage; and (iv) ring cleavage. The beta oxidation pathway leads to phenoxyalkanoic acids of shorter chain lengths and proceeds by a series of well studied reactions (Fig. 6).

BEHAVIOR OF PESTICIDES IN SOILS

195

Support for the occurrence of this sequence of reactions for phenoxyalkanoic acids with a side chain of more than two carbons comes from studies by Webley et a f . ( 1958), Taylor and Wain ( 1962), Gutenmann et al. (1964), and Gutenmann and Lisk (1964). For example, Nocardia opaca produced phenylacetate from 4-phenoxybutyrate and 2-chlorophenoxybutyrate from 2-chlorophenoxycaproate (Webley et af., 1958). RCH2CH,CH,COOH CoASH

I 1

ATP

RCH2 CH2 CH, C( 0)SCoA

FAD

-2H

RCH,CH=CH-C(O)-SCoA

OH H20

I

J

RCH~CHCH~-C(O)-SCOA

NAD+ 0 II

!-2H

RCH~CCH~-C(O)-SCOA

CoASH RCH2COOH

I

+

CH,-C(O)-SCoA

FIG.6. Beta oxidation of long-chain phenoxyalkanoic acids by soil microorganisms

The crotonic acid derivative of 2,4-DB has actually been isolated in soils (Gutenmann and Lisk, 1964). The position of ring hydroxylation is influenced by chloro-substitution and the specific microorganism. Ring hydroxylation by Aspergillus niger of omega-substituted, nonchlorinated phenoxyalkanoates occurs in the ortho and para ring position and was first described by Byrde and Woodcock (1957). A major product of 2,4-D metabolism in cultures ofA. niger was the 5-hydroxy-2,4-D (XVI I]), and 5-hydroxy-MCPA was the major product from MCPA (Faulkner and Woodcock, 1964). The site of hydroxylation may be different with pseudomonads since 6-hydroxy-2,4-D and 6-hydroxy-MCPA were reportedly produced from 2,4-D and MCPA, respectively (summarized by Loos, 1969). Cleavage of the ether linkage is a microbial process mediated by several bacterial species. Various soil bacteria have been reported to produce 2,4-dichlorophenol (XIX) from 2,4-D, 4-chloro-2-methylphenol from MCPA. and 4-chlorophenol from 4-chlorophenoxyacetic acid (Bollag

196

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

et al., 1967; Fernley and Evans, 1959; Gaunt and Evans, 1961; Loos et al., 1967). The work of Helling et al. (1968) shows that cleavage occurs between the aliphatic acid side chain and the ether-oxygen atom. Phenoxy'RO-acetic acid was metabolized to phenolJxO by resting cells and cellfree extracts from a MCPA-adapted Arthrobacter sp., in an 02-requiring process. Another soluble enzyme preparation obtained from the Arthrobacter sp. catalyzed the cleavage of the ether linkage of 2,4-D to 2,4dichlorophenol (Tiedje and Alexander, 1969). A proposed pathway involves oxidation of the methylene carbon to form the a-hydroxy-2,4-D derivative (XX). The latter compound is presumably cleaved to yield 2,4-dichlorophenol and glyoxylate. Ring cleavage appears to proceed through the intermediate formation of catechols from corresponding phenols and subsequent ring opening to form a chloromuconic acid. Enzymatic production of 4-chlorocatechol (XXI) from 4-chlorophenol and 3,5-dichlorocatechol (XXII) from 2,4dichlorophenol required both O2 and NADPH (Bollag et al., 1968). Ultimately 2,4-D, MCPA, and 4-chlorophenoxyacetic acid were shown to yield their corresponding chloromuconic acids (Evans and Moss, 1957; Fernley and Evans, 1959; Gaunt and Evans, 1961). Enzymes isolated from an Arthrobacter sp. catalyzed the conversion of 4-chloro- and 3 3 dichlorocatechols to cis,cis-3-chloro- and cis,cis-2,4-dichloromuconic acids (XXIII and XXIV) (Tiedje et al., 1969). The chlorinated cis,cismuconic acids either rearranged to more stable isomers or lactonized with displacement of the @-chlorineatom to form 4-carboxymethylenebut-2-enolide (XXV) and 2-chloro-4-carboxymethylenebut-2-enolide (XXVI). By a cometabolism process, 3,5-dichlorocatechol was converted to 2-hydroxy-3,5-dichloromuconicsemialdehyde (XXVII) by resting cells of a benzoate-grown culture of Achromobacter sp. (Horvath and Alexander, 1970). A recent advance in 2,4-D metabolism deals with the transformation of chlorinated ring fission products. The detection of succinic acid-14C from ring-labeled 2,4-D suggested that chloromaleylacetic acid (cis-1chloro-3-ketobut- 1-ene-1,4-dicarboxylic acid) was an intermediate in the pathway (Tiedje et al., 1969). Enzymes isolated from Arthrobacter sp. were subsequently shown to convert the chloromaleylacetic acid (XXIX) and maleylacetic acid (XXVIII) to succinic acid (XXX) (Duxbury et al., 1970). The cofactors NADH or NADPH were required in substrate quantities to convert the maleylacetic acids. On the basis of these latest findings, the authors have proposed that the last phase of phenoxyacetate metabolism proceeds through the steps shown in Fig. 7. The latest piece of research marks a milestone in herbicide metabolic research. One is able to trace the complete pathway of 2,4-D metabolism

BEHAVIOR OF PESTICIDES IN SOILS

9 d N

X

3:

8sg8 v-v-v-v

197

2

.a x D

198

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN A L E X A N D E R

by piecing together the various fragments of information that have accumulated over the past 20 years from research conducted in various laboratories of Europe and the United States. The organisms, enzymes, intermediates, and even the mechanism in a few instances, have been identified and characterized. b. s-Triazines. The widely used s-triazine herbicides exert their phytotoxic effects primarily through soil incorporation as opposed to contact herbicides such as 2,4-D. Consequently, there was great impetus to understand their reactions in the soil environment. The usual approach of enumerating soil variables that enhanced both triazine decomposition and microbial activity pointed, a priori, toward bioactivations in soils (Knusli et al., 1969). Laboratory investigations also led to the same general conclusions based on sterile versus nonsterile soil studies (Burnside et al., 196 1 ; Ragab and McCollum, 196 1). In reality, however, it appears that the chloro-s-triazines are primarily degraded by purely chemical reactions in soils; they probably represent a classic example of a major class of herbicides degraded by this mechanism (see Section 11, A, 4, b). The metabolism of s-triazines by soil microorganisms has been the subject of several reviews (C. I . Harris et al., 1968; Knusli et al., 1969; Kaufman and Kearney, 1970). Soil microorganisms do attack the chloros-triazines and remove the alkyl side chains. For example, the soil fungus Aspergillus fumigatus metabolized only the I4C-ethyl groups of simazine while the ring portion remained intact (Kaufman et al., 1963, 1965). Couch et al. ( 1965) also demonstrated that only the ethyl groups of simazine were degraded, not the ring portion of the molecule. A number of products, including 2-amino-4-chloro-6-ethylamino-s-triazine and the completely dealkylated ammelide have been isolated (Kearney et al., 1965b). Atrazine degradation by several soil fungi has recently been demonstrated by Kaufman and Blake ( 1970). The fungi included Aspergillus fumigatus, A . Jlavipes, A . ustus, Rhizopus stolonifer, Fusarium moniliforme, F. roseum, F. oxysporum, Penicillium decumbens, P.janthinellum, P. rugulosum, P . luteum, and Trichoderma viride. Metabolism proceeded by dealkylation, and no ring cleavage occurred. Two degradation proand ducts isolated were 2-amino-4-chloro-6-isopropylamino-s-triazine 2-amino-4-chloro-6-ethylamino-s-triazine. Although N-dealkylation appears to be a major pathway for the chloros-triazines by soil fungi, the major route in soils appears to be formation of the 2-hydroxy-s-triazine ( C . I. Harris, 1967a; Skipper et al., 1967). Degradation of ring- and methylthi~-*~C-labeled prometryne has been examined in Hagerstown silty clay loam maintained under aerobic and flooded conditions (Plimmer et al., 1970a). After 6 months, 77% and 86%

BEHAVIOR OF PESTICIDES IN SOILS

199

of the initial ring-I4C were present in the aerobic and flooded soils, respectively. Of the methylthio-lT, 3 3 % and 60% remained. Prometryne sulfoxide, prometryne sulfone, and hydroxyprometryne plus an unidentified compound were detected as degradation products. On the other hand, degradation of prometryne, simetryne, and various chloro- and methoxys-triazines in pure cultures of Aspergillus fumigatus appeared primarily by N-dealkylation (Kaufman and Plimmer, 197 1). Bioassay of microbial cultures treated with prometryne indicated the herbicide was also metabolized by Aspergillus niger, A . tamaru, A . Jlavus, and A . oryzae (Murray and Rieck, 1968). c . Phenylureas. Early investigations on the urea herbicides indicated that conditions favorable for microbial metabolism, i.e., high temperature, organic matter, and adequate moisture content, favored inactivation in soils. Other indirect evidence implicating microbial degradation was obtained from a comparison of sterile and nonsterile soils (Geissbuhler, 1969). Probably the earliest attempt to isolate soil organisms capable of decomposing phenylureas originated with G. D. Hill and his associates at duPont ( 1955). They isolated a Pseudomonas sp. which utilized monuron as a sole source of carbon as measured by manometric techniques. Subsequently, G . D. Hill and McGahen ( 1 955) isolated bacterial species of Xanthomonas, Sarcina, and Bacillus, and two fungi, Penicillium and Aspergillus, which utilized monuron as a sole source of carbon. Recent work from du Pont scientists (Belasco and Langsdorf, 1969) deals with the metabolism of siduronJT .in soils and by isolated organisms. Only ca. 50% of siduron, applied to Keyport silt loam at 10 Ib/acre, was recovered after 4-5 months. Two Pseudomonas spp. metabolized 49% and 33%, respectively, of the siduron in nutrient solution cultures. A soil fungus metabolized 88% of the siduron in 130 days. Schroeder (1970) examined the ability of 8 1 fungi and 13 bacteria to decompose linuron, monolinuron, diuron, and monuron. Ninety-two of the 94 microorganisms were able to demethylate these herbicides. Aspergillus nidulans was one of the most effective isolates and decomposed 52.8% of the linuron in culture solutions. Seventy-eight of the 94 microorganisms were able to degrade these four herbicides to chloroanilines. The availability of phenylureas l4C-labeled in ring, carbonyl and methylamine positions permitted detailed metabolic studies that led to a complete elucidation of the pathway and ultimately the oxidative enzymes responsible for the initial reactions. Although not entirely comparable, early metabolic studies in soils suggested that the carbonyl carbon appeared as COr prior to any other labeled carbon and that was followed by the methyl carbon ( G . D. Hill er al., 1955; Borner, 1965). The first

200

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

definitive work, by Geissbiihler et al. ( I963), showed that metabolism proceeded by successive removal of methyl groups followed by hydrolysis of the phenylurea to the corresponding aniline. Chloroxuron metabolism is shown as a representative example. Subsequently, Dalton et al.

fl

I1N-C-N

O 11 HN-C-N

,CH3

/

0

H

II

HN-C-NHI

\ 0

--

-

0

-

* o

- 0

CI Chlorox tiroii

(1966) described a similar sequence of reactions for diuron, based on their isolation of 3-(3,4-dichlorophenyI)-I-methylurea, 3,4-dichlorophenylurea, and 3,4-dichloroaniline. The N-methoxy group is more labile in culture solutions of Bacillus sphaericus than the N-methyl group (Wallnofer, 1969). Monolinuron, linuron, and metobromuron were metabolized within a short time by B. sphaericus, whereas monuron, diuron, fluometuron, and methabenzthiazuron seemed to be resistent to decomposition. Recently, Tweedy et al. (1970) have examined the metabolic fate of the aniline resulting from degradation of metobromuron. Pure cultures of Talaromyces wortmanii, Fusarium oxysporum, Bacillus sp., and Chlorella vulgaris rapidly acetylated p-bromoaniline to p-bromoacetanilide. The bacterial and algal species, however, could not metabolize the parent herbicide, metabromuron. The authors propose that acetylation is an alternate route to azobenzene formation, discussed with the carbamates in Section 11, B, 2, e. d. Aliphatic Acids. Only two herbicides in this class have ever been used extensively, dalapon and TCA. The fate of these two herbicides plus related halogenated acids in soils has been throughly reviewed (Foy, 1969; Kearney et al., 1965a; Leasure, 1964). Dalpon and TCA are degraded fairly rapidly in soils by microorganisms; the former disappears in about 2-4 weeks, the latter in about 4-8 weeks. The halogenated aliphatic acids have been a favorite class for structure versus activity studies. Increasing the number of halogens and the distance of the halide from the

BEHAVIOR OF PESTICIDES IN SOILS

20 1

carboxyl group are factors which tend to retard decomposition (Kaufman, 1966). Bacteria reported to metabolize dalapon or TCA include species of Bacillus, Pseudomonas, Agrobacterium, Arthrobacter, Micrococcus, Alcaligenes, and Flavobacterium. Enzymes have been isolated from an Arthrobacter sp. (Kearney et al., 1964) and a pseudomonad (Kearney et al., 1969a) which dehalogenate dalapon and TCA. In the case of dalapon, the product of the enzymatic reaction is pyruvic acid. e. Phenylcarbamates, Thiocarbamates, and Acylanilides. The carbamoyl group :N-C(0)- is common to this class of herbicides. and consequently they are treated together in this section of the review. As will be shown in the subsequent discussion, the carbamoyl linkage or the carbamate group is the initial site of hydrolysis. Representative herbicides subjected to metabolic studies in this group of compounds include propham, chlorpropham, and barban (phenyl carbamates); EPTC and pebulate (thiocarbamates); and propanil (acylanilide). The classical approach of examining soil variables, including sterile and nonsterile soils, suggested to early investigators that microbial metabolism was a major factor in degradation (Herrett, 1969; Fang, 1969). EPTC is probably metabolized by soil microorganisms, although bioassays show that release of 14C02from ethyl-labeled EPTC was slower than inactivation of the herbicide in soil (MacRae and Alexander, 1966; Kaufman, 1967). EPTC is a volatile substance, and consequently may disappear from the soil by vapor loss before microbial metabolism becomes a major mechanism. Several of the phenylcarbamates are also volatile, and may disappear before metabolic reactions fragment the molecule. Chlorpropham is degraded by soil bacteria identified as species of Pseudomonas, Flavobacterium, Agrobacterium, and Achromobacter (Kaufman and Kearney, 1965). An enzyme isolated from Pseudomonas striata cleaved the carbamate linkage to yield 3-chloroaniline, COz, and isopropanol (Kearney, 1965). The discovery that certain methylcarbamate insecticides, when mixed with chlorpropham in soil, would prolong the herbicidal activity suggested some interaction between the carbamates (Kaufman et al., 1970). Subsequent enzymatic studies showed that carbaryl was a competitive inhibitor of the purified chlorpropham-hydrolyzing enzyme. This knowledge has been applied to practical situations, where the herbicide chlorpropham does not persist long enough in soils to exert full season control of specific weeds. Commercial applications of the mixed herbicide-insecticide combination are now under examination as a possible mode of regulating the persistence of chlorpropham by combination with certain methyl carbamates. In addition to attempting to regulate persis-

202

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

tence by mixtures, a detailed study of molecular parameters that influence biodegradability was made (Kearney, 1967). Propanil, a rice herbicide, has been the subject of numerous metabolic investigations, primarily because unusual, and frankly unanticipated products resulted from 3,4-dichloroaniline. The pathways of propanil metabolism are shown in Fig. 8. Propanil is hydrolyzed by an enzyme isolated from a Penicillium sp. by Sharabi et al. ( I 969). The Penicillium enzyme was actually enriched on KarsilB, an acylanilide closely related

2.1

ci

2.1

(XXXIII)

t I

Adsorption to soil particles

Ci

\

(XXXII)

C1

t

1

CH3CH2COOH

3

!oz

col Cl

(XXXIV)

FIG.8. Propanil metabolism by soil microorganisms.

BEHAVIOR OF PESTICIDES IN SOILS

203

to propanil. The latter enzyme hydrolyzes a large number of structurally related anilides and certain preferred structures, favoring hydrolysis, were illustrated by these studies. In light of previous work, the metabolism of propanil to 3,4-dichloroaniline (XXXI) was not altogether surprising. What was surprising, however, was the nature and structure of some of the subsequent products. Bartha and Pramer (1967) isolated 3,3’,4,4’-tetrachloroazobenzene(XXXI I) - unexpected since condensation products are rare in soil metabolic studies. The implication that the azobenzene was related to a series of compounds of known carcinogenic properties prompted a detailed investigation of this class of products. Bartha et al. (1968) measured the ability of several mono- and dichlorinated anilines to form corresponding chlorinated azobenzenes. Orthosubstituted anilines failed to form azobenzenes. The enzyme peroxidase catalyzes the condensation reaction from two moles of 3,4-dichloroaniline (Bartha and Bordeleau, 1969: Bartha et al., 1968). The azobenzene was not detected in soils treated for 12 consecutive years with 2 and 4 Ib of diuron per acre (Belasco and Pease, 1969). The metabolism of the phenylureas is probably slower, and consequently aniline concentrations do not accumulate rapidly in soils. A more complex metabolite was isolated from Nixon sandy loam after high applications of propanil and was identified as 4-~3,4-dichloroanilino)-3.3’,4’-trichloroazobenzene (XXX I I I ) (Linke and Bartha, 1970). This latter product had previously been isolated from a photochemical reaction of 3.4-dichloroaniline and riboflavin 5phosphate (Rosen et al., 1970). A third high molecular weight metabolite isolated from a Japanese soil incubated with propanil was 1,3-bis(3,4dich1orophenyl)triazene (XXXIV) (Plimmer et al., 1970b). This rash of new metabolites probably raises some question about the significance of these materials in soil and their possible health-related significance. The work of Chisaka and Kearney (1970) suggests that these reactions are probably dose-response related phenomena that are not of major significance at normal rates of application. Rather, the adsorption of the aniline moiety to soil components is likely the dominant process. The ultimate fate in soils of metabolically produced anilines is not known. f. Dinitroanilines. The herbicides trifluralin, dipropalin, benefin and nitralin comprise a fairly recent class of dinitroanilines that are finding wide acceptance in weed control programs. Studies with trifluralin illustrate more clearly than any investigations conducted thus far the alteration in metabolic pathways as affected by aerobic and anaerobic conditions in soils. Under aerobic conditions, one might anticipate removal of one of the alkyl groups as a first step in the metabolism of trifluralin. The monopropyl trifluralin has been identified in soils in both field and laboratory studies (Probst and Tepe, 1969). Sequential removal of the second

204

CHARLES

s. HELLING, PHILIP c. KEARNEY, AND MARTIN ALEXANDER

propyl group occurs yielding the dealkylated product. Later steps in the aerobic pathway indicate reduction of the two nitro groups, eventually Under anaerobic condiforming 3,4,5-triarnino-cu,a,a-trifluorotoluene.

CF, Trifluralin

S02CH3 Nitrelin

tions, the nitro groups are first reduced, sequentially, before dealkylation occurs. The triamino derivative again appears as an intermediate common to both pathways. g . Dipyridyls. As discussed in Section 11, A, 1, b, the two dipyridyl herbicides, paraquat and diquat, are strongly adsorbed (and quickly inactivated) as organic cations onto soil particles. Nevertheless in soil enrichment cultures of an unidentified bacterium, paraquat was first demethylated, followed by ring cleavage to yield the carboxylated Nmethylpyridinium ion (Funderburk and Bozarth, 1967). Baldwin et al. ( 1966) have also isolated several microorganisms metabolizing paraquat, and specifically a yeast which utilizes paraquat as a sole source of nitrogen. No intermediate products were detected in these systems, however. A metabolic pathway for diquat has not been elucidated yet. h. Benzoic Acids. Several of the benzoic acid herbicides are rather persistent pesticides, and consequently have not been studied in solution culture work, owing to the difficulty of obtaining microorganisms indigenous to soils capable of metabolizing these herbicides. Therefore, some of the reactions proposed for benzoic acid metabolism are largely speculative, or based on reactions known to occur in plants. Dicamba conceivably loses its herbicidal activity by decarboxylation and/or demethylation of the methoxyl group. Neither of these products has been isolated. Dichlobenil is another aromatic herbicide less well studied from a metabolic standpoint in soils. One investigation revealed the presence of about equal amounts of dichlobenil and an oxidation product, 2,6-dichlorobenzoic acid, in one soil type (J. W. Smith and Sheets, 1967). In a more recent study, Verloop and Nimmo ( 1 970) examined the products resulting from dichlobenil maintained in a sandy soil for 8 months. More than half of the dichlobenil-14Capplied (2 ppm) had been metabolized, and 2,6-dichlorobenzamide plus three minor unknowns amounted for 95 % of

BEHAVIOR OF PESTICIDES IN SOILS

205

these metabolites. The benzamide is itself quite stable and 90% was recovered 6 months after a 2 ppm application. Chlorthiamid is converted to dichlobenil and thence to the benzamide in the field (Beynon and Wright, 1968). There is some question whether these transformations occur chemically or biologically (Section 11, A, 4, b). Chloramben (amiben) has been studied extensively in plants, and much is known about its persistence and physicochemical behavior in soils, but metabolic investigations in soils are limited. The microbial decarboxylation of chloramben was assumed by Wildung et al. (1968)to be the principal pathway of metabolism. Chloramben degradation in soils, as compared to, e.g., 2,4-D, remains imprecisely defined. In soils, DCPA undergoes a two-step hydrolysis of its methyl esters to yield the dicarboxylic acid, as measured by microcoulometric gas chromatography (Skinner el al., 1964: Gershon and McClure, 1966). Under field conditions the products are first, methyl 2,3,5,6-tetrachloroterephthalate, and then, 2,3,5,6-tetrachloroterephthalicacid. i. Arsenicals. Two organic arsenical herbicides of current interest are MSMA and cacodylic acid. MSMA-I4C was oxidized slowly to l4C0, in Hagerstown silty clay loam, with ca. 7% loss in 60 days (Von Endt et al.. 1968).The degree of MSMA oxidation in four other soils was directly proportional to organic matter content. Four isolated soil microorganisms metabolized MSMA to COz and inorganic arsenate (As5+).No arsenite (Asy+)was detected in the degradation process. The fate of inorganic arsenic is discussed elsewhere (Section IV, B). j . Miscellaneous. Bromacil and terbacil, two uracil herbicides, had a half-life of ca. 5-6 months on soils treated with radioactive herbicide at a rate of 4 Ib/acre. After one year trace amounts of residual activity

Bromcil

Terbacil

were present, primari,ly (90%) as the parent compounds (Gardiner et al., 1969).Four metabolites were detected: 5-bromo-3-sec-butyl-6-hydroxymethyluracil, 5-bromo-3-(2-hydroxy-1-methylpropyl)-6-methyluracil, 5bromo-3-(3-hydroxy- I-methylpropyl)-6-methyluracil,and an unknown. Neither 5-bromouracil nor 5-chlorouracil were found. Pyrazon is an important herbicide in sugar beet production. Drescher and Burger ( I 970)found little herbicide persistence in soils, and amounts

206

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

as high as 5000 ppm disappeared within 10-14 days. A major metabolite isolated from p y r a ~ o n - ' ~ was C identified as the dephenylation product, 5-amino-4-chloro-3(2H)-pyridazinone. The same metabolite was isolated by D. T. Smith and Meggitt (1970b), but they observed considerable dependence of persistence on edaphic and climatic factors. Higher organic matter and lower rainfall retarded herbicide loss, and field persistence was measured in months, not days. Diphenamid metabolism in soils resembles that of several other N , N dialkylamino pesticides. Demethylation occurs in sequence, producing first the monomethyl diphenamid (nordiphenamid) and then diphenylacetamide (Golab et al., 1968). The amide linkage is next cleaved to form diphenylacetic acid and several unknown metabolites. Exposure of herbicide-treated tomato plants to the soil fungi Trichodertntr iiride and Aspergillus candidus gave rise to both N-me t hyl-2,2-dip hen y lacet amide and 2,2-diphenylacetamide (Kesner and Ries, 1967). 3 . Fungicides

Historically the inorganic elements sulfur and copper have been used as fungicides to combat various plant diseases. Elemental sulfur was used to control powdery mildew in I802 (McCallan, 1967), but there is evidence for its use by the ancient Greeks. Bordeaux mixture [CuS04 Ca(0H)J has been used in France for many years on vineyard soils without any apparent residual phytotoxic effects. Copper is fixed in organic soils and consequently rendered inactive toward most plants. a. Thiocarbamates. In recent years, the organic fungicides have made a substantial contribution to plant disease control programs. These pesticides comprise a fairly diverse group of compounds, but their usage patterns are relatively small when compared to the insecticides and herbicides. A large family of dithiocarbamates and dimethyldithiocarbamates comprise an important class of fungicides. The compounds ferbam and ziram are the ferric and zinc salts of dimethyldithiocarbamate. Soil microorganisms as well as yeast cells form an amino acid adduct of sodium dimethyldithiocarbamate, identified as y-(dimethylthiocarbamoy1thio)-aaminobutyric acid (Kaars Sijpesteijn et al., 1962). The deaminated product, tentatively identified as the corresponding ketobutyric acid, was also detected. The disodium, manganese, and zinc salts of ethylene bis(dithiocarbamate) are known as nabam, maneb, and zineb, respectively. These materials are not stable in aqueous solution or soils, and their chemical degradation is discussed elsewhere (Section 11, A, 4, a). 6 . PCNB. Pentachloronitrobenzene (PCN B) is reduced to pentachloroaniline by a large number of soil microorganisms (Menzie, 1969).

+

BEHAVIOR OF PESTICIDES IN SOILS

207

Reduction is favored in soils by flooding (KOand Farley, 1969) and the resulting pentachloroaniline was reported to be stable in both moist and submerged soil. The formation of pentachloroaniline extends the activity of the PCNB in soils, since pentachloroaniline also shows some toxicity to Rhizoctonia solani. There is some evidence that pentachlorophenol is also a metabolite of PCNB (Menzie, 1969). c . Chloroneb. Chloroneb is slowly converted to a nontoxic metabolite in culture solutions of Rhizoctonia solani (Hock and Sisler, 1969). The metabolite was subsequently identified as 2,5-dichloro-4-methoxyphenol and apparently arises by cleavage of the O-CH, linkage by dealkylation. About 50% of the added chloroneb was degraded during the first 24 hours of incubation. Chloroneb was also metabolized to an unidentified product by Neurospora crassa. d. Mercurials. The mercury fungicides have come under critical examination in the United States after the recent unfortunate poisoning case in New Mexico and reports of methylmercury poisoning from Minamata and Niigata, Japan. Although the latter incidents were not caused by agriculture fungicides, nevertheless, the use of mercury compounds is being reevaluated in several nations. In soils, much of the mercury is lost, eventually, as vapors. When the nonvolatile phenylmercury acetate was applied to soil, it was microbially degraded to elemental mercury and lost as a vapor. Ethylmercury acetate appeared in the vapor phase as both metallic and organic mercury, while methylmercury gave methylmercury vapor and a trace quantity of mercury vapor (Kimura and Miller, 1964). The two mercury fungicides, 2-chloro-4-(hydroxymercuri)phenol and cyano(methy1mercuri)guanidine were shown to be inactivated by soil microorganisms (Spanis et al., 1962). The phenol was degraded by isolates of Penicillium sp. and Aspergillus sp. The guanidine was inactivated by several Bacillus sp. In soils, the more rapid decay of these two fungicides in nonsterile versus sterile samples suggests that biological factors are responsible for their degradation in the environment. A review of the mercury research in Sweden (Jernelov, 1969) shows that metallic mercury, inorganic divalent mercury, phenylmercury, and alkoxi-alkylmercury can all be converted to methylmercury. The latter compound undergoes biomagnification in the food chain, primarily in fish, and causes brain damage in humans consuming contaminated fish. Starting with metallic mercury, the first step is oxidation to the divalent mercury. This is a chemical reaction and takes place in the sediment layer of lakes and streants. The subsequent conversion of divalent inorganic mercury to methylmercury and dimethylmercury is a biological reaction.

208

CHARLES s. HELLING, PHILIPc. KEARNEY, AND MARTIN ALEXANDER

Microorganisms in river sediment can produce methyl- and dimethylmercury from divalent mercury under laboratory conditions. The reaction rate is enhanced by organic matter and increasing amounts of mercury in the sediment. A rapid rise in methylmercury content occurred when the concentration of inorganic mercury was increased from 1 to 10 ppm. Methyl- and dimethylmercury arise both under aerobic and anaerobic conditions. Under anaerobic conditions mercuric sulfide (HgS) may be produced, precipitating without forming the monomethylmercury. Ill. Effect of Pesticides on Soil Community

Pesticides are sought because they are toxic to specific groups of organisms. Although all these agents have a greater or lesser degree of specificity, it is not inconceivable that they may have an influence on the microbial or nontarget invertebrate residents of soil. Chemicals used as herbicides are chosen because of their effectiveness on weed species, but chlorophyll-containing plants from among the soil thallophytes might easily be affected as well. Insecticides reaching the soil, although screened for their usefulness in insect control, might well reduce populations of invertebrates and alter the composition of the faunal community. Fungicides are characteristically antimicrobial agents, and they are usually employed at high dosage rates, so toxicity to microscopic life below ground should come as no surprise. Because of their low specificities, the herbicides might well be detrimental to non-chlorophyll-containing genera, the insecticides to microorganisms, and the fungicides to components of the soil fauna. Tests to establish the possible influence of pesticides on the soil biota are of great importance. A compound inhibitory to the nitrifying bacteria would cause a diminution in the rate of nitrate formation; a plant relying on this anion as a nitrogen source might suffer, or leaching losses of nitrogen might decline. A chemical enhancing or suppressing carbon mineralization would make its presence known through the faster or slower pace of destruction of native soil organic matter or plant residues. A pesticide harmful to mycorrhizal fungi or Rhizobium might be undesirable because it prevented establishment of the mycorrhizal or root nodule symbiosis. Alternatively, a substance destroying the antagonists for a particular plant pathogen or harmful soil insect could be responsible for an increase in crop injury rather than the pest control that was initially sought. Hence, each new chemical that is introduced must be carefully investigated to determine whether it does harm to a segment of the soil community which is necessary for soil fertility, crop development, or pest-free plants. Some toxicity may be tolerable inasmuch as the benefit arising from pest con-

BEHAVIOR OF PESTICIDES IN SOILS

209

trol may far outweigh the detriment associated with the inhibition of the soil residents, but assessments of the relative gains or losses must always be made with considerable care. Unfortunately, an excess of repetitive work appears in this field of endeavor. Disruption of the soil community or a particular transformation by a few chemicals has been studied to such an extent that frequently no new, meaningful information is being obtained. Likewise the influence of dissimilar chemicals or other relevant questions concerned with pesticidecommunity interactions are entirely ignored. Some soil scientists are apparently more concerned with emphasizing the harm done - and among many of the chemicals so well studied, the toxicity cannot in fact be deemed consequential - than with establishing which of the available pesticides are safest to use in terms of soil fertility, crop production, and the maintenance of environmental quality. A number of difficulties are common to studies of the effects of pesticides on the subterranean biota. (i) Conditions in the laboratory are far different from those in the field, and fluctuations in temperature, soil moisture, or the presence of simple organic compounds excreted by a growing root undoubtedly modify the response of microorganisms or invertebrates. Environmental change is well known to alter the extent of inhibition. (ii) Despite the many advantages of using axenic cultures of fungi, bacteria, algae, or protozoa, it is extremely difficult to extrapolate from results obtained with such cultures to the natural habitat. Variability exists because of reactions between abiotic soil components and pesticides and because of the as yet largely unpredictable impact of neighboring species. (iii) A chemical added to soil at the extremely low levels often used for pest control is almost invariably not distributed homogeneously. Consequently, the concentration in one microenvironment may exceed a species’ tolerance while a short distance away individuals of the same species may be exposed to sublethal levels or remain wholly unexposed. (iv) A high percentage of pesticides are borne in nonaqueous solvents or carriers, and many of the biological responses attributed to the pest-control agent may in fact be the result of toxicity of the solvent o r the carrier. (v) Commercial formulations are far from pure, and some are notoriously contaminated. It is quite likely that a compound other than that on the pesticide label is the cause of the observed toxicity (Alexander, 1969). Various methods have been used to determine whether stimulation or inhibition of components of the soil community results from the introduction of pesticides. Some techniques show a detrimental effect when the pesticide is present in extremely low concentrations, while others only reveal an inhibition when the substance is present in a concentration

210

CHARLES S. HELLINQ. PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

far higher than that ever employed in agriculture. Some tests are designed to assess the response of a narrow group of organisms, while a few assess a possible change in a process catalyzed by a wide spectrum of species. A few of these techniques yield results of direct relevance to soil fertility and plant growth, but many yield information of ecological but not agricultural value. In general terms, these methods can be divided into four types: (i) Measurements of distinct processes in soil. These tests have included the following: formation of C 0 2or inorganic nitrogen from native soil organic matter, oxidation of ammonium to nitrate, reduction of added nitrate to Nz,nonsymbiotic Nzfixation in sugar-amended soil, O2uptake by unamended soil or samples receiving simple substrates, cellulose decomposition, formation of aggregates, or tests for selected “enzymatic” activities. (ii) Enumerations of the density of particular groups of organisms. The organisms counted in studies of pesticide effects include total bacteria, total fungi, Streptomyces, algae, cellulolytic bacteria and fungi, Azotobacter, Clostridium, Bacillus spores, mites, springtails, earthworms, aphids, nematodes, wireworms, and millipedes. (iii) Assessing a given response or change on some suitable plant species, as the appearance of nodules on legumes, formation of galls by nematodes, development of mycorrhizae, and colonization of roots by saprobic or pathogenic fungi. (iv) Tests involving a particular organism in enrichment or axenic cultures in liquid media or on agar. The procedure may entail measurements of growth rate, spore formation, cell yield, respiration, glycolysis, or the excretion of individual products. Among the microorganisms examined are: Aerobacter, Azotobacter, Nitrobacter, Nitrosomonas, Rhizobium, Rhodospirillum, Thiobacillus, and many other bacteria; actinomycetes; a large assortment of saprobic, mycorrhizal, and parasitic fungi; Saccharomyces species; Chlorella, Prototheca, Tolypothrix, and Scenedesmus among the algae; and Colpidium and Paramecium of the protozoa. The information obtained from each of these procedures depends on the response evaluated. An inhibition of the nodulation of legumes by Rhizobium must always be deemed significant, for the induction of nodulation by these bacteria is a necessary prelude to nitrogen fixation by the plant-bacterium symbiosis. Toxicity to mycorrhiza-forming fungi or to the initiation of mycorrhizal development must likewise be evaluated with care where these root associations are of importance to the prevailing flora or crop. Similarly, a suppression of nitrate formation may pose a serious problem for a plant which is a preferential nitrate-feeder. On the other hand, the significance in terms of soil processes or crop growth of

BEHAVIOR OF PESTICIDES IN SOILS

21 1

the results of many of the techniques widely employed is difficult to evaluate. Microbiological responses are easy to measure, but extrapolation to natural processes is often unquestionably difficult. Thus, it is not always clear what conclusions to draw from observations of a modest suppression in the numbers of cellulolytic bacteria, Azotobacter, a particular genus of nonpathogenic fungi, or a n individual category of invertebrates. The desire to maintain the biological equilibrium in soil for its own sake is praiseworthy, perhaps, but this desire must be tempered by the needs for producing food and feed. The enormous disturbance arising from changing virgin into cropped land is a greater ecological perturbation than that created by many of the pesticides. The issue at stake is not maintenance of a community for some abstract reason but rather maximizing productivity while minimizing environmental pollution. Any individual perusing the available literature is immediately struck by a conflict in the conclusions drawn. Two experimenters may use the same compounds and the identical techniques for measuring a response, but one concludes that there is no inhibition while the other states unequivocally that there is. The facile reader might attribute the differences to the use of dissimilar soils, and then prudence dictates that the more conservative conclusion is accepted, namely that toxicity does sometimes occur. It is impossible to evaluate many of the conclusions, however, because full details are not presented and a listing of controls is not given. Some of the suppressions reported clearly must be artifacts because of the phenomenally low pesticide concentrations that allegedly inhibit a group of normally nonsensitive organisms. The investigator is obliged to assess the biological changes taking place simultaneously in the absence of the pesticide formulation, those attributable to the solvent or carrier, the responses to major contaminating chemicals in the crude preparations commonly used in the field (and often also in the laboratory), and finally those specifically resulting from the pesticide itself. In excess of 500 papers now exist demonstrating that pesticides do, or do not, have an influence on a broad taxonomic category of soil microorganisms or invertebrates, a narrow taxonomic group, a process brought about by a small or a large array of underground inhabitants, or a particular species in culture media. A complete review is impossible, but a representative sample of findings is presented in Table 111. These findings must not be considered definitive because a concentration listed as toxic by one investigator has in some instances been reported as nondetrimental by a second; whether these differences arise from different soil types and communities or whether the experimental techniques are questionable is often difficult to establish. The kinds of responses that may be expected following the use of

212

CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTlN ALEXANDER

TABLE 111 Effect of Pesticides on Selected Organisms and Processes in Soil"

Pesticides Aldrin Ally1 alcohol Arsenite Atrazine Chlordane 2,4-D Dalapon Dazomet D-D@ DDT Demeton Diazinon Dieldrin DNOC EDB HCH Heptachlor Metham Methoxychlor Nabam PCP Simazine TCA Toxaphene

Toxic or Nontoxic Concentrationsb Legume ActinoInverteSoil Nitrifi- nodu- N mineralBacteria mycetes Fungi brates respiration cation lation ization 100 25'

500 70 100

25 34 150 5" 100

2SC

500 70 34 150 5" -

I00 2SC

500 75 100

25 34 150 5" 100

1500

1500

1500

40 100

40 -

40 100

200

200

200

1000

I00 60 100 50 2000

70 10 100

1000 2000

70 10 -

-

1000 100 60 100 50 500

70 10 100

13' 4/

300' -

63' -

-

70

512

500 512

1000

>U

150 23' 13 40 100

23p 1000 -

50 I50 150

133

50

-

33 20 50 75

-

100 100

100

64

64

60

60

-

5

29

4, 50 8 10 -

2 13 100

-

-

-

1000

23' 23e 435 -

-

-

" From data given in Alexander (1969), Braithwaite et al. ( 1958). Eno (1962), N. French et al. (1959), Fox (1964), and Koike (1961). Values given in parts per million unless otherwise indicated (2 Ib/acre considered as I ppm). Gallons per acre. Milliliters per kilogram. Nematodes. Earthworms.

herbicides and insecticides, the marked upset in the soil community usually associated with the use of fungicides and fumigants and the recolonization of these treated soils, selective toxicity to subterranean populations by these inhibitory agents, and the patterns of suppression of soil respiration, nitrification, nitrogen mineralization, and other transformations have been considered recently (Alexander, 1969) and in

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earlier reviews (Bollen, 1961 ; Kreutzer, 1963; Martin, 1963). Hence, little would be gained by repeating the information here once again. Rather, attention will be given to recent developments in studies of the effect of pesticides on the soil community or aspects not dealt with previously. There has been considerable recent interest in the changes in the fungus flora promoted by pesticides, especially among the plant pathogens. Alterations in species composition among the soil fungi resulting from the use of fungicides continue to attract interest, and marked changes are usually noted both immediately following application of the chemical and for several months thereafter. For example, Corden and Young ( 1965) have documented the modifications among the fungal inhibitants as a result of treatment with dazomet, nabam. and metham. It is now apparent, moreover, that pesticide residues still present in plant remains may alter the pattern of fungal colonization of these remains, and it is worthy of note that this selective effect is not restricted to fungicides, for herbicides may determine which species in a mixture of populations gains the ascendancy during the early phase of microbial colonization. Thus, the herbicides paraquat and MCPA can completely shift the outcome of competition between selected soil fungi (V. Wilkinson and Lucas, 1969). Further substantiating the view that pesticides, other than those specifically designed to control harmful microorganisms, act in a manner detrimental to fungi are the several observations that aldrin .added to soil causes a reduction in the severity of barley root rot, tomato wilt, clubroot of cabbage, and the take-all disease of wheat, diseases caused by Helminthosporium sativum, Fusarium oxysporum f. sp. lycopersici, Plasmodiophora brassicae, and Ophiobolus graminis, respectively (Channon and Keyworth, 1960; Richardson, 1957,1959; Slope and Last, 1963). The same insecticide decreases the Fusarium culmoruminduced damping-off of wheat seedlings, but evidently this suppression of the action of the fungus is not the result of absorption of the chemical by the plants and its conversion to an antimicrobial principle (Baghdadi, 1970). Monuron, dinoseb, 2,4-D, and dalapon similarly reduce infectior, of barley seedlings by H . sativum (Richardson, 1957). Conversely, pesticides may aggravate a disease situation rather than controlling it. This is particularly common among the fungicides which, because they are applied to soil at high dosage rates and owing to their harmful effects on many microbial groups, may eliminate competitors or parasites of the plant pathogen or suppress toxin-forming populations holding the pathogen in check. In the absence of its usual antagonist, the pathogen then more vigorously attacks and does greater damage to its host plant. Such an interpretation see'ms reasonable to account for the

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CHARLES s. HELLING, PHILIP c . KEARNEY, A N D MARTIN ALEXANDER

increase in severity of the strawberry wilt brought about by Verticillium albo-atrum(Rich and Miller, 1964) and the damping-off of Pinus seedlings caused by a species of Pythium (Gibson et al., 1961), in both instances the toxicant being PCNB. Even this type of action is not restricted to fungicides, for heptachlor and maleic hydrazide promote barley seedling infection by Helminthosporium sativum (Richardson, 1957), and herbicides increase the incidence of a Rhizoctonia solani disease of turfgrass (Madison, 1961). It is possible, in fact, that injury directly attributed to the use of preemergence herbicides may rather be the result of injury brought about by a stimulation of some subterranean parasite, in a manner as yet unknown, by the herbicide. This is illustrated in studies of the damage to sugar beets associated with the use of the herbicides pebulate and pyrazon. These herbicides at recommended rates do not reduce the sugar beet stand, but when R . solani is a potential threat, they may either stimulate the development of the fungus or predispose the sugar beets to infection in a way such that more injury is done to the host plant in the presence than in the absence of the herbicides (Altman and Ross, 1965). Moreover, herbicides are known from greenhouse trials to favor virus infection, as shown by the effect of 2,4-D in increasing the tobacco mosaic virus (TMV) content of Physalis fioridea or the number of TMV lesions on cucumber plants exposed to the virus. This apparent enhancement in host susceptibility to TMV infection and the enhancement of TMV biosynthesis has been ascribed to an activation of nucleic acid metabolism by the herbicide (Cheo, 1969). Plants may also be indirectly harmed by pesticides because of an inhibition of certain microorganisms concerned with the nitrogen cycle. Evidence is cited above to show that nitrogen mineralization and especially nitrification are susceptible to suppression by pesticides. Plant tests likewise have provided data suggesting an alteration in nitrogen availability or ammonia toxicity to the growing plant. Soil fumigation, in particular, brings about disturbances of these sorts. Tobacco, an excellent illustration, planted into methyl bromide-fumigated soil, a treatment which inhibits or abolishes ammonium oxidation, responds differentially to nitrogen fertilization, and higher yields are obtained with nitrate than with ammonium fertilizers. Analogous effects are not observed in nonfumigated soils, suggesting that tobacco is not obtaining the nitrate it uses preferentially when the nitrifiers are destroyed by the methyl bromide (Morris and Giddens, 1963). Alternatively, chemical treatments that eliminate or reduce the cell density of nitrifying bacteria may damage crops, not by virtue of depleting their nitrogen supply, but rather because the pesticide (most likely a fumigant), by inhibiting ammonium oxidation, allows ammonium to accumulate to levels injurious to roots (Uljee, 1964).

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This is particularly of concern at high fertilization rates. In a similar vein, Dubey (1 970) recently reported a location in Puerto Rico where the sugar cane was stunted, the plants were yellow, and the leaves were poor in nitrogen. The damage, apparently not arising because of the attack on the sugar cane by soil-borne parasites, could be overcome by the addition of inorganic nitrogen. Inasmuch as the prior crop on this site had been repeatedly treated with the fungicides maneb, zineb, and tribasic copper, Dubey concluded that the pesticides were directly responsible for the damage and that they influenced the plant by reducing the supply of available nitrogen. Studies of the algae have been sorely neglected. This oversight may be acceptable in nonflooded agricultural land, where it is assumed that the algae are of little consequence in those transformations important to crop development, but it surely is a major shortcoming in submerged rice soils. Investigation of axenic cultures of algae, moreover, indicate that they are remarkably sensitive to some of the widely employed pesticides, notably among the herbicides. Thus, growth ofChlarnydomonas reinhardi is totally prevented by 1 .O ppm of metobromuron or 0.5 ppm of atrazine, although this alga is stimulated by 0.5 ppm diphenamid in solution culture (Loeppky and Tweedy, 1969), and concentrations of 2,4-D and trifluralin lower than that recommended for weed control inhibit the Ne-fixing alga, Tolypothrix tenuis (Hamdi et al., 1970). Kiss (1967) has also observed the marked sensitivity of selected Cyanophyta, Chlorophyta, and Chrysophyta to herbicides. The opposite effect, an influence with major economic and fascinating biological implications, has been observed by Raghu and MacRae (1967), namely a stimulation of algae in flooded rice soils treated with lindane to control the rice stem borer. The algae here stand out because of their potential or actual role in nitrogen fixation and oxygenation of the water. The stimulation seemed to result not from a direct enhancement of algal development but, instead, from the suppression of animals that graze upon the indigenous algal species. Both the abundance of algae and the composition of the algal community were changed by the insecticide. Another means by which pesticides may possibly affect the soil inhabitants, mutagenicity, has recently come to light. Prasad and Pramer ( 1 968) and Prasad ( 1 970) noted that ferbam and propanil, as well as two products formed in the biodegradation of propanil, were mutagenic for two species of Aspergillus. Granted that the conditions for these tests were far different from those in nature and that no evidence for such an occurrence in soil is at hand, the possibility of a genetic change in the saprobes or plant parasites of soil must be borne in mind as one potential consequence of the use of these very important compounds in agriculture.

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CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

IV. Implications

A. PERSISTENCE Edaphic, climatic, and pesticide structural characteristics together largely determine the persistence of a pesticide in soil. These characteristics were discussed in Section I1 and are often interrelated. Adsorption strongly influences movement, while the depth of movement is dependent both on soil properties and rainfall received. The residue remaining at any depth reflects the conditions governing chemical or microbial degradation. Superimposed on all these factors is the innate nature of the pesticide, Uptake by plants has additional effect on persistence. The implications of persistence, simply stated, include (i) the time span over which a pesticide will remain effective, (ii) the danger of carryover to succeeding crops, and (iii) the possibility of adverse residue accumulation in other segments of the ecosystem. External manipulation of pesticide persistence is a highly desirable goal, from both agronomic and environmental standpoints (ifone can separate the two). Foy and Bingham (1969) reviewed methods for minimizing herbicide residues. These include the use of alternate control methods, increased efficiency and selectivity, and removal, inactivation, or alteration of persistence. Mass inoculation of soil with selected microorganisms represents an interesting, but apparently unsuccessful, attempt to modify pesticide persistence (Addison, 1968). Earlier research on persistence is summarized for herbicides (Sheets and Harris, 1965; Upchurch, I966), insecticides (Caro, 1969: Edwards, 1966; Lichtenstein, 1966; Marth, I965), fungicides (Goring, I967), and pesticides generally (Edwards, 1970; Kearney el al., 1969b). Kearney et al. (1969b) considered the relative order of decreasing persistence, by pesticide class, to be: chlorinated hydrocarbon insecticides > urea, triazine, and picloram herbicides > benzoic acid and amide herbicides > phenoxy, toluidine, and nitrite herbicides > carbamate and aliphatic acid herbicides > phosphate insecticides. Not included, but generally least persistent, are fumigants such as methyl bromide and dazomet. Persistence, as represented by time for 75- 100% loss, is ca. 2-5 years for chlorinated hydrocarbons, 2- I8 months for ureas and triazines, 1-6 months for the phenoxy herbicides, and 2-12 weeks for organophosphate insecticides. These figures represent a general guide to persistence in soil and are certainly not absolute values. Edwards (1 966) reported longer average persistence values for the chlorinated hydrocarbons. The average time in years for 95% disappearance, based on all available data, was DDT (10) > dieldrin (8) > lindane (6.5) > chlordane (4) > heptachlor (3.5) > aldrin (3).

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N o commonly accepted method exists for describing pesticide persistence in soils. Some workers use the expression “half-life,” assuming that the time necessary for dissipation of 50% of a pesticide residue is independent of concentration. This further assumes first-order reaction kinetics, which have been claimed for many nonvolatile pesticides. Edwards ( 1966), however, analyzed all available persistence data for chlorinated hydrocarbon insecticides and found that small applications disappeared proportionately faster than larger doses. Hamaker ( 1966) treated mathematical prediction of pesticide residues in more detail, pointing out that a large range of concentrations must be studied to reliably determine the appropriate rate law. He calculated the ultimate accumulation of residue in soil for annual additions of one concentration unit and loss of one half in the first year. Residues are shown immediately after addition for various assumed reaction orders: zero-order (M), halforder (3.4I), first-order (2.00), and second-order ( I .62). Classification of rate seems quite feasible in pure systems in which the pesticide undergoes, e.g., chemical degradation. Chemical hydrolysis of phosphorylated atrazine and microbial decomposition of AzodrinB in soil were predicted rather well by first-order kinetics, coupled with adsorption characteristics, in the laboratory (Furmidge and Osgerby, 1967). Loss of pesticides from soil in the field would be far more complex, with volatilization, leaching, adsorption, biological and/or chemical degradation occurring simultaneously. The following recent observations will illustrate factors influencing persistence. The azido-s-triazine W L 9385 readily decomposes chemically and has a half-life in moist soil of only 1-8 days (Barnsley and Gabbott, I966), notably shorter than other commonly used triazine herbicides. Methoxychlor was largely degraded by 20-26 weeks or 30-38 weeks in soils of 10% or 3% moisture content, respectively (Obuchowska, 1969). Under natural conditions, losses of this sort can occur by differential volatilization depending on the inherent pesticide volatility (see Section 11, A, 2, b). Higher soil moisture content, however, is likely more generally associated with increased microbial activity. For pesticides which are anaerobically metabolized, flooding the soil may cause very rapid loss. No lindane remained in a flooded sandy loam after 1 month (Yoshida and Castro, 1970), in contrast to the previously cited average persistence of 6.5 years (Edwards, 1966). Higher temperatures usually reduce persistence. Often seen in laboratory experiments, this conclusion was also reached after comparing herbicide persistence in the cooler northern United States with that in southern United States (C. I . Harris et al., 1969). If temperature alone is considered, persistence of pesticides in the tropics should be less than

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CHARLES

s. HELLING, P H I L I Pc. KEARNEY, A N D MARTIN ALEXANDER

in the temperate regions. In the laboratory, atrazine degraded 2-3 times faster with each lo" increase in temperature between 15"and 35°C (Roeth et al., 1969). Degradation of diazinon and thionazin (ZinophosB) was accelerated by higher temperature and moisture levels (Getzin, 1968). Soil type differences may outweigh temperature as a factor controlling persistence. For example, disulfoton and phorate were much more persistent after field treatment of Chillum silt loam in summer, than after similar application to Evesboro loamy sand in winter (Menzer ef al., 1970). There is a tendency for greater persistence of pesticides in soils containing relatively more organic matter and clay than in lighter-textured sandy soils. The phytotoxic persistence of soil fumigants was longer on loamy clay soils than a sandy loam, presumably because adsorption was greater in the fine-textured soils (Vanachter, 1968). The position of pesticide residues in the soil profile also influences their rate of dissipation. After 3 months, 61% more atrazine and 41% more fenac were recovered from samples placed at the 15-inch depth than at the 3-inch depth (C. 1. Harris et al., 1969). There was a positive correlation between fenac retention and soil organic matter content. Microbial activity is less in subsoil than nearer the surface, and this may partially account for the faster atrazine breakdown in incubated surface soil as compared to soil from deeper horizons (Roeth et al., 1969). The previous history of pesticide use may affect its persistence in soils, though only if microbial metabolism is a major route of loss. Thus Audus and others (summarized by Loos, 1969) noted more rapid breakdown of a phenoxyalkanoic herbicide in soils previously treated with the compound than in previously untreated soils. A microbial population had developed which was capable of metabolizing the herbicide and, sometimes, its analogs. Several recent long-term field experiments show this enrichment effect clearly. MCPA degraded significantly faster in soil which had received five annual applications of the phenoxy herbicide than in nonenriched soil (Fryer and Kirkland, 1970). Persistence of MCPA was inversely related to the number of previous applications. Similarly, the persistence of 2,4-D was shorter in soil from plots treated annually for 12 years, tested 8 months after the last application, than in soil from plots treated for the first time (Hurle and Rademacher, 1970). DNOC produced no such enrichment effect. The influence of prior microbial adaptation on parathion mobility was discussed earlier (Section 11, A, 2, a). Edwards ( I 966) summarized insecticide persistence as a function of formulation: granules > emulsins > miscible liquids > wettable powders and dusts. The relative order probably holds for all pesticides. If pesticides are soil incorporated, persistence is usually greater than when

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left at the surface, especially for volatile or photosensitive compounds. However, the fungicides captan and thiram were less persistent (halflives of 1-2 days) when well distributed in soil than when added as coatings on glass beads (little change at 2 1 days). Griffith and Matthews ( 1969) suggested that high local concentrations around the beads may inhibit detoxifying organisms, or that fungicide surface area has been significantly reduced by this means of incorporation. If the glass bead is regarded as a reasonable simulation of a seed, these results may explain the effectiveness of captan and thiram as seed dressings. In the future, metabolic inhibitors may be added to pesticide formulations to modify their persistence. When added with propham or chlorpropham, p-chlorophenyl methyl carbamate (PPG- 124) improves weed control by prolonging the herbicidal activity (Dawson, 1969). The mechanism is inhibition of microbial hydrolysis of the herbicides (see also Section 11, B, 2 , e). B.

BIOACTIVITY A N D UPTAKE

Bioactivity is of particular concern for pesticides applied intentionally to the soil. Dosage is varied according to the expected bioactivity, as is clear when commercial pesticide labels are examined: the recommended application rate usually increases from light to medium to heavy soils. Uptake of pesticides by plants is desirable when the plants are weeds or the pesticides are systemic insecticides or fungicides; it is undesirable when persistent residues remain in portions of the plant used for food or feed. Many previous studies have established a relationship between soil texture and bioactivity. If, for example, 12 pg of simazine produced an ED," (50% growth reduction) response in sand, a dose of 850 pg was required to achieve the same effect when chernozem soil was used (Voitekhova, 1969). Correlation studies have often shown soil organic matter to be most closely related to bioactivity. Recent examples include the herbicides atrazine, ametryne, prometryne, simazine, diuron, picloram, and fluometuron (Darding and Freeman, 1968; Day et al., 1968; Grover, 1968; Liu and Viade, 1968). Better correlations are sometimes obtained between ED,,) and adsorption of the herbicide (C. 1. Harris and Sheets, 1965). Bioactivity is often less predictable in the field than in greenhouse studies, suggesting climate is an influential factor. Insecticide bioactivity also varies among soils, bsing greatest in sandy soils containing little organic matter. Toxicity is usually greater in moist soils, conditions likely to increase volatilization. Dieldrin toxicity to Drosophila melanogaster (vinegar fly) was negatively correlated with

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CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

organic carbon, specific surface area, and soil pH (Hermanson and Forbes, 1966). DDT bioactivity was also principally related to soil organic matter: multiple regression also suggested complex interactions with fine clay, cation exchange capacity, and Fe (J. R. Peterson et ul., 1971). In both studies 97-98% of the variability in LDSo could be accounted for. The effect of soil moisture on phytotoxicity of herbicides is not entirely clear. With EPTC, increased moisture partially desorbs the herbicide, increasing plant injury. Atrazine and chloramben effectiveness was also increased, trifluralin decreased, and propachlor and alachlor were unaffected by additional water (Stikler et al., 1969). Picloram bioactivity decreased as soil moisture content increased, a decline which Grover (1970) attributed to reduced picloram concentration. Lambert ( 1966) considered herbicidal response to be directly proportional to its solution concentration, in turn dependent on the pesticide distribution coefficient and the soil water content. Green and Obien (1969) predicted atrazine concentration in the soil solution using Lambert’s equation modified for “effective water content,” i.e., total water minus 15-bar water. Significant changes in concentration occur only in low adsorption soils, so the effect of moisture content may reflect the ease of pesticide movement to the root and plant processes, such as absorption, translocation, and transpiration. Unless vapor movement is significant (as with trifluralin), movement of pesticides increases as soil water content increases. Soil moisture relationships with systemic insecticide uptake appear equally complex (Graham-Bryce and Etheridge, 1967). A common approach to understanding soil influence on pesticide bioactivity has been through the use of synthetic media. Mixtures of muck soil or peat with sand greatly reduced phytotoxicity of linuron, simazine, prometryne, and pyrazon, whereas montmorillonite clay was less effective (Doherty and Warren, 1969). Using the same technique, D. C. Scott and Weber ( 1967) demonstrated reduced phytotoxicity of paraquat and prometone in the presence of montmorillonite and kaolinite. Toxicity of 2,4-D and chlorpropham was decreased by anion-exchange resins and that of all four herbicides, by muck soil. Paraquat adsorbed on montmorillonite is much less available to plants than when adsorbed to vermiculite, kaolinite, or even peat (Damanakis et al., 1970; Weber et al., 1969a). The phytotoxicity of prometryne was less at pH 4.5 than 6.5 and this was attributed to greater herbicide adsorption at the lower pH (Weber et al., 1968a). I n the field, simazine injury to strawberries was more severe in limed plots (Leefe, 1968); since the original soil was pH 4.2, the effect may derive from greater adsorption (and less availability) or

BEHAVIOR OF PESTICIDES IN SOILS

22 I

faster hydrolysis to hydroxysimazine at low pH. Ineffective control of damping..off disease in acidic soils was attributed to rapid chemical decomposition of the fungicides thiram and ferbam (Kluge, 1969). The reduction of pesticide bioactivity and uptake by addition of activated carbon has been shown by many workers (Foy and Bingham, 1969). It seems especially effective for neutral molecules, with dalapon, picloram, and chloramben only weakly adsorbed. To be effective, several thousand ppm of carbon must be added to soil, so large-scale use appears unlikely. Bioactivity of arsenical pesticides in soils is an undesirable feature, unless soil sterilization is intended, since they are used only as foliar treatments. The inorganic arsenicals, now mainly calcium arsenate, lead arsenate (insecticides), and sodium arsenite (postemergence herbicide and defoliant for cotton and potatoes), are gradually being replaced in common use by organic pesticides including organic arsenicals such as MSMA. D S M A . and cacodylic acid. The use and behavior in soils of arsenicals hiis been reviewed in several recent publications (Jacobs et al., 1970a.b: Johnson and Hiltbold, 1969). Continued application of arsenates, especially in orchards, has led to phytotoxic arsenic residues. Sodium arsenite residues in Plainfield sand were harmful to succeeding vegetable crops, especially at applied rates of 90 kg/ha or more (Jacobs et al., I970a). (This rate is ca. I0 times the recommended annual application.) Damage to peas was identical both one and two years after arsenite application. Arsenic toxicity typically decreases with higher contents of clay and iron oxide, probably accounting for phytotoxicity occurring in the sandy Wisconsin soil. Removal of amorphous iron and aluminum by oxalate treatment eliminated or greatly reduced arsenic (as sodium arsenate) adsorption capacity in soils (Jacobs et ul., 1970b). Chemically, arsenic resembles phosphorus, also forming relatively insoluble salts with iron, aluminum, and calcium. Woolson et al. ( I97 I ) found that the phytotoxicity of arsenic in soils was related to its distribution in and solubility of these forms. The very slightly soluble ferric arsenate (K,s,,= 6 X lo-") was unavailable and essentially nonphytotoxic. Aluminum arsenate (Ks,,= 2 X and calcium arsenate (Ks,,= 7 x IO-'!') are slightly more soluble and consequently more phytotoxic. Plant response indicated a decrease in toxicity as the water-soluble and aluminum arsenates decreased and ferric arsenate formed. The soil chemistry of the arsenates is important, despite their declining use, since the fate of organic arsenicals is likely conversion to inorganic arsenates. Johnson and Hiltbold (1969) found little or no remaining organic arsenic one year after the last treatments of MSMA, DSMA, and MAMA to turf. The arsenic residues were associated with soil clay and with the iron fraction. To avoid the potential damaging levels

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CHARLES S. HELLING, PHILIP C. KEARNEY, A N D MARTIN ALEXANDER

of bioactive arsenic, it would seem prudent to monitor soil arsenic residues in regions of greatest use, such as the cotton production area of the southern United States. An extended discussion of pesticide uptake by plants is outside the intended scope of this review. Uptake of dieldrin by corn (Beestman et al., 1969) and DDT, dieldrin, endrin and heptachlor by various crops was negatively correlated with soil organic matter content (Beall and Nash, 1969); uptake increased in the order listed. In at least one report, the extent of D D T uptake depended more on its concentration in soil and the duration of root contact than on soil type (Hartisch et al., 1969). Uptake can also occur by direct volatilization of chlorinated hydrocarbon insecticides from soil to plant (Barrows et al., 1969; Nash and Beall, 1970). Aerial contamination is most severe on the lower leaves. Movement within the soil is also significantly related to pesticide bioactivity and uptake. Ametryne was safely used in banana plantings because it is less mobile than atrazine, which caused injury (Barba and Romanowski, 1969). The leaching of linuron and lenacil to shallow-sown flax seeds caused 20% loss of plants (Liefstingh and Blink, 1969); in highly organic soils, however, lenacil was inactive since it could not leach to the zone of germinating weed seeds (Ramand, 1969). Residues of TernikB appeared in untreated citrus trees, possibly originating from lateral movement of the insecticidelnernatocide after sprinkler irrigation (Hendrickson and Meagher, 1968). Uptake by orchard trees can be modified by the method of applying irrigation water. Lateral movement in furrow irrigation keeps the herbicide near the soil surface, whereas leaching during sprinkler and flood irrigation is primarily downward. Herbicides could then be absorbed by the tree roots, causing serious foliar damage (Lange and Fischer, 1969). TABLE IV Chemical Designations of Pesticides Mentioned in Text Common or trade name ACNQ Alachlor Aldicarb Aldrin Ametryne Amiben Aminocarb

Chemical name 2-Amino-3-chloro- 1.4-naphthoquinone 2-C hloro-2',6'-diethyl-N-(methoxymethyl)acetanilide 2-Methyl-2-(methylthio)propionaldehyde0(methy1carbamoyl)oxime 1,2,3,4,IO,IO-Hexachloro1,4,4a,S,8,8a-hexahydro1,4-endo,exo-5,8-dimethanonaphthalene 2-(Ethylamino)-4-(isopropylamino)-6-( methy1thio)-s-triazine see Chloramben 4-Dimethylamino-rn-tolyl methylcarbamate

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TABLE IV (continued) Common or trade name Amitrole Aramite Atratone Atrazine Azinphosmethyl AzodrinB Banol @ Barban Bayer 25141 Benefin Benomyl Bensulide 7-BHC Binapacryl Bromacil C-6989 Cacodylic acid Captan Carbaryl Carboxin CDAA CDE C Chloramben Chloranil Chlordane C hlordene Chlorfenvinphos Chloroneb C hloroxuron C hlorphenamidine Chlorpropham C hlorthiamid Ciodrin@ ClPC Cycloate 2,4-D Dalapon Dazornet 2,4-DB DCPA D-D@

Chemical name 3-Amino- I ,2,4-triazole 2-b-tet-t- Buty1phenoxy)- 1-methylethyl 2’-chloroethyl sulfite 24 Ethylamino)-4-(isopropylamino)-6-methoxy-s-triazine 2-Chloro-4-(ethylamino)-6-(isopropylamino)-s-triazine 0,O-Dimethyl S-[4-OXO- I ,2,3-benzotriazin-3(4ff)ylrnethyl] phosphorodithioate Dimethyl 3-hydroxy-N-methyl-cis-crotonamide phosphate 6-ChIoro-3.4-xyIyl methylcarbamate 4-Chloro-2-butynyl m-chlorocarbanilate 0,O-Diethyl 0-[p-(methylsulfinyl)phenyl] phosphorothioate N-Butyl-N-ethyl-a,a,a-trifluoro-2,6-dinitro-ptoluidine Methyl I-(butylcarbamoyl)-2-benzirnidazolecarbamate N-(2-Mercaptoethyl)benzenesulfonamide 0,O-diisopropyl phosphorodithioate See Lindane

2-sec-Butyl-4,6-dinitrophenyl3-methyl-2-butenoate 5-Bromo-3-sec-butyl-6-methyluracil p-Nitrophenyl-a,a,a-trifluoro-2-nitro-p-tolyl ether Hydroxydimethylarsine oxide N-Trichloromethylmercapto-4-cyclohexeneI ,2-dicarboximide I-Naphthyl methylcarbamate 5.6-Dihydro-2-rnethyI- I ,4-oxathiin-3-carboxanilide N,N-Diallyl-2-chloroacetamide 2-Chloroallyl diethyldithiocarbamate 3-Amino-2,5-dichlorobenzoic acid Tetrac hloro-p-benzoquinone I ,2,4,5,6,7,8,8-0ctachloro-2,3,3a,rh7,7a-hexahydro4,7-methanoindene 4,5,6,7,8,8-Hexachloro-3a,4,7,7a-tetrahydro-4,7methanoindene 2-Chloro- 1 -(2,4-dichlorophenyl)vinyldiethyl phosphate 1,4-Dichloro-2,5-dimethoxybenzene 3-[p-@-Chlorophenoxy)phenyl]- I , I -dimethylurea N’-(4-Chloro-o-tolyl)-N,N-dimethylformamidine Isopropyl rn-chlorocarbanilate 2,6-Dichlorothiobenzamide a-Methylbenzyl 3-(dimethoxyphosphinyloxy)-cis-crotonate See Chlorpropham S-Ethyl N-ethylthiocyclohexanecarbamate 2,4-Dichlorophenoxyacetic acid 2,2-Dichloropropionic acid Tetrahydro-3,5-dimethyl-2H1,3,5-thiadiazine-2-thione 4-(2,4-Dichlorophenoxy)butyric acid Dimethyl tetrachloroterephthalate 1,3-Dichloropropene and 1,2-dichloropropane (mixture) (continued)

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CHARLES s. HELLING, PHILIP c. KEARNEY, AND MARTIN ALEXANDER

TABLE 1V (continued) Common or trade name DDD DDE DDT Demeton 2.4- D EP Dexon@ Diazinon Dicamba Dichlobenil Dichlone Dichlormate Dichlorprop Dichlorvos Dieldrin Dimefox Dimethoate Dinoseb Diphenamid Dipropalin Diquat Disulfoton Diuron DMPA DNOC DSMA Dursbana Dyrene EDB Endosulfan Endothall Endrin EPTC Erbon Ethion Fenac Fenoflurazole

Chemical name See T D E 2,2-Bis@-chlorophenyI)-1, I -dichloroethene 2,2-Bis@-chlorophenyI)-I , ] , I-trichloroethane @,p' isomer) 0,O-Diethyl @and S)-[2-ethyIthio)ethyl]phosphorothioate Tris[2-(2,4-dichlorophenoxy)ethyl] phosphite p-Dimethylaminobenzenediazo sodium sulfonate 0,O-Diethyl 0-(2-isopropyl-4-methyl-6-pyrimidinyl) phosphorothioate 3,6-Dichloro-o-anisic acid 2,6-Dichlorobenzonitrile 2,3-Dichloro- 1,4-naphthoquinone 3,4-Dichlorobenzyl methylcarbamate 2-(2,4-Dichlorophenoxy)propionicacid Dimethyl 2,2-dichlorovinyl phosphate 1,2,3,4,10,IO-Hexachloro-6,7-epoxy-I ,4,4a,5,6,7,8,8aoctahydro- I ,4-endo,exo-S,8-dimethanonaphthalene Bis(dimethylamid0)phosphoryl fluoride 0,O-Dimethyl S-(N-methylcarbamoylmethyl) phosphorodithioate 2-sec-Butyl-4,6-dinitrophenol N,N-Dimethyl-2,2-diphenylacetamide 2,6-Dinitro-N,N-dipropyl-p-toluidine 6,7-Dihydrodipyrido[1,2-a :2', I '-clpyrazidinium salt 0,O-Ethyl S-2(ethylthio)ethyl phosphorodithioate 3-(3,4-DichlorophenyI)-I , I -dimethylurea O-(2,4-Dichlorophenyl)U-methyl isopropylphosphoramidothioate 4.6-Dinitro-o-cresol Disodium methanearsonate 0,O-Diethyl 0-3.5.6-trichloro-2-pyridyl phosphorothioate 2,4-Dichloro-6-(o-chloroanilino)-s-triazine I .2-Dibromoethane h.7.X.9.10.IO-Hexachloro-I .5.5a.6.9,9a-hexahydro-6.9niet hano-2.4.3-benzodioxathiepin-3-oxide 7-Oxabicyclol2.2. I Iheptane-1.3-dicarboxylic acid I.2.3.4.IO.10-Hexachloro-h.7-epoxy-I ,4,4a,S,6,7,8,8aoctahydro- I .4-rndo,rndo-S,8-dimethanonaphthalene S-Ethyl dipropylthiocarbamate 2-(2,4,S-Trichlorophenoxy)ethyl 2,2-dichloropropionate Bis[S-(diethoxyphosphinothioyl)mercapto]methane (2,3,6-TrichlorophenyI)acetic acid 5,6-Dichloro- I -phenoxycarbonyl-2-trifluoromethylbenzimidazole

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T A B L E IV (continued) Common or trade name Fenuron Ferbam Fluometuron Formetanate GS 13005 HCH Heptachlor lmidan @ loxynil lpazine lsobenzan lsocil lsodrin Karsilm Kerb@ Lenacil Lindane Linuron Malathion MAMA Maneb Matacilm MCPA MesuroP Methabenzthiazuron Metham Methoxychlor Metobromuron Mevinphos Molinate Monolinuron Monuron Morestan@ MSMA Mylone@ Nabam Naptalam Neburon Nitralin

Chemical name I , I-Dimethyl-3-phenylurea Ferric dimethyldithiocarbamate I , I-Dimethyl-3-(a,a,aY-trifluoro-m-tolyl)urea m-{ [(Dimeth ylamino)methylene]amino}phenyl methylcarbarnate 0,O-Dimethyl S-[2-methoxy- 1,3,4-thiadiazol-S(4H)onyl-(4)-methyl] phosphorodithioate I ,2,3,4,5,6-Hexachlorocyclohexane(various isomers) I ,4,5,6,7,8,8-HeptachIoro-3a,4,7,7a-tetrahydro-4,7methanoindene 0,O-Dimethyl S-phthalimidomethyl phosphorodithioate

4-Hydroxy-3,5-diiodobenzonitrile 2-C hloro-4-(diethylamino)-6-(isopropylamino)-~-triazine 1,3,4,5,6,7,8,8-0ctachloro-3a,4,7,7a-tetrahydro-4,7methanophthalan S-Bromo-3-isopropyl-6-methyluracil 1,2,3.4,10,IO-HexachloroI ,4,4a,5,8,8a-hexahydro-1,4endo,endo-5,8-dimethanonaphthalene N-(3,4-DichlorophenyI)-2-methylpentanamide See RH-3 IS 3-Cyclohexyl-6.7-dihydro-I H-cyclopentapyrimidine2,4(3H , 5H)-dione y- I ,2,3,4,5,6-Hexachlorocyclohexane 3-(3,4-DichlorophenyI)- I methoxy- I -methylurea 0,O-Dimethyl S-bis(carboethoxy)ethyl phosphorodithioate Monoammonium methanearsonate Manganous ethylenebisdithiocarbamate See Aminocarb 4-Chloro-2-methylphenoxyacetic acid 4-(Methylthio)-3,5-~ylylmethylcarbarnate 3 4 Benzthioazolin-2-yl)- 1,3-dimethylurea Sodium methyldithiocarbamate 2,2-Bis@-methoxyphenyl)- I , 1, I-trichloroethane 3-@-Bromophenyl)- I methoxy- I methylurea 2-Carbornethoxy- I -propen-2-yl dimethyl phosphate S-Ethyl hexahydro- I H-azepine- I-carbothioate 3-@Chlorophenyl)- I-methoxy- I-methylurea 3-@-Chlorophenyl)- 1, I-dimethylurea 6-Methyl-2-0x0- 1,3-dithio(4,S-b)quinoxaline Monosodium methanearsonate See Dazomet Disodium ethylenebisdithiocarbamate N- I-Naphthylphthalamic acid I -ButyI-3-(3,4-dichlorophenyl)I-methylurea 44 MethylsuIfonyl)-2,6-dinitro-N,N-dipropylaniline (continued)

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s. HELLING, P H I L I Pc. KEARNEY, A N D MARTIN ALEXANDER TABLE IV (continued)

Common or trade name Norea Paraquat Parathion PCN B PCP Pebulate Phorate Picloram Prometone Prometryne Propac hlor Propanil Propazine Propham Proximpham Pyrazon Pyrichlor RH-3 I5 Ronnel Sch radan Sesone Siduron Silvex Simazine Simetone 2.4.5-T 2,3,6-TBA TCA TDE Telodrina Temika TEPP Terbacil Terbutryn Tetraetatone Thionazin Thiram Toxaphene Tricamba Trietatone Trietazine Trifluralin Vapama

Chemical name

3-(Hexahydro-4,7-methanoindan-5-yl)I , I-dimethylurea I , 1 '-Dimethyl-4,4'-bipyridinium salt 0,O-Diethyl 0-p-nitrophenyl phosphorothioate Pentachloronitrobenzene Pentachlorophenol S-Propyl butylethylthiocarbamate 0,O-Diethyl S -(ethylthiomethyl) phosphorodithioate 4-Amino-3,5,6-trichloropicolinic acid 2,4-Bis(isopropylamino)-6-methoxy-striazine 2,4-Bis(isopropylamino)-6-methylthio-s-triazine 2-Chloro-N-isopropylacetanilide 3',4'-Dichloropropionanilide 2-C hloro-4,6-bis(isopropyl)-s-triazine lsopropyl carbanilate 0-(Phenylcarbamoyl)-2-propanonoxime 5-Amino-4-chloro-2-phenyl-3(2H)-pyridazinone 2,3,5-Tric hloro-Cpyridinol N-(1 , l -Dimethylpropynyl)-3,5-dichlorobenzamide 0,O-Dimethyl 0-3,4,6-trichlorophenyl phosphorothioate Octameth ylpyrophosp horamide 2-(2,4-Dichlorophenoxy)ethyl sodium sulfate I -(2-Methylcyclohexyl)-3-phenylurea 2-(2,4,5-Trichlorophenoxy)propionicacid 2-Chloro-4,6-bis(ethylarnino)-s-triazine 2,4-Bis(ethylamino)-6-methoxy~-triazine 2,4,5-Trichlorophenoxyaceticacid 2,3,6-Trichlorobenzoic acid Trichloroacetic acid 2,2-Bis@-chlorophenyl)- I , I -dichloroethane See lsobenzan See Aldicarb Tetraethyl pyrophosphate 3-terr-Butyl-5-chloro-6-methyluracil 2-(tert-Butylamino)-4-(ethylamino)-6-(methylthio)s-triazine 2,4-Bis(diethylamino)-6-methoxy-s-triazine 0,O-Diethyl 0-2-pyrazinyl phosphorothioate Tetramethylthiuram disulfide Octachlorocamphene (mixture) 3,5,6-Trichloro-+anisic acid 2-(Diethylamino)-4-(ethylamino)-6-methoxy-s-triazine 2-C hloro-4-(diethylamino)-6-(ethylamino)-s-triazine a.a.a-Trifluoro-2,6-dinitro-N,N-dipropyl-~-toluidine See Metham

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TABLE I V (continued) Common or trade name Vernolate WL 9385 WL 19805 Zectrana Zineb Zinophos@ Ziram Zytrona

Chemical name S-Propyl dipropylthiocarbamate 2-Azido-4-(ethylamino)-6-(tert-butylamino)-~-triazine 244-C hloro-6-ethylamino-s-triazine-2-ylamino)2-methylpropionitrile 4-Dimethylamino-3,5-xylyl methylcarbamate Zinc ethylenebisthiocarbamate See Thionazin Zinc dimethyldithiocarbamate See DMPA

V.

Summary

The behavior of pesticides in soils was reviewed from the standpoint of processes affecting pesticides (physicochemical and metabolic), the effect of pesticides on the soil microbiota, and the implications of these processes on persistence, bioactivity, and plant uptake. Adsorption, the most influential process affecting pesticides in soils, depends on both soil and pesticide properties. Adsorption usually is greatest in the order organic matter > high-charge clays > low-charge clays. Other significant soil factors include total surface area, water content, temperature, and pH. Pesticide properties which are relevant include overall chemical character and configuration, dissociation constant, water solubility, charge distribution, and molecular size. Movement occurs by leaching, volatilization, or runoff. Leaching includes diffusion and mass transfer components, both of which are inversely related to adsorption. Thus movement of pesticides is greatest in light-textured soils low in organic matter and clay. The relative movement of 82 pesticides is presented, showing that (i) acidic compounds are relatively mobile; (ii) phenylureas and triazines are of intermediate to low mobility; and (iii) chlorinated hydrocarbons and organic cations are least mobile. Volatilization of insecticides such as lindane was maximal when soil water content was equivalent to a surface monolayer. Surface loss is generally greater from moist than dry soils, however, because of water transport to the surface and by competitive displacement by water. Pesticides most likely subject to runoff loss are those not inherently mobile. The importance of photodecomposition as a process degrading pesticides in soils is uncertain. Generally, photolysis occurs more readily for compounds in solution, with soil inhibiting the reaction. Common photo-

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lytic reactions include dehalogenation, sulfur oxidation, and isomerization. Degradation by chemical reaction in soils may be a more common process than was previously realized. Hydrolysis, often pH-dependent, occurs with TEPP, benomyl, captan, proximpham, dazomet, and other compounds. Hydrolysis of chloro-s-triazines and some organophosphorus insecticides appears adsorption-catalyzed. Formation of I-hydroxychlordene from heptachlor and various isomers from dieldrin are rapid chemical reactions. Microbial metabolism is an important process by which many pesticides are degraded in soils. Molecular factors favoring pesticide metabolism are solubility, a low chlorine content and certain linkages readily accessible to enzymatic attack. Climatic and edaphic factors favoring microbial activity, i.e., high soil moisture, temperature, and organic matter, also favor pesticide metabolism. Bacteria, fungi, and actinomycetes contribute to the degradation of one or more classes of pesticides. Anaerobic microbes appear to degrade highly chlorinated persistent insecticides by reductive dechlorination at a more rapid rate than observed under aerobic conditions. The conversion of D D T to D D D and one proposed mechanism of lindane degradation are two examples of reductive dechlorination. Other important reactions catalyzed by microbial enzymes include dehalogenation, dealkylation, amide or ester hydrolysis, oxidation, and reduction. Use of specific microorganisms to decontaminate residual pesticides in soils has met with limited success thus far, usually under artificial conditions. The effects of pesticides on soil organisms and their biochemical processes has been the subject of numerous investigations. Effects of pesticides on soil biota conducted under laboratory conditions are difficult to extend to natural conditions owing to variability in temperature, moisture, organic matter, pesticide concentration, formulation effects, impurities, and the heterogeneous biotic population encountered in field soils. Techniques generally designed to determine the effect of pesticides on the components of the soil community have measured (i) distinct soil processes (e.g., COz production, nitrate reduction, N2-fixation, cellulose decomposition, and other biochemical processes); (ii) population density of specific groups of organisms; (iii) possible alteration of microbial reactions on suitable plant species; and (iv) changes in microbial growth or other processes in liquid media or agar. Persistence of pesticides reflects the sum of all other processes modifying pesticides in soils. Factors influencing persistence include the pesticide itself, soil type, moisture status, temperature, application rate, depth of placement, formulation, soil pH, and microbial activity. Prior

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PHYSIOLOGY OF THE RICE PLANT Yoshiaki lshizuka' Emeritus Professor, Hokkaido University, Japan

1.

Introduction

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

11. Static Approach: Analytical Studies o f t

A. Growth Analysis of the Rice Plant ................................................... B. Absorption of Nutrients ................................................................. C. Physiological Functions of the Component Organs of the Rice Plant ..... 111. Dynamic Approach: Fundamental Research for Higher Yield A. Blueprint to Obtain High Yields of Rice Using All Present B. The Search for Maximum Yield ....................................................... C. Problems of Plant Type ....... D. Translocation a E. Photosynthesis, Respiration, and Yield ............................................ F. Nutrient Supply ............ IV. Conclusion ......................................................................................... References ............ .............................................

I.

24 I 243 243 252 263 275 275 279 28 1 287 29 I 295 309 3 10

introduction

Rice is the staple food in Asian countries. I n 1966, out of a total world rice production of 235,071,000 tons, 232,052,000 tons (93%) were produced in Asia ( F A 0 Production Yearbook, 1967). I t is thus not surprising that most of the general and physiological studies of the rice plant carried out before 1950 were done in Asian countries. Takeyoshi (1 969) analyzed the bibliography on the rice plant. She found that, between I95 I and 1966, a total of 17,187 scientific papers had been published throughout the world on this subject. Of these, 7798 (about 45.4%) had been contributed by Japanese scientists. They had been written in 23 different languages, of which the most commonly used were English 41.9%, Japanese 35.4%, French, 5.4%, Italian 4.7%, Chinese 3.9%, and Spanish 2.3%. Almost all papers emanated from Asian countries. Rice is not an important food in well developed countries, and the majority of the scientists in these areas paid little or no attention to the growing of this crop. indeed, they found difficulty in obtaining the reports 'Present address: Asian and Pacific Council, Food and Fertilizer Technology Center, Taipei, Taiwan.

24 I

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YOSHlAKl ISHIZUKA

prepared in Asia. No more than seven books on rice cultivation had been written in the English language, viz. Girst (1953), Ramiah (1953), Is0 ( 1954), Matsuo ( I 96 I), I . Nagai (1 962), Chandraratna ( I964), and USDA ( I 966). Since 1960 agronomists of developed countries have shown an increasing interest in the study of the rice plant. The main reason for this changed attitude to a crop which is the main food of developing countries was the Truman “Point-Four Doctrine,” embracing as it did the freedom from hunger campaign. It was obvious that if developed countries wished to improve the living standards of developing countries, they would have to try to increase the production of rice in Asia. As Truman stated, the accumulation of knowledge about rice was comparatively small in advanced countries. Consequently, Western scientists were obliged‘ to begin studying this crop. Adair et af. (1962) summarized research that had been done in the United States. The establishment of the International Rice Research Institute in the same year in the Philippines by the Ford and the Rockefeller foundations was a very considerable contribution to the progress of rice research. Since 1962 a great deal of progress has been made in the study of the rice plant, particularly in the study of its physiology. At the same time, Japan, which had suffered serious damage during the war, recognized that her best means of rehabilitation was to achieve self-sufficiency in the staple food - rice. This could be done only by making fundamental studies of the plant, allied to practical research. During this period one of the important developments in the study of the rice plant was the increasing knowledge concerning its physiology and nutrition. In 1964 the results of research into the nutrition of the rice plant were summarized at a symposium on “The Mineral Nutrition of the Rice Plant” at the International Rice Research Institute. This symposium marked an epoch in the research on the physiology of the rice plant. One of the reasons for studying the physiology as well as the nutrition of the rice plant is to enable yields to be increased, thereby helping to increase food supplies in Asian countries. As is the case with all other crops, the rice plant is trying to have a heart-to-heart talk with us. If we closely observe the performance of the plant, the change in the color of crops, especially of the leaves, the growth process, and if sometimes we use the techniques of foliar analysis, we will be able to understand what the crops are trying to say to us. By understanding their complaints and giving them satisfaction by artificial treatments, we can expect good growth with the promise of higher yields. This is the key for the preparation of a blueprint for obtaining maximum yields under a given environment.

PHYSIOLOGY OF T H E RICE P L A N T

243

As this book concerns advances in agronomy, I wish to emphasize the nutritional physiology of the rice plant from the agronomic point of view. Consequently I have occasionally omitted quoting literature which treats the rice plant only as a material for the study of physiology. II.

Static Approach: Analytical Studies of the Growth of the Rice Plant

A.

GROWTHANALYSIS OF

THE

RICE PLANT

1. Growth of the Rice Plant

When rice seed is given favorable conditions it will germinate. Some time after germination it begins to increase in weight, synthesizing carbon dioxide and absorbing various types of nutrients, and it dies after producing new seeds. This is the simple ontogenic life cycle of the rice plant. In the past, the growth of the plant was considered to be a process of autocatalytic increase of weight, and research workers tried to express the process of growth by an equation, the so-called growth curve. After the discovery of photoperiodism and vernalization, it was shown that the growth of a plant is the composite of the growth (increase of materials) and the development (phase differentiation). Purvis, on the basis of anatomical studies of growth, pointed out the significance of the formation of flower primordia in higher plant life. In the case of the rice plant, heading is very uniform among tillers and phase differentiation is easy to recognize. This stage in the life cycle is very significant in determining the time of fertilizer application, as will be demonstrated later in this chapter. Ishizuka and Tanaka (1952) conducted a series of experiments on the growth of the rice plant, investigating both morphological and physiological factors. Figure 1 shows that there is a remarkable increase in the number of tillers until the time of panicle initiation. After panicle initiation there is a marked increase in the weight of leaves and stems. The height of the plant continues to increase until flowering time, mainly because of the increase in the length of leaves. After panicle initiation, the stem elongates rapidly because of the rapid growth of the panicle. After heading and flowering, the increase in the weight of the ear becomes very marked. From the viewpoint of physiology it is then reasonable to divide the growth period of the rice plant into three phases: these are vegetative (from seed germination to panicle initiation), reproductive (from panicle initiation to ripening), and ripening (from flowering to full maturity). Vegetative growth is characterized by tillering, reproductive growth by

244

YOSHlAKl ISHIZUKA

the growth of the ear as well as the stems, and ripening by the increase in the weight of the ear. Total weight-

FIG. 1. Growth of the rice plant in the paddy field. (A), Time of transplanting; (B), recovery from disorder induced by transplanting: ( C ) , tillering; (D), formation of flower primordia: (E), stem elongation; (F), flowering: ( G ) , milky stage: (H), dough stage; (I), incomplete ripening.

However, the above example refers only to the case of an earlymaturing variety which shows a clear sequence of growth..In the case of a late maturing variety, such as Indica in tropical regions, panicle initiations begins some time later than the time of maximum tillering. Here there appears to be a dormant period between the vegetative and reproductive phases. During this period the rate of increase in the weight of leaves and stems decreases, regardless of the elongation of the stem (Tanaka, 1964). Ishizuka and Tanaka ( 1954) studied the pattern of rice growth with respect to physiology, and measured the quantity of chlorophyll and the activity of catalase, amylase, and invertase, which appear to be closely related to photosynthesis and carbohydrate metabolism in the rice plant (see Fig. 2). In the vegetative phase, the amount of chlorophyll, as well as the activity of catalase, amylase, and invertase, increasingly reflects vigorous photosynthesis and translocation of assimilates. They reach their maximum at the panicle initiation stage. At the reproductive stage, although the quantity of chlorophyll and the activity of catalase are still high, the

PHYSIOLOGY OF T H E RICE P L A N T

245

activity of amylase and invertase begins to decrease. This means that, although assimilation is vigorous, the assimilated products are stored in siru where they are formed, and are not translocated through the plant.

I

FIG. 2. Enzyme activity at different stages of growth.

Finally, at the ripening stage, the amount of chlorophyll and catalase activity decrease. The activity of amylase and invertase increase considerably, indicating the vigorous translocation of assimilates to the panicles. Ishizuka and Tanaka ( 1954) also demonstrated the fluctuation in the levels of the three types of carbohydrate in the stem and leaves at various stages of growth. Figure 3 shows that, at the vegetative stage, the quantity of all three types of carbohydrate is very low, indicating that most of the carbohydrates that are assimilated are consumed to form protein. At the reproductive stage starch content increases considerably, as does the content of sugars, indicating the accumulation of starch in the leaves and stems over this period. The starch thus temporarily accumulated rapidly decreases at the ripening stage. Nonreducing sugar slowly increases, and reducing sugar also shows a temporary increase. This indicates that the starch stored in the leaves and stems is translocated to the panicles. However, the contribution of the starch that was stored in the leaves and

246

YOSHIAKI ISHIZUKA

stem to the formation of the panicles is comparatively small compared with the amount of starch assimilated after flowering.

i

I I I

I' I

\

i,

Starch

\

\

I

FIG.

3. Carbohydrate contents at different stages of growth.

Kurosawa et al. (1955) carried out a similar investigation on the carbohydrate content of the leaf and stem during the growth of the rice plant. As a result of these studies we can divide organic matter into three groups and demonstrate their fluctuation within the plant: ( 1 ) protein, which is the constituent of living protoplasm; (2) cellulose and lignin, the constituents of cell walls; and (3) starch, as stored material in the following sequence. Figure 4 explains the rate of deposition of these three major constituents at different stages of growth. 2 . Conception of Crop Ecology There are few crops as widely distributed throughout the world as rice. This crop not only is cultivated in tropical regions, but also is grown as far north as 49" N in Czechoslovakia and as far south as 35" S in Australia. Temperature and day length during the growing season are the most important factors controlling the growth of the rice plant. Moomaw (1964) compared six localities in rice-growing areas from north to south: Sapporo and Konosu in Japan; Taipei in Taiwan; Los Bafios in the Philippines; Bogor in Indonesia, and Bukit Merah in Malaysia (see Fig. 5 ) .

247

PHYSIOLOGY OF T H E RICE PLANT

Environmental conditions in the rice growing areas in temperate regions are considerably different from those of the tropics; these conditions determine both the growth habit of the rice plant and the techI00

A

C

D E F G

I

80 60 40

20

0 FIG.4. Rate of accumulation of organic constituents of the rice plant at different stages of growth. AA, protein; 0---0,cellulose; X - - - X , lignin; 0 0. carbohydrate. A-G as in Fig. I legend.

niques of cultivation. At the same time, there are a great many native varieties throughout the world, these being selected both botanically and sociologically as being best suited for each particular environment. The pattern of growth of a variety will reflect both the characteristics of that variety and the environment pertaining in the particular locality. The selection of local varieties has been influenced, either consciously or unconsciously, by the traditional methods of cultivation endemic to the particular region. Consequently, a recommended variety which is growing in a region is not a wild type, but a cultivated variety which has been bred and selected to suit the particular environment. Accordingly, I wish to use the term “crop ecology,” which is different from the concept of t h e ecology of wild plants. Ishizuka and Tanaka (1956) conducted a series of experiments to illustrate the concept of crop ecology. They compared the growth of rice plants in 8 localities from northern to southern Japan and obtained the results shown in Table I . This table indicates that, although rice is a cultivated crop, it shows pronounced ecological characteristics reflecting the particular environmental conditions. Tanaka and Vergara ( 1967) extended this concept to the tropical regions (see Fig. 6 and Table 11).

248

YOSHlAKl ISHIZUKA

Sapporo, Japan

Konosu, Japan

M .+Dw-Los Bafios, Philippines

Bogor, Indonesia

TaipebTaiwan

A

35

,

5ON 0 Bukit Merod, Malaysia

I

30 25

v

f 20 a

c

En E

15

f

to 5 0

FIG.5 . Agro-climatological characteristics of the main rice-growing months in Asia. (From Moomaw and Vergara, 1964.)

From the above we see that the tendency for the characteristics of the rice plant to vary from north to south in Japan was observed also on a worldwide scale, including the tropical regions. On the basis of these experiments, Tanaka expressed the opinion that “under such circumstances productivity should be measured in terms of the grain yield per unit area per day in the field, e.g., 80 kg/ha/day.” Therefore, I wish to describe the characteristics of the rice plant, taking into consideration the concept of ecology. Information obtained from the study of the physiology of the rice plant

TABLE I Morphological and Physiological Characteristics of the Rice Plant Grown from the North to the South in Japan"

North

South

Grain: straw ratio

N in straw

Locality

Shoot length (cm)

Hokkaido Tohoku Hokuriku Kanto Tokai C hugoku Shikoku Kyushu

97 107 107 105 109 108 125 I12

1.03 1.07 0.80 1.10 0.57 0.69 0.76 0.59

(%)

P,O, in straw (96)

Difference between maximum tiliering and formation of flower primordia (days)

0.63 0.5 I 0.45 0.49 0.42 0.46 0.42 0.42

0.32 0.15 0.24 0.15 0.16 0.09 0.14 0.08

-9 0 6 6 5 15 8 14

"From lshizuka and Tanaka (1956).

...

_h

/

/

FIG.6. The places where the experiments were undertaken. (From Tanaka and Vergara, 1967.)

TABLE 11 Grain Yield, Straw Weight, Grain:Straw Ratio, and Growth Duration at Various Localities in the Far East"

No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14

Location* Sapporo Konosu Taipei

Taichung

Pingtung

Variety Shin-Ei Norin 25 Tainan 3 Bir-me-fun Tainan 3 Guze Tainan 3 Bir-me-fun Tainan 3 Guze Tainan 3 Bir-me-fun Tainan 3 Guze

Season

1 St

1 st 2nd 2nd 1st I St 2nd 2nd I st I St 2nd 2nd

Weight at harvest (ton/ha) Grain Straw 5.09 4.44 4.6 1 3.93 4.08 4.9 I 4.25 4.44 4.16 5.22 5.42 5.41 3.12 4.09

4.34 3.82 3.72 3.61 3.43 3.7 I 3.72 5.00 2.80 3.71 4.42 5.03 3.42 5.21

Grain :straw ratio

Growth duration (days)

1.17 1.16 1.24 I .09 1.19 1.32 1.14 0.89 I .48 I .38 I .23 I .08 0.9 I 0.79

I59 159 137 133 144 133 I68 161 142 I39 159 159 125 I28

IS

16 17 18 19 20 21 22 23 34 25 26 27 28 29 30 31

C hengmai Huntra Bangkehn

Los Baiios

Bukit Merah Bogor

Dawley 4-2 Meung Naung 62M Tah Pow G a e w I 6 I C o w Kuang 88 Nang M o n S-4 Puang Nahk 16 Tainan 3 BPI-76 Peta Tainan 3 Peta Pe-bi-fun Subang lntan I17 221/BC IV Su kanandi 221/BC IV Su kanandi

Main Main Main Main Main Main Wet Wet Wet Dry Dry Off Main Main Main Off Off

2.24 4.35 2.99 3.18 3.57 4.18 5.10 4.29 3.21 5.69 6.04 3.19 3.45 3.93 3.32 4.73 4.83

4.90 15.52 6.93 6.07 7.22 10.50 4.63 6.37 8.48 4.63 6.75 4.05 5.84 4.75 4.2 I 4.63 4.97

0.46 0.28 0.43 0.52 0.49 0.40 1.10 0.67 0.38 1.23 0.90 0.79 0.59 0.83 0.79 I .02 0.97

I25 151

I70 I48 154 183 I23 136 I36 137 137 125 I47 147 147 140 151

“From Tdnaka and Vergara ( 1967). Sapporo and Konosu, Japan: Taipei. Taichung. and Pingtung, Taiwan: Chengmai, Huntra, and Bangkhen, Thailand: Los Banos. Philippines: Bukit Merah, Malaysia: and Bogor, Indonesia.

252

YOSHlAKl ISHIZUKA

in India will not directly apply to rice grown in other areas. However, the same fundamental principles controlling the growth of the rice plant in India will also apply to other countries. In other words, the growth of the selected variety ( F ) in India is the function of the Indian environment, i.e., e = environment Growth = F (e) When we insert the Indian data in (e), we obtain the characteristics of the growth of Indian rice. When we use data from Taiwan in (e), we obtain the characteristics of the growth in Taiwan. Consequently, the most important research into the cultivation of the rice plant concerns finding the form of the above equation. This is the goal of crop ecology, and it must be kept in mind in any study of the rice plant. B.

ABSORPTION OF NUTRIENTS

1. Absorption of Nutrients by the Rice Plant Grown in Cool Regions One of the most important factors controlling rice yield is the amount and method of fertilizer application. Consequently it is essential to investigate all aspects of fertilizer use. The objective of a fertilizer program is to supply the correct amount of nutrients required by the plant at its particular stage of growth. The results of research carried out to study the uptake of nutrients by the rice plant at different stages of its growth are discussed below. Plant nutrient uptake varies in different localities, even when standard methods of cultivation are used. This is particularly true of rice. As already stated in Section 11, A, 2, this is due to such controlling factors as the natural conditions of soil and climate and the man-induced conditions of variety, method of cultivation, and amount of nutrient applied. Studies on the process of nutrient uptake date back to 19 18, when Aso (19 18) published an illustrated book describing the nutrient uptake of the rice plant at different stages of growth. Gericke ( 1924) described the importance of various plant nutrients at various stages of growth. Ishizuka (1932) tried to explain the subject systematically. Of recent years there have been many more investigations in the rice growing areas of the world in an attempt to gain more knowledge as to the process of nutrient uptake in the rice plant (Sircar, 1958; Asana and Sarin, 1968; Sims and Palace, 1968). Reference will be made to these publications later in this discussion. The process of nutrient uptake at different stages of growth is the function of climate, soil properties, amount of fertilizer applied, variety of rice and the method of cultivation. Accordingly, I wish to illustrate these functions as they operate in cool, temperate, and tropical regions.

PHYSIOLOGY OF T H E RICE PLANT

253

In Sapporo, the northern type of rice plant is cultivated. Sapporo is situated on latitude 43" N , has a mean temperature of 7.2"C, and is frost free for only 140 days. The climate is too severe for the growth of tropical rice plants. Rice crops must be sown as early as possible in the spring in sheltered seedling beds, so that there will be the maximum available time for crop growth. Transplanting is the customary practice among rice growers in this region. Ishizuka and Tanaka (1952) reported on the nutrient uptake of the variety representative of the region. Their investigations showed that the weight of seedlings did not increase for the first 15 days after germination, but increased rapidly after 20 days. The absorption of nutrients, however, was already quite appreciable 15 days after germination. Figure 7 shows the percentage content of nutrients in the seedling plants grown in nursery beds which received 60 g each of N , PzOs, and KzO per 3.3 m2. Dry matter

P, 05

5

10 15 2 0 25 2 8 Days

F I G .7 . Nutrient content of the rice plant under nursery conditions. (From lshizuka and Tanaka. 1952.)

The decrease in the percentage of N , P r o a ,and KzO after the maximum value has been reached means that the rate of photosynthesis increases more rapidly than the rate of nutrient uptake. These seedlings were transplanted in an ordinary alluvial paddy field to which fertilizer had been applied at a rate of 75 kg each of N , Pro5, and KrO per hectare. Table 111 and Fig. 8 show the nutrient contents at each stage of growth. The percentage of nitrogen in the plant is high at the early stage of

TABLE Ill Contents of Nutrients of the Rice Plant Grown in the Field (Percentage of Dry Matter)"

Nutrient

N P,O,

KyO CaO MgO

SO:$ SiO, Ash

Plant part

Transplanting 1yv1

Cornp1et e recovery from the damage by transplanting 2o/v I

Leaf and stem Ear Leaf and stem Ear Leaf and stem Ear Leaf and stem Ear Leaf and stem Ear Leaf and stem Ear Leaf and stem Ear Leaf and stem Ear

4.10

3.35

-

0.99 -

3.63 -

0.59 I .06 -

-

0.48 -

2.95 0.74 1.1 1

1.04

1.01 5.97 15.1 I

11.99

-

-

"From lshizuka and Tanaka (1952).

-

5.72 -

Vigorous tillering 3/VII 3.90 -

0.65 3.03 -

0.60 1.17 0.66 8.03 15.99 -

Formation of flower primordia 18/VII 3.4 I 0.84 2.35 -

0.44 0.83 -

0.54 -

7.32 14.63 -

Stem elongation 28/VII 2.18 2.53 0.80 1.31 1.79 2.65 0.36 0.30 0.68 0.88 0.34 0.54 6.88 0.50 12.31 6.20

Flowering 8/VllI 1.43 1.30 0.79 0.48 1.40 0.67 0.38 0.15

0.60 0.82 0.28 0.23 7.24 6.66 11.84 8.90

Milky Dough stage stage 18/VllI 2/lX 0.94 1.28 0.58 0.59 1.38 0.63 0.48 0.14 0.57 0.46 0.14 0.24 9.52 4.70 13.89 7.20

0.74 1.26 0.34 0.71 1.69 0.49 0.55 0.12 0.61 0.40 0.12 0.22 11.85 3.50 15.29 5.70

Complete ripening 21/1X 0.74 1.26 0.29 0.71 1.98 0.38 0.57 0.10 0.59 0.40 0.10 0.22 12.63 3.45 16.35 5.60

.e

0

v1

2

>

xN C

255

PHYSIOLOGY OF T H E RICE P L A N T

growth, temporarily decreases slightly after transplantation, and then increases until the formation of the flower primordia. It then steadily decreases until the dough stage, when it remains nearly constant until the grain is completely ripe.

100 140

120

l/Vll

I/VIII

I/IX l/VIl

0 -

l/VlIl

l/lX

FIG.8. Nutrient uptake of the rice plant at different stages of growth (northern part). 0, total: 0---0,stem and leaves. (From lshizuka and Tanaka, 1952.)

The percentage of phosphorus is high in the seedling stage, decreases rapidly after transplantation, and then increases gradually, as the plant recovers from the damage done at transplanting, and reaches a high level at the time of the formation of the flower primordia. This high percentage is maintained until flowering time, when it decreases until the dough stage. The percentage of potassium is high at transplanting and decreases gradually according to the growth of the plant. It increases again after, flowering until complete ripening. The levels of calcium follow very much the same pattern as those of potassium.

256

YOSHlAKl ISHIZUKA

2 . Absorption of Nutrients by the Rice Plant Grown in Temperate Regions

Research on the nutrient uptake of the rice plant in temperate regions in Japan has been carried out by many scientists, especially by J. Takahashi and Murayama (1955), Tanaka (1957), Murayamaet al.( 1957), Hagiwara et al. (1958), and Shiraishi et al. ( I 962). Hagiwara et al. (1958), who studied nutrient uptake in the southern part of Japan, selected five paddy fields in an area in Kyushu, at a latitude of 33" N and with an annual mean temperature of 15.7"C. Table IV and Fig. 9 outline their results. TABLE 1V Nutrient Uptake of the Rice Plant in Kyushu" Leaf Item"

Date

Dry weight (8) July

2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7 July 2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7 July 2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7 July 2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7 July 2 20

Blade

5.0 I 9.05 13.4 I I1.50 12.14 -

69 I 1.379 2.468 2.493 2,949 427 992 1.993 2, I96 2,336 196.6 245.8 323.3 20 I .2 127.4 -

Sheath

Stem

5.5 I 11.77 18.33 13.28 15.58 898 2.044 3.85 1 3,208 3,795 3,332 2.76 I 3,332 125.3 179.6 193.9 116.9 126.8 -

-

9.04 9.86 11.36 -

-

Ear Stalk Panicle

4.29 2 I .46 35.0 I -

-

-

823 1.435 I .7X6 525 1,272 52 0 832 1,007

509 1,624 3,068 409 1.247 1,787 -

-

88.5 66. I 94.6

-

-

61.4 298.8 489.8 -

Whole plant 0.33 2.05 10.52 20.82 46.70 57.59 75.75 76 345 1,589 3.423 7.738 8,898 I 1,810 6 19 952 2,264 6.3 I4 7. I30 8,578 2.6 42.7 32 1.9 425.4 686.3 702. I 853.9 I .7 19.1

257

PHYSIOLOGY OF T H E RICE PLANT T A B L E I V fconrinrted)

Item”

Date

Blade

3 24 Sept. 13 Oct. I0 Nov. 7 July 2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7 July 2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7 July 2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7 July 2 20 Aug. 3 24 Sept. 13 Oct. 10 Nov. 7

38.3 55.0 66.2 28.4 20.6 -

Aug.

Leaf Sheath

Stem

Stalk

50.6 95.4 103.0 35.2 23. I

48.6 5 I .o 32.4

-

-

-

-

-

Ear

-

-

-

-

-

-

165.1

103.8 108.5 43.5 22.8 42.4 25.2 54.6 77.0 86. I 99.5 -

32 I .0 237.4 163.4 156.7 15.5 33.9 54.3 12.6 30.6 -

-

-

15.5 29.2 46.9 38.6 47.3 -

19.6 36.6 55.7 16.3 20. I -

-

-

-

100.9 269.9 38 I .4 12.0 14.0 14.4 9.5 16.3 17.0 -

I .o

1.1

-

I .8 8.5

2.6 8.5 14.4 12.3

-

16.3 13.7

6.5 2.1 1.9

3.5 7.4 5.2

13.0 22.9 29.0 -

-

I .6

I .9 3 .0 -

3.9 2.0 I .5 -

0.6 0.9 0.5

Panicle

16.1 116.6 185.5 -

35.0 95.5 144.5 7.2 14.9 27.3 3.3 23.5 26.5 I .5 2.9 5.2

Whole plant 88.9 150.4 240.5 233.3 263.5 2.8 63.4 268.9 429.5 429.8 574.5 754.0 0.4 8.3 40.7 88.5 152.1 139.5 174.8 0.5 6.7 35. I 65.8 119.3 97.5 I 12.4 0. I 0.6 2. I 4.4 22.6 41.9 36.9

“ From

Hagiwara e l a / . ( 1958). ”For I hill, 3 plants.

The time of seeding in Kyushu is much different from that in Hokkaido, where the duration of growth is shorter than in Kyushu. However, the relationship between nutrient uptake and process of growth is similar physiologically. The only difference is in the uptake of potassium and calcium. In Kyushu, almost all potassium absorbed throughout the plant’s life is taken up by the early part of the ripening period, while calcium is absorbed until heading time. On the other hand, in Hokkaido

258

YOSHIAKI ISHIZUKA

the uptake of potassium and calcium continues to the end of the growth period. q/hill

900

-

800

-

700

-

500 400 600

200 300

100

-

FIG.9. Nutrient uptake of the rice plant at different stages of growth in Kyushu. (From Hagiwara el a/., 1958.)

3 . Absorption of Nutrients by the Rice Plant Grown in Tropical Regions Reports on nutrient uptake in the regions of low latitude include those of Chiu et al. (1960a,b) in Taiwan, and of Kanapathy (1959), and Lockard (1959) in Malaysia, and of Sims and Palace ( I 968) in the United States. In India, Daster and Malkani (1933) studied nutrient uptake from the standpoint of cation and anion balance and the hydrogen ion concentration at different stages of growth. The reports on nutrient uptake from the standpoint of crop ecology are few.

PHYSIOLOGY OF T H E RICE PLANT

259

Tanaka ( 1957) compared the pattern of nutrient uptake of an earlymaturing variety (PTB-10, 110 days), a medium-maturing variety (T14 I , 150 days), and a late-maturing variety (BAM-9, 165 days). Table V and Fig. 10 outline the results he obtained. Generally, the difference in the nutrient-uptake patterns among different-duration varieties in India is quite similar to the difference among localities in Japan from north to south. In Taiwan, Chiu et al. ( 1 960a,b) published results of a comparison between japonica and indica varieties from the standpoint of nutrient uptake. The pattern of nutrient uptake in the south is different from that in the north. This may result partly from differences in cultural systems and mainly from ecological and morphological differences. Table VI shows a comparison o f the rice plant in Japan with that in India. Generally, the weight of the grain in one plant is not affected by the locality or temperature. However, the weight of the straw is low in high latitudes or low temperatures and high in the low latitudes or high temperatures. Consequently, the ratio of weight of grain to weight of straw is high in the high latitudes and low in the low latitudes. If we suppose that straw is the product of vegetative growth and grain of reproductive growth, we may use the grain : straw ratio as an index to the relative strength of vegetative and reproductive growth. It is probable that in the process of the rice plant’s growth, the period from the seedling stage to the maximum tiller-number stage represents the vegetative-growth phase, while the period from the maximum tillernumber stage to complete maturity represents the reproductive phase. Using this assumption, it may be reasonable to estimate that a close connection exists between grain : straw ratio and the period between the maximum tiller-number stage and the flower-primordia formation stage. Table V I I makes evident this relationship. I n short, compared with the rice plant in the north, the rice plant in the south has taller shoots, fewer panicles, smaller panicles, longer intervals between the maximum tiller-number stage and the flower-primordiaformation stage, and less nitrogen content. The process of nitrogen absorption is parallel to the growth characteristics, as shown in Fig. 1 1. This tendency is also observed within a rather limited area in Japan. The seedling before transplanting also has some characteristics which vary with locality. The seedling in the north must have a high nutrient content because the duration in the field is short. On the contrary, in the south, if the growth of the seedling is vigorous, retardation of nutrient uptake will occur in the later stage of growth. Accordingly, the farmer

TABLE V Dry-Matter Weight and Nitrogen Content of Different Duration Rice Varieties in India" Variety

Dry matter Plant and N (%) parts ~

PTB- I0 Dry matter (mg/hill) N (%) Ear T- I4 I Dry matter (mg/hill) N (%) Ear BAM-9 Dry matter (mg/hill) N (%o) Ear

-

~

~

~

10

0 ~

20

~

40

30 ~

50

Days after germination 60 70 80 90

100

110

120

130

~

Straw 0.20 0.50 1.60 5.10 9.70 15.20 18.40 14.70 6.70 13.50 Ear 2.10 Straw I .24 2.17 2.52 1.99 1.25 0.95 0.76 I .57 Ear 1.1 1 1.18 1.12 straw 0.20 0.80 2.30 8.40 15.60 24.40 36.30 53.40 68.70 72.20 67.50 62.90 41.10 6.80 10.60 22.10 30.90 Ear Straw 1.24 2.8 I 3.18 2.52 0.99 0.92 0.89 0.85 0.80 0.44 0.37 I .82 1.33 1.52 1.30 1.00 1.03 Ear Straw 0.30 0.90 3.10 8.50 18.60 30.60 42.60 47.60 48.50 55.00 70.00 72.50 68.10 51.80 47.20 6.00 14.00 21.50 28.10 Ear 1.06 1.00 1.99 1.20 1.04 0.78 0.64 0.65 0.53 I .40 I .oo Straw 1.17 2.96 3.18 2.51 1.04 1.12 1.07 1.05 Ear

"From Tanaka (1957).

PHYSIOLOGY OF T H E RICE PLANT

26 1

::h

P t b 10 ( E a r l y Duration)

10

20

40

days after transplanting

60

30 t (Late Dura t i o n )

I

' O t

t

Time of the formation of flower primordia

FIG. 10. Rate of nitrogen uptake of rice varieties of different durations in India. (From Tanaka, 1957.) TABLE VI Comparison of the Rice Plant in Japan and in India

Locality

Variety

Northern Japan Southern Japan India

Chusei-Eiko Asahi T-141

Shoot length (cm) 97 108

I54

Ratio, weight of ear: weight of straw

N in straw

1.03 0.69 0.50

0.82 0.55 0.37

("lo)

TABLE VII The Relation between the Time of Maximum Tillering and the Formation of Flower Primordia

Time Time of maximum tillering ( I ) Time of the formation of flower primordia (11) Duration (days) from (I) to (11)

Northern Japan (Hokkaido)

Southern Japan (Shikoku)

India (Cuttack)

Aug. 2

Aug. 4

Aug. 25

July 24

Aug. 19

Sept. 26

+ I5

t 32

-9

262

YOSHIAKI ISHIZUKA

adjusts the C : N ratio of the seedling in each district by experience (Table VI I I). rng N / hill

450

1

P t b 10

I50 days after transplanting

20 40 -60

mg N / h i l l BAM 9

L

600

300

i/ d I L I . 1

"ll"

LEAVES

20

60

160

120

FIG.I I . Nitrogen uptake of different rice varieties in India. (From Tanaka et al., 1959.) TABLE V l l l Characteristics of Seedlings at Transplanting Time in Japan from the North to the South Characteristic Hokkaido Tohoku Hokuriku Kanto Tokai Chugoku Shikoku Kyushu Temperature at the time of transplanting ("C) Length of seedlings (crn) Number of tillers Dry weight (g) N o/o (dry matter) P,OS o/o K2O % C:N

14

16

18

22

23

24

24

25

18

18

25

34

24

33

29

33

I

I

3

I

I

I

I

I

0.037

0.057

0.205

0.135

0.120

0.255

0.153

0.1 I5

2.96

2.44

4.18

1.72

1.48

I .44

1.16

1.12

0.94 4.80 9

0.7 I 4.79 9

I .09 5.00 9

0.89 4.52 13

0.57 4.93 13

0.63 3.09 20

0.63 4.24 20

0.74 4.30 20

'I

PHYSIOLOGY O F THE RICE PLANT

263

C. PHYSIOLOGICAL FUNCTIONS OF T H E COMPONENT ORGANS OF T H E R I C E PLANT

I . Concept of Functional Units In expressing their opinion on the concept of functional units of the rice plant, Ishizuka and Tanaka (1963) stated that the development of a rice plant should be considered as an assembled body containing many units of different ages. The unit out of which the rice plant is constructed is repeated at each node, and consists of a leaf, a tillered bud, and an internode, as shown in Fig. 12.

FIG. 12. Constitution of a unit of rice plant.

If any one of these construction units is separated from an individual plant and given the appropriate environment, it can develop into a separate and entire plant. Each tillering bud which is stimulated into growth develops a culm with a series of nodes and accompanying structures, the same as the original plant. It follows that each tiller has the potential to produce a panicle at the uppermost internode of the stem. Tanaka ( 1 961) designed an experiment at the ripening stage of the rice plant. They observed the distribution of '?C assimilated in the 12/0 leaf, as shown in Fig. 13. The distribution of I4C was highest in the ear because the culm (ear, 12/0) is the pathway of I4Cassimilated in 12/0. At t h e same time a measurable quantity of"C was found to be distributed in the culm (12/0-1 ]lo). On the contrary, no measurable amount was found in the leaf of I l/O, and in the culm ( I I/O- lO/O). Thus, generally speaking, the leaf blade mln, the leaf sheath m/0 and culm, m/n-(m-n)/n, make a growth unit in the rice plant. I t is common to express the nitrogen content of, for example, leaves at flowering time as x % . If, however, we take this to mean that, at flowering time, the nitrogen content of each leaf is x%, it will be misleading. If

264

Y OSH I AKI ISHIZU KA

each unit, as described above, is examined precisely or microchemically, the percentage of nitrogen at flowering time is only the mathematical mean of each different leaf on the unit. It does not represent any of the physiological activity of the leaf on the individual unit at flowering time.

Q,

2562

FIG.13. Distribution of “C assimilated at 12/0 leaf at milky stage.

From this point of view, a plant can be considered as a sequence of individual structural units, and the age of the whole plant does not mean the age of the individual structural unit. 2. Leaf Tanaka ( I96 I ) planned a series of experiments designed to evaluate the contribution which leaves make to the yield of the rice plant. First he recorded the dry weight of leaves on the main stem to measure the weight fluctuations at successive stages of growth. Before describing these investigations it is necessary to clarify the system of leaf nomenclature. Figure 14 shows the nomenclature of leaves as suggested by Nakayama. This system is commonly adopted by rice scientists. Under this method, the third leaf on the main stem, for example, would be symbolized by 3/0, where 0 means the main stem. According to Tanaka, the dry weight of a leaf increases at its early stage of growth, reaches a maximum, and then decreases. After a period this weight decrease ceases and the weight remains constant. It is thus obvious that at certain stages of growth of the rice plant, the weight of some leaves is increasing and of others, decreasing. That is, the increase

PHYSIOLOGY OF T H E RICE PLANT

--

L

0

W

265

Lo

U

2

a

266

YOSHlAKl ISHIZUKA

in the total weight of a plant at any given moment is the algebraic sum of the increase and decrease of weight of the component leaves. Regardless of the increase or decrease in the total weight of the plant, some leaves are gaining weight and others are losing weight. The growth of the rice plant can be considered to be a chain reaction. The growth of 1/0 is indispensable to the growth of 2/0, and 3/0 grows with the help of 2/0 and I/O. Generally n / 0 is formed with the help of (n-l)/O, (n-2)/0,and (n-x)/O, and contributes to the growth of (n+ I)/O, (n+2)/0, and (n+x)/O. The meaning of x will be explained later. A leaf at its maximum weight appears to discharge the greatest physiological function of all the leaves at that particular time. Tanaka named this leaf the "Active Center Leaf." T o illustrate this concept, he determined the photosynthetic activity of leaves at varying positions on the main stem, as shown in Table IX. H e concluded that the leaves on the TABLE IX Photosynthetic Activity of Leaves at Various Position on the Main Stem"

Date of Measurement

Leaf

June 28

July 27

Sept. 4

COr uptake (Mg1100 cm2/hr)

13.0 36.6 58.7" 15.0 18.3 26.6* 20.3 14.1 1I.]* 6.1

"From Tanaka (1961). "7/0 is just its morphological expansion on June 28. "*shows the active center leaf at each stage.

main stem can be classified by their functions into the following four groups, as shown in Fig. 15. The leaves ( 1 /0-2/0), which emerge at the seedling stage, influence the ability of the plant to recover from the transplanting operation. Leaves (3/0-S/O), which emerge while the plant is recovering from transplanting, affect the number of tillers. Leaves (6/0-9/0), which emerge during tillering, affect the elongation of the stem and the formation of spikelets, while (lO/O- 12/0), emerging during the elongation phase, influence the degree of ripening.

267

PHYSIOLOGY OF T H E RICE P L A N T

Establishing

::::I-

Tillering Elongation and spikelet formation Ripening

FIG. 15. Diagram of the characteristic predominant function of each leaf on main stem. (From Tanaka, I96 I .)

From these facts it may be generally concluded that the growth during any given stage is mainly influenced by the ability of the leaves formed at one stage to contribute to the growth of the next stage. In other words, rice plants develop phase by phase. This concept greatly influenced future research. T o clarify the relationship between leaves on the main stem, Tanaka carried out many experiments, the conclusions from which are shown in Table X. TABLE X The Distribution of 'T Assimilated at I I/O, 9/0, 7/0 (cpm/lOmg) ~~

Organ Ear primordia Leaf blade

6-tiller Roots

Dry weight

I210 I I10 1010 910 810 710 -

4 52 I94 143 102 50 28 I03 368

~~

'Twas assimilated at 7/0

9/0

1 I/O

30 I67 77 50 25 20 38126 2209 623

1585 7333 240 41 33427 22 10 1757 325

2665 I4004 1921 50 12 14 26 41 209

On July 27 either 1 I/O, 9/0, or 7/0 was exposed to 'TOn, and the distribution of I4C after 24 hours was estimated. At this stage either lO/O or 1 1 / O was the active center leaf. The I4C assimilated at 7/0 was vigorously translocated to the roots and tillers; I4C assimilated 9/0 was actively translocated to 12/0, to the ear primordia and to the elongated stem. A considerable amount of I4Cwas translocated into the tillers and roots. The I4C assimilated at 1 l / O entered very actively into the 12/0, ear and elongating stem. In this case very little was translocated to the tillers or roots. From these results, it is evident that after the beginning of internode

268

YOSHlAKl ISHIZUKA

elongation, there is a division of activities among leaves. The upper leaves which have elongated internodes are intimately related to the growing point of the stem on which the leaf emerges. The lower leaves which have no elongated internode are intimately related to roots of the stem and also to tillers. The assimilation products of the lower leaves translocate to roots and are consumed there by respiration. This respiration promotes absorption of elements by roots. The elements, thus absorbed, translocate to the active center leaves and also growing points of the shoot. The assimilation products of the active center leaves translocate to the growing points, where they are taken into constituents of the growing organs. In this way, each leaf discharges its characteristic functions corresponding to its position. The same type of experiment was conducted on August 2 1, at the milky stage. IJC was assimilated at 12/0, lO/O, or 8/0, as shown in Table XI. TABLE XI The Distribution of '"C Assimilated at 810, 1010, I210 Dry weight

Organ Ear Leaf blade

1210 I I10 I010 910 810

Roots

-

505 I40 2 10 190 I20 70 5 00

I T was assimilated at 810

1010

I210

60 I06 66 50 40 5 I360 444

3 70 I60 130 26560 34 0 0

2562 36 I24 0 0 0 0 0

The I4C assimilated at 8/0 translocated actively to stem base and roots. However, it does not enter appreciably into upper leaves, stem, and ear. On the other hand, the I'C assimilated at 12/0 actively enters into the ear. In this case, no translocation to roots and leaves occurs below I1/0, the behavior of l'C assimilated at 1 O/O is intermediate between the case of 810 and 12/0. During the maturing phase, assimilation products in the flag leaf or the next leaf, enter into ear, but they do not move downward. The assimilation products in the lower leaves which have no elongated internode enter into stem base and roots, but not into upper organs. From the investigations of Tanaka it was evident that the nutrient contents of a leaf at a given stage will influence future growth, as well as yield.

PHYSIOLOGY OF T H E RICE P L A N T

269

Other scientists (Hasegawa, 1960; M . Nagai, 196 1) began to study the significance of the nutrient content of a definite leaf at a specific stage of growth, from the point of view of leaf diagnosis. Angladette (1964) summarized the results of investigations on the foliar analysis of the rice plant.

3 . Tillers Does tillering result in increased yields? This is a complex problem. Duncan (1969) stated in his discussion that it is disturbing to realize that tillering plants, such as rice, are usually grown in a multiple-plant hill, which the computer has shown to be the worst way to grow this crop. This is not to say that a tillering plant might not have advantages in specific localities, e.g., in Japan, where the individual plants are normally set out by hand. It is a matter of plant geometry and of the ability to control tillering. Chandler expressed his opinion, quoting the research of Tanaka et al. ( 1966a) as follows: “ I t is generally conceded that the traditional tall tropical varieties are usually heavy-tillering. In the early variety-fertilizerinteraction studies conducted at I R R I , as well as elsewhere, these highly vegetative varieties were compared with the medium-tillering, but shorter ponlai varieties which respond much better to heavy applications of nitrogen. The conclusion was rightfully reached from these studies that a medium-tillering variety should be sought and that too-heavy tillering would result in excessive mutual shading within each hill, even at a fairly high planting distance.” When we try to get higher yields by promoting tillering, we must study the physiological and nutritional relationship between the mother stem and the tillers. The nutrients necessary to produce vigorous tillering are N , P, and S in the presence of sufficient carbohydrates. Hisamura ( 1956) observed it positive correlation between N content at the tillering stage and the number of tillers. Kiuchi and Ishizaka (1960) recognized the significance of the absorption rate of N in promoting tiller-numbers, and Oshima ( 1962) pointed out the significance of soluble nitrogen in the stem. K. Yamasaki (1960) reported that environmental conditions do not influence the initiation of the tiller bud, which appears at the outer basal part of the leaf sheath. However, t h e growth of the initiated tiller bud is greatly influenced by environmental conditions. Tanaka also estimated that the critical percentage of leaf nitrogen which will support the growth of a tiller is 3.5%; when this figure falls to 2.5%, the growth of the tiller ceases. For phosphorus, Honya ( 1958) estimated the critical percentage to be 0.25% Pro,. In my opinion the critical concentration of SO, should be very much the

270

Y O S H l A K l ISHIZUKA

same as for P20,. N. Takahashi et al. ( I 956) investigated the relationship between the growth of tillers and the nutrient supply and concluded that, in all cases, in the potassium- and phosphorus-deficient plant, soluble carbohydrates increase in the stem as the tiller develops. Nakata (1967) and Tanaka and Garcia (1965) also made extensive studies on the factors controlling tillering in rice. 4 . Stem

In the early stages of growth there is no elongation of the stem. During the middle stage of growth the lower internode begins to elongate; later, the upper nodes begin to elongate. Arashi and Eguchi ( 1955) made exact studies of the pattern of elongation. They also studied the pattern of accumulation of starch in the stem in temperate regions, while Tanaka ( I958b) repeated this investigation with rice in a cool region. However, because the part played by the stem is relatively unimportant from the physiological point of view, relatively little work has been done in this field. Because of the correlation between the nature of the stem and susceptibility to lodging, the morphology of the rice stem has been fairly extensively investigated. 5 . Ear The growth of the ear will have to be discussed in two parts: (1) the growth of the panicle before flowering; (2) the growth of the panicle after fertilization; this is the process of ripening. In part 1 the number of spikelets in an ear and the size and health of the spikelets will be studied, while in part 2 the factors influencing the weight of the grain will be considered, along with the ripening percentage. The process of the growth of the panicle was carefully studied by Matsushima ( I 957), and the processes whereby each spikelet in an ear is ripened were extensively investigated by Nagato and Sugawara (1952). There are two approaches to the study of the ripening process of rice; the first is biochemical and the second is to find out the relationship between leaf and ear, and how to increase yields. The way in which organic substances are accumulated in the ear has been studied by many scientists, e.g., Togari et al. (1954), Togari and Sato ( I 96 I), Murayama et al. ( I 9 5 3 , Soga and Nozaki ( I 957), Asada ( 1963a), Aimi ( 19601, and lshizuka and Tanaka ( 195323). Their researches were mostly designed to answer the three following questions: (1) D o all leaves directly contribute to the ripening of the crop? (2) Does the carbohydrate which was stored in the sheath before heading

PHYSIOLOGY OF T H E RICE PLANT

27 I

contribute to the ripening? (3) How many leaves should we normally have at the time of ripening to get a high yield? As already discussed in Section 11, C, 2, it is evident that the 3-4 leaves from the flag leaf will considerably influence ripening. lnosaka ( 1 958) demonstrated that, in the case of the translocation of metabolites from leaves to ear, each panicle branch has a close connection with a definite leaf, by observing the distribution of 3sP assimilated by the flag leaf and the leaf second from the flag leaf 7-10 days after heading. Of course, the growth of the ear is very much dependent upon the amount of solar energy. Matsushima (1957) carefully investigated the effect of shading on the number of ears and number of spikelets on the panicle, as well as on ripening, grain weight, and yield. He also studied the influence of applications of nitrogen, and concluded that 150 kg N per hectare produced the maximum number of ears by giving an equilibrium between photosynthesis and the nitrogen concentration in the body of the plant. I t also produced the maximum number of grains per ear. Grain sterility when nitrogen is applied at 150 kg/ha is only slightly greater than when nitrogen is applied at 75 kg/ha, but is considerably greater than when it is applied only at 30 kg/ha. The less the amount of nitrogen applied, the greater will be the weight of 1000 grains. Hisamura ( 1956) found a close connection between the percentage of nitrogen in the leaf and the number of spikelets on the one panicle, and showed a linear correlation between these within the limits of I .5-3.5% N in the leaf. Kiuchi and lshizaka ( I 960) found that the percentage of N in the leaf must be greater than 1.2% if seventy spikelets are to be maintained on the one panicle. Tokari et al. ( 1958) conducted many experiments to ascertain why sterility increases with heavy nitrogen dressings, and also studied another form of sterility induced by heavy applications of nitrogen applied under conditions of inadquate light intensity. Heavy applications of nitrogen also produce a decrease in the amount of budding of spores on the stigma. It was found that, under similar conditions, the amount of germinated pollen on the stigma was reduced, this being attributed to the increased occurrence of incomplete dehiscing of the anthers and the abnormal behavior of the filaments at the time of flowering. I n lndica rice, which is believed to have a higher percentage of sterility than Japonica rice, it was found that sterility was closely related to the degree of nitrogen response. According to the work of Ota and Yamada ( 1965) in Ceylon, heavy applications of nitrogen fertilizer greatly increased the incidence of sterility, sometimes up to nearly 100% in the case of a low nitrogen-response variety, whereas sterility was less in a high nitrogen-response variety.

272

YOSHIAKI ISHIZUKA

These relationships were also demonstrated in experiments conducted at Kamikawa Agricultural Experimental Station, Japan, as shown in Table XI1 TABLE XI1 The Relationships between Nitrogen Applications and Yield Components N applied (kg/ha) Length of plant (cm) Number of ears Main stem Tillering, 1st order Tillering, 2nd order Number of grains Main stem on panicle Tillering, 1st order Tillering, 2nd order Main stem Sterility (%) Tillering, 1st order Tillering, 2nd order Main stem Weight of 1000 grains (g) Tillering, 1st order Tillering, 2nd order N percentage Panicle Leaf and stem

0 80

I

75 91 I

150 I02 I

300 I13 I

600 I I3 I

3.2

4.0

4.5

4.9

5.8

I .2 83

2.2 92

3.8 123

3.5 I07

2.5 99

48

60

79

79

68

21 19

31 21

41

37

44 59

35 65

13

18

50

76

82

7 27.6

22 26.3

81 25.8

84

25.2

93 25.5

26.7

26.5

25.4

25.3

23.7

26.9 1.18 0.40

25.8 1.26 0.36

24.3 I .25 0.64

17.4 1.33 1.79

14.4 1.36 1.96

It is widely recognized that, in the case of the rice plant, the lower the nitrogen supply at the heading stage, the greater will be the accumulation of carbohydrates (Fujiwara et al., 1951; N. Takahashi et al., 1956). In practice, it would appear that the maximum total weight of grain is obtained when the concentration of nitrogen in the leaf is from 1.0 to 1.2% (Kumura, 1957), and Kiuchi and Ishizaka (1960) reported that, to obtain the maximum weight for each individual grain, the concentration of nitrogen in the leaf should be 1.2-1.8% at the time of heading and 0.9-0.85% at harvest time. 6 . Root

The roots of the rice plant comprise (a) embryonic root and (b) adventitious roots. Inada and Baba (1952, 1955, 1957, 1960, 1962) con-

PHYSIOLOGY OF T H E RICE PLANT

273

ducted a series of experiments to determine the physiological function of the roots. In their investigations they divided the roots into four types, according to color and age, and defined the function of each type. When a root appears from the base of the node, it is necessary that nitrogen be provided from the mother node. Okajima (1958) found that, when the nitrogen content of the culm exceeds 1 %, new roots continue to appear. Under such circumstances the nitrogen content of the new root is about 1.5%. When the nitrogen content of the base of the culm is 1 %, the generation of new roots ceases, and the existing roots elongate to a marked extent. When the nitrogen content drops to 0.75%, the generation of new roots and elongation of existing roots cease. This means that the ratio of protoplasm and membrane substance is controlled by the carbohydrates translocated from the leaves and by the amount of nitrogen that has been absorbed. Roots thus developed have to maintain life in stagnant water. Consequently the physiology or behavior of the roots of rice plants will greatly differ from those of upland crops. The first investigations were designed to study the process of respiration. Inada divided the roots into four groups, based on their age, and demonstrated that the younger the root, the more active was its respiration. In any one root respiratory activity and the activity of cytochrome oxidase are greater at the tip than at the base. Conversely, the activity of dehydrogenase is greater at the base. In the case of a young root, the active movement of the hydrogenase system and high potentiality of the cytochrome oxidase promote the activity of the whole respiratory system. At the same time, in the young root-tissues, the cells are in a state of high turgidity with a high level of protoplasm, and are in an optimum condition for an active metabolism providing there are adequate levels of N and K. On the contrary, an old root or the basal portion of a root differ from a young root in that they are in a more oxidative state, with a weaker activity of the dehydrogenase system. The above facts suggest there are two types of respiration. To understand the activity of the root of rice plant, we must take the factor of metabolic absorption into consideration. As discussed earlier, oxygen produced in the leaves by photosynthesis is translocated through the plant to roots (Alberta, 1953; Van Raalte, 1940; Arikado, 1954; Aimi, 1960). The rice plant, in common with other plants of swampy soil, has the ability to oxidize the rhizosphere, as was demonstrated by Kumada ( 1948) and Mitsui el al. ( 1948). In order to evaluate this oxidizing ability, Nomoto and Ishikawa ( 1950) proposed using a-naphthylamine (a-NA),

274

YOSHlAKl ISHIZUKA

which is converted after oxidation to oxynaphthylamine which develops a red color. Mitsui et al. ( 196 I ) reported that the acetate which was produced in the root from acetyl-CoA is decomposed to COz via the glycolic acid cycle, producing HeOn during the process. This H z O z is decomposed by a catalase, with the production of Or, which becomes a source of oxygen available to the roots. When a paddy soil is in a reducing condition it produces HeS, which will inhibit root respiration. However, the On translocated from the leaves to the roots will enable the plant to survive this condition. The formation of H n S procedes rapidly at a pH of 7.0 in the presence of Fe, where the rice roots have iron oxide deposited on their surface. According to Okajima (1958), the ability of the rice root to reduce the medium is largely dependent on the nutritional status of the plant. He investigated the production of H,S in nutrient solutions which received varying sources of N ; the results are shown in Fig. 16. S" rn g / pot

I

42

S"

i.

S"

A

0 ,,ne

4

JLIY

2

ULI

Y

30

A 4

27

FIG. 16. The relation between time of nitrogen application and production of S" in media. (From Okajima. 1958.)

The experiment showed that the reducing effect of the root has no correlation with the stage of growth of the rice plant, but is a phenomenon which occurs under conditions of nitrogen deficiency. Arikado (1965, 1967) compared the relationship between respiration and nutrient absorption under different redox potentials.

275

PHYSIOLOGY OF THE RICE PLANT

Dynamic Approach: Fundamental Research for Higher Yield

Ill.

A.

BLUEPRINTTO OBTAINH I G H Y I E L DO F RICE U S I N G ALL PRESENT KNOWLEDGE

I . Statistics of Rice Yields Even though the same variety of rice and adequate fertilizers are used, great differences still exist in rice yields among farmers -even in the same region. If, within a region, the lower yields could be brought up to the levels obtained by good farmers, the production of the region would obviously be increased. To this end, agronomists have started to prepare a blueprint showing how average farmers, under normal conditions can obtain a definite yield per hectare. What will we consider to be a high yield? As shown in Table XI11 the yield of brown rice in Japan in 9 0 0 was ~ ~ approximately 1 ton/ha; recently a yield of 4 tons per hectare was recorded. Table XIV shows the national average yield of rice-producing countries in the world. TABLE X l l l Change of Yield (metric tons) in Japan since 800 A D Average

Chronicle

of rice field (million ha)

Total yield (million tons)

Yield (tons/ha)

I05

106

I550

150- I20

I720

I64

I80 31s

I .o I I .65 I .92

I840 1878- I887 1900- 19 I7

I56 258 300

300 477 794

I .92 1.85 2.64

1938- I942

318

953

2.99

1956-196.5

313

I238

3.95

800-900

"( Morinaga)

Remarks

-

Systematic introduction of irrigation system -

Scientific varietal improvement U s e of fertilizers Heavy use of fertilizers and agricultural chemicals

276

YOSHlAKl ISHIZUKA

TABLE XIV Rough Rice; Area, Yield per Hectare, and Production in Some Selected Rice-Growing Countries I968 ( F A O )

Country Brazil Burma Cambodia Ceylon China (Taiwan) Dominican Republic El Salvador India Indonesia Italy Japan Laos Malaysia (West) Mexico Nepal Nicaragua Pakistan Panama Peru Philippines Portugal Republic of Korea Spain Thailand UAR USA Vietnam (South)

Area ha)

Average yield (tons/ha)"

4.29I" 4.516' 2,376 s72 837

1.583 I .469 I ,482 2.378 3.9 I3

( I000

89"

20" 36.722" 7.760 I54 3,280 960" 456 I67 I , I I 9" 27 I1.513 1 30"

63 3,199 33 1,246" 63 6.799 506 9.52 2,300

I .65 I 2.500

1.547 I .96S

5.260 5.713 .817 2.377 2.724 I .98 I

2.407 1.650 1.162 3.063 I .250 4.636 3.908 6.349 1.618 4.644 5.018 I .956

Production metric tons)

( 1000

6,792" 6,636" 3.52I 1,360

3,275 147" 5 0

5 6.787" I 5.249

810 18,740 78411 1,084 455 2,217" 65 18,994 151"

193 4,000 IS3 4,869" 400 1 1.000

2,350 4,777 4,500

"Note: Yield information (kg/ha) computed by IRRI based on figures in published table (except Burma, Dominican Republic, and El Salvador). "Area and production figures are for 1967. L. Area and production figures are for 1966.

According to the above figure, it would be reasonable to aim for a goal of 6 tons/ha at the present time. 2 . Conception of Yield Components

When we want to get a good supply of water, we have to have a large vessel and fill it with water. However, if the vessel is too large, compared with the supply of water, this will be inefficient. To get a high yield, we have to have an adequate number of kernels, all of which we must fill with starch. Consequently, it is necessary to

277

PHYSIOLOGY OF T H E RICE PLANT

have an exact knowledge of the causal relationships and the time sequences of the processes of yield production. In grain crops, the process of yield production may be divided into the following three phases: ( 1 ) formation of organs for nutrient absorption and photosynthesis; (2) formation of flower organs and “yield container” in the above sense; (3) production accumulation of “yield contents.” According to Matsushima (1957) (Fig. 17), the upper limit of kernel

NUMBER OF PANICLES PER UNIT AREA I

RIPENED GRAINS

1000 KERNELS

OF KERNELS I (

1

I

l

l

I

1

I l l

1

I

10

20

JUNE JULY AUG 25 10 20 I

SEPT. I

20

OCT I

I I-

20 > c a

a.

c Q

10

W

2

LO

3

_I

v) a

5

Z

a a I-

v) c

0

I

FIG.17. Schematic representation of the yield-determining process at Konosu. (From Matsushima, 1957).

278

YOSHlAKl ISHIZUKA

growth is imposed in rice plants by the size of the hulls, which is determined I week before heading (flowering). Thus, the “physical” capacity for grain yield, which can be broken down into the following three components, is determined at a comparatively early stage of growth: Capacity of “yield container” = (number of panicles per (number of spikelets per panicle) X (size of hull)

El) X

The number of panicles is determined about 10 days after the maximumtiller-number stage; and the number of spikelets per panicle, about 10 days before flowering. Practically speaking, the number of panicles per m’ means the number of panicles on a hill with normal and medium growth times the number of hills in 2. This number reflects the environmental conditions at the maximum tillering stage, including nutrition, and the photosynthetic activity of the related leaves. The number of spikelets means the average number of spikelets in a panicle. This will be determined by the difference between the number of spikelets initiated and of those that do not develop. T o get a higher yield, we must first make the container as large as possible, because we cannot expect a yield greater than the capacity of the container. Then the yield determination will be dependent upon the

Y o = (percentage of spikelets bearing a ripe grain) x (average weight of a grain) Ripening percentage means the total number of perfectly ripened spikelets divided by the total number of spikelets on a panicle. Normally, a well ripened spikelet is one with a specific weight greater than 1.06. This percentage depends chiefly upon the nutritional conditions provided for the rice plant after heading, as well as climatic or photosynthetic conditions. Low temperatures below 15°C at the time of pollen-cell division and the time of pollination will decrease this percentage. The length of sunshine hours after pollination also influences this figure. The weight of grain is also a major factor influencing yield. Usually this is expressed by the weight of 1000 brown rice grains. As described by Matsushima, this is affected by the photosynthesis of the active leaves after heading, as well as by the level of nutrition of the rice plant. However, we must keep in mind that a reciprocal relationship exists between yield containers and yield determiners. When we expect to get higher yields, the container must be large; however, if the size of container exceeds a certain limit, it becomes dif-

PHYSIOLOGY OF T H E RICE P L A N T

279

ficult to fill it and results in a decrease in yield because of the production of many poor grains. T o keep harmony between the two, a careful study of the nutrient conditions of the rice plant must be made throughout the life of the plant. This problem is discussed further in Section 111, F, 1.

3 . An Example of Cultural Manipulation The anticipated yield of brown rice from 10 ares (1000 iii') can be expressed theoretically by the following equation.

Yield (of brown rice) from 10 ares = No. of spikelets per m' (No. of ear/m2X No. of spikelets/ear) x percentage of spikelets bearing ripe grain X average weight of grain (based on 1000 grains) X 1000 For example, the following combination of yield components would result in a yield of 600 kg/lO ares (6 tons/ha) 600 kg/lO ares = 32,000 spikelets/K2 (400 ears/K2 X 80 spikelets/ear) X 0.85 (fraction of spikelets with mature seed) ~ 0 . 2 g2 (22 g/lOOO grains) x 1000

It would seem that this type of blueprint would not be too difficult to follow. The number of spikelets per ear and the weight of 1000 grains are important. T o obtain 6 tons/ha we need: (a) 25 pIants/m'; (b) 16 effective tillers/plant; (c) 80 spikelets/ear; (d) 85% of spikelets with mature grain; (e) 0.022 g/seed. Under reasonably good weather conditions, the above blueprint could be implemented using the ordinary japonica varieties, which are widely cultivated in Japan. The application of fertilizer, however, requires knowledge based on research and field trials. This topic is discussed in Section 111, F, I .

B. THESEARCH FOR M A X I M UYIELD M

To what degree can we raise the yield of crops? This is one of the problems which has attracted a great many scientists. Miiller ( I 960), Bonner ( I96 I ), Takeda ( I962), Murata ( 1963, and Tsunoda ( 1962) all explored this problem in connection with rice production. Recently, this problem was discussed theoretically by a symposium held at the University of Nebraska and edited by Eastin et a f . (1968). I n this section, I will express some opinions as to how maximum yield of rice may be obtained.

280

YOSHlAKl ISHIZUKA

Most people when discussing this subject, emphasize that the following factors are of major importance: (a) total solar energy per acre per day; (b) the energy of the light waves which will be utilized for photosynthesis; (c) its absorption by the leaf; (d) efficiency of transformation of solar energy to chemical energy; (e) efficiency of assimilation; (f) time taken to produce the yield factor; (8) distribution of assimilates to the storage points. The Japanese scientists mentioned above made a trial calculation using the above factors, as shown in Table XV. (a) is fixed by the locality (in Japan, the estimate is 4000-5000 kcal). (b) The figure is calculated by Loomis (1963). (c) By the study of plant TABLE X V Energy Efficiency and Rice Yield: Trial Calculation (Tsunoda) Takeda ( 1962)

Factor

Anticipated maximum yield

(a) Total solar energy 5000 per m-'/day (kcal) 50 (b) % of energy of wave utilizable for photosynthesis ( c ) Rate of absorption 100 by leaf (%) (d) Conversion rate to 30 chemical energy (%) (e) Ratio of pure assimi40 ates against total assimilation (%) Degree of utilization 6.7 of energy in field (%) (b)x(c)x(d)x(e) Pure assimilate at 333 m2/day (kcal) (90 g rice) (a)x(b)x(c)x(d)x(e) (f) Days required to 40 produce it under above conditions 100 (g) Distribution ratio Yield per rd (kcal) 13,333 (a)(b)(c)(d)(e)(D(g) (3.6 kg) Yield of rice per 36 ha of land (tons)

Tsunoda ( I 962)

Murata ( I 965) Anticipated maximum yield

Average yield in Japan

Maximum yield in Japan

Anticipated maximum yield

3865

4000

4000

4000

44

50

50

50

91

80

92

92

27

7

10

20

50

50

50

50

5.5

1.3

2.3

4.6

210 (60)

53

(15)

92 (27)

184 (53)

40

28

40

80

100

100 I470 (0.42) 4

8400 (2.4) 16

I00

I00

3680

14,700 (4.2) 42

( 1.05)

II

PHYSIOLOGY O F T H E RICE P L A N T

28 1

population density or LAI-it will not be difficult to keep this 100. (d) There have been a great many discussions on this factor; perhaps it can be improved by breeding, because this factor is related to the structure of the chloroplast of the leaf. (e) Generally it is estimated that 40% of total assimilation will be consumed by respiration; the possibility of decreasing inefficient respiration will be discussed in Section 111, E, 1. (0 This is the time necessary to produce the yield factor, in this case to produce the ear. At present, 30 days are required. However, to get a greater yield, we have to increase this time by another 10 days. This will be very hard to achieve in practice. In a n y case, with our present knowledge, the aim should be to obtain 10 tons/ha, because some farmers have already achieved this level of production. Future research must be aimed at producing 10-30 tons/ha.

C. PROBLEMS OF PLANTTYPE 1 . Japonica and Indica

Oryza sativa L is divided into four subspecies. However, the great majority of the varieties of cultivated rice, numbering over 8000, are either indica or japonica. The major differentiating characteristics of indica and japonica are I i sted : Indica: caryopsis elongated, thin, narrow, and slightly flattened. Ratio of length to width (3.1-3.5): 1. Usually awnless, or possessing short and smooth awns. Glumellae and leaves slightly pubescent, with short, thin hairs. Leaves pale green, the upper leaf frequently forming an acute angle with the culm. Japonica: Broad, thick caryopsis, rounded in transverse section. Ratio of length to width 1.4 : I to 2.9 : 1 . Awned or awnless, also intermediate forms. Glumellae hairs long and fairly thick. Leaves narrow, dark green, the upper leaf forming an obtuse (in some cases an acute) angle with the culm. The distribution of japonica rice is rather small compared with that of indica rice. It is generally recognized that the japonica variety is much more productive than the indica variety, which has a rather poor response to nitrogen. It used to be considered that, in the tropics, application of nitrogen generally did not greatly improve rice yields. It is quite important, if we wish to promote the freedom from hunger campaign, to make sure whether or not the poor response of the indica variety to applications of nitrogen is an intrinsic characteristic.

282

YOSHIAKI ISHIZUKA

Tanaka made a series of experiments to investigate this problem from the aspect of plant nutrition because many leading geneticists had also emphasized the importance of breeding varieties capable of giving a good response to nitrogen (Matsuo, 1952; Baba, 1954; Oka, 1956; Beachell and Evatt, 1961). Tanaka ( 1964) demonstrated the difference between two varieties in their response to nitrogen in the field, as shown in Table XVI. TABLE XVI Comparison between Japonica and lndica in Their Response to Nitrogen Applications" Nitrogen level (kg/ha) Type and varieties

Difference (b) - (a)

0 (a)

I00 (b)

1.99 1.92 2.80 I .85 1.91 2.35 4.70 5.34

2.3 I 2.02 2.99 2.10 2.37 3.2 I 5.18 5.41

0.32 0.10 0.19 0.25 0.46 0.77 0.38 0.20

4.83 3.39 2.48 I .98 3.0 I

6.02 4.66 2.10 1.17 I .95

1.19 I .27 - 0.38 - 0.8 I - 1.06

Japonica KINMAZE

NORIM-25 FUJISAKA-5 NORIN-8 TAMANISHIKI

OBANAZAWA

CHIANUNOT-242 TAINAN-3 lndica TAICHUNG-

1

CENTURY PATNA

23 1

PETA

59-368 ACHEHPUTEH

"Datafrom Tanaka ( 1 964).

It is clear that all japonica varieties are responsive to nitrogen, but some indica varieties are responsive whereas others are not. However, Tanakaalso found that the varieties which had not responded to nitrogen in the field gave a marked response when they were grown in a pot and received enough sunshine.

2 . Improvement of Indica Rice: Creation of IR-8 In the first place, Tanaka ( 1 964) conducted an experiment in which he compared the effect on the yield of rice of high rates of nitrogen (see Table XVII). Table X V l l shows clearly the tendency for indica rice to be unresponsive to application of nitrogen, the use of which actually reduced yields.

283

PHYSIOLOGY OF T H E RICE PLANT

TABLE X V l l Reaction of lndica and Japonica Rice to Nitrogen Application"

Type and varieties

Yield under no nitrogen (tons/ha)

Yield under 100 kg N/ha (tons/ha)

I .99 2.35 4.70

2.3 I 3.12 5.18

+ 0.77 + 0.48

2.48 I .98 3.0 I

2.10 1.17 I .95

- 0.38 - 0.8 I - 1.06

Difference

Japonica K I N M A Z E (Japan)

(Japan) C H I A N U N C 242 (Taiwan) lndica PETA (Philippines) 56-368 (Ceylon) A C H E H PUTEH (Malaya) OBANAZAWA

+ 0.32

"Data from Tanaka (1964).

However, when Tanaka planted the same variety in a pot, not in a community, and gave the plants enough sunshine, he obtained entirely different results, as shown in Table XVIII. TABLE X V l l l Differences in the Responses to Nitrogen under Independent and Community Cultivation"

Cultural conditions Separate cultivation Under community surrounded by rice plants No N fertilizer 100 kg N fertilizer

Amount of N applied 0.90 I .80

0.00

0.45

20"

48

67

79

I54

18

38 17

57 36

85 30

I I5 30

15

3.60

"Data from Tanaka ( 1964). "Values are expressed as weight of plant in grams.

He concluded that the negative response to fertilizer was due to mutual shading because of the vigorous growth of leaves following the heavy application of nitrogen. Figure 18 shows the vigorous growth of rice plants after the application of nitrogen, resulting in heavy mutual shading. However, if we can breed a medium-tillering variety with a rather short, stiff straw, it will be more likely to respond to applications of nitrogen.

284

YOSH I AKI ISHIZUKA

FIG. 18. Native variety and improved variety. (Courtesy IRRI.)

Beachell and Jennings achieved remarkable success by adopting this principle, and they succeeded in breeding a new variety, which they named IR-8, and which promises a yield of 6-7 tons/ha under favorable conditions. IR-8 itself is not perfect as it has some defects. However, we must applaud the achievement of these two workers. We are now confident that it is possible to breed for any locality a

PHYSIOLOGY OF THE RICE PLANT

285

variety of rice plant which will be very responsive to applications of nitrogen and have the promise of producing a high yield (International Rice Research Institute, Annual Report, 1964).

3 . ldeotype and Variety As shown in the preceding section, it is clear that when we consider the yield of rice in the field, it is not sufficient to study each individual plant as a separate unit. At the same time we have to study the growth in the field where each plant is a member of a community. Loomis and Williams (1969) expressed their ideas on this subject and stated: “The primary productivity of communities made up of autotrophic green plants is initially dependent upon photosynthesis. The patterns of chlorophyll display at each level of community organization reveal features which can be related to light interception and photosynthetic activity, and hence, to production. Studies on the comparative morphology of such displays should reveal principles useful for designing more efficient crops. It is important that we identify these principles since existing patterns are not necessarily the most efficient for intensive agriculture a consequence of natural selection, even under a strong influence of man, having occurred principally in poverty environments and having emphasized parameters of fitness in addition to primary productivity.” To get a high yield, the balance between photosynthesis and nitrogen absorption is very important. Heavy nitrogen applications will produce a vigorous growth of leaves. However, vigorous growth of a plant beyond certain limits will induce increased mutual shading, which will adversely effect the yield. Accordingly, a plant type that has the potential for a high rate of photosynthesis and low respiration after a heavy application of nitrogen may be the ideal type to produce a high yield. Thus research in developing the type of ideal plant based on this ideotype has recently commenced, both experimentally and with a computer model. Loomis and Williams ( 1 969) and Monteith (1 969) tried to visualize the ideotype of general crops from the aspect of crop performance based on light absorption or interception and radiative exchange. Murata ( 1969) carried out similar investigations based on the physiological responses to nitrogen. As the result of his investigations, Matsushima ( 1957) proposed an ideotype for the rice plant: 1. The plant should have an adequate number of spikelets per plant or per unit area to obtain the target yield.

286

YOSHIAKI ISHIZUKA

2 . It should be short in culm height as well as in panicle length, and have many culms as a safeguard against lodging and to increase the percentage of ripened grain. 3 . Its upper three or four leaf blades should be short, thick, and erect to increase the light-receiving efficiency and consequently the percentage of ripened grain. (The leaf area index should be nearly 5 . ) 4. It should keep absorbing nitrogen, even in the period after heading, to increase the percentage of ripened grain. 5 . It should have as many green leaves per culm as possible (the number can be considered as an index of healthiness). 6. Its heads should emerge in early August (in Japan) so that it may be exposed to at least 20 continuous sunny days after heading to increase the amount of photosynthetic products at the ripening stage. Chandler discussed the same problem on several occasions. He also summarized the so-called ideotype of the rice plant precisely (Chandler, 1969) and practically as “Dwarf Rice-A Giant in Tropical Asia” (Chandler, 1969). Figure 18 illustrates the points he emphasized: 1. Culm length is the most important single factor affecting lodging resistance and nitrogen responsiveness. 2 . Culm strength is associated not only with the length but also with the thickness of the culm and with the tightness and durability of the leaf sheath that wraps the stem. 3. Nitrogen-responsive varieties show less relative internode elongation when heavily fertilized than do the unresponsive varieties. 4. Short, erect leaves of medium width are associated with high yielding capacity and nitrogen responsiveness. 5 . The tillering of the rice plant is strongly influenced by genetic factors and by the nitrogen level in the soil. 6. When varieties are short ( 100 cm or less) and have erect leaves and sturdy stems, inherent high tillering capacity seems to be a distinct advantage. There is no evidence in the literature that grain yield in such plant types is decreased by a too heavy tillering capacity, and no optimum and specific leaf area index has yet been identified for maximum yield. 7. Nitrogen levels in the soil greatly influence the number of panicles per square meter and, to a lesser degree, the number of spikelets per panicle and the number of filled grains. The influence on 1000-grain weight is negligible. 8. The newly created, nitrogen-responsive tropical varieties have a grain : straw ratio of about 1 . 1 , whereas the traditional tall, leafy varieties average about 0.55, depending upon the individual variety and upon the environmental conditions under which it is grown.

PHYSIOLOGY OF T H E RICE P L A N T

287

9. The new, heavy-tillering, short, erect-leaved, nonlodging varieties, such as IR-8, show essentially no change in yield when direct sown (thus, in a dense stand) or when transplanted at distances of 10 x 10 to 30 x 30 cm, and in some cases up to 35 x 35 cm if excellent cultural practices are followed. 10. The low-tillering to medium-tillering varieties, if short and stiffstrawed, yield best at close spacing at all nitrogen levels. I I . The traditional tall, leafy, tropical rice varieties generally yield best at wide spacing (50 X 50 cm), when grown at high fertility levels and when solar radiation is low. If sunlight is plentiful and nitrogen is more limiting, they yield better at somewhat closer spacing. 12. The point is emphasized that the combined morphological characters of the new plant type exemplified by the I R-8 variety are so important that they will be incorporated in all future rice varieties in the tropics which are developed for use under conditions of reasonably good water control. Furthermore, it is possible that this plant type may even gradually replace the conventional, but improved, rice varieties now used in the temperate zone. D. TRANSLOCATION A N D METABOLIC SINKS Translocation is one of the most important functions in crops. The studies of translocation are necessary not only from the standpoint of pure physiology, but also from the point of view of agronomy, because they involve numerous phenomena that have a direct relationship with high yields. Recent progress in the study of the mechanisms of translocation is described precisely by Biddulph ( 1969). I n this chapter, 1 wish to discuss some research on the practical aspects of rice cultivation. The rice plant often suffers from so-called cold damage, or low temperature damage, in a cool summer even though under such conditions the production of leaf and stem is very similar to that in a normal year. The only difference is in the growth of the ear, that is, the translocation of assimilates from the leaves to the ear. Thus, if one is aware of the biochemical mechanisms involved, it may be possible to devise some mean by which ripening may be promoted. However, at present this is just a hope. Fukai and Kushizaki ( I 952) compared rice plants grown in a year with a cool summer with those grown in a normal year, as shown in Table XIX. Table XIX indicates that the total dry matter production in a cool summer is more than 80% of that produced in a normal year; on the other hand, the grain:straw ratio is extremely low where cold damage has occurred, i.e. the translocation of assimilates has been low. It is con-

288

YOSHIAKI ISHIZUKA

TABLE X I X Grain:Straw Ratio of the Rice Plant in a Normal Year and in a Cool-Summer Year at Hokkaido" Cool summer year

Grain yield (kg/ha) Index Total yield (kg/ha) Index Grain: straw ratio

Normal year

1926

I93 I

1941

1945

4180 I00 8814 I00 90

2100 50 10720 122 24

1942 46 6997 79 83

I342 32 3702 42 57

1661 40 7522 85 28

"Data from Fukai and Kushizaki ( I 952).

venient to discuss translocation in two parts ( I ) translocation of nutrients absorbed by the plant, (2) translocation of assimilate to the storage organs. In a general report on the translocation of mineral nutrients in the rice plant, Tanaka ( 1 956) made a series of analyses of each mineral nutrient in the leaves of the main stem at the panicle initiation stage. Figure 19

0 0.5 1.0 1.5 0 0.4 0.20.3 0 0.2 040.60 8 4.0%

FIG. 19. Content of nutrients in the leaves on the main stem at panicle initiation stage. (From Tanaka, 1956.)

shows a very clear pattern of nutrient distribution. The percentage contents of N , P, and K are higher in the upper leaves than in the lower ones. However, Ca distribution is higher in the lower leaves. Tanaka also examined the pattern of accumulation and translocation of these elements in the leaf. During the lifetime of the leaf, some nutrients will accumulate during growth, and, after reaching a maximum ( x ) , de-

289

PHYSIOLOGY OF THE RICE PLANT

crease again, translocating to other leaves or other organs until the leaf finally dies ( y ) . In this case, we can express the degree of mobility ( m ) as

m =x--Y x 100 X

Ishizuka and Tanaka (1958) calculated the mobility of each element in the leaves of the rice plant under normal growing conditions (see Table XX). TABLE XX Mobility of Elements in the Leaves Leaf

N

P

K

Ca

Mg

S

4/0 1 I/O Mean: l/0-12/0

40 77 67

33 91 79

58 25 40

0 0 6

57 43 53

48 46 55

The mobility of each element can be arranged in the following sequence: P > N > S > Mg > K > Ca. This compares favorably with the results obtained by Bukovac and Wittwer (1957). Studies on the pattern of translocation of mineral nutrients in plants advanced rapidly as a result of the use of radioactive isotopes. A number of reports were published dealing with this aspect of research in the case of the rice plant, particularly in the distribution of individual elements in the plant tissue. Tanaka ( I 966a-d) carried out a series of experiments on Fe (Tanaka, I966a), Mn ( 1 966b), A1 ( 1966c), and SiOr ( 1966d) in the leaf, stem, and root of the rice plant (see Table XXI). Levels of Mn and SiO, are low in the root and high in the old leaves, whereas Fe and A1 accumulate in the root in large quantities and are also high in the culm. Iron is not distributed evenly in the culm, accumulating only at the nodes. TABLE XXI Content of Minor Elements in the Rice Plant" Fe (PPm)

Mn (PPm)

Al (PPm)

SOp

Plant part Young leaf Old leaf Stem Root

196 336 2,224 9,800

5,000 16,100 4,500 2,000

207 469 1,360 2,210

3.40 7.88 3.05 0. I4

Data from Tanaka ( 1966).

(%)

290

YOSHIAKI ISHIZUKA

The assimilated products of the leaf are translocated to the growing points as a form of glucose. To illustrate this point, Tanaka (1958b) carried out a series of experiments and established the distribution pattern of assimilates. He treated the 5/0 leaf with radioactive COz when 6/0 leaf was just beginning to develop, and observed the distribution of 14C in the plant. He found that the assimilate accumulated in leaves and roots, which were growing vigorously. It translocated from 510 to 6/0, 2/2, and I /3, these three leaves being under so-called simultaneous growth at that stage. These assimilates were incorporated into cellulose or lignin, which are the constituents of the cell wall, and did not move again. Tanaka ( 1958b) observed that the redistribution of assimilates, once translocated to the new leaf, depends a great deal upon the nutritional condition of the plant, especially for nitrogen (see Table XXII). TABLE XXII Change of Dry Weight and Nitrogen Content during Ripening"

Dry weight (g) At heading time (a) At harvesting time (b) Difference (a - b) Mobility

(9) 100

Nitrogen (mg) At heading time At harvesting time Difference Mobility 'I

6 0 ppm N

15 ppm N

34.7 58.7 - 14.3

29.7 23. I 6.6

-33

22

1220 604 616 50

467 74 393 84

Data from Tanaka ( I 958b).

In order to study the pattern of translocation of elements from the leaves to the ear, Ishizuka and Tanaka (1960) compared the weight of the shoot at heading time with that at harvesting time under different nutritional conditions. They proved that in the case of N, P, S, which are the constituents of protoplasm, the decrease of these elements in the shoot is quite remarkable, especially so in the case of P. This means that in the case of translocation of assimilates to the ear, P plays a role not only as the constituent of protoplasm, but also a special role at the time of ripening. It has been generally assumed that the carbon contained in the grains

PHYSIOLOGY OF T H E RICE P L A N T

29 1

of rice plants is derived mainly from photosynthetic products originating from the leaves after the flowering stage. To clarify this matter, Kasai (see Kasai and Asada, 1959) planned a series of experiments on the role of phosphorus in ripening, using radioisotope techniques. He concluded that 60-80% of the total phosphorus absorbed at each stage of growth was translocated to the grain. However, ‘InP which had been absorbed by the roots after the flowering stage was translocated to the grain in considerably smaller amounts than the 32P which h’ad been absorbed before flowering. In addition he studied the fate of phosphorus translocated to the grain. The presence of phytin and other-phosphorus components in the grain was confirmed by Fuiiwara and Mitsuhashi ( 1948), and Aimi and Konno (1958). Glucose 1-phosphate was identified by Kurosawa et al. (1957), and ribonucleic acid by Matsushita ( 1958).

E.

PHOTOSYNTHESIS,

RESPIRATION, A N D YIELD

1 . Photosynthesis, Respiration, and Growth Eficiency

The yield of rice means the accumulation of solar energy by way of photosynthesis

consequently the efficiency of storage of assimilated solar energy is of extreme importance. The improvement of variety (breeding) and cultivation practices, especially the improvement of environmental conditions such as soil improvement and advanced techniques of fertilizer application and plant protection are all subordinate to the efficiency of the storage of solar energy, which is a limiting factor for rice yield. When the amount of fertilizer is abundant, the ability of the crop to assimilate solar energy and the efficiency of the formation of storage organs will become limiting factors for getting increased yields. As the amount of solar energy in any one-place is fixed, the question is how to utilize this solar energy by the improvement of plant performance, as stated in Section 111, C, 2. Even though the total amount of solar energy may be high, if the efficiency of the plant in converting its energy to storage materials is low, and if the plant consumes a large amount of energy just for maintenance and there is insufficient surplus energy to spare for the formation of storage organs, yields will be low. Scientists who anticipated that this stage would come in the near future began to study the efficiency of production

292

YOSHlAKl ISHIZUKA

of storage materials in storage organs, from the viewpoint of the economy of energy. According to the classical view, photosynthesis and respiration are two opposite processes that proceed simultaneously and independently in all green tissues. Respiration has thus been believed to proceed at the same rate in light and in darkness, and as a consequence, gross photosynthesis in illuminated plant parts has commonly been calculated by the formula: W=P-R

where W = rate of dry matter production, P = rate of photosynthesis, and R = rate of respiration. This equation means that to get W higher, we must keep P as high as possible and R as low as possible. This conception is reasonable if P and R are independent variables. However, in the higher plant this is unthinkable because, to keep a vigorous growth, respiration, which is connected with metabolic absorption, is to some degree indispensable. In an ordinary crop, it is believed that, when photosynthesis is proceeding normally, the rate of respiration is a function of the rate of photosynthesis and will be usually expressed as 0.4 X P = R . If so, W = P - R = P - 0.4 P

= 0.6 P

and it will be a simple function of photosynthesis. Accordingly, it is reasonable to state that, to keep high, it is necessary to keep P high. On the contrary, it is not reasonable to try to keep R as low as possible. This is the most essential point to consider in trying to get higher yields. Tanaka and Yamaguchi (1968) introduced the concept of growth efficiency.

w

Dry matter production N

=

W W + R )

where R = the amount consumed by respiration for the production of W , measuring the growth rate, photosynthesis, and respiration at different stages of growth in the field. They concluded that in an actively growing rice plant in which respiration is well geared to growth, the growth efficiency is about 60%. However, in the case of rice plants suffering from mutual shading and having a large amount of excessively elongated internodes, the efficiency is lower than 60% because of the respiration in the organs that are not directly contributing to growth.

293

PHYSIOLOGY OF T H E RICE P L A N T

The variation in the growth efficiency under different cultural conditions and also at different growth stages indicates that, for a high dry matter production, not only is a high rate of photosynthesis necessary but also a high efficiency of respiration is required. (Fig. 20).

-.-

100 N .... I.... ON

i

\1-

OL 0

,

Panicle Flowering in1tiation

20

40

60

80

100

,

I20

Days after transplanting

FIG.20. Growth efficiency of (From Takana, 1968.)

PETA

population at 0 and 100 kg of nitrogen per hectare.

However, it is still not clear whether or not R contributes to growth as a source of energy. Some of R will be consumed without any positive contribution to growth. Then, the above equation should be modified to N=

W W +(Re

+ Rn)

where Re= respiration that contributes to growth, and Rn = respiration that does not contribute to growth. T o obtain a high efficiency of growth, it is necessary to measure the value Rn and try to bring this value as low as possible. Regardless of whether or not photorespiration belongs to Rn, the topic needs to be studied, as will be discussed in the next section. At present, it is very difficult to estimate Re and Rn separately. 2. Photorespiration The presence of light-stimulated respiration in photosynthesizing tissue was postulated by Rabinowitch ( 1945). Pioneering work of Decker ( I 955) also indicated clearly the presence of such a type of respiration. Jackson and Volk ( I 970) used the term “photorespiration” to include

294

YOSHl AKI I SH IZU KA

all respiratory activity motivated by light, regardless of the method by which CO, is released and Op consumed. Those plant species which fix COz primarily by the photosynthetic carbon reduction cycle apparently have very sizable respiratory rates in light, have high carbon dioxide compensation points, and hence may be referred to as high compensation species (Calvin and Bassham, 1962). In those plant species which fix COz via C4-dicarboxylic acid cycle, photorespiration will be difficult to detect (Hatch and Slack, 1970). These plants have a very low COz compensation point, or a greater ability to deplete the surrounding atmosphere to a very low COz concentration, and hence may be referred to as low Compensation points (Downton and Tregunna, 1968). Characteristics differentiating species with and without photorespiration are well summarized by Hofstra and Hesketh ( I 969). In earlier studies of rice, it was shown that the rate of 14Crelease from the previously assimilated I4C was different in light and dark (Nishida, 1962), “and that light had an effect on the respiration of the rice plant during a subsequent dark period (J. Yamaguchi and Tanaka, 1967). Recently, Akita et al. ( 1969) studied photosynthetic characteristics of the rice plant compared with other crops and revealed that the former has a relatively high COz compensation point and that this point increases with increasing temperature, presumably because of increased photorespiration. In addition, rice plants lack the chlorophyllous parenchymatous bundle sheath in the leaves which is a characteristic of plant species with a high photosynthetic rate. The above information indicates that the rice plant differs in photosynthetic characteristics from tropical grasses of high photosynthetic rate. However, as Rabinowitch stated, the question is still of great interest to those who are dealing with problems of plant productivity. Stoy (1969) stated that it is practically impossible-or at least extremely difficult - to make exact measurements of the rate of photorespiration under normal growth conditions since the simultaneously occurring photosynthesis interferes with and counteracts the respiratory gas exchange. For a long time, therefore, the existence of photorespiration was much questioned, but today the positive evidence is so overwhelming that there hardly can be any doubt as to its reality. However, we urgently need to know its exact biochemical nature, and why it seems to be absent in some species. Of special importance is the question whether or not it depends on a real biochemical difference between species. Although it is clear that the rice plant has a relatively high photo-

PHYSIOLOGY OF T H E RICE P L A N T

295

respiration, to discuss the possibility of attempting to breed a new variety which has either no or a low photorespiration, will, at present, be somewhat premature.

F. NUTRIENTSUPPLY 1. Function of Major Elements a n d Their Application

There have been a great many investigations on the physiological function of mineral nutrients. These have been summarized in the book “Mineral Nutrition of the Rice Plant” published in 1964. Fundamentally, the function of the major elements in the growth of the rice plant is not much different from what it is in other cereal crops. Consequently, I wish to omit the general studies of physiological or biochemical functions common to other cereal crops and restrict my discussion only to the physiological function closely associated with the attainment of higher yields. No one will object to the statement that, to get a higher yield, it is essential to understand the use of nitrogen, the most important of the major elements. When we regard the soil only as a medium to transfer mineral nutrients to crops, it is believed that the best way to apply fertilizers is to apply nutrients to coincide with the demands of the particular crop. Thus, this discussion deals mainly with this point, because this is believed to be the best way to get maximum yield under given circumstances. a . Nitrogen. The function of nitrogen is discussed in relation to (1) yield of constitutional components and (2) yield of determining components. lshizuka (1932) endeavored to find the optimum stage of growth at which an application of fertilizer would have the maximum effect on crop yield. In connection with this problem, Kimura and Chiba ( I 943) introduced the concept of “partial efficiency” of nitrogen absorbed by the plant as a way of expressing the utilization of absorbed nitrogen for grain production. The term “partial efficiency” of nitrogen refers to the increase in grain yield divided by the increase in the absorbed nitrogen for a given period of rice growth. Thus, the partial efficiency of nitrogen absorbed by a plant at successive stages can be calculated as follows: Y(n) - Y(n-I) N(n) - N(n- I )

= Partial

efficiency of N at period (n-1) to (n)

N(n) = N absorbed by plant which received N from the beginning of growth to thedate(n), N(n-l)=to thedate(n-l),Y(n)=yieldofplotN(n).

296

YOSHIAKI ISHIZUKA

Using medium maturity variety, they found the maximum partial efficiencies for grain production appeared twice under condition of moderate nitrogen supply as shown in Fig. 21.

00 0 >.

.50 6 0 .c

L

al

f3 4 0 )

20

FIG. 21. Partial efficiency of nitrogen for yield at different stages of growth. (From Kimura and Chiba, 1943.)

However, in the case where there was an abundant supply of nitrogen, Kimura and Chiba observed only the first peak, at the most active tillering stage, and the second peak did not appear to any extent because of the abundant storage of nitrogen. Working with an indica variety in India, Tanaka et al. ( 1 959) found two peaks of partial efficiency where levels of nitrogen were low (10 ppm), the first peak occurring during the vegetative stage, about 35 days before flowering and the second peak occurring just after flowering. In the case of high nitrogen levels (60 ppm), only one peak period of partial efficiency occurred, at the early stage of growth, about 50 days before flowering. The nitrogen uptake of indica varieties having different periods of maturity was investigated at Cuttack. It was found that there were two peaks in the rate of nitrogen uptake, one at the maximum tillering stage and the second at the panicle-development stage. Because of this evidence, they concluded that the nitrogen requirements of the rice plant are high at the maximum tillering stage and again at the ear development stage. Matsushima ( 1957) made a comprehensive investigation in which he examined nitrogen requirements at different stages of growth from the viewpoint of the effects on yield. To clarify how and when the grain yield

297

PHYSIOLOGY OF T H E RICE PLANT

of rice is determined, he analyzed the yield to ascertain its constitutional components, as well as how and when each component is determined, as shown in Fig. 17. He conducted a series of experiments to find out the influence of nitrogen applied at different stages of growth on the yield of rice and obtained the results as shown in Fig. 22. He observed the marked 2000 r

t

1 2 3 4 5 6 7 8 9 1011 1213 14!516

Treatment No. Days from heading

1 l 1 1 1 l 1 1 1 1 1 l 1 l 1 58 48 38 28 (8 8 2 ';lnr 53 43 33 23 13 3 I: .+ ? 0 Time o f top-dressing

-0 0

m

c

0

z

FIG.22. Effect of an unusually heavy dressing with nitrogen on the percentage of ripened grains as well as grain yield at successive growth stages. (From Matsushima, 1957.)

298

YOSHIAKI ISHIZUKA

negative result obtained from applying nitrogen about 33 days before heading (Matsushima, 1969), and he proposed the following practices to obtain an ideal plant, the so-called “V-shape” theory. ( 1 ) Use healthy seedlings to make the plant absorb ample nitrogen at the early tillering stage to ensure that the necessary number of tillers are produced as early as possible, so as to obtain the target yield. (2) Decrease the supply of nitrogen, or supply no nitrogen, during the growth stage covering the 7090 leaf number index (i.e., over the period of 42- 18 days prior to heading). This will minimize lodging and decrease culm height and panicle length. The length of the three or four upper leaves will also be reduced and the leaf blades will be erect and thick. (3) Let the plant keep on absorbing nitrogen during the period after heading, by top dressing with nitrogen just after the stage of reduction division of meiosis or at the full heading stage, to increase the percentage of ripened grains. This statement is sound and reasonable when we consider the theoretical aspect of rice nutrition. However, during the I R R I symposium, the comment was made that, in the case of actual paddy fields, the nitrogen must be applied to the soil, and Matsushima’s argument would be valid only if the plant were able to absorb nitrogen instantaneously through its roots. This will depend on the condition of soil and on the natural supply of nitrogen. Accordingly, it was suggested that the plant itself should be studied at the time of top dressing (Ozaki, 1954; Wallihan and Moomaw, 1967; Angladette, 1964). b. Phosphorus. It is a well known fact that lowland rice gives little response to phosphatic fertilizers, although upland crops which are grown on the same soil type show a good response. However, if the phosphorus content of the soil is very low, the rice plant will not grow normally. As mentioned in Section 111, D , because the remobilization of phosphorus from the old tissues to the growing tissues is quite remarkable, it is not necessary to consider applying phosphatic top-dressing to the rice plant. It is a general practice to supply only one application to the paddy field, either before seeding or before transplanting. Generally speaking, as the power of the soil to fix phosphate ions is considerable, the effect of the applied phosphate will last for a long time and there will be very little leaching. Consequently, the method of application of phosphatic fertilizers is not so complex as that of nitrogen. However, one interesting fact has been observed concerning the physiology of phosphorus. This is the effect it has on the tolerance of the rice plant to cold injury. It is generally thought that, when the rice plant

299

PHYSIOLOGY OF T H E RICE PLANT

is cultivated in tropical regions, there will be no problems due to cold temperatures. However, in the northern areas of rice-cultivating countries and mountainous regions of tropical Asian countries, cold damage may be experienced, although the degree of damage differs according to the locality. Hakkaido, in Japan, is the northern limit of rice cultivation in respect to the temperature of the growing season; sometimes rice suffers cold damage because of a cold summer season. I n such a case, phosphorus applications show interesting results. Fukai and Kushizaki ( 1 952), summarized the results of the effect of three manurial ingredients on the growth of t h e rice plant from I926 to 1948, comparing the yield in good, normal, and poor years (because of cool summers), as shown in Table XXIII. TABLE X X l l l Effect of N , P, and K for Rice Yield at Good Summer Year and Cool Summer Year"

Year Good summer year Cool summer year

No fertilizer 3.18'' (60) 1.13 (75)

-N

-P

-K

4.08 (76) I .63 (94)

4.33 (81) 0.88 (50)

4.92 (92) 1.84 (106)

Complete plot 5.34 ( 100)

1.74 (100)

"Data from Fukai and Kushizaki (1952). "Values are expressed as tons per hectare.

In the case of a year when a cool summer is anticipated, it is absolutely essential to give adequate phosphorus to the rice plant to prevent low yields. To clarify the reason for this, Ishizuka et al. (1962) carried out an experiment on the effect of phosphorus application in a cool summer year. Figure 23 compares the growth of the rice plant with and without phosphorus, as well as the phosphorus and nitrogen content of the plant, at the important stages of growth. It shows clearly that, without P, growth is very slow, compared with that of the plot supplied with P. Figure 24 shows the growth of rice plants irrigated with cold water compared with the growth of rice plants irrigated with water of normal temperature, in the same experimental area. The pattern of phosphorus absorption and plant growth on the plot irrigated with cold water is very similar to that of - P plot in Fig. 23. Consequently a combination of no phosphate and cold irrigation water in a cool summer will result in a very serious reduction in yield.

3 00

YOSHIAKI ISHIZUKA

N o of tillers

PO ,% ,

21

I

June I

+P

I

July I

Aug I

June 1

Sept I

July I

Aug I

Sept I

FIG.23. Growth of the rice plant with and without phosphorus fertilizer. (From lshizuka ef al., 1962.)

June I

July

I

Aug 4

Sept I

OCI

4

FIG.24. Growth of the rice plant under high temperature and under low temperature. (From Ishizuka et a/., 1962.)

PHYSIOLOGY OF T H E RICE P L A N T

30 I

I t is a general tendency of land utilization in rice-growing countries to cultivate rice on alluvial soils and to cultivate upland crops on diluvial or tertiary soils. However, the progress of industrialization of Asian countries has resulted in factories beginning to occupy alluvial soil because of the ease of transportation. Thus there is a tendency for rice growing areas to encroach onto diluvial soil which shows a severe phosphorus deficiency. Under these circumstances, it was suggested that, to develop these diluvial soils for rice cultivation, heavy applications of phosphatic fertilizers just after initial development would produce very successful results (Honya, 196 I). c. Potassium. Of course, potassium is an indispensable nutrient. However, there are many diversified studies, and it is very difficult to summarize them briefly. Fortunately, Noguchi ( 1966) published a summarized report on this subject, as a publication of the International Potash Institute, entitled “Potassium and Rice.”

2. Function of Minor Elements and Their Application Over the past 20 years remarkable progress has been made in the study of the part minor elements play in the nutrition of plants of agronomic value. However, in the case of the rice plant, it has been rare to find plants in the field suffering from a shortage of a n y minor element, partly because of the part played by irrigation water in maintaining the supply of these nutrients, and also because the rice plant requires lower levels of minor elements than do other crops. Recently, because of developments in breeding and cultivation techniques, the yield of rice has been markedly increased. This has resulted in the absorption of an increased quantity of nutrients with a consequent decrease in their levels in the soil, so that workers have begun to observe some minor-element deficiency symptoms in the paddy field. At the same time, rice cultivation has expanded to areas less suitable for the purpose, because of acidity, alkalinity, or extremely high organic matter contents of the soil. Soils of this nature are far more likely to be deficient in one or more minor elements, to the detriment of the rice crop, so in recent years this subject has been of increasing interest to agronomists, who have published a number of papers on the topic. This section deals not only with theoretical studies made with culture solutions, but also with results obtained in farmers’ fields. a. Iron. In 1932, Kimura found a distinct difference between rice and barley in their ability to utilize phosphorus in the presence of iron.

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lshizuka et al. (1961) reported that under solution culture 0.1 ppm of iron in solution increased the yield of rice, up to 10 ppm of iron gave no further increase, and a concentration greater than 10 ppm reduced the yield. Since 1940, many iron-deficient soils have been identified in Japan, where much of the soil has been derived from acid rocks, such as liparite and granite. These soils are called Akiochi Soils, and on them rice crops frequently show symptoms of “Akiochi disease.” After extensive investigations, Shiori and Harada ( 1943) succeeded in controlling this disease with heavy dressings of red clayish soil or iron-rich materials. Y. D. Park ( I 967) also reported this type of soil in Korea. T. Yamasaki (1942) found chlorosis of rice plants in alluvial soil, where a basal application of lime had been supplied. His investigations revealed that the disorder resulted from a shortage of available iron in the soil. A similar condition was found to be quite common in rice-growing countries in the tropics, according to Tanaka and Yoshida, who recently made a survey of micronutrient deficiencies in rice-growing countries. They found this type of soil in many places, including India and Malaysia. At the same time they found many cases of iron excess in rice plants cultivated in paddy fields derived from latosols. 6. Manganese. Manganese is one of the microelements required in comparatively large amounts by the rice plant. lshizuka et al. ( 1 96 I ) reported the results of solution experiments on the manganese requirement of the rice plant. A concentration of less than 0.1 ppm increased the yield only slightly, and concentrations above 10 ppm reduced the yield. In Japan, manganese is being regularly applied to some Akiochi paddy fields, where manganese deposition is often seen in the horizon under the plow sole, because rice plants grown in Akiochi soils showed a higher content of iron and a lower content of manganese than in plants grown in ordinary soils, because of root destruction by &S. Pattanaik (1950) found that the addition of I ppm and 5 ppm of manganese increased the catalase activity of rice roots and leaves, respectively. c. Copper. Although physiologists have defined the part played by copper in plant nutrition, the only account of copper deficiency in paddy fields is that of Joshi. On the contrary, there are many reports concerning the excess of copper in irrigation water which has passed through a copper mining area. Ishizuka (1940, 1942) found that copper was easily absorbed by the rice plant in a culture solution, and that a large amount of the element

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accumulated in the growing point of the root. Accordingly, nutrient uptake was considerably inhibited, and if the Cu concentration exceeded 50 ppm, the rice plant failed to grow. Ishizuka observed that the growth of the rice plant was nearly normal with a Cu level of under I ppm, while severe toxicity resulted with a Cu level in excess of 1 pprn. d . Boron. In a study on the effect of boron on the growth of the rice plant using culture solutions, Tokuoka and Morooka (1936) reported that tillering and stem length were affected where the boron content in the solution was greater than 20 ppm. N o effect of boron application on the rice plant was observed when the boron content was below 20 ppm. According to Hirai (1950), the quantity of boron absorbed by rice plants was only 10.5 g/ha. This indicates that rice plants require far less boron than do other crops. Hirai (1948) also reported that the boron content of rice varied in different parts of the plant and was greater in the stem and leaf and less in the roots. Pattanaik ( 1950) reported that, when rice was grown in a nutrient solution of 1 ppm boron, catalase activity was increased. There are no reports of boron deficiency in paddy soils except for that of Mandal et al. (1959) in India. e . Zinc. Tokuoka and G y o (1942) found that adding I ppm of Zn to a culture solution increased the yield of rice; 5 ppm produced a toxic effect, the zinc content of leaves being 0.0027%; 10 ppm killed the plant. Ishizuka and Tanaka (1962), when growing rice in culture solution, noted zinc deficiency symptoms with a zinc concentration of 0.0 14 ppm in the culture solution, and toxicity at a level of 10 ppm. They suggested that the permissible lower range of zinc in rice would be 15 ppm in the dry matter of leaf. On the other hand, in a pot experiment Hosoda (1942) produced an effective response when less than 7 5 ppm of zinc was added to the rice plant, and toxicity appeared with the addition of 250 ppm. However, in recent years, many zinc deficiency symptoms have been observed in calcareous paddy soils throughout all rice growing areas, particularly in India. This matter is discussed below. f. Molybdenum. Ishizuka and Tanaka ( I962), in water culture of rice plants, confirmed that rice did not show any deficiency symptoms, even when the content of molybdenum in plant tissues was 0.04 ppm. At a concentration of I ppm in the nutrient solution, the rice plant showed signs of toxicity, and the content of molybdenum in the plant was 4 ppm. Ishizuka and Tanaka suggested that the upper limit of molybdenum content in the rice plant might be less than 2 ppm. However, Yamasaki and others have suggested that rice yields in Japan could be increased by raising the rice seedlings in upland nursery beds. In

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this case, Yamasaki et al. (1958) recommended the use of molybdenum, because in these cases rice plants are expected to absorb nitrate nitrogen. Here, molybdenum would be necessary because it is related to the reduction of nitrate in the plant. g . Chlorine. I t is not necessary to discuss the chlorine requirement because, although it may be essential for the growth of the rice plant, the concentration of chlorine in irrigation water is almost of the order of a milligram per liter. The problem is rather an excess of chlorine as NaCl in paddy fields along the coast or on newly reclaimed polder areas. Accordingly, extensive studies on salt damage to rice have been conducted for many years. Shimose (1954) reported that rice plants grew normally in culture solutions with less than 0.5% of chlorine but would not grow with more than 0.8%.With an increase of chlorine content in the solution, protein nitrogen decreased and the soluble nitrogen in the plant tissue increased. Pearson ( I96 1 ; Pearson et al., 1965) made a comprehensive study on the effect of salinity on rice at several growth stages (Pearson and Bernstein, 1959) and showed that the tillering stage is the most susceptible to salinity. Ehrler ( 1960), however, reported that higher osmotic pressure depressed grain yield much more than vegetative growth, but that chloride salts were not specifically inhibitory for rice. Tagawa and Ishizaka ( 1963, 1964) carried out a series of experiments on the tolerance of rice plants to salinity. h. Silicon. Whether or not silicon is essential to the rice plant has long been the subject of conflicting views (Lewin and Reiman, 1969). A large number of investigations seem to demonstrate that silicon is responsible for “improved growth” of the rice plant (Okawa, 1936; Ishibashi, 1936; Okamoto, 1959; Mitsui and Takato, 1963; Yoshidaet al., 1959; Okuda and Takahashi, 1965). The way in which silicon affects rice growth is still obscure. Silicon is absorbed by the rice plant in very large amounts. T. Yamasaki made an analysis of the nutrient content of sample rice plants from the field crop which produced the top yield in Japan. More than 2 tons of SiOr was absorbed by the rice, or ten times the quantity of nitrogen. It would not be unreasonable to ascribe some physiological functions to silicon. On the other hand, by using water culture experiments under wellmanaged conditions Yoshida et al. (1959) proved that silicon does not directly increase the dry matter production of the rice plant during vegetative growth provided the silica content of the plant is not less than 0.07%.

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The silica content of straw collected from farmers’ fields in Japan ranged from 4 to 20%, with an average of 1 I %. When the silica content of the straw is less than 1 I % , silicate application generally causes a significant increase in rice yields (Imaizumi and Yoshida, 1958). Thus the beneficial effect of silicate application on rice yields in the field differs from the problem of its essentiality. Miyake and Adachi ( 1922) have already proved that silicon will increase the resistance of the rice plant to rice blast disease. Since then many scientists have proved that the absorption of silicon increases the resistance of the plant to fungal diseases and pests (Volk ef al., 1958; Sasamoto, 1953; Ishizuka and Hayakawa, 1949). For this reason, it is often difficult to determine whether the effect of silicon on rice growth is direct or indirect. Silicon nutrition is also related to decreased transpiration (Yoshida et al., 1959), increased oxidizing power of roots, and detoxification of some heavy metals (Okuda and Takahashi, 1965). Yoshida (1965) and Yoshida et al. (1969) by their histochemical approach, revealed that silicon tends to be deposited as silica gel under the cuticle of the leaf, forming a thick layer, the so-called “cuticle-silica double layer.” The presence of this double layer may well explain why increased absorption of silicon increases the resistance to disease and insects and suppresses transpiration. One of the visual characteristics of the rice plant grown under silicondeficient conditions is drooping leaves. Applications of silicon tend to maintain erect leaves, and applications of nitrogen tend to cause drooping leaves (Yoshida ef al., 1969). The effect of silicon on leaf angle and effect of leaf angle on photosynthesis of the rice canopy have recently been studied (Iwato and Baba, 1961; Cock and Yoshida, 1970). These studies indicate that a difference in leaf angle alone can account for differences in photosynthesis of the canopy of 10-40%. This effect is usually obtained at high nitrogen levels, and the magnitude of the effect on grain yield is about 10%; it is quite likely that silicon improves rice growth by maintaining more erect leaves, hence increasing photosynthesis in the field (Fig. 25). Recently minor element deficiencies have been reported in some countries (Ponnanperuma and Yuan, 1966; Rodrigo, 1964; Mehrotra and Saxena, 1967; Karim and Manzoorf, 1967). Just recently, Tanaka and Yoshida ( 1 970) made a comprehensive survey on the physiological disorders of rice in various rice growing countries in Asia and investigated local names for disorder symptoms (see Table XXIV and Fig. 26). This will be a useful reference for those engaging in further research on this problem.

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FIG.25. Effect of silicon in maintainingerect leaves. (Courtesy of Dr. Yoshida.)

3. Agricultural Studies in Connection with Nutrient Supply

Throughout the rice growing countries of the world there is a wide range of rice varieties and traditional cultural techniques, especially those relating to fertilizer application. I t is thus extremely difficult to record all the reports dealing with rice research. However, I wish to mention some reports dealing with research into fertilizer application in rice growing countries. The studies were done in Africa (Angladette, 1957; Dabin, 1951; Irvin, 1958; Kashairy, 1957; Bredero, 1966), Burma (Wit, 1957), Ceylon (Chandraratna and Fernando, 1954; Allahabod, l966), Hungary (Dzubay, 1958), India (Abhichandani and Patnaik, 1959; Basak and Klemme, 1959; Gupta, 1959; International Potash Institute, 1959; Ramiah, 1956; Verma, 1960; Daji, 1966; Simsiman et al., 1967; Pillai, 1967; Panse and Abraham, 1966), Indonesia (Goor, 1952), Iraq (AlFakhry, l960), Korea (J R. Park et al., 1963, Madagascar (Velly et al., 1966), Malaya (Allen, 1952), Mysore (Bhatta, 1956; Marasimha, 1953), Pakistan ( A h and Lillah, 1960), the Philippines (Abarra, 1952; Calma et al., 1952, Simisiman et al., 1967), Surinam (Have, 1958), Taiwan (Cheng and Chiang, 1954; Chu and Ma, 1954; S . C. Changet al., 1953); Thailand (Bhapkpar, I960), Trinidad (Tidburg, 1956), and the United

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TABLE XXlV Physiological Disorders of Rice Reported from Various Rice-Growing Countries" Country Burma

Ceylon Columbia Hungary India

Indonesia Japan

Physiological disease Amiyi-Po Myit-Po Yellow leaf Bronzing Espiga erecta Bruzone Khaira disease Bronzing Yellowing Mentek Akiochi Akagare I

Korea Malaysia Pakistan Portugal Taiwan (in southern parts United States

Akagare I I Akagare 1 I I Aodachi Hideri-Aodachi Straighthead Akiochi Penyakit Merah (yellow type) Pansukh Hadda Branca Suffocating disease Straighthead Alkali disease

Possible cause(s)

K deficiency P deficiency S deficiency Fe toxicity ? ? Zn deficiency Fe, Mn, H a s toxicities ? Virus disease? HrS toxicity, K, Mg, Si deficiencies K deficiency (Fe toxicity) Zn deficiency I toxicity 1

'? ,?

H2S toxicity, K, Mg. Si deficiencies? Virus disease ?

Zn deficiency Cu deficiency? Virus disease , I

Fe deficiency

"Data from Tanaka and Yoshida ( I 970).

States (Beacher, 1952; Green and Stoner, 1952; Jones, 1952; Wells, 195 1 ; Adams, 1967; Beacher and Wells, 1960) De Datta and Magnaye ( 1969) made a general survey on the forms and sources of fertilizer nitrogen for flooded rice. Rice research has by no means been confined to fertilizer application, and there are a number of interesting reports dealing with other facets of rice culture. J. Takahashi et al. ( 1 967) tried to obtain a high yield by using photosensitive varieties and modifying their growing conditions.

x

LEGEND P = Phosphorus deficiency K = Potassium deficiency Fe = Iron deficiency Si = Silicon deficiency Mg = Magnesium deficiency Zn = Zincdeficiency S = Sulfurdeficiency Fe tox. = Iron toxicity I tox. = Iodine toxicity H2S tox. = Hydrogen sulfide toxicity FIG.26. Nutritional disorders of rice in Asia. (From Tanaka and Yoshida, 1970.)

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Prashar ( I 970) tried to define the factors, and especially the optimum cutting height, which govern yields from ratooned rice, in order to obtain improved yields by this practice. Tanaka ( I 964) tried to establish the optimum population density or arrangement of hills per definite area with respect to growth efficiency. Thus, in all rice-growing districts, investigations are being carried out to establish the most suitable techniques for the particular environmental conditions. Simultaneously, every effort is being made, by demonstrating their superiority over existing methods, to persuade farmers to adopt these new techniques. IV.

Conclusion

During the period from 1900 to 1930, rice scientists attempted to define techniques that would enable farmers to obtain maximum yields from existing varieties under conditions of minimal fertilizer use. After 1930, the introduction of chemical fertilizers and the pressure of a rapidly expanding population caused agronomists to explore the possibility of increasing yields by improving the nutritional condition of crops. As a result of this work yields were increased to a level that had previously been thought to be unattainable. As a consequence of the increased use of chemical fertilizers, the nutrition of the rice plant was studied by plant physiologists, who made a considerable contribution to the knowledge of this subject. The results of this research were so spectacular that it is little wonder that many workers believed that the only way in which rice yields could be increased over a short period of time was through the application of fertilizer. Consequently, studies on the physiology of the rice plant were intensified in the effort to define all the nutritional factors affecting its growth. At the same time, as a result of the introduction of new high-yielding varieties, the condition of the soil became a factor limiting yield, as these new varieties needed soils with a higher level of fertility than did the varieties previously grown. I t is also essential to remember that these new varieties will give their maximum yield only when adequate supplies of irrigation water are available. At the present time 80% of Asian paddy fields depend on monsoonal rains. A considerable increase in irrigation projects will be necessary before we can obtain the full benefit from their use. When the geneticist has bred the ideal type of rice, and all essential cultivation techniques have been established, the question arises whether we have achieved the ultimate yield. Future rice research will have two objectives. One is to improve the

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quality of rice, and the other is to breed a new variety that is highly efficient in converting solar energy to storage energy. In both cases it will be essential for the geneticist and plant physiologist to work together in close cooperation.

ACKNOWLEDGMENT

I would like to express my sincere thanks to Dr. N. C. Brady for the encouragement he has given me, and to Drs. A. Tanaka, H. Okajima, and S. Yoshida for their help in summarizing some topics. My thanks are also due to Dr. R. F. Chandler, Jr., for allowing me to make full use of the l R R l library. I also appreciate the work done by Miss E. Takeyoshi, who helped me to prepare the list of references in Japan, and of Mr. A. V. Allo, who helped me to produce this chapter in English, a language which is not my mother tongue.

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Loomis, R. S., and Williams, W. A. 1969. I n “Physiological Aspects of Crop Yield,” pp. 28-47. Amer. SOC.Agron. Mandal, S. C., Alli, M. A,, and Mukherjee, H. N. 1959. J. Indian SOC.Soil Sci. 4,79-85. Matsuo, T . 1952. Bull. Nut. Inst. Agr. Sci., Ser. D 3, 1-1 1 I . Matsuo, T. 1961. “Rice Culture in Japan.” Yokendo. Matsushima, S. 1957. Bull. Nut. Inst. Agr. Sci., Ser. A 5, 1-271. Matsushima, S. 1969. Jap. Agr. Res. Quart. p. 4. Matsushita, S. 1958. Mem. Res. I n s t . Food Sci.. Kyoto Univ. 14,24-29. Mehrotra, 0. N., and Saxena, H. K. 1967. IndianJ. Agron. 12, 186-192. Mikkelsen, D. S., and Lindt, J. H. 1966. Rice J. 69, 74-79. Mitsui, S., and Takato, H. 1963. Soil Sci. Plant Nutr. (Japan) 9,49-58. Mitsui, S., Hashirnoto, Y., and Terasawa, S. 1948. J. Soil Sci. Manure (Tokyo) 19,59-61. Mitsui, S., Kumazawa, K., and Ueda, M. 1961. J. Soil Sci. Manure (Tokyo) 32, 11-14. Miyake, K., and Adachi, M. 1922. J. Biochem. (Tokyo) 1,223-239. Monteith, J. L. 1969. I n “Physical Aspects of Crop Yield,” pp. 89- 110. Amer. SOC.Agron. Moomaw, J. C., and Vergara, B. S. 1964. I n “Mineral Nutrition of the Rice Plant,” pp. 328. Johns Hopkins Press, Baltimore, Maryland. Muller, D. 1960. I n “Handbuch der Pflanzenphysiologie” (W. Ruhland, ed.), Vol. 5, pp. 255-268. Springer-Verlag, Berlin and New York. Murata, Y. 1965. Nogyo Gijutsu 20,451-456. Murata, Y. 1969. I n “Physiological Aspects of Crop Yield,” pp. 235-259. Amer. SOC. Agron. Murayama, N., Yoshino, M., Oshima, M., Takeara, S., and Kawarazaki, Y. 1955. Bull. Nar. Inst. Agr. Sci., Ser. B 4, 123-164. Murayarna, N., Yoshino, M., and Kawarazaki, Y. 1957. J. Soil Sci. Manure (Tokyo) 28, 327-330. Nagai, I. 1962. “Japoni,ca Rice.” Yokendo. Nagai, M. 1961. Nagai, M., and Nakaya, H. 1965. Proc. Tokai Br. Crop Sci. Soc. (Jap.) 42,36-39. Nagato, K., and Sugawara, K. 1952. Proc. Crop Sci. SOC.Jap. 21, 77-79. Nakata, K. 1967. Bull. Nara Univ. Educ. Nat. Sci. 15,95-103. Narashimha lyengar, B. 1953. Mysore Agr. J . 29,79-91. Nishida, K. 1962. Plant Cell Physiol. 3, I 1 1 - 1 24. Noguchi, Y. 1966. “Potassium and Rice,” pp. 1-102. Int. Potash Inst. Nomoto, K., and Ishikawa, M. 1950. J. Soil Sci. Manure (Tokyo) 20,66-67. Oka, H. 1956. J . Agr. Ass. China [N.S.] 13, 35-42. Okajirna, H. 1958. J. Soil Sci. Manure (Tokyo) 29, 175-180. Okamoto, Y. 1959. Proc. Crop Sci. SOC.Jap. 28,35-40. Okawa, K. 1936. J . Soil Sci. Munure (Tokyo) 10,95- I I0 and 4 15-4 19. Okuda, A., and Takahashi, E. 1965. I n “Mineral Nutrition ofthe Rice Plant,” pp. 123- 146. Johns Hopkins Press, Baltimore, Maryland. Oshima, M. 1962. J. Soil Sci. Manure (Tokyo) 33,243-246. Ota, Y., and Yamada, N. 1965. J. Jap. Trop. Agr. 33,460-466. Ozaki, K. 1954. J. Soil Sci Manure (Tokyo) 2520-24. Panse, V . G . , and Abraham, T. P. 1966. Indian Farming 16,58, 138-139, and 153. Park, J. R., Park, C . S., and Kim, I. S. 1965. Res. Rep. Ofice Rural Develop., Suwon, Korea 8,257-261. Park, Y. D. 1967. Res. Rep. Ofice Rural Develop., Suwon, Korea 10,23-35. Pattanaik, S . 1950. Plant Soil 2 , 4 18-4 19. Paul, J. 1966. Farm J. Guyana 27, 17-19. Pearson, G. A. 1961. I n t . Rice Comm. News Lett. 10, 3 15-319.

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Pearson, G. A., and Bernstein, L. 1959.Agron. J. 51, 654-657. Pearson, G. A., Ayers, A. D., and Eberhard, D. L. 1965.Soil Sci. 102, 151-156. Pillai, K. M. 1967.Indian J. Agron. 12, 15 1-155. Ponnanperuma, F. N., and Yuan, W. L. 1966.Nature (London) 211,780-781. Ramiah, K . 1953.“Rice Breeding and Genetics.” Indian Agr. Res. Counc. Ramiah, K. 1956.lnt. Rice Comm., News Lett. 10, 1-9. Ravinowitch, E. 1. 1945.I n “Photosynthesis and Related Process,” Vol. I , p. 599. Wiley (Interscience), New York. Rodrigo, D. M. 1964. Trop. Agr. (Ceylon) 120,219-226. Sasamoto, K. 1953.Appl. Entomol. 9, 109. Shiori, M., and Harada, T. 1943.J . Soil Sci. Manure (Tokyo) 17,375-376. Shiori, M . , and Yoshida, M . 1951.J. Soil Sci. Manure (Tokyo) 22,53-56. Shiraishi, K., Kubota, M., and Yanai, T . 1962.Bull. Kochi Agr. Exp. Sta. 3,60-78. Sims, J . L., and Palace, G. A. 1968.Agron. J. 60,692-696. Simsiman, G. V.,D e Datta, S. K., and Moomow, J. C. 1967.J. Agr. Sci. 69, 189-196. Sircar, S. M. 1958. J. Sci. Club 11, 165-175. Soga, Y., and Nozaki. M. 1957.Proc. Crop Sci. Soc. Jap. 26, 105- 108. Stoy, V. 1969.I n “Physiological Aspects of Crop Yield,” p. 186. Amer. SOC.Agron. Tagawa, K., and Ishizaka, N. 1963.Proc. Crop Sci. Soc. Jap. 31,249-252 and 337-341. Tagawa, K., and Ishizaka, N. 1964.Mem. Far. Agr., Hokkaido Univ. 5,77-88. Takahashi, J . 1969.lnt. Rice Comm. 26,39-44. Takahashi, J., and Murayama, N. 1955.Bull. Nat. Inst. Agr. Sci., Ser. B 4,85-112. Takahashi, J . et al. (1967). Takahashi, N., Okajima, H.,Takagi, S., and Honda, T. 1956.Bull. lnst. Agr. Res., Tohoku Univ. 8,91-116. Takeda, T . I960.1n“Rice Cultivation,” pp. I3 I- 178.Matsuo, Japan. Takeda, T. 1962. Symp. Jap. Soc. Agr. Meteol. pp. 29-38. Takeyoshi. E. 1969. Nogyo Gijutsu 24, 266-271. Tanaka, A. 1955.J. SoilSci. Manure (Tokyo) 26,413-418. Tanaka, A. 1956.J. Soil Sci. Manure (Tokyo) 27,145-148 and 223-228. Tanaka, A. 1957.Nogyo Cijutsu 12,302-306. Tanaka, A. 1958a. J . Soil Sci. Manure (Tokyo)29,241-245. Tanaka, A. 1958b. J. Soil Sci. Manure (Tokyo) 29,291-294 and 327-333. Tanaka, A. 1964.lnt. Rice Res. Inst.. Tech. Bull. 3, 1-80, Tdnaka, A. 1961.J . Fac. Agr., Hokkaido Univ. 51, Part 3, 449-550. Tanaka, A. 1963. lnt. Rice Res. lnst.. Annu. Rep. pp. 35-60. Tanaka, A. 1964. l n t . Rice Res. lnst., Annu. Rep. pp. 49-86. Tanaka, A., and Garcia, C. V. 1965.Soil Sci. Plant Nutr. (Tokyo) 11,9-I3 and 129- 135. Tanaka, A., and Vergara, 9. S. 1967.lnt. Rice Comm. News Lett., Spec. lssuepp. 26-42. Tanaka, A., and Yamaguchi, J. 1968.Soil Sci. Plant Nutr. (Tokyo) 14,110-1 16. Tanaka, A., Patnaik, S., and Abhichandani, C. T. 1959 Proc. Indian A c d . Sci., Sect. B 49, 207-2 I6 and 2 17-226. Tanaka, A., Kawana, K., and Yamaguchi, J. 1966a.Int. Rice Res. l n s t . , Tech. Bull. 7,1-46. Tanaka, A., Leo, R., and Navasero, S. A. 1966b.Soil Sci. Plant Nutr. (Tokyo) 12,158-162. Togari, Y., and Sato, K. I96 1. Proc. Crop Sci. Soc. Jap. 29,7 1-74. Togari, Y., Okamoto, Y., and Kumura, A. 1954.Proc. Crop. Sci. Soc. Jap. 22,95-97. Tokuoka, M., and Gyo, 0. 1942.J. SoilSci. Manure (Tokyo) 13,211-216. Tokuoka, M., and Morooka, H. 1936.J . Soil Sci. Manure (Tokyo) 10, 189-200. Tsunoda, S. 1962.Symp. Jap. Soc. Agr. Meteol. pp. 39-46. USDA. 1966. “Rice in the United States.” U . S. Dep. Agr., Washington, D.C.

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PHOTOSYNTHESIS AND CROP PRODUCTION Dale N. Moss and Robert 6. Musgrave University of Minnesota, St. Paul, Minnesota, and Cornell University, Ithaca, New York

I. 11. 111.

IV. V. VI. VII. VIII.

Introduction ..................................................................................... Yield and Net Photosynthesis Factors Limiting Photosynthesis .......................................................... A. Concepts Prior to 1960 ., .. B. New Concepts Evolved after 1960 ................................................ Breeding for Photosynthetic Efficiency ................................................. Selecting for Low r Traits in High r Species ......................................... Selecting for Photosynthetic Rates within Species ......... Breeding for Plant Type ..................................................................... Managing Photosynthesis ................................................................... References .......................................................................................

I.

317 317 320 320 322 327 327 328 33 I 334 334

Introduction

As research on factors limiting crop production has intensified in recent years, much attention has been drawn to the process of photosynthesis and many research groups have initiated investigations of factors limiting this process under field conditions. Intuitively, one can easily visualize that higher rates of photosynthesis in a crop variety should lead to higher yields. The relationship of photosynthetic capability and crop yield is not a simple one. Yield is an integration of the effects of numerous factors on many physiological processes and morphological components. Indeed, a direct cause and effect relationship between photosynthesis and yield has yet to be established. An attempt, however, is made in this article to review the large volume of recent work on photosynthesis and evaluate these results in terms of the relationship of net carbon dioxide fixation and yield of various crops and to assess the potential to improve crop yield by developing varieties with enhanced capacity to fix C O X . II.

Yield and Net Photosynthesis

Net photosynthesis is generally defined operationally and is measured by analyzing the change in CO, content in air surrounding the leaves or 3 17

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plants under investigation. Dark- and photorespiration are measured and d e h e d by similar gaseous exchange techniques. The term “gross photosynthesis’’ is generally taken to be the sum of net photosynthesis and dark respiration. This definition is operationally acceptable despite its obvious inadequacy. The total dry matter production of a crop, except for the relatively small mineral component, is equal to net photosynthesis. Not all of the dry matter that a crop plant produces is harvested, however, since dry matter is distributed among roots, tops, and into storage organs. One would expect a more direct relationship between yield and photosynthesis in a crop where a major portion of the plant is harvested than in a crop where only the fruit, grain, or other storage organ is taken. Even in forages, however, where all of the aboveground portion of plants is harvested, the relation may not be close. A genotype with a high rate of photosynthesis may also have a high rate of respiration or a high root: shoot ratio so that the net result is a lower weight of forage than a contrasting genotype with lower photosynthetic and respiratory rates or a lower root:shoot ratio. For fruit or grain crops the factors other than photosynthesis which control yield may be even more numerous. Thus, few would believe that all genotypes which have a high capacity to fix CO, will also be high yielding. Despite the fundamental nature of the question before us, little direct experimental evidence can be cited to confirm a direct relationship between photosynthetic rate and crop yield. Evans ( I97 1 ) argues that if photosynthesis were a major component of yield, then in at least some high-yielding varieties, the yielding ability should be due to superior photosynthesis. He has been unable to show this in wheat. In fact, he found that primitive poor-yielding wheats had higher photosynthetic rates of the flag leaves than did flag leaves of present-day high-yielding varieties . A contrasting argument can be made for numerous crops, however, including wheat. Again, indirect evidence must be cited. Several factors which are known to affect crop photosynthesis also affect yield in the same direction. Yields of numerous species are decreased by shade. Stinson and Moss (1960) found grain yield reductions of I 1-45% in I I varieties of maize grown in a shade tent, which reduced light intensity by one-third. Pendleton and Weibel ( 1965) found that any shading after flowering reduced the grain yield of wheat. The magnitude of the yield reductions was directly related to the degree of shading. Black (1963) found that dry matter production by subterranean clover was highly correlated with the amount of solar radiation which the crop received. Blackman and Black (1959)

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investigated the effect of light on dry matter production in 13 herbaceous species. They concluded that for all species the assimilation rate of unshaded plants was limited by light, even in midsummer. A possible major reason for the low yield of rice in the tropics is overvegetation (Tanaka et al., 1966). Overvegetation causes the plants to become highly mutually shaded. Maximum utilization of light for net photosynthesis is thus not possible. It must be emphasized, however, that the relation between radiation and crop yield can be extremely complex and is by no means dominated by the effects on photosynthesis alone (Evans, 197 1). Providing additional CO, to crops also strongly affects yields, presumably by sustaining greater rates of photosynthesis. Attempts to increase CO, around field grown plants have been few, however. COr added directly to the ambient air in crop canopies in the open field is rapidly mixed with the atmosphere and lost to the plants. This fact can be appreciated readily when one realizes that a large amount of COamoves from the atmosphere into the plant canopy during active photosynthesis and this occurs despite the fact that the gradient in COr concentration is very small. If an attempt is made tQ increase markedly the COz concentration around leaves, then a steep gradient exists away from the leaves and transport of CO, away from the plants to the atmosphere is especially rapid. Despite these difficulties, some attempts have been made to increase the concentration of atmospheric C 0 2 within the crop canopy in the field. Cumming and Jones (19 18) and Lundegardh (1927) attempted this for several years. Although they reported dramatic yield increases, it is difficult to have confidence in their results since it seems highly improbable that CO, concentrations of the ambient atmosphere were actually increased appreciably by their treatments, and they made no measurements of atmospheric COaconcentrations. Thomas and Hill (1949), in short-term experiments, enriched the atmosphere of enclosed field plots with CO:! and found a linear relationship between CO, concentration and apparent photosynthesis for increases of C o t up to 12 times the normal air concentration for sugar beets and up to 8 times for tomatoes. The net photosynthesis doubled when the COz increased by a factor of 2.5 to 3. Unfortunately, they did not continue these experiments throughout the season so that direct information on both net photosynthesis and yield are not available. However, the worldwide practice of C O r feeding in greenhouses to increase yields of many different species (examples: cucumbers, carnations, lettuce, tomatoes) and many varieties of each species is strong evidence that yields of most species and genotypes, whether the measured yield is

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a storage organ or vegetative material, would be greater if more photosynthate were produced by these plants. Greenhouse culturing is generally done 'in months of low light intensity when photosynthesis of the entire plant would be low. In those conditions, additional photosynthesis possibly could have a greater effect on yield than during seasons when higher light intensity sustained a higher rate of plant photosynthesis. R. L. Cooper and Brun ( I 967) grew soybeans (Hark and Chippewa-64 varieties) in enclosures in a greenhouse in 350 and I350 ppm CO,. Yield of seeds was about 50% greater and of straw about 60% greater in the higher COz concentration. Hardman (1970) then grew Hark soybeans in enclosures in the field during two summers at normal atmospheric CO, (300 ppm) and at 1200 ppm C 0 2concentrations. He found 57% more straw and 43% greater seed yield in the enriched atmosphere. Thus, there seems to be little doubt that enhanced photosynthesis does lead to greater yields, even in intense summer light when photosynthesis is at its peak. The question of how yield is related to photosynthesis could be more rigorously tested if photosynthetic capacity could be manipulated and measured concurrently with the resultant yield and/or yield components. Two different approaches come readily to mind. We may manage present gentoypes to increase their photosynthesis and we may attempt to develop new varieties which have increased photosynthetic capacity. The following discussion reviews efforts that are being made in each of these areas. Ill.

Factors limiting Photosynthesis

To learn to manipulate crop canopies to enhance their photosynthesis, or to be most efficient in breeding varieties with enhanced photosynthesis, one must first know what limits photosynthesis in crops growing in the field. An abundance of information has been published on this topic within the last decade resulting in significant changes in the thinking of many physiologists and plant breeders who are concerned with crop yields. The reader will appreciate better what these changes have been and how they have affected crop management and breeding if we review the status of knowledge of about a decade ago. A.

CONCEPTS PRIORTO 1960

Prior to 1960, reports had been published on two major attempts, both in the 1930's, to study factors limiting photosynthesis in canopies simulating normal field conditions. Heinicke and Childers (1937) enclosed an apple tree in a glasshouse and measured its rate of COs absorption in the

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varying climatic conditions of light and temperature found during a growing season. Thomas and Hill ( I 937) constructed gas-tight glasshouses in which they measured the C 0 2 exchange by wheat and sugar beet plots throughout the growing season. These earlier efforts involved chemical or electrical conductivity determinations of C 0 2 absorption by hydroxide solutions. I t was not until the advent of the commercial infrared gas analyzer which simplified the analysis for CO, that further attempts were undertaken to study photosynthesis in the field. Thomas ( I 955) reviewed the literature up to I955 on environmental effects on photosynthesis of plants growing in the field. This earlier work will not be reviewed in detail in this paper except to establish the status of published scientific thought at the beginning of the 1960 decade. From that work, the following picture emerges. 1. Light

Heinicke and Childers (1937) reported that photosynthesis in the leaf canopy of a young apple tree was light saturated at a light intensity of about 4500 ft-c in June, July, and August. Thomas and Hill (1937) found similar values for light saturation in alfalfa, wheat, and sugar beet plots. Bohning and Burnside (1956) reported that the light saturation of photosynthesis of individual leaves of many s u n species was near 2000 ft-c with maximum rates in all species of about 20 mg CO:! dm' hr-l. Verduin and Loomis (1944) reported that maize leaves were light saturated at 2500 ft-c. Thus, the concept was firmly established that photosynthesis in individual leaves of most field grown crops was light saturated at about one-fourth full summer sunlight. The value was higher for crop canopies because of varying leaf angles and shading; however, during midday all leaves in the canopy were thought to function at near light saturation capacity.

2.

co,

It was known that the intensity of light required to saturate photosynthesis of single leaves could be altered somewhat by changing the carbon dioxide concentration of the atmosphere. Chapman and Loomis (1953) found individual leaves on field grown potato plants were saturated at 3000 ft-c in normal air, at 4200 ft-c in air containing 0.06% CO, and not until 5200 ft-c in 0.15% COZ.

3. Temperature Temperature was thought to have a differential effect on photosynthesis and dark respiration because respiration was a chemical process which

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would have a Qlo= 2 or 3. Photosynthesis, in contrast, consisted of both temperature-dependent “dark” reactions and nontemperature-sensitive photoreactions. At low temperatures the dark reactions were thought to be limiting, and it was believed that “true” photosynthesis should increase with increasing temperature. Since at moderate temperatures photosynthesis is greater than respiration, the net photosynthesis should also increase. At higher temperatures the temperature insensitive photochemical reactions would become limiting. Since respiration would continue to increase with tempetature, however, the net photosynthesis would be lower at higher temperatures. This concept is described in the review by Thomas ( 1 955). In summary of this earlier work the picture emerges of field crops operating at near optimum temperatures for photosynthesis during much of the day and with the crop canopy saturated with light during the better part of midday on clear days. It seemed clear that the low COa concentration of the atmosphere was the predominant factor of the environment limiting photosynthesis. It was with that picture in mind that we first began measuring photosynthesis in the field in an attempt to understand which factors were limiting the yield of field maize in upstate New York.

B. NEWCONCEPTS EVOLVED AFTER I960 I . Maize Photosynthesis From our earliest measurements made on field plots, it was apparent that photosynthesis of leaves in the maize crop canopy did not respond as a light-saturated, COJimited unit (Musgrave and Moss, 196 I ; Moss er af., 1961). Figure I shows the photosynthesis of highly fertilized and densely planted maize plots on a clear and, from the inset, a cloudy day. Clearly, the crop photosynthesis was almost directly proportional to light intensity. No evidence of light saturation was found. For all measurenients over the course of a season the correlation coefficient for the relationship of photosynthesis to light intensity was 0.95. It seemed readily apparent that not all the leaves in the canopy were operating at the same rate although the average rate for all leaves was near 30 mg C o ndm+ hr-I at midday; indeed, Hesketh and Musgrave (1962) soon reported that healthy maize leaves exposed to full sunlight had rates of photosynthesis of more than 50 mg C 0 2 dmPa hr-l-a rate not thought to be possible in air containing only a normal concentration of CO,. They also found that individual maize leaves were not fully saturated with light even at the 10,000 ft-c intensity of direct sunlight. These unique and unexpected experimental results on photosynthesis in maize caused us to reconsider the inaccurate concept we had gleaned

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from the literature. Reexamination of the earlier report of light saturation in maize leaves by Verduin and Loomis ( 1944) revealed that they worked with Cellophane leaf envelopes which had no temperature control. At 25

r

__ Assimilation _ _ _ Solar Radiation

20

15

10

5

I

5AM

lo

10 A M

3 PM

8 PM

F I G . I . The photosynthetic response of a maize canopy to light on a clear and on a cloudy day (inset). Adapted from Moss et al. (196 I ) and Moss (1964).

lower light intensities their photosynthetic light response curve was identical to that of Hesketh and Musgrave (1962). At high light intensities, however, some of their leaves wilted from the excessive heat build up in the leaf envelope and gave low rates of photosynthesis. Other leaves had rates as high as those found by Hesketh and Musgrave. Unfortunately, Verduin and Loomis chose to “average” these extremely variable rates at high light intensities by drawing a regression line on their graph, and this gave an apparent, but faulty, light saturation.

2 . High Rates Also Found in Other Species The photosynthetic responses we had observed in maize were not unique to this species but were also found in other fast-growing grasses such as sugarcane and sorghum (Hesketh and Moss, 1963; Moss, 1964; Fig. 2). El-Sharkawy and Hesketh ( 1 965) soon found a number of other species which had the high rates of C O z fixation and lack of light saturation of maize, including several tropical grasses and species in the genus Amaranthus, the first dicots known to have such high rates. Thus, it became apparent that the “sun” and “shade” plant classification of photosynthetic responses as used by Bohning and Burnside was inadequate; an

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DALE N . MOSS A N D ROBERT B. MUSGRAVE

additional category needed to be included for plants which had the photosynthetic light response of maize. Many crop species, such as tobacco and red clover, were found to have photosynthetic responses to light which were identical to those of the “sun plants” reported by Bohning and Burnside (1956), however. Their report was accurate as to the responses of shade plants as well. During the last decade much information has accumulated about the group of plants which have photosynthetic traits similar to maize. Since this information is of importance to certain efforts being made to breed plants for photosynthetic efficiency, it seems appropriate to review this literature in some detail here and to compare the characters and processes associated with photosynthesis in the contrasting types of crop plants. 3 . C O , Compensation Point

In 1962, Moss reported that, contrary to the previous reports for many species, maize and sugarcane had CO, compensation points of less than 10 ppm COz. Under the same experimental conditions, orchardgrass, tobacco, geranium, and tomato had compensation points of 60 ppm CO, or greater. Meidner ( 1 962), at about the same time, confirmed the low Compensation concentration for maize. He used the capital Greek letter gamma, r, to symbolize the CO, compensation concentration. We shall use that symbolism in the remainder of this manuscript when referring to the CO, compensation point. Associated with low CO, r is a unique ability to capture C 0 2 in low concentration atmospheres. Moss ( 1 962) found that corn and sugarcane leaves retained two-thirds of the photosynthetic rate they had in normal air when the ambient concentration was only 100 ppm. In contrast, orchardgrass, tobacco, and tomato had only one-third the normal rate. Thus, not only was the rate of photosynthesis lower in normal air for the latter species, but they were relatively more affected by CO, stress conditions. Many crop species have an enhanced respiration in the light (Moss, 1966). This phenonenon, known as photorespiration (Decker, 1970), is thought by many workers to be involved in the relatively low rates of photosynthesis found in species which possess it. Maize and other low r plants do not photorespire. There is an extensive literature on photorespiration which has been reviewed recently by Jackson and Volk (1970), and it need not be reviewed here. We do point out, however, that photorespiration has been linked to glycolate metabolism (Zelitch, 1958). Glycolate metabolism has been linked, in turn, with photosynthetic rates (Zelitch, 1965, 1966) and with the presence in leaves of cell organelles called peroxisomes (Tolbert et al., 1968, 1969). The extensive literature

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on peroxisomes has been reviewed by Tolbert and Yamazaki (1969). Low r plants lack photorespiration and have few leaf peroxisomes.

4 . Higher-Optimum Temperature The temperature responses of photosynthesis in temperate and tropical Gramineae differ strikingly. Temperate species show optimal growth and net photosynthesis at about 20”-25”C, whereas the tropical grasses, including maize, have optima between 30” and 35°C (Murata et al., 1965; Evans et al., 1964; J. P. Cooper and Tainton, 1968). The higher optimum temperature of the tropical grasses is believed to be associated with the lack of photorespiration in these species, for in high r plants like the temperate Gramineae, COz evolution can be shown to increase in light more or less in proportion to photosynthesis, and the rate of increase is markedly higher at higher temperatures (Jolliffe and Tregunna, 1968; Hofstra and Hesketh, 1969).

5 . Pathway for Carbon Fixation In 1965, Kortschak et al. reported that sugarcane fixed carbon in photosynthesis by a pathway which was different from the “Calvin Cycle” and which resulted in the formation of oxaloacetate, malate, or aspartate as the first stable product, instead of the expected 3-phosphoglyceric acid. This discovery was confirmed by Hatch and Slack ( 1 966). Hatch et al. (1967) then showed that this same pathway functioned in several tropical grasses-but not in temperate grass species or in most dicots. Thus, another characteristic was added to the unique features of this group of plants. A thorough review of the biochemical differences between species having the Calvin Cycle and those having the C-4 dicarboxylic acid cycle for CO, fixation is given by Hatch and Slack ( I 970). 6 . LeafAnatomy

Downton and Tregunna (1968) showed that the species found to have the C-4 pathway by Hatch et al. ( I 967) all hadr near 0 ppm while species with the Calvin pathway all had r greater than 40 ppm. They also reported that all low r plants had a characteristic leaf anatomy with the minor vascular bundles surrounded by a prominent chlorenchymatous bundle sheath. They drew attention to some earlier work by Rhodes and Carvalho (1944) on the vascular bundle arrangements in maize. In that work Rhodes and Carvalho pointed out that the vascular bundle sheath cells contained many unusually shaped chloroplasts that were specialized for starch production. They speculated that these chloroplasts had a sequential role in the photosynthetic reactions of the leaf of maize plants.

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Hodge et al. (1 955) and Laetsch et al. (1 965) reported that the vascular bundle sheath chloroplasts in maize and sugarcane were morphologically distinct in structure from the mesophyll chloroplasts. The bundle sheath chloroplasts had few or no grana, but they had very dense and highly organized lamellae throughout the entire chloroplast. Downton and Tregunna (1 968) suggested that this arrangement of chlorenchymatous vascular bundle sheaths with chloroplasts specialized for starch production was a distinguishing characteristic of low r (C-4) species. Furthermore, from their literature review and measurements of carbon dioxide compensation points on 30 species, they suggested that low r and C-4 pathway were characteristics that would be valuable in distinguishing the genetic origins of species. Krenzer and Moss ( 1 969) sampled 325 grass species and confirmed clearly the distribution in grasses that Downton and Tregunna had suggested. The relationship between green vascular bundle sheaths and compensation points is not as simple, however, as Downton and Tregunna had visualized. Crookston and Moss ( 197 1) measured compensation points in 88 dicotyledonous species, all of which had green vascular bundle sheaths. Only 3 of these 88 species had low CO, compensation points. The vascular bundle sheaths in these 3 species, however, had all the characteristics found in maize including the morphologically distinct chloroplasts and the specialization in these chloroplasts in regard to the starch formation. The chloroplasts in the bundle sheaths of the other dicot species were indistinguishable from chloroplasts in other mesophyll cells. Thus, the distinguishing nature of the specialized bundle sheath still held true. Laetsch (1968) found that the chloroplasts in bundle sheaths of amaranthus and atriplex species, which have the C-4 pathway for photosynthesis and low r, also contained grana. Thus, he suggested that the presence or lack of grana in bundle sheath chloroplasts was not one of the distinguishable characteristics of these species. He found, however, that the bundle sheath chloroplasts in these species had a characteristic peripheral reticulum consisting of many interlocking vesicles around the outer membrane envelope. He suggested that, indeed, this reticulum is one distinguishing difference between the bundle sheath and other mesophyll chloroplasts in C-4 plants which holds true for all plants thus far examined. Moss and Rasmussen ( I 969) found that the bundle sheath chloroplasts in maize accumulated large amounts of radioactive label when leaves were fed 14C02for 90 sec or less and immediately frozen and dried while frozen. Sugar beet leaves, however, showed no localization of 14C02in leaves during the same period of exposure to 14C02. A some-

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what similar experiment was reported by Pristupa (1 964) on maize and barley. Moss and Rasmussen interpreted their data to indicate that the bundle sheath chloroplasts were capable of fixing an inordinately large amount of carbon dioxide and, indeed, they speculated that the high rates of photosynthesis found in maize may in part be due to specialization in the chloroplast system. This view is opposed by work indicating that the enzyme responsible for initial COz fixation in C-4 plants, phosphoenolpyruvate carboxylase, is apparently located largely in mesophyll cells (Slack, 1969; Hatch and Slack, 1970; Berry et al., 1970; Bjorkman and Gauhl, 1969). Thus, the relationship between the two kinds of chloroplasts found in C-4 plants and their role in the high rates of photosynthesis possible in these plants is not known at this time. IV. Breeding for Photosynthetic Efficiency

I n the preceding sections we have discussed a number of physiological processes that are associated with high rates of COz fixation in certain species including a number of crop species. Many other crop species lack these characters and have much lower rates of net photosynthesis. One possible avenue to markedly changing the photosynthetic capacity of crops such as small grains would be to search for individual plants within these species which had the photosynthetic characteristics of maize. Some attempt along that line has been made and will be discussed hereafter. A second possible approach to improving photosynthetic capacity would be a more typical plant breeding effort of seeking genetic variability for photosynthetic rates within species. This approach would depend for success on finding superior genotypes and on finding heritabilities for photosynthetic rates sufficiently large that progress could be made in improving the rate in otherwise desirable genotypes. A discussion of the work in this area and the research problems associated with it is also given hereafter. The two approaches suggested above are involved with attempts to change the photosynthetic capacity of leaf tissue. A third effort which could lead to higher yields is to breed plants which have a more appropriate form to lessen the effect of environmental limitations to photosynthesis. Efforts in this area have much in common with efforts to manage photosynthesis of present crop varieties by cultural practices; they are discussed in the final section of this paper. V. Selecting for Low

r Traits in High r Species

From the discussion in previous sections it is apparent that the differences between the photosynthetic components in low r species com-

3 28

DALE N. MOSS A N D ROBERT B. MUSGRAVE

pared to a high r species are very complex. Thus, it is unlikely that the genetic control of the differences is simple or that it would arise by a simple mutation. Nevertheless, the entire complex of features discussed above has arisen numerous times in evolutionary history for it is found in a number of unrelated families in both monocots and dicots. Therefore, the tendency for this complex to develop would seem to be stronger than might be expected from the probability that many different processes and traits would undergo simultaneous mutation. Downton and Tregunna (1968) suggested that the complex of traits associated with photosynthesis was fundamentally distinct and could be used to define taxa. However, they found that the Atriplex genus contained species of both types. [Several other genera, as presently classified, also contain both high and low r species (Downton et al., 1969; Moss et al., 1969).] Bjorkman et al. (1970) have succeeded in obtaining viable crosses between low r Arriplex rosea and high r Atriplex hastata. A . rosea was the female parent, and all the F1 hybrids were high r. These F, hybrids produced viable seeds indicating considerable genetic compatabilities. Thus, it does not appear that the genetic differences are as great between at least some low and high r plants as might be expected from the species association for the contrasting types that is observed. Since the probability of finding a low r plant in a high r species was unknown, however, Menz et al. (1969) sought a method to screen large populations of high r plants for a low r plant. They developed a screening technique which was based on the different capacities between illuminated high and low r plants to extract CO, from the air. By placing seedlings of high r species in a closed system with maize seedlings, all planted in sand, a COa stress atmosphere was created, by means of the ability maize seedlings had to extract CO, from the air, which was lethal to high r plants. This system was tested on many high and low r species and shown to be totally reliable in differentiating between the two types of plants. This system was used to screen the USDA world collection of soybeans (Cannell et al., 1969) and has been used to date to screen approximately 10,000 oat seedlings and more than 50,000 wheat seedlings (Moss, unpublished data). No low r plants have been found in these species. Thus, it does not appear that low r plants will readily be found in high r species. VI. Selecting for Photosynthetic Rates within Species

A number of laboratories are attempting to identify genotypes with superior photosynthetic capacity in a number of different species. Pearce et al. (1968) found photosynthetic rates in alfalfa leaves were related

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to leaf dry weights. Pearce et al. (1969) found a range of photosynthetic rates in alfalfa clones of 20-50 mg CO, dm-, leaf hr-l which were positively correlated with specific leaf weight differences of 1.9-5.3 mg cm+. Clones were selected from four different alfalfa populations which differed in both these traits. Although the specific leaf weight was strongly influenced by age and environment (Barnes et al., 1969), they suggested nevertheless, that it was a convenient, economical, and rapid method to classify the genotypic capacity of clonal photosynthesis. Brun and Cooper (1967) reported that H A R K soybean had a greater photosynthetic rate than CHIPPEWA in 45 of 48 light intensity-COz concentration combinations which they used. Dornhoff and Shibles ( 1970) found photosynthetic rates of soybean leaves were highly correlated with specific leaf weights. Varietal differences in photosynthesis ranging from 29 to 43 mg CO, dmP2leaf hr-I were correlated with specific leaf weight differences of 3.3-4.6 mg cm-'. Thus, the potential to select for photosynthetic rate in soybeans seems good; again the simple method of selecting for specific leaf weight would seem to be an effective procedure. Wilson and Cooper ( 1969a-e) have done similar work with grasses and have carried these efforts considerably further. They made selections for photosynthetic rate in Lolium perenne L. clones, crossed them, and studied the heritability of photosynthetic rate in succeeding generations. They found that photosynthetic rates were negatively correlated with average mesophyll cell size. Thinner leaves had smaller cells and, interestingly, greater specific leaf weight. They found the fastest rates of light-saturated photosynthesis in narrow, thin leaves with small mesophyll cells and much chlorophyll per unit volume. A half-diallel cross was performed among six Lolium perenne genotypes from populations of contrasting origin. Narrow-sense heritabilities from the analysis without parents were 0.70 for light saturated photosynthesis (Wilson and Cooper, 1969e). Ape1 and Lehmann (1969) measured photosynthetic rates in 115 varieties of barley. They found that environment and nutrition changed the rate but the ratio of varieties remained constant. The mean of adapted varieties was near to the extreme positive value (20-22 mg C O, dm-2 hr-') from a range of I 1 to 22. This emphasizes one of the problems that has come up repeatedly in a number of different studies; although a range in photosynthetic rates of nearly 2 times the low rates are often reported, many adapted varieties have rates near the positive maximum. What many workers may be seeing to cause variability are low rates in poorly adapted lines. It is difficult to see how yields can be improved by breeding for photosynthesis unless genotypes can be identified which are superior to present varieties.

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Wallace and his co-workers have done extensive analysis of the physiological basis for yield differences in two bean (Phaseofus vufgaris L.) Varieties, MICHELITE-62 and R E D KIDNEY. lzhar and Wallace (1967) summarized the work on photosynthesis. Photosynthesis of MICHELITE62 exceeded RED K I D N E Y by 3 1 % over a range of light intensities. From the photosynthetic efficiencies Of R E D KIDNEY and MICHELITE-62, their F1 and Fz progenies, and a backcross to RED K I D N E Y , they suggested that “the varietal difference in net C o n exchange rate is quantitative, that there may be relatively few genes involved, and that there is some dominance for the low photosynthetic efficiency of Red Kidney.” Heichel and Musgrave (1969) studied photosynthetic rates in 27 varieties of maize. They found a range from 28 -+ 2 to 85 3 mg COz dmP2 hr-I when grown under field conditions at high temperatures and radiation, Single crosses in this test and in another involving seven varieties had 3 4 % higher photosynthesis than the mean of their inbred parents. Consideration of this apparent heterosis for photosynthesis along with a finding that the within inbred variations in photosynthesis equaled those of open-pollinated varieties prompted an effort, starting in 1 9 6 7 , to select high and low photosynthetic strains from inbreds. Four inbreds which were the parents of a promising experimental hybrid in the Cornell corn breeding program were chosen for this effort. The purpose was to evaluate the dependence of yield on photosynthesis by comparing the yielding abilities of hybrids of these special strains and of the original inbreds under a range of populations to produce varying degrees of competition for light. Five generations of selection (using portable leaf chambers on field grown plants at the early tassel stage and infrared CO, analysis) and selfing have been used thus far in an attempt to create 6 high and 3 low photosynthetic strains of each of the 4 inbreds. Averages of their 1970 leaf photosynthetic rates are listed in Table I from unpublished data. The ranges from high to low appear large enough to be useful for examining the contribution of photosynthesis to yield. However, the variation

*

TABLE I Photosynthetic Rates (rng COr d m P hr-’) of High and Low Strains of Maize lnbreds Inbred ~~

6 High

3 Low

76 56 68 64

45

~

C153 Oh5 I A

loB8 Ny82 I

29 37 33

PHOTOSYNTHESIS A N D CROP PRODUCTION

33 1

of the individual rankings within and between the high and low groups from one generation to the next has tended to be large, especially for Oh5 1 A. Four of the six high-ranking strains of C I53 and two of its three low-ranking strains have been consistent. Representatives of the high groups of the other two inbreds have performed consistently over the seasons but their lows have been erratic. Much of the switching in rank within the low groups is associated with substitutions forced by failure to obtain successful pollination of the plants of lowest photosynthetic capacity. Preliminary yield trials involving single-crosses of several of the photosynthetic strains were conducted in 1969 and 1970. Due to insufficient seed these trials were poorly replicated, the plots were small without guard rows, and only one population could be investigated. Leaf and canopy photosynthetic rates were measured only on one replicate in 1969 and two in 1970. Hence the photosynthetic effects on yield could not be determined accurately. Results and observations do indicate, however, that single crosses of photosynthetic strains of inbreds exhibit differences in height, color, leaf display and earliness and so must be expected to have variations in other factors not easily detected but likely influencing yield. This could seriously interfere with identifying any true relation between photosynthesis and yield. The work discussed above from many institutions suggests that photosynthetic rates do differ markedly among varieties in many crops. In some of these crops it appears that superior genotypes have been identified o r selections have been made from genetic lines which have improved capacity for photosynthesis. In some cases it appears that few genes control the differences and that heritability is sufficiently high to promise success in breeding improved varieties with a higher capacity for photosynthesis. VII. Breeding for Plant Type

The photosynthetic light response curve is not linear for any species, as indicated in Fig. 2 . Indeed, for many species, light more intense than about 1/4 sunlight is not only of no value for photosynthesis but supplies much additional energy to a leaf which must be dissipated. At midday in summer, when the sun is nearly directly overhead, the average intensity of light, I, striking a leaf is

I = I, cos 0 where I = intensity of the light striking the leaf surface, I , = intensity on a horizontal plane, 0 = angle of leaf with the horizontal plane.

DALE N. MOSS A N D ROBERT B . MUSGRAVE

332

If we assign the symbol A to a given area of soil, then the maximum area of leaves above that soil that could receive direct sunlight if all the leaves were horizontal and the sun were directly overhead would also equal A . If all leaves were borne at an angle and appropriately distributed in space, however, the light intensity at the leaf surface would be I,, cos 0, but the area of leaves that could be lighted directly would be A/cos 0.

r

1

I

I

I

1

MAIZE

ORCHARDGRASS

c

B E E T -TOBACCO)

-

I

a OAK (MANY WOODY SPECIES) MAPLE

0

I 05

I 1.0

(-"SHADE"PLANTS)

I 1.5

I 2 .o

I N C A N D E S C E N T LIGHT Ly m i n - '

FIG. 2. The light response curves of leaves of various species. Adapted from Hesketh and Moss (1963).

If leaves were light saturated at 1/4 full sunlight then, theoretically, photosynthesis of a crop canopy in full sunlight could be increased by approximately 4-fold, compared to horizontal leaves, if all leaves were borne at an angle 75.5" (cos = 0.25) because the intensity at the leaf surface would be 1/4 that on a horizontal leaf (still a saturating intensity), but the area of leaves receiving that intensity would be 4 times as great. Obviously, the conditions for this dramatic increase in canopy photosynthesis will seldom, if ever, be found in an actual plant canopy. Leaves are not linear, nor rigid, nor are they distributed in space so that all direct sunlight is intercepted. The sun is not always directly overhead, and it approximates that position for only a small portion of the day. Nevertheless, leaf angle does have an appreciable effect on light penetration into crop canopies for much of the day. Pearce et al. (1967) tested the effect of leaf angle on barley seedlings by germinating densely seeded flats placed at angles with the horizon. This resulted in leave angles of about 18", 53", and 90". They found sig-

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333

nificantly more light penetrated the upright leaved stands and resulted in approximately 2-fold greater photosynthesis per unit ground area. Watson and Witts (1959) found that the net assimilation rate of cultivated more upright-leaved sugar beets was greater than the more prostrateleaved wild beets when the leaf area index was 2.5 but identical for LA1 of I or less. Pendleton et al. (1968) compared photosynthesis and grain yield in maize isolines which differed for leaf angle and on plots of droopyleaved maize where the leaves were mechanically positioned upright. They found a significantly greater grain yield from upright-leaved lines or treatments and relative efficiency of light utilization of 2.7 for leaves mechanically positioned at an angle of 7 I" compared to horizontal leaves. Maize isolines with erect (liguleless) and droopy leaves were also compared at Cornell. These were grown in three replications at 70,000 plants per hectare in 75-cm rows oriented in N-S direction. Total dry matter yields of tops were equal while grain yield was higher- 135- 1 17 bushels per acre-for the droopy leafed type. Light interceptions were equal in August and September, but the droopy leafed variety intercepted 24% more than the erect in mid-July. Canopy photosynthetic rates were also equal in August and September, averaging 80 mg COZdm-2 ground ly-' radiation. In mid-July canopy photosynthesis, like light, for the droopy leafed variety was 24% higher than for the erect. The leaf photosynthetic rate for the droopy leafed variety was higher by 10% in July but lower by 10% in August and September. Light response curves for the !eaves of both varieties were of the nonsaturating type and the maxima at 11,000 ft-c averaged nearly equal at 58 mg COXdm-? leaf hr-I for four samplings. Respiration rates of tops were equal (20 mg C 0 2dm-' ground hr-') in mid-July and August for the two varieties. In September the rate of the droopy leafed variety increased nearly 50%. Thus as might be expected for a crop that does not exhibit light saturation a t one-fourth full sunlight intensity, there were no measurable beneficial differences between the two types of canopies that could be attributed to the erect leaf type (from unpublished data of Musgrave and Grogan, 1970). Chandler (1969) attributes the superiority of new high yielding rice strains largely to the plant form. H e suggests that the critical elements of form are short rigid culm and upright leaves. The upright leaf character, he feels, is even more important at high levels of nitrogen fertilization when enhanced tillering would otherwise cause excessive shading. Donald (1968) reviewed the effects of plant type on photosynthesis and made a strong case for breeding for plant ideotypes. H e described the ideal ideotype for wheat as having a short, strong stem; few, small erect leaves; an erect ear; awns; and a single culm per plant. H e concluded that "Eventually most plant breeding may be based on ideotypes."

334

DALE N . MOSS A N D ROBERT B. MUSGRAVE

Plant characters other than those studied by the above-mentioned workers may prove important in affecting photosynthesis. Miskin and Rasmusson ( 1970) found that stornatal frequency varied by 2-fold among barley varieties in the field. The differences found in the field were confirmed in the greenhouse using 50 cultivars. It would seem, therefore, that the diffusive resistance of leaf surfaces may be subject to genetic manipulation. Thus, many possibilities exist to alter plant form with the potential to change yield. Although we may not think of this plant design work as “breeding for photosynthesis” it is obvious that the mechanism by which these breeders hope to change yield is by changing the photosynthetic capacity of crop varieties. VIII. Managing Photosynthesis

Many of the cultural practices utilized in growing crops also have a major part of their effect through the mechanism of photosynthesis. Poorly fertilized plants have low rates of photosynthesis; drouth may have its greatest effect by causing stomatal closure and thereby reducing photosynthesis; optimum planting dates take advantage of the light and temperature regimes of nature that best fit the photosynthetic optimum of the species concerned and we could go on listing examples almost endlessly. The important point is that much that has been done in the past in managing crops has resulted in greater photosynthesis as well as greater economic yields. Much recent management research (row widths, planting patterns, cropping densities, double cropping) has arisen because of some of the results on photosynthesis research and from such photosynthetic management evaluations as reflecting light into crops (Pendleton et al., 1966, 1967) or alternating strips of contrasting plant types to try to increase light utilization (Pendleton et al., 1963). Thus, at present there is a large and continuing research effort in public institutions, by private companies, and by individual farmers to devise ways to increase photosynthesis by breeding for biochemical capacity or plant type or by proper management with the goal in mind that higher yields will result. REFERENCES Apel, P., and Lehmann, C. 0. 1969. Photosynrherica 3, 255-262. Barnes, D. K., Pearce, R. B., Carlson, G . E., Hart, R. H., and Hanson, C. H. 1969. Crop Sci. 9, 42 1-423. Berry, J. A . , Downton, W. J. S., and Tregunna, E. B. 1970. Can. J . Bot. 48,777-786. Bjorkman, O., and Gauhl, E. 1969. PIanta 88, 197-203.

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Bjorkman, 0.. Gauhl, E., and Nobs, M. A. 1970. Carnegie f n s t . Washington, Yearb. 68, 620-633. Black, J. N . 1963. Australian J . A g r . R e s . 14, 20-38. Blackman, G. E., and Black, J. N. 1959. Ann. Bot. (London) [N.S.] 23,51-63. Bohning, R. H., and Burnside, C. A. 1956. A m e r . J. Bot. 43,557-561. Brun, W. A,, and Cooper, R. L. 1967. C r o p Sci. 7,451-454. Cannell, R. Q., Brun, W. A., and Moss, D. N. 1969. Crop Sci. 9,840-84 I . Chandler, R. F., Jr. 1969. “Physiological Aspects of Crop Yield,” pp. 265-285. Amer. SOC.Agron., Madison, Wisconsin. Chapman, H. W., and Loomis, W. E. 1953. Plant Physiol. 28,703-716. Cooper, J. P., and Tainton, N. M. 1968. H e r b . A b s f r . 38, 167-176. Cooper, R. L., and Brun, W. A. 1967. C r o p Sci. 7,455-457. Crookston, R. K., and Moss, D. N. 1970. Plant Physiol. 46,564-567. Cummings, M. B., and Jones, C. H . 1918. Vermont Agr. Exp. Sta., Bull. 211, 1-56. Decker, J. P. 1970. Arizona State Univ.,Bioenp. Bull. 10, 1-20. Donald, C. M. 1968. Euphytica 17,385-403. Dornhoff, G. M., and Shibles, R. M. 1970. C r o p Sci. 10,42-45. Downton, W. J. S . , and Tregunna, E. B. 1968. Can. J. Bot. 46,207-215. Downton, W. J. S., Berry, J., and Tregunna, E. B. 1969. Science 163,78-79. El-Sharkawy, M.. and Hesketh. J. D. 1965. C r o p Sci. 5 , 5 17-521. Evans, L. T. 1971. In “Productivity of Photosynthetic Systems,” pp. 42 1-425. Proc. Trebon IBP/PP Symp. P U D O C Wageningen, Netherlands. Evans, L. T., Wardlaw, 1. F., and Williams, C. N . 1964. I n “Grasses and Grasslands” (C. Barnard, ed.), pp. 102-125. Macmillan, New York. Hardman, L. L. 1970. Ph.D. Thesis, University of Minnesota. Hatch, M. D., and Slack, C. R. 1966. Biochem. J. 101, 103-1 I I . Hatch, M. D., and Slack, C. R. 1970. Annu. R e v . Plant Physiol. 21, 141-162. Hatch, M. D., Slack, C. R., and Johnson, H. S. 1967. Biochem. J. 102,417-422. Heichel, G. H., and Musgrave, R. B. 1969. C r o p Sci. 9,483-486. Heinicke, A. J., and Childers, N . F. 1937. Cornell Univ., Agr. Exp. Sta., Mem. 201,3-52. Hesketh, J. D., and Moss, D. N. 1963. Crop Sci. 3, 107-1 10. Hesketh, J. D., and Musgrave, R. B. 1962. C r o p Sci. 2,31 1-3 15. Hodge, A. J., McLean. J. D., and Mercer, F. V. 1955. J . Biophys. Biochem. C y f o l . 1,605619. Hofdra, G., and Hesketh, J. D. 1969. Planta 85,228-237. Izhar, S., and Wallace, D. H. 1967. C r o p Sci. 7,457-460. Jackson, W. A., and Volk, R. J. 1970. Annu. R e v . Plant Physiol. 21, 385-432. Jolliffe, P. A,, and Tregunna, E. B. 1968. Plant Physiol. 43,902-906. Kortschak, H. P., Hartt, C. E., and Burr, G. 0. 1965. Plant Physiol. 40, 209-213. Krenzer, E. G., Jr., and Moss, D. N . 1969. C r o p Sci. 9,619-621. Laetsch, W. M. 1968. Amer. J. Bot. 55, 875-883. Laetsch, W. M., Stetler, D. A,, and Vlitos, A. J. 1965. Z. Pjanzenphysiol. 54.472-474. Lundegardh, H . 1927. Soil Sci., 23,417-453. Meidner, H. 1962. J. Exp. Bot. 13,21(4-293. Menz, K. M., Moss, D. N., Cannell, R. Q., and Brun, W. A. 1969. C r o p Sci. 9,692-694. Miskin, K., and Kasmusson, D. C. 1970. C r o p Sci. 10, 575-578. MOSS,D. N. 1962. Nature (London) 193,587. Moss, D. N . 1964. In “Forage Plant Physiology and Soil-Range Relationships,” Amer. Soc. Agron.Spec. Publ. 5,1-14. MOSS, D. N. 1966. Crop. Sci. 6,351-354.

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Moss, D. N., and Rasmussen, H. P. 1969. Planr Physiol. 44, 1063-1068. Moss, D. N., Musgrave, R. B., and Lemon, E. R. 1961. Crop Sci. 1,83-87. Moss, D. N., Krenzer, E. G., Jr., and Brun. W. A. 1969. Science 164, 187-188. Murata, Y., lyama, J., and Honrna, T. 1965. P roc. Crop Sci. SOC.Jap. 34, 154- 158. Musgrave, R. B., and Moss, D. N. 1961. Crop Sci. 1, 37-41. Pearce, R. B., Brown, R. H., and Blaser, R. E. 1967. Crop Sci. 7,321-325. Pearce, R. B., Brown, R. H., and Blaser, R. E. 1968. Crop Sci. 8,677-680. Pearce, R. B., Carlson, G. E., Barnes, D. K., Hart, R. H., and Hanson, C. H. 1969. Crop Sci. 9,423-426. Pendleton, J. W., and Weibel, R. 0. 1965. Agron. J . 57,292-293. Pendleton, J. W., Bolen, C. D., and Seif, R. D. 1963. Agron. J. 55, 293-295. Pendleton, J. W., Peters, D. B., and Peek, J. W. 1966. Agron. J. 58,73-74. Pendleton, J. W., Egli, D. B., and Peters, D. B. 1967. Agron. J. 59,395-397. Pendleton, J. W., Smith, G. E., Winter, S. R.,and Johnston, T. J. 1968. Agron. J. 60,422424. Pristupa, N. A. 1964. Sov. Planr Physiol. 11,38-42. Rhodes, M. M., and Carvalho, A. 1944. Bull. Torrey Bot. Club. 71, 335-346. Slack, C. R. 1969. Phytochemistry 8, 1387-1391. Stinson, H. T., and Moss, D. N. 1960. Agron. J . 52,482-484. Tanaka, A., Kawano. I., and Yamaguchi, J. 1966. Int. Rice Res. Inst., Tech. Bull. 7,1-46. Thomas, M. D. 1955. Annu. Rev. Planr Physiol. 6, 135-156. Thomas, M. D., and Hill, G. R. 1937. Plant Physiol. 12,309-383. Thomas, M. D., and Hill, G. R. 1949. In “Photosynthesis in Plants” (J. Frank and W. E. Loomis, eds.), Chapter 2, pp. 19-52. Iowa State Univ. Press, Arnes. Tolbert, N. E., and Yamazaki, R. K. 1969. Ann. N . Y. Acad. Sci. 168,325-341. Tolbert, N. E., Oeser, A., Kisaki, T., Hagernan, R. H., and Yamazaki, R. K. 1968.5. Biol. Chem. 243,5179-5 184. Tolbert, N. E., Oeser, A., Yamazaki, R. K., Hageman, R. H., and Kisaki, T. 1969. Plant Physiol. 44, 135- 147. Verduin, J., and Loomis, W. E. 1944. Planr Physiol. 19, 278-293. Watson, D. J., and Witts, K. J. 1959. Ann. Bor. (London) [N.S.] 23,431-439. Wilson, D., and Cooper, J. P. 1969a. N e w Phyrol. 68,627-644. Wilson, D., and Cooper, J. P. 1969b. N e w Phytol. 68,645-655. Wilson, D., and Cooper, J. P. 1969~.N e w Phytol. 68,1115-1 123. Wilson, D., and Cooper, J. P. 1969d. N e w Phytol. 68, I 125- 1135. Wilson, D., and Cooper, J. P. 1969e. Heredity 24,633-649. Zelitch, 1. 1958. J. Biol. Chem. 223, 1299- 1303. Zelitch, I. 1965. J. Biol. Chem. 240, 1869-1876. Zelitch, I. 1966. Planr Physiol. 41, 1623-1631.

NITRIFICATION RETARDERS AND SLOW-RELEASE NITROGEN FERTlLIZERS Raiendra Prasad, G. B. Rajale, and B. A. Lakhdive’ Division of Agronomy, Indian Agricultural Research Institute, New Delhi, India

Introduction ........._................................, ................. ...... ...... ...... ......... A. Recovery of Applied Nitrogen .................................................. B. Causes of Low Recoveries ..................................... C. Ways to Reduce Nitrogen Losses .................................................... D. Concept of Nitrification Retarders and Slow-Release Nitrogen Fertilizers ........................... . ., . . .. ... ... ....... ..... . I I. Nitrification Retarding Properties of Agricultural Chemicals ..... .. ................ A. Herbicides ................................................................................... B. Insecticides ..................................... ................... C. Fungicides ........................................................................... D. Fumigants ................................................................ I l l . Nitrification Retarders ............................................ A. 2-Chloro-6-(trichloromethyl)pyridine (N-Serve) .... B. 2-Amino-4-chloro-6-methylpyrimidine ( A M ) ..., .., .... ..... ... ... ... ........... .. C. Dicyandiamide (Cyanoguanidine) .. ...............................

I.

337 338 340 34 1

342 342 343 344 3 44 345 345 348 355 356 ....................................... . ..... . ...... ......... ................... 357 358 E. 2-Sulfanilamidothiazole (ST) ...., ........... ... ... ... ... . ... .. ................................. 358 358 B. Oxamide ................................................. ............... 361 363 365 366 E. U rea-acetaldeh yde .................................................... 366 367 3 67 368 3 69 ................ 370 K. Nitrogen-Enriched Coal ............ ... ........ ...... 37 I V . Coated Fertilizers .... .................... ... , ... . .. . ... ......... ......................... ....................... A. Sulfur-Coated Urea .......... .. . .. . ....... . 37 I B. Fertilizers Coated with Inert Materials __.... .................................. 374 375 ............... VI. Concluding Remarks ............................. ... ... ... 376 References ., .., .., .., ....................... ..... . . . . ... .... .

I.

Introduction

Fertilizer nitrogen has contributed largely toward meeting man’s needs for food and fiber. Since it is one of the costliest inputs in agricultural ‘Present address: Department of Agronomy, Punjabrao Krishi Vidyapeeth, Akola, Maharashtra, India.

337

338

RAJENDRA

PRASAD, G.

B.

RAJALE, AND

B.

A. LAKHDIVE

production, its efficient use has been the subject of study since the very dawn of scientific agriculture. This paper presents some of the findings of agronomic interest as related to latest trends and developments in the field of fertilizer N with reference to nitrification retarders and slowrelease N fertilizers.

RECOVERYOF APPLIEDNITROGEN The data from lysimeter experiments in the United States and the United Kingdom as reviewed by Allison (1955) revealed a N recovery of 21-79%. Values of 60% and above were obtained when grasses such as sudangrass and timothy were used. In pot-culture experiments the recoveries of applied N have generally been high and range between 30% and 92% (Table I ; also Allison, 1965, 1966). Many of these experiments employed 3-6 cuttings of forage, and some workers utilized fertilizer containing I5N. In field experiments the recovery of applied N is generally 50% or below (Table I , also A. E. Martin and Skyring, 1962; Allison, 1965, 1966). Recoveries above 50% are reported with grasses (e.g., Weir and Davidson, 1968), although Allison (1965) quotes recovery of 50% for bromegrass and crested wheatgrass grown on a Prierre clay at Newell (South Dakota) and only 20% for wheatgrass grown on a calcareous Bowdoin clay in Montana. Rice crop has recorded some of the lowest recoveries (Sanchez and de Calderon, 197 1). Recovery of fertilizer N is generally determined by difference method, i.e., the difference between uptake with applied N and with none. Terman and Brown ( 1 968) made an interesting study and have suggested the use of linear regression technique for determining the check plot values and for calculating the recovery of applied N. Depending upon the plus, minus or no deviation of the observed check plot values from the calculated values, 3 types of N-uptake curves were characterized. Different conclusions resulted from percentage recoveries estimated by the usual “difference method” for each type of N-uptake curve. No further reports on this suggestion have appeared but the technique needs a fair trial, although this questions the validity and usefulness of providing a check in experiments. Many agronomists may find it difficult to reconcile with this suggestion as the entire argument is based upon an extrapolated point. Terman and Brown (1 968) also observed that for most routine N-efficiency experiments, labeling with I5N may have little advantage over use of unlabeled fertilizers if multiple rates are employed. Allison ( I 965) also observed that the simple nontracer method is usually preferable for use by agronomists, as the chief concern is practical evaluation of fertilizer response. This is really a useful comment, and workers in less developed A.

339

NITRIFICATION RETARDERS

TABLE I Recovery of Fertilizer Nitrogen by Crop ~

Crop

Source of N

A. Field experiments Wheat

Wheat Corn

Rate

(%)

63 Ib/A I26 IbIA

23-39 27-35

Ammonium 60- 140 kg/ha sulfate 80-240 kg/ha

34-39

50- 100 kg/ha

25-32

Sorghum

35-75

Sorghum Rice (transplanted)

Urea Urea

120 kg/ha

58.5

180 kg/ha

10-30

Rice (transplanted)

Urea

150 kg/ha

34.3

Rice (transplanted) Pangolagrass (Digitaria decumbens) B. Pot experiments Corn

Sudangrass

R hodesgrass (Chloris guyana)

~

Recovery

40- 120 kg/ha Sodium nitrate Ammonium 40- 120 kg/ha sulfate Urea 50- 150 kg/ha

39.6

Urea

1 I4 Ib/A

53-68

100-800 mglpot

62-93

Ammonium 37.5-600 sulfate mg/pot (labeled) Ammonium 25-400 Ib/A nitrate (labeled)

Location

Reference

Widdowson el al. ( 1964) New Delhi Dutta (India) ( 1967) Bomme New Delhi Gowda ( 1968) Srivastava New Delhi ( 1 966) New Delhi Roy ( 1969) Lambayeque Sanchez (Peru) and de Calderon (1971) Lakhdive New Delhi ( I 968) Rothamsted

(U.K.)

19.4

28-34

38-76

38-6 I

New Delhi

Rajale ( I 970) Trinidad Weir (W. Indies) ( 1969)

Muscle Shoals (U.S.A.)

Terman and Brown ( 1968) Legg and Allison ( I 959) Brisbane J. P. Martin ( I 963) (Australia)

countries with no '"N facilities therefore need not get much concerned and should generate data so that a better understanding of fertilizer N recovery under diverse conditions is obtained.

340

RAJENDRA

PRASAD, G .

B. RAJALE, A N D B. A. LAKHDIVE

B. CAUSESOF Low RECOVERIES The shortfall in recovery of applied N to some extent may be due to immobilization or retention as ammonia (Bremner, 1965; Mortland and Wolcott, 1965; Nommik, 1965; and Williams, 1966) of a part of N but mainly due to known or unaccountable N losses. Crop recovery of immobilized N (residual or carry-over effects) could vary from mil (Boischot and Gouere, 1945) to 49% (White et al., 1958) depending upon rainfall, soil conditions, and previous crop. With respect to newer N fertilizers, Hauck ( 1969) suggested studies for different soil and crop conditions on ( 1 ) solubilization of organic matter and its mineralization as affected by materials such as ammonium polyphosphates, and (2) effects of microbial competition for ammonium released at a slow continuous rate in case of slow-release N fertilizers. The available limited data do not conclusively show that ammonium retention process could result in significant reduced response to applied N (Hauck, 1969). Mechanisms of N loss from soil are well established, and excellent reviews on the subject are available (A. E. Martin and Skyring, 1962; Skyring and Callow, 1962; Allison, 1965; Broadbent and Clark, 1965; Quastel, 1965; Hauck, 1969). From the agronomic viewpoint, three processes appear to be of practical significance: ( I ) leaching in light soils and in areas of heavy precipitation or intensive irrigation (P. K. De and S. Digar, 1954; Ponnamperuma, 1955; Johnston et al., 1965; Okuda er a/., 1959; Raney, 1960; Prasad and Turkhede, 197 1); (2) volatile losses, such as ammonia from surface applied urea and, to some extent, ammoniumcontaining fertilizers (Volk, 1959, 196 1 ; Watson et al., 1962; Gasser, 1964; Acquaye and Cunningham, 1965); these losses are also reported from submerged soils (Sreenivasan and Subrahmanyam, 1935; S. P. Gupta, 1955; A. C. Das and Kahn, 1967), and some workers even found these to be higher under submerged than aerated conditions (Blasco and Cornfield, 1966; Delaune, 1968); and (3) denitrification in submerged soils. Although denitrification may take place in localized anaerobic pockets in aerated soils (Broadbent and Stojanovic, 1952; Corbet and Woolridge, 1940; Allison er al., 1960), the process achieves significance in submerged soils (Pearsall and Mortimer, 1939; Pearsall, 1950; Yamane, 1957; Bremner and Shaw, 1958; Greenland, 1962; International Rice Research Institute, 1967: Akhundov, 1967; MacRae et al., 1968). The soils and areas worst affected by this process are those subjected to alternate submergence and drying (Patrick and Wyatt, 1964; Prasad and Lakhdive, 1969; Rajale, 1970). (See Fig. 1 .) The principal crop grown is rice; the present yield levels are low, but recent crop improvements suggest great production potentialities (Swaminathan, 1965; Chandler, 1966), and consequently large demands for fertilizer nitrogen.

34 1

NITRIFICATION RETARDERS El. Drained

A . Flooded

700 r -

.

Moderately reduced

-

c

E *

g 5

100 .

o'

-100

Reduced Highly reduced

U

3

Reduced

-300 C. Flooded

4

+

Drained

FIG.I . Field conditions in areas subjected to alternate submergence and drying.

c.

W A Y S TO

REDUCE NITROGEN LOSSES

Losses of applied N can be reduced by proper placement, timely application, and foliar fertilization. The practices to be adopted will vary with the soil, crop, climate, irrigation, and source and level of nitrogen. Losses, such as volatilization of ammonia resulting from surface application of urea or ammonium-containing fertilizers, can be avoided by incorporating these in soil and, in the case of anhydrous ammonia, by injection in soil at proper depth and moisture. I n the case of rice, soil placement of nitrogen in the reduced (Fig. 1) layer considerably reduces N losses and thereby increases utilization of applied N (Abhichandani and Patnaik, 1955, 1959; Nagarajah and Al-Abbas, 1965a,b; Patrick er al., 1967; N. P. Datta and Venkateswarlu, 1967; Velly, 1967; Broadbent and Mikkelsen, 1968; Aleksic et al., 1968). Timely application of N is another important and well established practice. Considerable literature is available on fall vs. spring application of N ; see, for example, results reported by Bardsley er al. from Mississippi ( 1 960). To this may be added the practice of split or fractional application, the objective being to supply N in fractional dosages coinciding with the stages of plant growth when it is needed and utilized most in grain production. Split application is recommended for most crops under temperate as well as tropical conditions. An alternative to soil application is foliar spraying of urea. When it is sprayed at sufficient canopy, losses of nitrogen are greatly reduced. Use of a low-volume sprayer permits easily an application of 25-30 kg of N per hectare. Urea is absorbed rapidly by plants, a large part entering within 2 hours. Absorption is practically complete within 2 days (Freiberg

342

RAJENDRA PRASAD, G . B. RAJALE, A N D B . A. LAKHDIVE

and Payne, 1957; Impey and Jones, 1960). Many workers in India have found partial application of N through foliage better than application of all nitrogen through soil for rice and wheat (R. De et al., 1967; Mahapatra and Sharma, 1963; Sahu and Lenka, 1967; Sharma, 1970).

D. CONCEPT OF NITRIFICATION RETARDERS A N D SLOW-RELEASE N FERTILIZERS Leaching and denitrification losses of fertilizer N occur mainly when applied in or after its conversion to nitrate form. Inhibition or retardation of nitrification of applied ammonium and amide N can thus reduce these losses and increase the efficiency of applied N. Gorging’s work (1962a,b) triggered this thinking in the minds of some agronomists and fertilizer technologists and has finally led to the development of fertilizers blended with chemicals having nitrification inhibitory properties. Another approach which the agronomists and fertilizer technologists have been pursuing for quite some time is the development of slowrelease N fertilizers. The objective here is to develop fertilizer materials that will release or permit in solution only small quantities of N at a time, which can be utilized by the growing plants, and this reduces the chances of loss. This can be achieved by ( 1 ) using chemical compounds having such properties per se, or (2) by physically coating semipermeable membranes or inert materials onto the otherwise soluble fertilizer granules. Parr (1 967) has discussed the possibilities in detail. Both approaches have yielded some useful promising materials, and the results of agronomic evaluation of such materials are discussed in subsequent sections. Ill.

Nitrification-Retarding Properties of Agricultural Chemicals

Agricultural chemicals are directly or indirectly added to the soil when they are employed to control weeds, insects, diseases, parasites, etc. Besides achieving the main objective of destroying a specific pest, often these substances affect nonparasitic soil microorganisms by reducing their activity. Nitrifying organisms have also shown sensitivity to some agricultural chemicals. The toxic effect of a particular chemical varies greatly with dosage, soil properties, and environmental factors (Bollen, 1961; J. P. Martin, 1963). In general, soil fumigants and fungicides exert a greater inhibitory action on nitrifying bacteria (Stark et al., 1939; Kincaid and Volk, 1952; Wenseley, 1953) as compared to insecticides and herbicides in amounts commonly applied to control a pest. Although soil scientists investigated the nitrification inhibitory properties of the agricultural chemicals quite early, the beneficial effects to the crops from inhibition of nitrification in soil from agronomic point of view did not receive much attention. The effect of agricultural chemicals on inhibition of

NITRIFICATION RETARDERS

343

nitrification has been excellently reviewed by Fletcher (1960), J . P. Martin (1963, 1966), Eno (1958), Domsch (1963) and Audus (1964); the subject is only briefly discussed here, mainly highlighting the findings. For convenience of discussion, the chemicals have been classified into four groups: herbicides, insecticides, fungicides, and fumigants. A. HERBICIDES Most of the herbicides do not have nitrification inhibitory property at normal rates used in field to control weeds. However, in solution culture experiments and laboratory soil perfusion and percolation studies, herbicides showed a tendency to retard nitrification. Among the inorganic herbicides, sodium chlorate (Latshaw and Zahnley, 1927; Stapp and Buckteeg, 1937; Lees and Quastel, 1945; Smith et al., 1945), ammonium thiocyanate (Smith et al., 1945), and sodium arsenite (Quastel and Scholefield, 195 I ) retarded nitrification in soil. Sodium chlorate at 0.04 M achieved about 50% inhibition of ammonia oxidation and complete inhibition of nitrate oxidation for 4-7 days. Sodium chlorate was a specific inhibitor of nitrite oxidizers. The phenoxyacetic herbicides at normal field application rates had nil or little effect on nitrification, but some concentrations in solution culture checked nitrification (Flieg, 1952). High concentration of 2,4-D (500 ppm) injured nitrifying bacteria severely (Smith et al., 1945). Phenoxybutyric acid herbicides (2,4-DB) and phenylacetic acid herbicides (2,3,6-TBA) even at normal field application depressed nitrification (Chandra, 1964) for 8 weeks. p-Chloromercuribenzoic acid (PCMB) also showed nitrification inhibitory properties (Vlassak, 1962). Trichloroacetic acid (TCA) (Otten et al., 1957) and dalapon (Otten et al., 1957; Worsham and Giddens, 1957; Keller, 1961) at 20-40 Ib/A were quite toxic to nitrifiers, but their effect did not last long. Acetamides (CDEA and CDAA) caused initial suppression of nitrification; at a normal rate of application the effect was overcome in a month (Otten et al., 1957; Teater et a f . , 1958). Among urea herbicide compounds, monuron at 1 1 kg/ha inhibited nitrification temporarily, whereas diuron and neburon did not exert an inhibitory effect (Caseley and Luckwill, 1965). Toxicity to bacterial culture was related to solubility of herbicides; monuron, being highly soluble, was most toxic. I n a test using a pure culture of nitrifying bacteria, Nitrobacter agile was more sensitive to monuron. Hale et a f . ( I 957), however, could not confirm the nitrification inhibitory property of monuron. Carbamate compounds (propham, chloropropham, CDEC, diallate) depressed nitrification in soil at a field rate of application (Quastel and Scholefield, 1953; Hale et af., 1957; Otten et al., 1957; Teater et al.,

344

RAJENDRA PRASAD, G. B. RAJALE, A N D B . A. LAKHDIVE

1958; Chandra, 1964), but triazine herbicides had no effect on nitrification (Amantaev e? al., 1963; Caseley and Luckwill, 1965). In soil perfusion studies, however, 6-9 ppm of simazine slowed the rate of nitrification, being toxic to Nitrobacter agile (Farmer and Benoit, 1965). Szabo ( I 964) reported 2-methyl-mercapto-4,6 bis-isopropyl-aminostriazine (Al- 1 1 14) considerably inhibited nitrification. In substituted phenols, PCP was more toxic to nitrifying bacteria (Hale e? al., 1957) than DNOC and dinoseb. Matsuguchi and Ishizawa ( 1 968) found PCP to largely inhibit nitrification, while DNOC was only moderately toxic to Nitrosomonas europea (Jensen and Peterson, 1952). A concentration of 25 ppm of DNOC and dinoseb inhibited nitrification for 2 months (Douros, 1960). Wen (1967) observed that the fertilizer effect of urea contained in PCP was enhanced due to suppression of nitrification. Amitrole at 2-4 Ib/A was found to be enough to inhibit nitrate formation for 14 days (Otten et al., 1957), but pyramin, even applied at 100 kg/ha in loamy sand and sandy loam soil, did not (Jung, 1964). B. INSECTICIDES As in case of herbicides, most of the insecticides, when used at normal rate of application, do not inhibit the nitrification; as much as 5 times the normal field application of BHC, aldrin, and chlordane was necessary to bring inhibition of nitrification (Sinha, 1961). Aldrin up to 100 Ib/A and chlordane up to 300 Ib/A had no effect on nitrification (Shaw and Robinson, 1960). Even if insecticides retarded nitrification, it was only temporarily (Singh and Mehta, 1964). In laboratory studies, many insecticides at high concentrations showed toxicity of varying order to nitrifying organisms. According to A. L. Brown ( I 954), aldrin, dieldrin, and chlordane were most toxic to nitrifiers; D D T was least toxic; and lindane and heptachlor had intermediate toxicity. On the other hand, Eno and Evereth ( 1 958) observed that nitrate production decreased by heptachlor, lindane, and BHC and remained unchanged by chlordane, aldrin, and dieldrin. V. C. Gupta and Shrikhande (196 1) observed a decrease in bacterial number when D D T was applied at 50 ppm or more. Walker and Stojanvic (1968) reported retardation of nitrification when DDT, dieldrin, and malathion were applied at 2-16 ppm of soil. C. FUNGICIDES Fungicides are very effective in retarding nitrification, even when applied at normal rate. The effect of dithiocarbamate compounds on nitrification was studied in detail. Nitrification of (NH& SO4 in soil was inhibited for about 28 days by ferbam at 3.5 X mole/kg soil, for 25 days by manzate at 2.1 X mole/kg soil, and 17 days by zineb at 2.1 X mole/kg soil (Jaques e? al., 1959). Vapam at 224 kg/ha (Munnecke and Ferguson, 1960) or at 560 liters/ha (Koike, 1961) inhibited nitrifica-

NITRIFICATION RETARDERS

345

tion for 4-8 weeks: higher rates up to 448 and 896 kglha completely prevented nitrification (Munnecke and Ferguson, 1960). Harada (196 I ) and Nishihara ( 1 962) found vapam and dithare to be effective nitrification retarders and observed less leaching and denitrification losses of nitrogen from soil when these chemicals were used. Nabam and mylone, applied at field rates to fresh fertile soils of Oregon, completely suppressed nitrification for 30 days; but after another 30 days nitrification rate increased to half the normal rate (Chandra and Bollen, 1961). Maneb and anbam fungicides were found to retard nitrification (Nishihara and Tsuneyoshi, 1964). Other sulfur compounds were also tested and found to possess nitrification inhibitory property (Hirabayashi et af., 1967). Nitrification of ammonium sulfate and urea was retarded by sublimed sulfur, dithane wettable powder, dithane dust, monzet wettable powder, monzet powder, and lime sulfur. Several other fungicides, e.g., dyrene (Dubey, 1968), IMTD (Radwan, 1965), and chlorophenates (Mikkelsen, 1963, inhibited nitrification for different periods. Retardation brought an improvement in crop growth and yield (Nishihara, 1962; Mikkelson, 1965). D. FUMIGANTS Fumigants have a high nitrification inhibitory property, probably because they come in contact with a greater part of soil mass immediately after application. Methyl bromide alone (Winfree and Cox, 1958; Tillett, 1964) or mixed with chloropicrin and propargyl bromide (Good and Carter, 1965) caused nitrification retardation, but ethylene dibromide had little or no effect on nitrification. Fumigation with dichloropropenes (Good and Carter, 1965), D D (Koike, 1961; Elliot and Mountain, 1963; Mehta et af., 1963; Tillett, 1964; Gassar and Peachey, 1964), and Telone (Wolcott et al., 1960; Koike, 196 1 ; Elliot and Mountain, 1963) inhibited nitrification. Telone-EDB, however, reduced nitrification only temporarily (Tillett, 1964). Dowfume W-85 at 89 liters/ha inhibited nitrification for 4-8 weeks (Koike, 196 I). Other soil sterilants, Dazomet and metham sodium, were also quite effective in retarding nitrification in field and glass house (Gasser and Peachey, 1964). Ill.

Nitrification Retarders

I n recent years a large number of chemicals, including potassium chloride (Hahn et al., 1942), potassium azide (Hughes and Welch, 1968), dicyandiamide, thiourea, isothiocyanates (Kinoshita et af., 1966; Harada et al., 1964), mercapto compounds (Brown et al., 1956; Frederick et al., 1957; Millbank, 19591, pyridine, pyrimidine, anilines (Andreeva and Shcheglova, 1967) and triazine derivatives have been tested for their nitrification retarding properties. Physical and chemical properties of widely tested nitrification retarders are summarized in Table 11. All

w

P QI

E

m

TABLE I I Important Physical and Chemical Properties of Widely Tested Nitrification Retarders

Chemical (patent name) (Manufacturer)

Solubility in organic solvents (g/ I00 ml)

Melting point ("C)

Solubility in water (g/100 ml)

64.5

0.004 at 20°C

Acetone

Ethanol

I53 at 20°C

23 at 20°C

Solubility in anhydrous ammonia (g/ 100 ml)

Stability

F

L

2-Chloro-6-(trichloromethyl)pyridine (N-Serve) (The Dow Chemical Co., Midland, Michigan)

2-Amino-4-chloro-6-methylpyrimidine (AM) (Mitsui-Toatsu Industries Inc., Tokyo, Japan)

I 82

0.127at20"C

3.016at 25°C

1.157at 25°C

38 at 23°C

4.9 at 25°C

Half-life of degradation process at 20°C was 22 days in one soil but only 4 days in another. N-Serve is lost from the soil by volatilization and degradation to 6-chloropicolinic acid. (Dow Chemical Co., 1962: Shattuck and Alexander, 1963) The amount of AM recovered from treated soils was a logarithmic function of time.

> r rn

> z

0

m

Dic yandiamide

207.8

2.3 at 13°C

-

10.3 at 13°C

Thiourea 2-Sulfanilamidothiazole (ST) (Mitsui Toatsu Chemicals, Inc., Tokyo, Japan)

180.2 200.4

9.2 at 13°C 0.06 at 26°C

-

Soluble 0.436at 30°C

Adsorption by soil colloids was believed to be the predominant process by which AM is immobilized in soils (Toyo Koatsu Industries, Inc., 1965a) Dicyandiamide is decomposed in the soil, and after it is reduced to below toxic level nitrification goes on normally (Nommik. 1958)

-1

-

94 in 28%. aqua ammonia at 15°C

After 40 days of incubation of 20"C, 15.3% of applied ST was recovered (Mitsui Toatsu Chemical, Inc., Tokyo, 1968)

w

P 4

348

RAJENDRA PRASAD, G . B . RAJALE, A N D B . A. LA K H D IV E

these chemicals are white crystalline solid or amorphous materials. The melting point of N-Serve is lower compared to that of other chemicals. Since the vapor pressure of AM and ST is lower than that of N-Serve, the latter volatilizes faster. While dicyandiamide and thiourea are fairly soluble in water, the other three chemicals are almost insoluble. N-Serve is fairly soluble in organic solvents, and the fertilizer N can be easily blended with it by using a solution in organic solvents which can later be recovered. Since the solubility of AM and ST in organic solvents is low, these chemicals have to be mixed as such with the fertilizers. N-Serve and AM are fairly soluble in anhydrous ammonia and are stable in contact with liquid or aqua ammonia, hence their use with liquid fertilizers is also possible. AM tends to decompose and volatilize under acid conditions and should not be kept for long in association with acid fertilizer materials. Specific data on manufacturing costs for these inhibitors are not available. The retail price of N-Serve is $14.50 per gallon, used as directed, 1 gallon will treat 2.67-4.0 acres depending on application. Most of these materials are being manufactured on a small scale only, and the real economics of their use can not be judged by their present costs. The fact should not be overlooked that the cost of production of any material can be greatly reduced by increasing production, and this of course will depend upon the demand. A. 2-CHLORO-6-(TRICHLOROMETHYL)PYRlDlNE (N-SERVE) Under laboratory as well as field conditions, N-Serve inhibited nitrification of ammonium and amide fertilizers at rates varying from 0.2 to 2.0% of N (Goring, 1962a,b; McBeath, 1962; Turner et al., 1962; Gasser and Penny, 1964; Nielsen and Cunningham, 1964; Vlassak, 1964; Ansorge et al., 1967; Sabey, 1968). Data reported by Sabey (1968) are presented in Fig. 2. Retardation of nitrification by N-Serve is brought about mainly due to toxicity to ammonium-oxidizing autotrophs of genus Nitrosomonas (Goring, 1962a). N-Serve was also found to be toxic to autotrophs of Nitrobacter sp., but possessed a low-order toxicity to organisms or enzymes converting urea to ammonia, to organisms converting nitrite to nitrate, to the general fungus and bacterial populations, and to seedlings of many plants and heterotrophic nitrifying bacteria (Shattuck and Alexander, 1963). McKell and Whalley (1964) recorded that NServe, when applied at 1- 10 ppm of soil before sowing, had little effect on survival of rhizobium and nodulation of lucerne roots, but high rates (20 ppm) severely depressed seedling growth and resulted in morophological changes in nodules and deformation of root tips. The effect of N-Serve is reduced with the passage of time, showing thereby that the toxic effect of N-Serve is slowly and gradually reduced

NITRIFICATION RETARDERS

349

and ultimately the population of microorganisms is reestablished, but the return to normalcy may require some time. Goring ( 1962a) studied the effect of reinfestation by the nitrifying bacteria on the control of nitrification by N-Serve. Nitrification proceeded more rapidly in reinfested than in uninfested soil, Presumably the chemical destroys the majority of the nitrifying organisms and is then decomposed to nonlethal concentrations. The rate of recovery of nitrification thus depended on the recovery of the surviving nitrifying organisms and was, therefore, enhanced by repeated reinfestation. With N-Serve, only partial control of nitrification is obtained (Goring, 1962b; Lakhdive, 1968). This is expected in view of the fact that the entire soil mass is not treated with the chemical. N-Serve is coated on or mixed with the N fertilizers, but does not necessarily get distributed in lethal concentrations throughout the entire soil zone to which fertilizer N moves. Furthermore N-Serve and the ammonium nitrate are subject to differential volatilization or leaching losses. Due to the volatilizing nature of N-Serve, it gives better control of nitrification when placed in the soil. Gasser and Penny ( 1964) compared broadcast and placement of N-Servetreated fertilizer. When fertilizer was broadcast on the soil surface, nitrification was retarded more by the double rate of N-Serve (2% of weight of N applied) than by the half rate. When fertilizer was placed in the soil both rates of N-Serve retarded nitrification equally.

Date of sampling

FIG.2. Effect of N-Serve and 2-amino-4-chloro-6-methylpyrimidine (AM) on nitrificaAmmonium sulfate; ----,ammonium sulfate tion rate in ammonium sulfate-treated soils. and N-Serve ( I ppm, soil basis): - . - ., ammonium sulfate and AM (3 ppm, soil basis). (Data from Sabey, 1968.) (Nitrification rate defined as nitrates expressed as percentage of total inorganic N.)

-.

350

RAJENDRA PRASAD, G. B . RAJALE, A N D B. A. LAKHDlVE

Nitrification is an aerobic process, and it is generally presumed that flooding a soil, and the consequent production of anaerobic conditions, inhibit nitrification. Hence, one would not expect any beneficial effect of N-Serve under flooded conditions. Contrary to this expectation, workers at IRRI (International Rice Research Institute, 1967) showed that soil samples receiving N-Serve contained up to 40 ppm more extractable ammonium than the soil samples treated with ammonium sulfate alone (Fig. 3). Similarly, at the end of 40 days of incubation under water-logged

FIG.3. Extractable ammonium in soil fertilized with N-Serve-treated, AM-treated, and untreated urea under flood conditions. (International Rice Research Institute, 1967.)

conditions Rajale and Prasad (1970b) obtained up to 12 ppm more ammonical N with samples treated with N-Serve than with untreated samples. These results indicate that even under flood conditions some nitrification of fertilizer N occurred and the nitrates formed were lost. The presence of N-Serve prevented this nitrate formation. Patrick and Mahapatra (1968) also observed that some nitrification may occur even under completely waterlogged conditions, due to the presence of facultative anaerobes which utilize the diffused oxygen and iron and manganese compounds as electron acceptors. By keeping the fertilizer N in ammonium form, N-Serve is reported to decrease the denitrification (Mitsui et af., 1964) and leaching (Hoflich,

NITRIFICATION RETARDERS

35 1

1968; Janert et al., 1968) losses of N. In a laboratory experiment, when the soil after receiving 100 ppm N was subjected to waterlogged conditions for 10 days after incubation at field capacity for 10 days, ammonium sulfate recorded a loss of 47 ppm N ; this was reduced to only 10-1 1 ppm in the presence of N-Serve (Prasad and Lakhdive, 1969). In percolation studies, the amount of inorganic N in the percolate was greatly decreased by the treatment of urea with N-Serve (Nishihara and Tsuneyoshi, 1968). Using I5N, Carter et al. (1967) showed that the greatest advantage of adding N-Serve to retard nitrification was to hold the N in the root zone for longer periods of time. The beneficial effect of N-Serve, under field/pot culture conditions has been reported by several workers for many crops. Most interesting results have been reported with upland rice, subjected to alternate wetting and drying. In India, increased yield of irrigated upland rice (Prasad et al., 1966, 1970b; Lakhdive and Prasad, 1970; Rajale, I970), and higher recovery of applied N (Prasad, 1968) and reduction in N losses (Lakhdive, 1968) were achieved by the use of N-Serve. Treatment of urea with NServe gave an increase in grain yield of rice of 680, 660, and 270 kg/ha in case of rice varieties Taichung Native-1, IR-8, and N.P.130, respectively (Prasad and Bains, 1968). These upland rice fields were subjected to alternate wetting and drying. In Japan normally two or three split applications of N are recommended for rice. Rice culture systems are mainly two. One is the common rice culture involving transplanting of the young rice seedling on water-logged fields and the other a newer culture, where seeds are first sown under upland conditions and then flooded about one and half months later. In the latter case, almost all N applied in the form of ammonium or urea as basal dressing nitrifies before flooding and nitrates thus formed are subjected to leaching and denitrification. Field experiments conducted at different centers in Japan (International Rice Commission, 1966) showed that ammonium sulfate treated with N-Serve increased the yield of rice by 15-20% over untreated ammonium sulfate. Nishihara and Tsuneyoshi ( 1 964, 1968) also reported that yield of rice and uptake of N was higher in N-Serve-treated urea plots as compared to that in untreated urea plots. In Louisiana, Patrick et al. (1968) observed that although under laboratory conditions N-Serve was very effective in preventing conversion of ammonium to nitrate N, no significant increase in yield of rice was obtained under field conditions by its use. It is, however, interesting to note that N-Serve treatment gave an increase of the order of 280 and 440 kglha of brown rice over check at 40 and 160 kg N/ha. Results of Patrick et al. ( I968), Rajale ( 1 970), and International Rice Commission (1966) are presented in Fig. 4. Besides rice, increased yields of irrigated sugar beet, sweet corn, cot-

NITRIFICATION RETARDERS

353

leaching. Devine and Holmes ( 1 964) found that N was much less effective when applied in autumn than in spring on light soils and when the winter was wet. O n medium-heavy or heavy clay loam soils, N applied in autumn increased the yield of winter wheat less than equal N applied in either March or May (Widdowson et al., 1961). This indicates the loss of N mainly from leaching of nitrates in the fertilizer o r that formed on nitrification of ammonium salts, but some nitrates may also be lost by denitrification. Under these conditions nitrification retarders help to reduce these N losses. At Rothamsted, Gasser ( 1965) observed that N-Serve at 2% of the applied N prevented nitrification of ammonium sulfate applied during autumn, and ryegrass sown next spring yielded more with treated than with untreated ammonium sulfate. In case of wheat, when fertilizer was applied in the autumn, N-Serve-treated ammonium sulfate gave higher grain yield than untreated ammonium sulfate, although all yields with autumn applied fertilizers were less than those obtained with the corresponding spring-applied dressings (Gasser and Penny, 1965). The beneficial effects of nitrification retarder are likely to be greater on light soil because of rapid leaching of nitrates. On a sandy loam soil of Woburn (U.K.), N-Serve-treated ammonium sulfate given in autumn increased yield of winter wheat by 3.5 cwt with 75 Ib N and by 5.4 cwt/acre with 150 lb N/acre, whereas on a clay-loam soil of Rothamsted, N-Serve had no effect (Gasser and Hamlyn, 1968) (Fig. 5). Ammonium and nitrate fertilizers have often been compared for various crops (Cooke, 1964), but few experiments have used a nitrification retarder to prevent oxidation of the ammonium to nitrate. Gasser et al. ( I 967) found that N-Serve decreased the yield of ryegrass at the first cutting on grassland soils receiving ammonium sulfate, but increased it on soil receiving calcium nitrate, suggesting that changing the proportions of nitrate to ammonium by adding N-Serve altered the growth rate and yield of ryegrass. Subsequent investigations at Rothamsted (Spratt and Gasser, 1970) showed that initially wheat and ryegrass grew better and took up more N with ammonium sulfate treated with N-Serve (2% of the N applied) than with calcium nitrate. However, final yields of dry matter did not differ between forms. Kale differed from wheat and ryegrass; early growth was similar with the two forms, and later growth and N uptake were better with calcium nitrate than with ammonium sulfate treated with N-Serve. This preference of kale for nitrate N may be associated with its large cation uptake (Cunningham, 1964). N-Serve is also reported to prevent large accumulations of nitrate in plants. Therefore treating ammonium fertilizers with N-Serve may allow fertilizer to be applied at higher rates. Nowakowski and Cunningham (1966) and Nowakowski (1968) reported that N-Serve, by inhibiting

354

RAJENDRA PRASAD, G . 0. RAJALE, AND 0. A. LAKHDlVE

nitrification of ammonium nitrogen, influenced the chemical composition of Italian ryegrass by keeping low the amount of nitrate in the plant. In wheat, on a clay loam soil increase in the nitrate content of plants was 8000

Ammonium sulfate Ammonium sulfate t N- serve I %

7000

Ammonium sulfate+N-serve 2 %

e

$b g

6ooo 5000

c

0

2

'E

4000

y

3000

F B .-

0

84.08kg N/ho

168.15kg N/ho

Woburn expt station

56,05kgN/h

112.10kgN/ho

Rothamsted expi stotion

FIG.5. Wheat grain yield on sandy loam (Woburn) vs. clay-loam (Rothamsted) soils fertilized with autumn-applied vs. spring-applied N-Serve-treated or untreated ammonium sulfate. (Data from Gasser and Hamlyn, 1968.)

significantly less with N-Serve-treated than with untreated ammonium sulfate. On a sandy loam soil, wheat given ammonium sulfate with and without N-Serve contained similar amounts of nitrate N (Nowakowski and Gasser, 1967). The differential behavior of N-Serve in these two different soils may be due to rapid loss of N-Serve from sandy loam soil than from the clay-loam soil, which contains more organic matter and more clay. The findings of Redemann et al. ( 1964) support this contention, as these workers recorded that the rate of loss of N-Serve varied from soil to soil and was slowest in soils rich in organic matter. The nitrate content of spinach was reduced when ammonium sulfate treated with N-Serve was applied (Bengtsson, 1968). Phosphate uptake by wheat (Nielson et al., 1967) and bromide uptake by sorghum (Chao, 1966) were found to increase by the application of N-Serve-treated ammonical fertilizers.

NITRIFICATION RETARDERS

355

B. 2-AMINO-4-CHLORO-6-METHYLPYRIMIDINE(AM) Like N-Serve, this chemical is toxic to ammonium-oxidizing autotrophs of the genus Nitrosomonas which are responsible for the oxidation of ammonium to nitrate. AM applied at 5-6 kg/ha and mixed with fertilizers, effectively retarded the nitrification of urea and leaching of N (Mitsui Toatsu Chemicals, Inc., 1969). Prasad and Lakhdive (1969) found AM to be quite effective in retarding nitrification of ammonium sulfate and checking subsequent N loss due to waterlogging. Rajale and Prasad ( 1970b) studied the nitrification of urea as affected by AM and observed that nitrification of untreated urea was almost complete in 20 days. When urea was treated with AM at 5 ppm, only 74% of ammonium was nitrified within 20 days. At higher concentrations, AM was still more effective. Even at the end of 40 days of incubation, the nitrification rate (nitrates expressed as percentage of total inorganic N) of urea treated with AM at 10 ppm of soil was 76% as against 100% in the case of urea. Sabey ( 1968) in U.S.A with field incubation of soil in plastic bags found that AM suppressed the nitrification of ammonium sulfate for about 1 month. In view of these findings, the results of Patrick et al. ( 1968), who reported that AM failed to materially inhibit nitrification, are difficult to reconcile. From the published details, it is not possible to explain such results. Under water-logged conditions also, AM had a distinct effect on conservation of ammonium. At the International Kice Research Institute (1967), soil samples receiving AM-treated (4ppm in soil) ammonium sulfate contained more ammonical N than untreated samples. When urea was treated with AM, the ammonium N content of the treated samples was higher by about 7-10 ppm than the untreated samples (Fig. 3). The losses of N due to alternate submergence and field capacity moisture were considerably reduced by treating urea with AM (Rajale, 1970). The loss of applied N with AM-treated urea was 63% as against 95% with untreated urea. Field tests carried out in Japan (Toyo-Koatsu Industries, Inc., 1965b; Nishihara and Tsuneyoshi, 1968) showed that yields of transplanted as well as direct-seeded rice were increased by the use of 5-6 kg of AM per hectare along with the ammonical fertilizers. In field experiments at New Delhi in India, treatment of ammonium sulfate (Lakhdive, 1968) and urea (Rajale, 1970) with AM increased the yield of irrigated upland rice. Similarly, in a demonstration trial the yield of irrigated upland rice was higher with than without AM-treated urea (Prasad and Bains, 1968). In another experiment the increase in grain yield of upland rice was more pronounced under alternate wetting and drying than under continuous

356

RAJENDRA PRASAD, G. B. RAJALE, AND B. A. LAKHDIVE

submergence (Rajale, 1970) This is expected in view of the fact that under alternate wetting and drying conditions the losses of N from soil are higher and AM prevented these to some extent. The increase in yield of rice due to nitrification retarder also led to a higher uptake and recovery of applied N. In a pot culture experiment, Prasad ( 1968) found that AM-treated ammonium sulfate gave 27% higher recovery of N by rice over untreated ammonium sulfate. In Trinidad, urea treated with AM resulted in about 25% higher yield of Pangolagrass over untreated urea, while the efficiency of utilization of N was increased by 60% (Weir and Davidson, 1968). Contrary to above findings, Patrick et a f .( 1968) observed no increase in rice yield in the field due to AM treatment of fertilizer N. As in the case of N-Serve, the data of Toyo Koatsu Industries, Inc. (1965b) show that the use of AM-treated fertilizers prevented high accumulation of nitrate N in ryegrass. Only few workers (Sabey, 1968; Prasad and Lakhdive, 1969; Rajale and Prasad, I970b) compared N-Serve and AM and found that both were equally effective in retarding the nitrification of ammonical fertilizers. Similarly, in field tests also (Prasad et al., 1970a; Rajale, 1970) the increase in grain yield of upland rice from N-Serve and AM was more or less same. However, Patrick et al. ( 1968) showed that while N-Serve was very effective, AM did not materially inhibit nitrification. D. DICYANDIAMIDE (CYANOGUANIDINE) The inhibitory effect of dicyandiamide on nitrification was known even in the first decade of this century. Several early workers (Brioux, 1910; Ulpiani, 1908; Jacob et al., 1924) observed that dicyandiamide may inhibit nitrification of ammonium fertilizers in the soil. Nommik (1958) reported that at high concentration of calcium cyanamide a considerable part of cyanamide was converted to a nitrogen compound which decomposed in the soil only very slowly and in whose presence nitrification was retarded. Judging from its biological effects, it seemed most likely to be dicyandiamide. Dicyandiamide applied at the rate of 5.5-24% of N increasingly retarded nitrification. In winter the nitrification was stopped for 5 months and reduced the leaching losses of N by 67% (Soubies et al., 1962). Reddy ( I964a) found that dicyandiamide retarded nitrification of ammonium sulfate at all rates (5-25 ppm) applied to Georgia soils and complete nitrification occurred only after a long time. Inhibitory effect of this compound on different fertilizers was in the following order: ureaformaldehyde, urea, ammonium chloride, ammonium sulfate, ammonium nitrate, ammonium sulfate plus organic matter (Reddy and Datta, 1965).

NITRIFICATION RETARDERS

357

Further, it was noted that the inhibitory effect of dicyandiamide on nitrification was partially counteracted by the addition of organic matter. In the presence of organic matter, decomposition of dicyandiamide was rapid. High exchange capacity and absorbing power or organic matter may be responsible for this rapid rate of dicyandiamide decomposition. Addition of dicyandiamide to the N fertilizer applied to winter wheat increased the productivity of the applied N (Soubies et af., 1962). Use of this compound is suggested on N fertilizers at the rate of 5- 12% (Anonymous, 1964). In Japan, Nishihara and Tsuneyoshi (1964, 1968) recorded increased yields of rice and greater absorption of N when urea was treated with dicyandiamide as compared to untreated urea. Ammonium sulfate treated with dicyandiamide increased the yield of rice by 19% over untreated ammonium sulfate (International Rice Commission, 1966). At higher concentrations dicyandiamide is toxic to the plant. The toxic effects of dicyandiamide differed with plant species. Coastal bermudagrass tolerated high rates of dicyandiamide; oats, wheat, maize, and cotton were moderately injured and tomatoes were severely injured by the higher rate of dicyandiamide ( I 6.7 ppm N). However, when mixed with N fertilizers at lower rates (not exceeding 16.8 kg/ha) it may benefit plant growth (Reddy, I964b).

D. THIOUREA Thiourea retarded nitrification by lengthening the lag period prior to exponential growth of Nitrosomonas although it did not kill the organisms (McBeath, 1962). Even at low concentration (0.3 mM) ally1 thiourea was found to inhibit nitrification (Quastel and Scholefield, 195 1). However, at Rothamsted thiourea was found to retard nitrification when mixed with soil in large amounts (Hamlyn and Gasser, 1968). Ally1 thiourea is reported to be a specific inhibitor for a microbiological system oxidizing ammonia to hydroxylamine (Lees, 1963). Lees ( 1946, 1963) recorded that the treatment of soil enriched with nitrifying organisms, with copper chelators such as potassium ethylxanthate, sodium diethyldithiocarbamate, and salicylaldoxime at 4 mM concentrations brought about retardation of nitrification, suggesting thereby that the inhibitory effect of thiourea and allylthiourea on nitrification was possibly caused by their combination with metallic ions, such as copper, that may be required for nitrification. Thiourea applied at the rate of 56 kg N/ha to Laveen clay loam and Superstition sand gave a higher yield of barley as compared to ammonium sulfate and showed a marked residual effect (Fuller, 1963). Experiments conducted at 8 different centers in Japan showed that thiourea-treated ammonium sulfate gave 18% higher yield of rice over untreated am-

358

RAJENDRA PRASAD, G . B. RAJALE, A N D B. A. LAKHDIVE

monium sulfate (International Rice Commission, 1966). In another series of experiments at 6 locations in Japan the increase in grain yield of rice by thiourea was about I 1 % (Hamarnoto, 1966).

E. 2-SULFANILAMIDOTHIAZOLE (ST) Recently, Mitsui Toatsu Chemicals, Inc., Japan (1 968) introduced ST (2-sulfanilamidothiozole) as a nitrification retarder. This chemical when applied at 1-10 ppm on soil basis retarded nitrification of urea. Increased yield of direct seeded and transplanted rice, barley, and spinach were obtained by using ST. IV.

Slow-Release Nitrogen Fertilizers

The goal in developing slow release nitrogen fertilizers is having nitrogen release rated to the requirements of growing plants and thereby reducing the wasteful losses of N. Two general ways to achieve this are (1) synthesis of chemical compounds with inherently slow rates of dissolution and (2) the application of coatings or moisture barriers to the surface of water-soluble fertilizer particles. The chemical and physical properties of some of the important fertilizer materials with low rates of dissolution are presented in Table 111. For most of these materials, the amount of surface area exposed determines the rate of dissolution. The particle size thus determines the rate of release with the larger particles releasing their nitrogen most slowly. This property is well exhibited by oxamide, isobutylidenediurea, crotonylidenediurea, glycoluril, and metal ammonium phosphates. The slow release of urea form and the triazines, on the other hand, depends upon their resistance to microbial decomposition. The concept of controlled release of plant nutrients has been discussed by Army (1963), Army and Ware (1964), Hauck (l964), Nelson and Hauck (1969, National Institute of Agricultural Sciences, Japan (1966), and Parr (1967). Prasad (1966) reviewed the early work done in slow-release nitrogen fertilizers. The growing interest in these fertilizers is evident by the publication of two books (Powell, 1968; Araten, 1968) entirely devoted to this subject. A brief discussion on some important slow-release N fertilizers follows.

UREA-FORM This is produced commercially by reacting urea with formaldehyde. A whole series of compounds, ranging from relatively soluble to completely insoluble, are possible, depending on the ratio of urea to formaldehyde in the final product. Since the methyleneureas constitute the insoluble portion of the urea-form, the agronomic value of the product relates directly to the amount and type of methyleneureas in the product and the A.

359

NITRIFICATION RETARDERS

amount of untreated urea. Association of American Fertilizer Control Officials has defined urea-form fertilizers as follows: “Urea-formaldehyde fertilizer materials are reaction products of urea and formaldehyde conTABLE 111 Important Physical and Chemical Properties of Some Slow-Release N Fertilizers

Chemical

Formula

Urea-form Oxamide lsobutylidenediurea (IBDU) Urea-acetaldehyde (urea-Z) Crotonylidene diurea (CD-urea or Floramid) Difurfurylidene triureid Glycoluril CzH,(CONZHZ), Triazines Ammeline (CN)s(NHz)ZOH Cyanuric acid (HNCO)s.2Hn0 Melamine Metal ammonium phosphate Cobalt N Hr phosphate Copper NH4 phosphate Ferrous NH, phosphate Magnesium NH, phosphate Manganese NHI phosphate Zinc NH, phosphate N-enriched coal

Percent N

Solubility in water (g/ I00 ml) Traces 0.02 0.0 1-0. I

31.38

ca. 0.4

32.5

0.12

24.99

Hardly soluble

39.4

0.1 at 17°C

49.4 -32.1

0.008 at 23°C 0.27 at 17“C,melting point > 360°C -Melting point > 250°C

CONH,POq.H,O

6.9

CUNHqPO.t’H,O

1.0

F e NH,PO.,.H,O

7.0

0.095

Mg NH,POd.H,O

8.3

0.14

Mn N H 4 P 0 4 . H Z 0

7.2 7.5 9.19

taining at least 35 per cent nitrogen, largely in insoluble but slowly available form. The water insoluble nitrogen in these products shall test not less than 40 per cent active nitrogen activity index for the urea-formaldehyde compounds as determined by the appropriate AOAC method.” The activity index for urea-formaldehyde compounds is defined as

360

RAJENDRA PRASAD, G. B. RAJALE, A N D B. A. L A K H D I V E

A1 =

% CWIN- % HWIN % CWIN

where A1 is the activity index, CWIN is the percentage of nitrogen insoluble in cold water (25"C), and HWIN is the percentage of nitrogen insoluble in hot water (98-100°C). The quantity of cold water-insoluble nitrogen is the source of the slowly available nitrogen. The rate at which the cold water-insoluble nitrogen becomes available depends upon its quality as determined by its activity index. Thus the quantity and quality of cold water-insoluble nitrogen determines the suitability of urea-form products as fertilizers. Urea-form is being currently produced by E. I. du Pont de Nemours and Co. Inc. at Belle, West Virginia, under the tradename Uramite and by Hercules Powder Co. at Louisiana, Missouri, and Hercules, California, under the tradename Nitro-form. A new development is the ureaformaldehyde solutions, and Hawkeye Chemical Co. has plans to produce these at 120 short tons per day. Their product will be called Nuform 30 and will contain 29-30% N (based on a U : F mole ratio of 1.6: 1). Allied Chemical Corp. also makes urea-formaldehyde solutions. Rate of mineralization of urea-form is generally governed by the urea: formaldehyde ratio and increases with increasing U :F. Urea-form U :F less than 1.0, shows strong resistance to decomposition when applied to the soil; accordingly, it is of little value as an N fertilizer. Urea-form with U :F 1.5 and 3 showed reasonable mineralization (Ishizuka and Takagishi, 1959) Among the various formaldehyde derivatives of urea, the methylol urea types mineralized slowly and continuously over a long time as compared to methylene-type derivatives. Dimethylonurea did not nitrify for 2 months or more when added at 10 mg N per 25 g soil (Takagishi and Ushioda, 1961). Mineralization of urea-form in soil also depends upon the size of the molecule and decreases with an increase in molecular size. Long and Winsor ( 1960) observed that methylenediurea and dimethylenetetraurea decomposed too rapidly, whereas tetramethylenepentaurea in a mixture with other higher members of series was highly resistant. As a contrast to the molecular size, granule size did not affect mineralization of urea-form (Hays et al., 1965). The soil temperature and pH also affect mineralization of urea-form. The rate of nitrate production from urea-form was generally 2-5% higher in soils with a initial pH of 5.7 as compared to those having a pH value of 7.0. Urea-form appears to be of limited value to plants if applied to soils with temperatures less than 15°C during growing season (Basaraba, 1964).

NITRIFICATION RETARDERS

36 1

Urea-form is used mainly on turfs and lawns, where the growing season is long and the rate of nitrogen consumption is fairly steady. It has no residual salt effect and does not scorch foliage (Winsor and Long, 1958). With field crops, particularly upland crops the performance of urea-form has generally been no good (Iswaran et al., 1961). With maize and cotton ammonium nitrate produced a higher yield than a fertilizer containing variable proportions of nitrogen as urea-form (Scarbrook, 1958). On a silt loam soil, increases of yield from applied nitrogen containing up to 53% N as urea-form were not significantly different from increases from the use of other N fertilizers. On the other hand, yields were significantly reduced when N fertilizer containing 88% or more of urea-form was used (Killian, 1964). Widdowson et al. (1962) observed that the yields of Italian ryegrass from urea-form were similar to those from nitrochalk at the first cutting, but nitrochalk produced much larger yields in later cuttings. Recovery of N over a three-year period was 54% with ureaform and 90% for nitrochalk. With low land rice the performance of urea-form has been variable. S. N. Datta et al. (1962) and S. N. Datta and Iswaran (1964) reported 'that urea-form products were not inferior to uncombined urea in their effect on yield of rice. Increased yield of rice with urea-form as compared to urea and ammonium sulfate was recorded by Akhundov ( 1965). Hayase ( 1967) also opined that urea-formaldehyde condensates were superior sources of N for rice. On the contrary, in pot experiments in Japan urea-form gave a lower yield of rice as compared to urea, while in field experiments it gave the same yield as ammonium sulfate (Hamamoto, 1966). The reason for its poor effectiveness could be that it was only slightly or too slowly decomposed by anaerobic soil microbes in rice fields. Gopalswamy et al. (1969) also obtained a lower yield of rice with urea-formaldehyde as compared to ammonium sulfate and urea. This could be due to use of a short duration variety Adt. 27.

B. OXAMIDE Oxamide is a diamide of oxalic acid and contains 3 1.8% N. This chemical has been extensively studied by the Tennessee Valley Authority (TVA), Monsanto, and others as a possible slow-release material. TVA research on the manufacture of this chemical has concentrated on the production of cyanogen from hydrogen cyanide by two alternative routes, namely, using nitrogen dioxide or copper oxide. The cyanogen is then hydrolyzed in concentrated hydrochloric acid to produce oxamide. Oxamide is nonhygroscopic, nontoxic, and nonexplosive and undergoes dissolution in soil at a rate which varies according to granule size-the smaller the granules, the more rapid is the rate of dissolution (DeMent et al., 1961). In an uncropped soil, conversion of N in oxamide to am-

362

RAJENDRA PRASAD, G. B. RAJALE, A N D B. A. LAKHDIVE

monium and nitrate was essentially complete in 1 week with 60-mesh oxamide, but much slower with - 4 6-mesh oxamide. By controlling the rate of dissolution, the granule size of oxamide also affects the yield and N uptake by the plant. All Rothamsted ryegrass grass with ammonium nitrate and powdered oxamide produced higher yields at the first cutting, while the two granulations (2-4 mm and 7-9 mm) of oxamide produced higher yields at the second and third cuttings. At the first cutting, grass removed highest fertilizer N from ammonium nitrate and least from large granules (7-9 mm) of oxamide. On the other hand, at the third cutting grass recovered most N from the granulated oxamides. However, the total recovery of applied N for the three cuts was highest for ammonium nitrate, and least for large granules of oxamide (Gasser and Penny, 1965). In another pot experiment with three soils powdered oxamide and small granules (2-4 mm) behaved like ammonium nitrate and had no further effect on the growth of ryegrass after 120 days of sowing. The intermediate-sized granules (4-6 mm) produced as much dry water initially as the rapidly acting forms and continued to increase yields until 260 days after sowing; they also gave highest total yields between 100 and 260 days. The largest granules (9-1 1 mm) increased yields less in the initial stages, but the grass produced dry matter at an almost constant rate from 50 days after sowing to 300 days (Gasser and Jephcott, 1966). Thus response to oxamide tended to be delayed with an increase in granule size. In the United States DeMent et al. (1961) observed that N uptake by one crop of corn forage in greenhouse pots from - 4 6- and - 28 35-mesh oxamide were approximately 22 and 89%, respectively, of the uptake from ammonium nitrate or 60-mesh oxamide. Nitrogen recoveries by three successive corn crops from 800 mg N applied as oxamide ranged from 44 to 64% on unlimed (pH 5.2) Hartsells fine sandy loam and from 60 to 82% on this soil limed to pH 7.5. These recoveries were similar to those from ammonium nitrate and considerably higher than those from an equal application of N as ureaformaldehyde. Similar results were reported by Engelstad et al. (1964). Nitrogen availability from fine oxamide as compared with nitrolime (calcium ammonium nitrate) was studied in the Netherlands in pot experiments using perennial ryegrass, flax, and spinach as test plants. Rate of release as well as recovery of N were equal for the two fertilizers (Dilz and Steggerda, 1962). Beaton et al. (1 967) also obtained lower recovery of N by orchardgrass from oxamide (65%) as compared to ammonium nitrate. Increased yield by using oxamide as compared to urea and ammonium sulfate were obtained for barley and vegetables in Japan (Ogata and Kensuke, 1959b). In a field experiment in the United States using I5N, Westerman and Kurtz (1 968) compared urea and oxamide as sources

+

+

+

NITRIFICATION RETARDERS

363

of N for Sudangrass. The total yield of dry matter was higher for oxamide than for urea. There was no significant difference between the two sources with respect to dry matter yield in first and fourth cutting, however, the yields of dry matter for oxamide in second and third cuttings were significantly greater than those of urea. Lowland conditions again differ from the upland conditions with respect to suitability of oxamide. Ogata and Kensuke ( I 958) from Japan reported that oxamide leached out less than urea and could supply little N to the plant at earlier stages of growth but could supply it in fair amount in later stages. A timely supply of N to the plant and less nitrite accumulation helped the oxamide to raise the yield of rice by 24-45% over urea. At higher levels oxamide gave a higher yield of rice than did urea. Powdered oxamide acted as fast as urea or ammonium sulfate and gave a slightly lower yield of rice (Ogata and Kensuke, 1959a,c). Applied in high doses, oxamide did not retard germination or the growth of plants (Ogata and Yoshinouchi, 1958). The high production costs of oxamide have inhibited its further development. The TVA suggests that, based on rough estimates, the manufacturing cost for a 100 short tons per day plant would be about twice that for ammonium nitrate. Therefore, the real solution for future development of oxamide seems to reduce the cost of production which for the present seems quite difficult.

C. ISOBUTYLIDENEDIUREA (IBDU) IBDU is a condensation product of the reaction between urea and isobutyraldehyde in a 2 : 1 mole ratio. Mitsubishi Chemical Industries, Ltd., Tokyo, report that they have built a plant at Kurosaki to produce 40-44 thousand metric short tons per year of mixed fertilizers containing IBDU. Besides straight IBDU fertilizer, Mitsubishi manufactures five mixed fertilizers containing IBDU, where part of the N is supplied by IBDU and the rest as ammonium sulfate, urea, or diammonium phosphate. The grades of the mixed fertilizers are 15- 15- 15, 16- 10- 14, 18- 1 111, 20-12-12, and 10-10-10. Straight IBDU and the first 4 grades are sold for vegetable and fruit crops; the 10-10-10 grade is intended for rice. Eighty percent of the N in this grade is supplied by IBDU, and the remaining 20% by urea. IBDU is sparingly soluble in water, has less concentration hazard, less hygroscopicity, and a lower caking tendency. It can be mixed with any other fertilizer excepting strongly acidic superphosphate (Mitsubishi Chemical Industries, Ltd., Tokyo, 1964, 1966). The rate-limiting step in the conversion of IBDU to plant-available form appeared to be the dissolution of IBDU, which is strongly influenced by size and hardness

364

RAJENDRA PRASAD, G. B. RAJALE, AND B . A. LAKHDIVE

of the granules (Hamamoto, 1966). The rate of dissolution increased with a decrease in granule size, lowering of pH, increase in temperature and soil moisture. Microbial activity did not affect its rate of dissolution. Plants made effective use of IBDU in pH ranges from below 5 to above 8. However, conversion of IBDU to urea and ammonium or nitrate N did not occur as readily under alkaline conditions as in acid soils. The slow mineralization of IBDU due to high pH did not appear to present a serious problem in using IBDU in soils up to at least pH 8.3 (Lunt and Clark, 1969). Rajale and Prasad (1970a) reported that under waterlogged conditions the mineralization rate of I BDU (0.7-2 mm) was higher than that at field capacity moisture. Two important characteristics from fertilizer management viewpoint are (i) high safe application rates and (ii) time required for complete mineralization. As regards the first characteristic, Lunt and Clark (1969) found that IBDU applied upto 32 lb N/lOO ft2 (1562 kg N/ha) mixed into soil had negligible detrimental effects on Alta fescuegrass. This rate is 5- 10 times higher than safe limits with conventional fertilizers. In regard to time required for complete mineralization, Gasser et al. (1968) at Rothamsted observed that ammonium nitrate, IBDU powder as well as small granules (0.5-0.8 mm) were equally effective in increasing yields of S.22 ryegrass. The medium size granules (0.8-1.5 mm) were inferior to these forms when applied at 112 kg N/ha but were equally effective when applied at 336 kg N/ha. Benzian (1967) obtained good results with IBDU applied to Sitka spruce nursery seedlings. The largesized granules always produced the lowest yield. Experiments with Sitka spruce at Kennington indicated that the difference between IBDU and nitrochalk in respect to dry matter yield and N concentration were very small and inconsistent. However, at Wareham nitrochalk was better than IBDU (Benzian and Freeman, 1968). Nitrogen release from IBDU was inadequate in the initial stages of Kentucky bluegrass (Moberg and Waddington, 1968). For this reason Isobe and Abu-Zeid (1968) suggested that a mixture of the IBDU and urea may be desirable than either of them alone. A fertilizer product 18-6-12, prepared with two-thirds of N from IBDU produced a better rated turf at effective rates of application (McAlpine, 1968). Considerable work on IBDU as a source of N for rice has been done in Japan (Hamamoto, 1966; International Rice Commission, 1966). In pot experiments, it was observed that IBDU gave 12% higher weight of panicles as compared to urea. When IB 9-9-9 (5-8 mm) was used, similar results were obtained. In field experiments, I B 9-9-9 applied as basal fertilizer at the beginning gave a higher yield as compared to the usual two or three applications of urea. Field experiments conducted

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by the Ministry of Agriculture and National Institute of Agricultural Sciences of Japan showed that IBDU increased the yield of rice by 20% over ammonium sulfate when given in two doses (Hamamoto, 1966). IBDU gave 25% higher yield of rice over ammonium sulfate applied as basal dressing. When IBDU was treated with thiourea, dicyandiamide, and N-Serve, the yield increases were 30, 30, and 32%, respectively, over ammonium sulfate (International Rice Commission, 1966). In India, Rajale ( 1970) recorded a significantly higher yield and recovery from IBDU as compared to that from urea. Experiments conducted on upland crops in Japan also showed that IBDU gave increased yield as compared to ammonium sulfate or urea applied in 2 or 3 split doses. With Italian ryegrass a single application of IBDU was 24-53% more effective than 4 split applications of urea on an equivalent N basis (Mitsubishi Chemical Industries, Ltd., Tokyo, 1964). Increased yields of tomato, lettuce, carrot, sweet corn, Italian ryegrass, orchardgrass, and turf were obtained by using IBDU as compared to ammonium sulfate or urea (Mitsubishi Chemical Industries, Ltd., Tokyo, 1966).

D. GUANYLUREA Guanylurea is produced from calcium cyanamide by acid treatment. Pure guanylurea can be produced by hydrolyzing dicyandiamide in acid medium, but at present dicyandiamide is produced from calcium cyanamide. Although there are several salts of guanylurea, the most important forms as fertilizer seem to be sulfate or phosphate because of their simplicity in production, high nutrient content, and smaller hygroscopicity. Though most of the slow-release N fertilizers are only slightly soluble in water, guanylurea is different from others and is fairly soluble in water. Although it has relatively large water solubility, it is adsorbed by the soil colloids and the leaching loss is very small. The results of a study (International Rice Commission, 1966) showed that the whole molecule of guanylurea phosphate could be adsorbed on soil colloids. Guanylurea is adsorbed by soil colloids in two different forms: (i) an exchangeable form which could be exchanged with potassium, and (ii) a more firmly held form which could not be extracted with 10% potassium chloride solution. The amount of exchangeable guanylurea and clay content in soil, and nonexchangeable guanylurea and phosphate-fixing capacity of the soil were well correlated (International Rice Commission, 1966). An important characteristic of this compound is that it is decomposed more easily by anaerobic microorganisms in the flooded soils than by aerobic microbes in upland soils. When guanylurea was applied to upland soils, mineralization did not proceed even after 50 days of incubation at

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30°C, whereas in flooded soils the mineralization was rapid. In flooded soils about 80% of the N applied as guanylurea was mineralized within 20-30 days of incubation. Mineralization of guanylurea in soil is markedly affected by the redox potential or the amount of ferrous iron, readily decomposable organic matter and guanylurea adsorbing capacity of the soil (International Rice Commission, 1966). Because of this property, guanylurea is considered to be a good fertilizer for flooded rice (Hayase, 1967). From its mineralization pattern, guanylurea can be considered to be rather a “late” available N fertilizer, as a basal dressing or starter with guanylurea can give steady release of N over a considerable period of plant growth. Experience in using guanylurea in Japan (Hamamota, 1966; International Rice Commission, 1966) has shown that it is capable of increasing the yield of flooded rice. However, under upland conditions guanylurea does not seem to have any advantage over conventional fertilizers. On the other hand, guanylurea nitrate and guanylurea phosphate were found to be toxic to corn (Terman et al., 1968). Thus guanylurea holds promise only for flooded rice. Apart from this, the major drawback of guanylurea as a fertilizer is its cost of production. Again when guanylurea is made from calcium cyanamide, it contains only about 7% N , and therefore its use in compound fertilizers is also limited. E. UREA-ACETALDEHYDE Scheffar ( 1 956) investigated the condensation products of urea and acetaldehyde. These were called “urea-Z’ compounds and, like ureaform, were perhaps a mixture of more than two compounds. The product mainly consisted of ethylenediurea and 2-ethylene-3-urea and contained unreacted urea and ethylolurea in small quantities. Kuntze (1959) observed that urea-Z gave lower yields of ryegrass as compared to calcium nitrate but increased the uptake of P, K, and Mn and decreased the uptake of Ca by the grass. Scheffer et al. (1 964) reported results comparing urea-Z with urea and calcium ammonium nitrate in field trials with oats, sugar beet, wheat, and rape. Urea-Z increased the yields and P content and narrowed the P :Ca ratio in crops. Pot experiments on rice in Japan revealed that urea-Z was as effective as urea (Hamamoto, 1966). Urea-Z seems more promising in the near future, because acetaldehyde is produced in large quantities as an end product of the petroleum industry and may become the cheapest aldehyde.

F. CROTONYLIDENEDIUREA (CDU) is preThis material (2-oxo-4-methyl-6-ureidohexaydroxypyrimidine) pared from the reaction between crotonaldehyde and urea. Jung ( 196la,b) has described the preparation of CDU. This material is manufactured by

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Badische Anilin and Soda Fabrick Ag., Ludwigshafen, Germany, under the trade name Floranid and by Chisso Corporation in Japan. The decomposition of CDU in soil (Jung, 1963b) and availability of N from CDU for ryegrass and other crops have been studied (Jung, 1961b,c, 1963b). CDU provided a long-lasting steady supply of N to ryegrass and wheat, suffered very little leaching, and was better tolerated by wheat and sunflower at high concentrations. On a sandy loam soil, the N from C D U for a wheat-maize-oats rotation was equally, though more slowly available than that from urea. The size of granules was also reported to affect the mineralization of CDU; as the size increased from I to 4 mm, less N was recovered by the plants (Jung, 1963a). In a laboratory study at Rothamsted, when CDU was incubated only 8- 15% of it decomposed in 24 weeks at 7°C. At 25"C, it decomposed faster, the rate depending on the soil used and amounts applied. Decomposition was faster in a sandy loam than in a clay-loam soil (Gasser, 1970). CDU supplied N very slowly over a prolonged period, and ammonium sulfate gave a higher yield of ryegrass than CDU (Gasser and Jephcott, 1964). Floranid and calcium nitrate applied to meadow at 250 kg N/ha were equally effective (Stahlin, 1967). However, Skirde ( 1967) reported that herbage yield and N uptake were about 10% lower with Floranid applied at 210 kg N/ha per year in the spring as compared to split application (7 equal dressings) of ammonium nitrate limestone. In Japan, CDU gave lower yields of rice as compared to ammonium sulfate (Hamamoto, 1966). Its usefulness for rice is limited because N release under waterlogged conditions is too slow to produce normal growth. It also leaches down in irrigation water (Hamamoto, 1966). G . DIFURFURYLIDENE TRIUREID

The Yoshihara Seiyu Industries, Japan, have developed this compound; it is a condensation product of urea and furfural. Since the compound is only slightly soluble in water, speed of decomposition is almost the same as of urea-Z. A compound fertilizer containing this compound has been manufactured on a small scale in Japan, using furfural as a by-product of edible oil refining process (National Institute of Agricultural Sciences, Japan, 1966). Results on its agronomic evaluation are still awaited. H. GLYCOLURIL This is prepared by a reaction between urea and glyoxal in the presence of HCl. The material has been investigated by Monsanto Co., but economics are reported to be unfavorable for development of a commercial program. Beaton et al. (1967) obtained a significantly low yield of orchardgrass with glycoluril as compared to ammonium nitrate. The per-

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PRASAD, G.

B.

RAJALE, AND

B. A. LAKHDIVE

centage recovery of N was also less (49%) as compared to ammonium nitrate (74%). Similarly, the yield of rice with glycoluril was very low as compared to urea (Hamamoto, 1966).

I. TRIAZINES Urea and ammonia react under heat and pressure to form the triazines (ring compounds containing 3 C and 3 N atoms) such as cyanuric acid, ammelide, ammeline, and melamine. The triazines contain 32-66% N and nitrify slowly at first but at a much faster rate after 10-15 weeks. During a 13-week incubation study, only about I % of N in the melamine portion of melamine nitrate, phosphate, or sulfate was nitrified (Scholl et al., 1937). Clark et al. (1957)observed that potassium and sodium cyanurates nitrified slowly for 6 weeks, but had nitrified almost completely after 9 weeks. Ammeline and mixtures of ammelide and ammeline nitrified at maximum rates between 9 and 12 weeks of incubation, while very little nitrification of melamine was observed over a 15-week period. Nitrification of N released from cyanuric acid, ammelide, ammeline, or melamine was studied by Hauck and Stephenson ( 1 964), and their results are presented in Fig. 6. The nitrifying capacity varied inversely lmr Webster

0

1

silty loam

6

12

18

24

Hartsells fine sandy Iwm

0

6

12

18

24

Weeks after incubation

FIG. 6. Effect of soil type on nitrification of triazines. ---, Cyanuric acid; -.-., ammelide; -..-.., a m m e l i n e r - t melamine; -, urea (-8+ 12 mesh); --, ureaform (-8+12 mesh). (Data from Hauk and Stephenson, 1964.)

with the number of amino groups on the triazine ring. The size of granule also has an effect on nitrification. Melamine and cyanuric acid powders nitrified slightly faster than solutions and considerably faster than - 8 12 mesh granules of these materials. An initial fungal attack on the

+

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triazine ring, followed by ammonification and nitrification, may explain why the powdered material degraded at a faster rate than its solution, while the relatively few particles in the -8+ 12 mesh treatments provided considerably less surface area and were thus degraded at the slowest rate. The nature of the soil also affects the nitrification of triazines (Fig. 61, various chemicals behaving differently in different soils. Melamine and ammeline are reported to nitrify very slowly in paddy soil over a 10-week period (Konishi and Imanishi, 194 I). In a greenhouse experiment, Terman et al. (1964) found that the availability of N to four crops of fodder maize and to four cuttings of bermudagrass decreased in the order: urea, cyanuric acid, ammelide, urea pyrolyzate ammeline, melamine. Cyanuric acid was toxic initially, hut most of its N became available for succeeding crops. Triazines do not appear to be very promising as slow-release N fertilizers. Wakabayashi and Masahiko (1 969, 1970a,b,c) made detailed studies on the nitrification inhibitory properties of s-triazines and their derivatives. They reported that haloalkyl groups, especially trihalomethyl groups, are required for high nitrification-inhibiting properties ( 1969). Amino groups also imparted some inhibitory properties to monoamino-striazines (1970). Melamines and their derivatives were of little use as nitrification inhibitors ( 1 97 la). Similarly, cyanuric acid and its derivatives showed no remarkable inhibitory effect ( 1 970). J.

METALAMMONIUM PHOSPHATES

Several divalent metals form ammonium phosphates. Minerals of magnesium, ferrous iron, zinc, manganese, copper, cobalt, and molybdenum are of particular interest both as a potential source of slowly available N and as a source of the nutrient cation (Bridger et al., 1962). In this respect magnesium ammonium phosphate (MgAP) and ferrous ammonium phosphate (FeAP) are of greatest interest, since Zn, Mn, Cu, Co, and Mo may develop toxicity if used in quantities required to supply adequate amounts of N. W. R. Grace and Co. are producing a magnesium ammonium phosphate material called “Mag-Amp” which analyzes 8-400-14 (Mg). A newer material, called “MagAmp with K” analyzing 7-40-6- 12 (Mg) has been recently announced. The company is marketing this product in the United States, United Kingdom, and continental Europe for nonfarm use; the U.S. price is in the range of $400 per short ton. Nitrogen from metal ammonium phosphates becomes available at a rate greater than would be expected from the solubility of the compounds, and it is evident that nitrifiability rather than solubility is the main factor controlling the availability of the nitrogen to plants. The rate of nitrifica-

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RAJENDRA PRASAD, G. B. RAJALE, A N D B. A. LAKHDIVE

tion varies with granule size-the larger the granules, the slower the rate. Crop response to metal ammonium phosphates is also thus largely affected by granule size. The response by first corn crop in pot experiments decreased markedly with increase in granule size (Terman and Taylor, 1965). As for the relative efficiency of metal ammonium phosphates, the percentage recoveries of nitrogen by the first 6-week crop of corn in pots for MgAP (hexahydrate), MgAP (monohydrate), FeAP, and monoammonium phosphate were 63, 44, 41, and 7 1 , respectively. A second 6week crop was also taken, and the total percentage recoveries of nitrogen for both the crops were 77, 53, 57, and 7 I for these four nitrogen sources, respectively (Terman and Taylor, 1965). This group of fertilizers is of particular interest for the production of container nursery stock, flower crops, landscape installations, and turf grass (Lunt and Kofranek, 1962; Lunt et al., 1962, 1964; McCall and Davidson, 1966). K. NITROGEN-ENRICHED COAL Efforts made at Central Fuel Research Institute, India, by Mukherjee et al. ( 196 1) to oxidize coal to humic acids, which were subsequently ammoniated for incorporation of extra N , produced a slow-release coal fertilizer. Further research by these workers led to a process of simultaneous oxidation and ammoniation. The resulting product was named Nenriched coal and is reported to contain as much as 14-22% total N, onethird of it being in the available form. Coal oxidation and ammoniation has been also studied in Canada, by the Alberta Research Council. Subbituminous coal is said to be used, at a temperature of 570"F, and the simultaneous oxidation-ammoniation method is employed. A 20-22% N content in the product is claimed. Mukherjee and Lahiri (1965) reported that N-enriched coal was more efficient as a fertilizer than ammonium sulfate over a period of 3-4 years. The superiority of N-enriched coal was ascribed to its residual effect as well as to its humus content. Contrary to this, other reports suggest that N-enriched coal is a poor source of N. Beaton et al. (1967) obtained a very low yield of orchardgrass with coal as compared to ammonium nitrate. The recovery of added N was only 39% with coal as against 74% with ammonium nitrate. Field experiments with wheat and maize by Prasad et al. (1968) showed that there was no direct response to Nenriched coal. However, where N-enriched coal was applied to wheat, a significant first residual effect was recorded on the succeeding maize crop. When this material was applied to maize, no residual effect on succeeding wheat crop was observed. For rice also this material was found to be a very inferior source of N (Rajale, 1970). This can be clearly explained with the help of laboratory studies (Rajale and Prasad, 1970a), where it

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was observed that mineralization of coal was too slow and even after 40 days of incubation was only 15%. Apart from the very slow release rate of N from N-enriched coal, its manufacturing and transport costs are likely to be high. It is generally argued that it contains humic acids and other organic constituents that may be helpful in improving soil physical condition or may even act as growth promoters. The workers have, however, failed to demonstrate these values of N-enriched coal, and this material as such seems to be of little value as an N fertilizer. V.

Coated Fertilizers

Coating of the fertilizer has been the subject of study by many research organizations, and a great many coating materials and methods have been tested. Release of the fertilizer from this coated granule is achieved through one or more of the following mechanisms: (i) water vapor entering through the coating, which is broken down by increased internal osmotic pressure: (ii) degradation of the coatings through microbial and abrasive action: and (iii) controlled or inhibited movement of dissolved salt out through tiny pores in the coating. In the first two mechanisms, once the coating is broken, fertilizer release is complete. The third mechanism is interesting in respect to slow release of fertilizer. In this process, as additional water enters through tiny pores, nutrient solution passes out to the soil. Nutrient release is thus metered at a fairly steady, although usually declining rate. Increase in temperature increases the pressure within the coated granule and thus accelerates the rate of release. Since elevations in temperature usually accelerate the rate of nutrient uptake by plants, this has the effect of adjusting somewhat the available nutrient supply to plant’s needs. With this type of coating the release rate of nutrient tends to be independent of pH, microbiological activity, and other environmental factors. A. SULFUR-COATED UREA The work at TVA has resulted in the development of sulfur-coated urea (Rindt et al., 1968). Thiokol Chemical Corporation (1967) has also developed S-coated urea. The TVA process for the manufacture of Scoated urea is comparatively simple, coating being carried out in a rotary pan in which the fertilizer granules are sprayed with molten sulfur from an air-atomizing nozzle and then in a second pan in which a wax sealant, which contains about 0.5% coal-tar oil to kill microorganisms that might break down the coating fast, and conditioner are applied to the sulfurcoated granules. The process adopted by TVA has the advantage of low

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RAJENDRA PRASAD, G. B. RAJALE, AND B . A. LAKHDIVE

manufacturing costs, but even then it will be 25-50% more per pound of nitrogen than in urea. Release of N from S-coated urea may be controlled by the thickness of the coating, placement, microbicides, temperature, and time of contact with the soil (Allen, 1968). Lunt ( 1 967) found that, after the first day, the release rate of N from S-coated urea was about 1% per day. A single application to turf of S-coated urea maintained yields for about 14 weeks at maximum growth. On sandy loam and loam soils, when irrigation practices were carefully managed to avoid large leaching losses of N, Lunt ( I 968) obtained as good yield of corn and recovery of N from a single application of S-coated urea as from 3 split applications of uncoated urea. Under conditions of high leaching, crop yields and N recovery from Scoated urea were higher as compared to uncoated urea (Fig. 7). The chief 5600 r

Low irrigation

High irrigation

Boot 01

,

56.05

112.10''

c

224.20

56.05

.

112.10'

l

o

224.20

Kilograms nitrogen per hectare

FIG.7. Corn yield and recovery of nitrogen after application of S-coated and uncoated urea under conditions of high or of low irrigation.

effect of using S-coated urea was to delay forage production until later in the season and better distribution of protein through the season (Allen et al., 1968). Mays and Terman ( 1968) observed that single spring application of S-coated urea gave same yield of coastal bermudagrass and more uniform seasonal distribution of forage and protein as compared to 3 split applications of ammonium nitrate and nitric phosphate. The total annual yields of fescue forage were usually similar with ammonium nitrate and

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urea and resulted in higher first-cutting yields'while S-coated urea resulted in higher later-cutting yields (Mays and Terman, 1969).S-coated urea when applied at high rates do not cause burning of the plant whereas uncoated urea may do so under certain conditions. In tests with very high rates of N applied to bermudagrass turf, uncoated urea nearly killed the turf, whereas ammonium nitrate caused moderate burning of the foliage. S-coated urea, however, gave maximum yield response with no sign of burning. In an experiment with corn seedlings, uncoated urea applied in the row to supply I12 kg N/ha killed all seedlings, while S-coated urea caused no damage. For ornamental plants in containers, Furuta et af. (1968) considered S-coated urea to be an excellent source of N. Single application of S-coated urea could supply an adequate amount of N for several months' growth. Under highly reduced waterlogged soil conditions, little or no urea was hydrolyzed from S-coated urea (Delaune, 1968). Rajale and Prasad ( 1 970a) also observed that mineralization of S-coated urea was. slower under waterlogged conditions as compared to that under field capacity moisture. Reduction of the outer layer of sulfur to sulfide and formation of precipitate of ferrous sulfide around the pellet apparently effectively sealed the pellet and prevented urea from coming in contact with urease. In the presence of roots of rice plant, however, urea was released. Oxygen from rice roots was apparently able to oxidize the ferrous sulfide around the pellet and release the urea. Experiments conducted at All-India Coordinated Rice Improvement Project showed that during the Kharif (summer) season of 1969 plots treated with S-coated urea resulted in more productive panicles, a lower grain to straw ratio and a higher spikelet sterility than those fertilized with common urea. These trends indicate that S-coated urea was better than the common urea. But this was not reflected in the ultimate grain yield and there was no significant difference in the grain yield of rice due to S-coated urea and common urea. This was attributed to the incidence of bacterial leaf blight (All-India Coordinated Rice Improvement Project, 1969). In the rabi (fall-winter) season 1970, S-coated urea yielded on an average 1836 kg/ha more than the basal application of common urea. Without any incorporation, the use of S-coated urea resulted in a grain yield response almost twice as high as with common urea. With a shallow or deeper incorporation the grain yield response to S-coated urea was about 50% higher than with ordinary urea (All-India Coordinated Rice Improvement Project, 1970). It may be mentioned that in all these trials a treatment with urea plus sulfur was also included, and there was no yield increase due to this treatment, an indication that the response obtained with S-coated urea is due to slow release of nitrogen, and not due to sulfur.

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RAJENDRA PRASAD, G. B. RAJALE, A N D B . A. LAKHDIVE

Results of the work with S-coated urea are quite promising. Sulfur has an advantage over other coating materials in that it is a plant nutrient itself. There are still some problems in adopting the method of coating to a continuous operation, and TVA Scientists are working on this and other associated problems. The material is now being widely tested.

B. FERTILIZERS COATEDWITH INERT MATERIALS To achieve the objectives of the controlled release concept, attempts have been made to cover fertilizer granules with urea and ammonium nitrate with rather inert, water-resistant coatings or membranes. These include various polymeric substances, such as polyethylene, acrylic, acetate and other resins, waxes, and paraffins; gums; tars, pitches; vacuum-evaporated metals: asphaltic substances and others (Jung, 1960; Lunt et al., I96 I : Oertli and Lunt, I963a.b.c: Skogley and King, 1968: Pencheva et al., 1969). Recently, Slack ( 1 968) presented an excellent review covering the patents on coated fertilizers. Archer Daniels Midland Co., U.S.A., and Badische Anilin and Soda Fabrik A.G., Germany, are known to be working with coated fertilizers. Archer Daniels Midland Company’s fertilizer is called “Osmocote”; the coating they have developed is an unspecified polymer of the type that regulates nutrient release by osmotic water exchange. However, this company has now discontinued the production and sale of its product. Badische Anilin and SodaFabrik is reported to be making use of the polyene polymer and copolymer of butadiene and 2-methylstyrene as coating material. Oertli and Lunt ( 1 962a) reported that the rate of release of nitrogen from coated granules of ammonium nitrate was influenced by coating thickness and temperature, but was not significantly influenced by soil pH and microbial activity. They (Lunt and Oertli, 1962) also demonstrated the ability of coated fertilizers to supply nitrogen effectively to maize under excessive leaching conditions. Encapsulation of fertilizers with polyethylene membranes effectively controlled the rate of release of the fertilizer constituents for maize and Kentucky bluegrass in the field, but did not significantly increase the yield or recovery of the fertilizer nutrients (Dahnke et al., 1963). Heilman et al. (1966) reported that resin-coated ammonium nitrate was more efficient than uncoated ammonium nitrate at the same rates in increasing forage yield and nitrogen content of bluegrass. Leaching losses of nitrogen were also reduced by coating ammonium nitrate. In leaching studies, 94% of the uncoated urea was recovered in 1 day, compared to 49% recovery of N from coated urea ( 1 3.2% resin) in 4 weeks of intermittent leaching (M. J. Brown et al., 1966). Patrick et al. (1 964) reported that plastic coated ammonium sulfate and urea were superior in increasing rice yield as compared to uncoated

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materials when applied subsurface before planting and that asphaltcoated materials were inferior to uncoated materials. They attributed the superiority of plastic coated materials to the slow release of nitrogen from the pellet and the inferiority of the asphalt-coated materials to a very slow release rate which failed to meet nitrogen need of the crop. In a later study, Patrick and Peterson ( 1 967) observed that resin-coated ammonium sulfate increased the yield of rice grain by about 235 kg/ha over uncoated ammonium sulfate when the fertilizer was applied preplanting. Similar increase in yield with resin coated urea over uncoated urea was obtained. Simsiman et al. ( 1967) observed that the highest grain yield of rice (770 1 kg/ha) was obtained from a medium-release emulsified asphalt and paraffin (EAP) coated ammonium sulfate material (EAP 3 0 3 2 ) placed at 15 cm depth. In Trinidad, EAP 3033 and EAP 3032 resulted in an increase of 1725 and 865 kg of rice grain per hectare over uncoated ammonium sulfate applied on equal nitrogen basis (70 kg N/ha) (Ahmad and Whiteman, 1969). If done at low cost, coating of N fertilizer is a very effective way of cutting down the N losses and thereby increasing the effectiveness of applied fertilizer N. VI.

Concluding Remarks

The available research results clearly indicate that crops remove only a part of applied N , the recoveries being fairly low in areas with warm temperatures and copious rainfall. Rice-growing areas subject to alternate drying and flooding deserve a special mention. It is these areas where use of nitrification retarders and slow release N fertilizers holds promise. Reports on the evaluation of these materials, although few, are encouraging. A study of economic feasibility of the use of these materials has not been possible, since most of these materials are still in the development stage and are being produced on a pilot-plant basis. Needless to add that commercial and pilot plant costs are far apart. The authors are of opinion that the blending cost of the fertilizer N with the nitrification retarders should not exceed much over a 10-15% surcharge on N cost. Similarly slow-release N fertilizers should be available at a similar price. To achieve this, research with indigenous materials and industrial waste products must be initiated within a country, and organizations like the Tennessee Valley Authority, U.S.A., could provide guidance and help to local agricultural scientists and technologists. ACKNOWLEDGMENTS The authors are grateful to Drs. M . S. Swaminathan, S. S. Bains, Rajat D e , 1. C. Mahapatra, B. A. Krantz, and B. C. Wright for encouragement and help.

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AUTHOR INDEX Numbers in italics refer to the pages on which the complete references are listed. A

Abarra, L. A,, 306,310 Abdaul, Samad, A., 310 Abhichandani, C. T., 296, 306, 310, 314, 34 I , 376 Abraham, T. P., 306,313 Abu-Zeid, O., 364, 378 Ackerman, W. L., 35.47 Acquaye, D. K., 340,376 Acree, F., Jr., 176, 230 Adachi, M., 305, 313 Adair, C. R., 28, 47, 242, 310 Adams, D., 307,310 Adams, J. B., Jr., 205, 232 Adams, R. S.. Jr., 151, 152, 220, 229, 230, 237 Addison, D. A., 2 16. 229 Adelson, B. J., 178, 191, 236 Aebi, H.,200, 232 Agnihotri, N. P., 151, 231 Ahlrichs, J. L , I5 1, 153,232,233,235 Ahmad, N., 375,376 Ahmed. M . K., 191,229 Aimi, R., 270, 273, 291,310 Akhundov, F. G., 340,361.376 Akita, S., 294, 310 Al-Abbas, A. H., 341,380 Alberta, T., 273,310 Aleksic, Z., 341, 376 Alexander, L. J., 33,48 Alexander, M., 177, 186, 195, 196, 201, 209, 212, 229, 230, 231, 232, 233, 234, 236, 346, 348,382 Al-Fakhry, A., 306, 310 Alim, A., 306,310 Allan, J., 190, 229 Allen, E. F., 306,310 Allen, S . E., 3 12, 366,376, 382 Alli, M. A., 303, 313 Allison, F. E., 338, 339, 340,356,376,378, 379 Allmendinger, D.F., I 12,143

Altman, J., 2 14,229 Amantaev, E., 344,376 Ancajas, R. R.,340,379 Anderson, J. P. E., 186, 187,229,235 Anderson, L E., 360, 378 Andreeva, E. A., 376 Andriessers, F. G., 348, 382 Angladette, A., 269, 298, 306, 310 Ansorage, H , 348, 35 I , 376, 378 Aomine, S., 150, 152, 153, 229, 234 Apel, P., 329, 334 Arashi, K , 270,310 Araten, Y., 358, 376 Arikado, H.,273, 274,310 Armiger, W.H., 222, 229 Armstrong, D. E., 177, 178, 179, 205,235, 240 Army, T. J., 358, 376 Arurkar, S. K., 179,229 Asada, K., 270, 291,310,312 Asai, R. I., 169, 177, 229 Asana, R. D., 252,310 Ashton, F. M., 163, 235 Aso, K., 252,310 Atkins, J. G., 28, 47 Attoe, 0. J., 374, 377 Audus, L. J., 172,229,376 Axley, J. H., 221, 240 Ayers, A. D., 304, 314 Ayers, W. A., 92, 94, 96, 98, 104, 107 B

Baba, T., 272, 282,310, 312 Bache, C. A., 191,229 Baghadadi, A. M., 2 13, 229 Bailey, G. W., 149, 150, 151, 152, 154, 156, 161, 181,229, 237, 238 Bailey, L. D., 92, 102, 109 Bains, S. S., 351, 355, 356, 381 Baker, H. M., 199,234 Baker, H. R., 160,239 Balasubramannian, A., 92, 98, 101, 106, 107

385

386

AUTHOR INDEX

Baldwin, B. C., 204, 229 Balster, C. A., 55, 86, 87 Bandurski, R. S., 95, 108 Banejee, A. K., 370,380 Barba, R. C., 222, 229 Barber, D. A., 91, 95, 101, 102, 103, 107 Bardsley, C. E., 341, 376 Barker, P. S., 184, 229 Barnes, D. K., 329,334,336 Barnett, A. P., 165, 229 Barnsley, G. E., 180, 217,229 Barrett, T. W., 119, 141 Barron, R. P., 169, 237 Barrons, K. C., 164,229 Barrows, H. L., 222, 229 Bartha, R., 203,229, 236 Barthel, W. F., 177, 187,229,230,237 Basak, M. N., 306, 310 Basaraba, J., 360, 376 Bassham, J. A., 294, 311 Bautista, E. M., 190, 236, 238 Beachell, H. M., 28, 47, 242, 282, 310 Beacher, R. L., 307,311 Beall, M. L., Jr., 177, 201, 222, 229, 234, 237

Beard, W. E., 165, 183, 186, 233 Beaton, J. D., 362, 367, 370, 376 Beckley, V. A., 54, 87 Beestman, G. B., 222,229 Behrens, B., 198,230 Beitz, H., 222, 233 Belasco, I. J., 163, 199, 203, 230, 238 Belima, N. I., 97, 109 Belser, N. O., 180, 230 Bender, F. W., 123, 130, 141 Benedict, H. M., 119, 141 Benesi, H. A., 175, 176,230, 232 Bengtsson, B. L., 354,37.6 Benjamini, E., 174,230 Bennett, E., 14, 25, 28, 47, 48 Bennett, H. H ,54, 87 Bennett, 0. L., 35 I , 377 Benoit, R. E., 344,377 Benvenue, A., 177,230 Benzian, B., 364, 376 Bernstein, L , 304, 314 Beroza, M , 176, 230 Berrer, D , 198, 235 Berry, C. D , 35.47

Berry, C. R., 112, 123, 141 Berry, J . A., 327,334, 328,335 Besemer, A. F. H., 162,239 Bettenay, E., 55, 65, 66, 67, 68, 69, 70,86, 87

Beynon, K I., 180, 192, 193, 205,230 Bhappar, D. C., 306,311 Biddulph, D., 287, 3 1I Bidwell, R. G. S., 92, 102, 109 Biggar, J. W., 149, 152, 153, 154, 157,236 Bigger, J. H., 187, 232 Bingeman, C. W., 199,234 Bingham, S. W., 2 16, 22 I , 232 Birch, W. R., 93, 107 Birrell, K. S., 176, 230 Bjorkman, O., 327, 328,334, 335 Black, J. N., 3 18, 335 Blackburn, G., 55, 86 Blackman, G. E., 93, 107, 3 18, 335 Blackmore, A. V., 55, 65, 68, 69, 70, 86 Blair, D. P., 185, 237 Blake, J., 170, 178, 198, 234 Blasco, M. L., 340, 376 Blaser, R. E., 328, 332, 336 Blink, G., 235 Bloom, J. R., 92, 105, 108 Blouin, G. M., 371, 381 Boehm, M., 2 14, 232 Boersma, L., 159, 160, 236 Bohn, W. R., 192,230 Bohning, R. H., 321, 324, 335 Boischot, P., 340, 376 Bolen, C. D., 334, 336 Bollag, J.-M., 196, 230, 234 Bollen, W. B., 213, 230, 342, 345, 376, 377

Bomme Gowda, A., 339,376 Bond, R. D., 55,86 Bonner, J., 92, 99, 108, 279, 311 Bordas, E., 176,231 Bordeleau, L. M., 202. 203, 229, 238 Borner, H., 92, 108, 179, 230 Boush, G. M., 187, 188, 192,236 Bovey, R. W., 164,230 Bowen, G . D., 92, 94, 98, 101, 102, 103, 108

Bowman, B. T., 151,230 Bowman, M. C., 176, 177,230 Bozarth, G. A., 204,232

AUTHOR INDEX

Braham, J. M., 356,378 Braithwaite, B. M.,212, 230 Brams, E., 103, 108 Brandt, C. S., 113, 115, 126, 138, 141, 142, 143 Bray, M. F., 204,229 Bredero, T. Y., 306,311 Breece, J. R.,373,377 Bremner, J. M.,340, 376 Brennan, E. G., 112, 122, 128, 132, 141, 143 Brewer, R. F., 132, 141 Brezhev, D. D., 44,47 Bridger, G. L., 369, 376 Briggs, G. E., 90, 108 Briggs, G. G., 152, 155, 181,230 Brioux, C. H., 356,376 Broadbent, F. E., 340, 341, 376 Broeshart, H., 341, 376 Brown, A. L., 344, 376 Brown, B. E., 368, 382 Brown, C. B., 156, I8 I , 230 Brown, E. H., 379 Brown, M.A., 338, 339,382 Brown, M. J., 374, 376 Brown, R. H., 328, 332, 336 Brown, W. T., 376 Bruce, W.M., 33,49 Brun, W. A., 320,328,329,335,336 Bucksteeg, W.,343, 382 Bukovac, H. J., 289,311 Bull, D. L., 192, 231 Bulygina, E. V., 93, I08 Burchfield, H. P., 169, 171, 176, 181, 230 Burger, T. F., 205, 231 Burleson, F. R., 122, 123, 128, 134,142 Burnside,C.A.,321, 324,335 Burnside, 0. C., 150, 164, 181, 198, 218, 230, 238 Burr, G. 0..335 Burstrom, H. G., 94, 108 Burton, W. L., 169,240 Butler, B. E., 5 5 , 62, 82 Byrde, R. J . W., 195, 230 C

Cady, J. G., 62, 80, 8 I , 84,86, 88 Calderbank, A., 150, 151, 153, 168, 230 Callow, B. J., 340, 382 Calma, V C., 306,31I

387

Caivect. R.,174, 230 Calvin, M., 294, 311 Cameron, J. W., 123, 124, 141 Campbell, F. J., 117, 122, 141 Cannell, R. Q., 328, 335 Cantwell, A. M., 127, 141 Cardiff, E. A., 112, 118, 125, 126, 133, 134, 139,141,143,144 Carlson, G. E., 329, 334, 336 Carney, C. B., 78, 87 Caro, J. H., 216, 222, 229, 230 Carrol, J. W., 116, 143 Carroll, R. B., 172, 230 Carter, F. L , 177, 189,230 Carter, H B., 117, 123, 144 Carter, J: N., 340, 351, 376, 377 Carter, R. L., 176, 230, 345, 378 Carvalho, A., 325,336 Caseley, J. C., 165, 230, 343, 344, 377 Casida, J. E., 174, 185, 191, 229, 231, 237 Castro, C. E., 180, 185, 230 Castro, T. F., 190, 217, 240 Cavalot, C., 352, 381 Celton, J., 306,315 Chacko, C. 1.. 184,230 Chandler, R. F., Jr., 28,43,44,47, 286,311, 333,335,340,377 Chandra. P., 343, 344, 345,377 Chandraratna, M. F., 242, 306, 311 Chang, C. W., 95, 108 Chang, R. K., 159,230 Chang, S. C., 306,311 Chang, T. T., 43,47 Chang, W. L., 311 Channon, A. G., 213,230 Chao, J. N., 311 Chao, T. T., 354,377 Chapell, W. E., 343, 344, 378 Chapman, H W., 321,335 Chapman, R. K., 191,232 Chapman, T., 160,230 Chase, F. E., 344. 378 Chaussidon, J , 174, 230 Chen, J.-Y. T., 169, 237 Chen, P. R., 177,230 Cheng, S . C., 306,311 Cheo, P. C., 214,231 Chesters. G.. 149. 177, 178, 179, 180, 181, 190, 205, 222, 229, 235, 236, 237, 240

388 Chiang, C. T., 306, 311 Chiba, H., 295, 296, 312 Chiba, M., 190, 240 Childers, N. F., 320, 321, 335 Chin, W.-T., 231 Chisaka, H., 198, 203, 231, 237 Chiu, T. F., 258, 259,311 Choubey, S. D., 311 Chu, H. F., 306,311 Churchward, H. M., 55, 86 Clark, F. E., 91,108,340,376 Clark, J. A., 13, 27,47 Clark, K. G., 368, 377 Clark, S. B., 364, 370, 379 Clark, T. F., 36, 49 Clarke, A. R. P., 55, 86 Cliath, M. M., 165, 239 Cobb, F. W., Jr., 133, 144 Coe, R. R., 119,142 Coffey, G. N., 54,86 Cohen, J. M., 166,231 Cole, A. F. W., 130, 143 Coleman, N. T., 153, 174, 232, 236 Cooke, G. W., 353,377 Cooper, F. E., 93, 100,109 Cooper, J. P., 325, 329, 335, 336 Cooper, R. L., 320, 329,335 Cope, J. T., Jr., 369, 382 Coppedge, J. R., 192,231 Corbet, A. S., 340,377 Corden, M. E., 173, 213, 231, 239 Corey, R. A., 191,231 Corky, C., 187, 229 Cornfield, A. H., 340,376 Correll, D. S., 35, 47 Corsi, R., 153, 232 Costonis,A. C., 121, 128,141 Couch, H. B., 92, 105, 108 Couch, R. W.. 198,231 Covar, R. R.,352,379 Cowley, G. T., 187,235 Cox, R. S., 345, 383 Craddock, J. C., 19, 27, 28,48 Crafts, A. S., 90, 91, 93, 99, 108 Craig, J. C., 93, 100, 109 Cranner, B. H., 93, 108 Crawford, E. D., 152, 158, 159,239 Creech, J. L., 12, 34,47,48,49 Creveling, R. K., 132, 141

AUTHOR INDEX

Crocker, R. L., 5 5 , 62, 63, 64, 77, 79, 80, 86 Crocker, W., 112,141 Crookston, R. K., 326,335 Crosby, D. G.. 166, 167, 176, 231, 239 Cruz, M. I., 151, 155, 181,238 Cullinan, F. P., 25, 47 Cummings, M. B., 3 19, 335 Cummins, D. G . , 36,49 Cunningham, R. K., 340, 348, 353, 376, 377,380 Cutkomp, L. K., 220, 237 D

Dabin, B., 306,311 Dahm, R. G., 28,48 Dahnke, W. E., 374,377 Daines, R. H., 112, 120, 122, 128, 132, 141, 142, 143 Daji, J. A., 306, 311 Dale, S. W., 173, 231 Dalton, R. L., 200, 231 Damanakis, M., 220, 231 Dangarwala, R. T., 345,380 Daniels, R. B., 61, 62, 76, 77, 78, 80, 85, 86,88 Danielson, L. L., 172, 238 Darding, R. L., 219, 231 Darley, E. F., 112, 118, 122, 123, 125, 127, 128, 129, 133, 134, 142, 144 Das, A. C., 340, 377 Das, U. K., 351, 352, 377, 381 Daster, R. H., 258, 311 Datta, N. P., 341, 356, 377, 381 Datta, S. N.,361, 377, 378 Daun, R. M., 340,379 Dauterman, W. C., 174, 177,230, 231 Davidson, H , 370,379 Davidson, J. G., 338, 356, 383 Davidson, J. M , 159, 160, 230, 231 Davies, L., 192, 230 Davis, D. E., 198, 231 Davis, D. R., 114, 122, 141, 144 Davis, R. 0. E., 368, 382 Davis, W. M., 54, 86 Dawson, J. E., 18 1, 196,230,231,234,239, 343,344,380 Dawson, J. H., 219,231 Dawson, R. A. G., 353,378

3 89

AUTHOR INDEX

Dawson, V. T., 343,382 Day, B. E., 219. 231 De, P. K.. 340. 377 De, R., 342,377 Dean, C. E., 114. 141 Dean, G., 133, 144 de Calderon, M., 338, 339,381 DeCandolle, A. P., 92. 108 Decker, J. P., 293, 311, 324, 335 De Datta, S. K.. 306, 307, 311, 314, 375. 382 Delaune. R. D.. 340, 373.377 DeMent, J. D., 361. 362, 369,377,382 Denny, P. J., 15 I , 235 DeRoo, H. G., I3 I , 144 Detling, K. D., 176, 232 Devine, J. R., 353, 377 Devine, T. E., 123, 142 Devlin, R. M.. 90, 108 Dewey. J . E., 191. 231 Dickson, A. D., 28.48 Digar, S., 340, 377 Dilz, K., 362, 377 Ditman. L. P., 2 18. 236 Dixon, J. 8.. 151, 231 Dochinger, L. S., 123, 130, 141 Dodge, A. F., 33. 35, 47. 48 Doherty, P. J., 152. 220, 231 Domsch, K., 362,377 Domsch, K. H., 172.237 Don, J., 62, 86 Donald, C. M., 333. 335 Dornhoff, G. M., 329,335 Dorough, H. W., 192, 231 Douros. J. D., 344, 377 Dowler. C. C., 164, 230 Downs, R. F., 118, 142 Downs, W. G., 176, 231 Downton, W. J. S., 294.311, 325, 326, 327. 328,334, 335 Drennan, D. S. H., 220,231 Drescher. N.. 172, 173, 205. 231 Dubey, H. D., 215,231, 345,377 Dubrov. A. D., 93, I08 Duff. R. B., 195. 240 Duffy, J. R., 177, 231 Dugger. W. M.. Jr., 125, 126, 134, 135, 136, 139, 141, 144 Dumenil, L., 340, 383

Duncan, W. G., 269,311 Dunigan, E. P., 153. 231 Dunning. J. A., 126, 127, 129, 130. 132, 135, 136, 138, 141, 142 Dunstan, G. H., 166. 234 Dupuis, G., 198, 235 Dutta, C. H., 339. 377 Duxbury. J. M., 196. 231, 239 Dzubay, M., 306,311 E

Earle. F. R., 35. 47 Eastin, J. D. 279, 311 Eastin, E. F., 168, 231 Eastman. J. D., 164, 229 Eaton, P. M., 120, 144 Eberhard, D. L., 304. 314 Ebner, L., 200,232 Eckert. J. W., 172, 237 Ecobichon, D. J., 185, 231 Edgington, L. V., 17 I , 237 Edwards, C. A., 161, 164, 216, 217, 218, 231 Edwards, W. M., 222,229 Eggurn. B. 0..29.48 Egli. D. B., 334.336 Eguchi, H., 270,310 Ehlers, W., 165.231 Elgar, K., 192,230 Elliot, J. M.. 345,377 El Nawawy, A. S., 2 15,233 Elrick, D. E., 159,231,234 El-Sharkawy. M., 323,335 Engelbert, L. E., 374,377 Engelstad, 0. P.. 362,377,379 Engle, R. L., 123, 135, 138,141 Eno, C. F., 212, 231, 344, 377 Ensminger. L. E., 369, 382 Erh, K. T., 159, 231 Erlanson, C. O., 13.48 Esser. H., 198, 235 Etheridge. P., 220, 232 Evanari, M., 92, 108 Evans. A. W., 200.231 Evans, L.T., 318,319. 325,335 Evans, W. C., 196. 232 Evatt. N. S., 28. 47, 282. 310 Everett. P. H., 344, 377 Everett, T. R., 28, 4 7

3 90

AUTHOR INDEX F

Fang. S. C . , 20 I , 232 Farley, J. D., 207, 235 Farmer, F. H , 344, 377 Farmer, V. C., 195, 240 Farmer, W. J., I5 I , 165,231, 232, 234, 239 Faulkner, J. K., 195, 232 Faulkner, M. D., 341, 381 Feder, W. A., 117, 122, 124, 133,141, 143 Fenton, S. W., I5 I , 230 Ferguson, J , 344, 345, 380 Fernando, L. H., 306,311 Fernley, H. N., 196,232 Figon. C. L., 352, 381 Fike, W. T., 36.49 Finlayson, D G., 187, 240 Finnerty, D. W., 199. 234 Fischer, B. B., 222, 235 Fishbein, L , 173, 231 Fisher, H H , 38, 47, 48 Fleck, E. E., 175. 176, 232 Fletchall, 0. H., 150, 239 Fletcher, W. W., 343. 377 Flieg, O., 343, 377 Flint, R. C., 364, 378 Focht, D D , 186,232 Folckemer, F. B., 176, 232 Fomenko, B. S . , 105, 108 Fontanilla, E. L , 2 18. 236 Forbes, C., 220, 234 Fowkes, F. M., 176, 232 Fowler, E. D., 54.86 Fox, C. J. S., 2 12, 232 Fox, F. L., 122, 123, 126, 130. 141, 142 FOY.C. L., 91, 93, 99, 100. 108, 163, 200, 2 16, 22 I , 232, 235 Frankel, 0. H., 25, 28. 48 Frederick, 1. B., 175, 240 Frederick, L. R., 377 Freed. V. H., 154, 160,232, 236 Freeman, G. D., 93, 100, 109 Freeman, J. F., 2 19, 231 Freeman, S. C. R., 364, 376 Freiberg, S. R., 341, 377 French, A. L., 185, 232 French, N., 2 12,232 Frey, D. G., 78, 86 Frissel. M. J., 153, 156, 232 Fryer, J. D., 162, 218, 220, 231, 232

Fuhremann, T. W., 187,235 302, 312 Fujita, 0.. Fujiwara, A., 272, 291, 311 Fukai, T., 287, 288, 299, 311 Fukuto, T. R., 174, 230 Fuller, W. H., 357, 377 Funderburk, H. H., Jr., 198, 204, 231, 232 Furmidge, C. G. L , 152, 217,232 Furtick, W. R., 198, 238 Furuta, T., 373, 377 Fusi, P., 151, 153, 232. 236, 238 G

Gabbott, P. A., 160, 180, 217, 229, 230 Gabelman, W. H , 123, 135. 138, 141 Gadet, R., 356, 357, 382 Galston, A. W., 99, 108 Galvez, N. L., 306, 31I Gamble, E. E., 61, 76, 77, 78, 79, 80, 81, 84, 85,86 Gannon, N., 187,232 Garb, O., 92, 108 Garcia, C. V , 270, 314 Gardiner, H. C., 15 I , 159,235,236 Gardiner, J. A., 205, 232 Gasser, J. K. R., 340, 345, 348, 349, 353, 354, 357, 362, 364, 367, 377, 378, 380, 382 Gauhl. E., 327,328,334,335 Gaunt, J. K.,196,232 Gautam, 0.P., 370,381 Geissbuhler. H , 199,200.232 Gentry. H. S., 3 1, 35, 47, 48 Geoghegan, M. J., 204,229 Gericke, W. F., 252. 311 Gershon, H., 205, 232 Getsinger, J. G., 37 I , 381 Getzin. L. W.,178, 179, 190, 1 9 1 . 218,232 Giam. C. S., 167, 233 Gibson, 1. A. S., 214. 232 Giddens, J. E., 214,237,343,383 Gile, L H., 5 5 , 70, 71, 72. 73, 74, 75, 76, 86,87 Gilmour, C. M., 198, 238 Gilmour, J. T., 153, 232 Glater, R. A., 120, 141 Clickman, M., 133, 143 Glinka, K. D., 54, 8 7 Golab, T., 206, 232

AUTHOR INDEX

Goldman. A,, 175. 236 Good, J. M., 345,378 Gopalswamy. A,, 361,378 Goring, C. A. I., 150, 152, 158, 161, 216, 232,233,342,348,349,378 Gorlitz, H.. 35 1, 378 Gouere, A., 340,376 Graetz, D. A., 149,236 Graham-Bryce, I. J., 149, 158,220,232 Gramlich. J. V., 198,206,231,232 Gray, R. A., 163, 172, 173,232,233 Greaves, M. P., 101, 108 Green, R. E., 149, 159, 181, 220, 233, 237 Green, V. E., Jr., 28,47, 307,311 Greenland, D. J., 149, 152, 233, 340. 353, 378 Greig, J. K., 36, 49 Griffith, G., 54, 87 Griffith, R. L., 219, 233 Grineva, G. M., 106, 107, 108 Grist, D. H., 242, 311 Grodzinsky, A. M., 92, 108 Groskopp, M. D., 374,377 Grossenbacker, K., 103. 108 Grossman, R. B., 71. 73, 74, 75, 76, 86 Grove, J., 168, 238 Grover, R., 149. 219, 220,233 Griinzel, H., 171, 234 Guardia, F. S., 170. 178, 201. 234, 235, 237 Guderian, R., 115, 136, 141 Guenzi, W. D., 165, 183. 186,233 Guillemet, F. B., 132,141 Gunner, H , 178, 192,233 Gunther. F. A,, 169, 177.229 Gupta, S. P., 306,311, 340,378 Gupta. V C., 344,378 Gutenmann. W. H., 195,233 Gyo, O., 303,314 Gysin, H., 180,233 H

Haagen-Smit, A. J., I 12, I 13, 129, 142 Haas, J. H., 123, 142 Haden. W. W., 360,378 Hagberg, W., 29, 48 Hageman. R. H., 324,336 Hagiwara, T., 256, 257, 258, 311 Hahn, B. E.. 378

39 1

Hale, M. G., 92, 98, 108, 343, 344, 378 Halisky. P. M., 127, 141 Hall, R. C.. 167, 233 Haller, H. L., 175, 176, 232 Hamaker, J. W., 150, 152, 164, 217, 233 Hamamoto, M , 358, 361, 364, 365, 366. 367. 368,378 Hamdi, Y A,, 2 15,233 Hamlyn, F. G., 353, 354, 357,377, 378 Hance, R. J.. 149, 152, 153, 156, 157, 181, 233 Handley, R. A., 108 Hanna, G. C., 33.48 Hansen, E. A., 169, 237 Hanson, A. A,, 10.48 Hanson, C. H., 123, 142, 329,334, 336 Haque, R., 154, 160,232, 236 Harada, T., 302, 314, 345, 378 Harai. K , 303, 311 Hardman, L. L., 320, 335 Hardy, A. V., 78, 87 Hardy, E. L., 70.87 Harlan, H. V.. 28, 48 Harlan, J. R., 25,28,48 Harner, F. M., 133, 144 Harper. H. J., 378 Harris, C. I., 153. 163. 198, 200, 216, 218. 2 19.233, 235, 238 Harris. C. R., 177, 187, 189, 19 I , 233,236, 239 Harris, R. F., 180, 229 Hart, R. H., 329,334, 336 Halter, R. D., 151, 233 Hartisch, J., 222, 233 Hartley. G. S., 157, 164, 233 Hartt, C. E., 335 Hasegawa, G., 269. 311 Haselbach, C., 200, 232 Haselhof, E., 112, 142 Hashimoto, Y., 273, 313 Hatch. M. D., 294, 311, 325, 327. 335 Hauck, R. D., 340, 358, 368,378, 380 Hauser, E. W., 165, 229 Have, H. T. E. N., 306.311 Hawley. J. W., 55.70.7 I , 72,73,74,75,76, 86, 8 7 35.47 Hawley, W. 0.. Hayakawa, T., 291,312 Hayakawa, Y., 305,312

392

AUTHOR INDEX

Hayase, T., 36 I , 366, 378 Hayman, D. S., 91, 92, 105. 109 Hays, J. T., 360,378 Haywood, J. H , 112. 142 Head, G. C., 91,93, 108 Heagle, A. S., 133, 142 Heck. W. W., 113. 117, 120, 122, 123, 126, 127. 129, 130. 131, 132, 133. 135, 136, 141, 142, 144 Hedgcock. G. G., 133, 144 Heggestad. H. E., 112, 113, 114, 118, 122. 123. 128, 129, 134, 142, 143, 145 Heichel, G. H., 330, 335 Heilman, M. D., 374,378 Hein. E. R., 168, 233 Hein, M. A., 29, 49 Heinisch. E., 222. 233 Helling,C. S., 157. 159, 160. 161, 162, 163. 166. 196,230, 233, 234, 235 Henderickson, R., 222, 234 Hendricks, R. H., 128. 144 Henze. R., 366, 382 Hepting. G. H., 123, 141 Hermanson. H. P., 220. 234 Herrett, R.,A., 201,234 Hesketh, J. D., 294. 312, 322. 323, 325. 332,335 Hewitt. W. B., 112, 144 Hiatt. A. J., 9 I . 94, 108 Higgins, J. J., 36, 4 9 Hildebrand, D. C., 91, 92, 104. 109 Hill, A. C., 113, 118, 122, 135, 140, 142 Hill. D. W., 184. 234 Hill, G. R., 319, 321, 336 Hills, F. J., 169, 234 Hiltbold, A. E., 181, 221, 234, 236 Hindawi. I. J., 120, 126, 127, 130. 131, 133, 136, 138, 142, 144 Hinden, E., 166, 234 Hinesly, T. D., 220, 239 Hingston, F. J., 5 5 , 65, 66, 68. 69, 70, 8 6 Hinman, W.C.. 354.380 Hirabayashi, S., 345, 378 Hirai, K , 303. 311 Hirose, A., 299, 300,312 Hisamura, Y., 269, 271. 311 Hitchcock, A. E.. 112, 118, 119, 142, 143. 145 Hobbs, J. A., 159, 238

Hock, W. K., 207,234 Hodge, A. J., 326. 335 Hodge, W. H., 12, 13.48 Hodges, G. H., 123. 132, 136, 143 Hoflich. G., 350, 378 Hofstra, G., 294, 312, 325, 335 Holladay, J. H., 165, 229 Hollowell, E. A., 29, 48 Holly, K., 220, 231 Holmes, M. R. J., 353, 377 Homan, C., 112, 142 Honda, S., 350, 380 Honda, T., 270, 272.314 Honma. M., 350,380 Honma. T., 325,336 Honya, K., 269,312 Hoopingarner, R. A., 185, 232 Hope. A. B., 90, 108 Hori, S., 340, 380 Horrobin, S., 180. 234 Horvath, R. S., 196, 234 Hosler. C. R., 114, 142 Hosoda, K , 303,312 Howard, F. L , 342, 382 Howell, J. V , 5 I , 8 7 Howell, R. K , 123, 142 Howlett, F. S., 33. 34. 48 Hsu. S. C., 258, 259, 311 Huang, K. S., 306,311 Hubbard, W. A., 362, 367, 370,376 Hughes, T. D., 378 Hulcher, F. H , 343, 344,378 Hull, H. M., 112, 126, 127, 128, 129, 131, 142 Hummer, B. E., 2 18. 233 Humphrey, R. R., 70, 8 7 Hunt, C. B., 87 Hunt,C. M ,361,362,369.377,382 Hurle, K.. 218, 234 Hurtt, W., 91. 93. 100, 108 Hussain, S. S., 92, 108 Hutton. J. T., 5 5 , 86, 87 I

Ibaraki, K., 220. 239 Idnani, M. A., 36 I , 377, 378 Igarashi, M., 246. 312 Igaue. I., 291, 312 Igue, K , 165, 234

AUTHOR INDEX

Ilyaletdinov, A,, 344, 376 Imaizumi, K., 305, 312 Imanishi, A., 369, 379 Impey. R. L., 342,378 Inada. K., 272. 312 Inoue, K., 152, 153. 229, 234 Irvin, H.,306, 312 Isensee, A. R., 167, 186, 2 16,234, 235 Ishibashi, H.,304, 312 Ishikawa, M., 273, 313 Ishizaka, H.,269, 271. 272, 312 Ishizaka, N., 304,314 Ishizawa, S . , 380 Ishizuka, Y., 243, 244, 245, 247, 249, 252, 253, 254, 255, 263, 270, 289, 290, 295, 299, 300, 302, 303, 305, 312, 360, 370 Iso, E., 242. 312 Isobe, M., 364. 378 Isphording. W. C., 78. 8 7 Iswaran, V.,361,377, 378 Ito. H., 5 , 43, 48 Ittihadieh, F., 340, 379 Ivanov, V. P., 96, 105, 108 lyama, J., 325, 336 Izhar. S.. 330. 335 J

Jackson, W. A., 293,312, 324,335 Jacob, K. D., 356.378 Jacobs, L. W., 166. 221, 234 Jacobson. J. S.. I 13, 119, 122, 140, 142 Jacobson, L.. 108 Jane, A., 2 12,230 Janert. R., 348. 35 I . 376, 378 Jaques, R. P., 344.378 Jaworski, C. A., 352,378 Jenkins, M. T.. 26. 48 Jenny, H.,103. 108 Jensen, C. R., 165,232 Jensen, H. L., 378 Jephcott. B. M., 362, 367, 378 Jernelov. A., 207, 234 Jodon. N. E.. 28. 47 Johnson, F., 112. 143 Johnson, H.. Jr., 123, 124. 141 Johnson, H. S., 325.335 Johnson, L. R., 22 I , 234 Johnson, M. R., 176,232 Johnston, T. H.,28. 47

393

Johnston. T. J., 333, 336 Johnston, W. R., 340.379 Joley, L. E., 12. 48 Jolliffe, P. A., 325. 335 Jolliffe, V. A., 2 19. 231 Jones. C. H.,3 19,335 Jones, D. D., 91, 93, 94, 109 Jones, G. H.G., 54.87 Jones, J. L., 133. 142 Jones, J. W., 28, 48, 307, 312 Jones, Q., 35, 48 Jones, W. W., 342,378 Jongen. P.. 5 5 , 8 7 Jordan, H. V , 341,376 Jordan, L. S., 2 19. 231 Jordan. R. H., 5 5 , 62, 63, 64, 86 Joshi, N. V., 312 Joshi. S. G.. 312 Juhren. M., 118. 125, 126, 127, 134, I42 Jumar, A., 171, 234 Jung. J.. 344, 366, 367, 374, 379

K Kaars Sijpesteijn, A., 206,234 Kanapathy, K., 258, 312 Karim. A. Q. M. B., 305, 312 Karlson. K. E., 29, 48 Kasai, Z., 291. 310, 312 Kashairy, M. A., 306. 312 Kaslander, J., 206, 234 Katz, M., 112. 142 Katznelson. H.,105. 108 Kaufman, D. D., 160, 170, 178, 194. 198, 199. 200. 20 I , 205. 233, 234, 235, 237, 239 Kawana. K., 249,25 1,269.314 Kawano. I., 3 19,336 Kawarazaki, Y., 256,270,313 Kawashima. Y.,310 Kay, B. D., 159.234 Kearney. P. C., 166, 167, 170, 178. 183, 186, 194, 198. 200, 201, 202, 203, 205, 216, 221, 231, 233, 234, 235, 237, 239, 240 Kearns. C. W., 183, 236 Keaton, J. A., 165, 239 Keeney, D. R., 166, 221, 222. 229, 234 Keller. T., 343. 379 Kendrick, J. B., Jr., 112, 123, 127, 142, 143

394

AUTHOR INDEX

Kensuke, H., 362, 363,380 Kerlinger, H. 0..164, 233 Kerr, A., 92, 105, 108 Kerr, E. D., 133, 142 Kesner, C. D., 206,235 Keyworth, A. G., 2 13.230 Khan, J. A., 340,377 Kilgore, W. W., 171, 235 Kilian, K. C., 361, 379 Killinger, G. B., 36, 4 9 Kim, I. S., 306, 313 Kimura, J., 295, 296,312 Kimura, Y., 207, 235 Kincaid, R. R., 342, 379 King, H. M., 108 King, J. W., 382 King, P. H., 160, 161, 235, 236 King, W. E., 7 I , 87 Kinoshita, Y., 378, 379 Kirinuki, T., 345, 378 Kirkland, K , 162, 2 18, 232 Kisaki, T., 324, 336 Kiss, A., 2 15, 235 Kitagishi, K., 304, 305, 315 Kiuchi, T., 269, 27 I , 272, 312 Klein, L K , 93, 108 Klein, W. H., 125, 141 Klernme, A. W., 306,310 Klingebiel, U. I., 167, 168, 203, 237 Kluge, E., 221, 235 Knake, E. L., 220, 239 Knight, B. A. G., 150, I5 I , 235 Knight, R. C., 112, 142 Knowles, C. O., 169, 179, 229, 235 Knsiili, E., 180, 198, 233, 235 Knudson, L., 93, 108 KO, W.-H., 207, 235 Kofranek, A. M., 370, 374,379, 380 Koike, H., 2 12, 235, 344, 345, 379 Konishi, K., 369, 379 Konishi, S., 310 Konno, S.,291, 310 Konrad, J. G., 177, 178, 179, 235 Kopylov, B. A., 374, 381 Koren, E., 163, 235 Koritz, H. G., 126, 131, 135, 144 Kortschak, H. P., 335 Kottlowski, F. E., 5 5 , 7 I , 8 7 Krenzer, E. G., Jr., 326, 328, 335, 336

Kreutzer, W. A., 2 13, 235 Krotkov, G . , 92, 96, 109 Krupp, H. K., 159,231 Kubota, M., 256, 314 Kudyshev, T., 344,376 Kumada, K , 273,312 Kumagai, K., 5 . 4 3 , 4 8 Kumura, A., 270,314 Kuntze, H., 366, 379 Kuo, E. C. Y., 151,235 Kurosawa, H., 246, 291,312 Kurtz, L. T., 362,383 Kushizaki, M.,287, 288, 299, 311 1

Lacasse, N. L., 116, 143 Laetsch, W. M., 326, 335 Lahiri, A., 370,380 Lakhdive, B. A., 339, 340, 349, 351, 355, 356,379, 381 Lambert, S. M., 152, 155, 220, 235 Lamont, T. G., 368,377 Landau, E., 115, 143 Lange, A. H., 222,235 Langford, W. R., I I , 29. 48 Langsdorf, W. P., 199, 230 Lapham, J. E., 54, 8 7 Lapham, M. H., 54.87 Larson, R. E., 38. 48 Last, F. T., 213, 238 Latey. J., 132, 144 Laties, G. W., 102, I08 Latshaw, W. L., 379 Lauer, F. I., I I , 48 Lavy, T. L., 150, 158, 159, 181, 218, 230, 235, 238 Leach, L. D., 169, 234 Leasure, J. K., 200, 235 Ledbetter, M. C., 118. 143 Ledger, M., 2 14,232 Lee, G. B., 149, 190, 236, 237 Lee, L. T., 258, 259, 31I Lee, T. T., 132, 143 Leefe, J. S., 220, 235 Leenheer. J. A., 153,235 Lees, H., 343, 357, 379 Legg, J. O., 339,379 Lehrnann, C. O., 329,334 Lehr, J. R., 379

AUTHOR INDEX Lemon, E. R., 322, 323, 336 LeMone, D V., 71.87 Lenain, M., 356, 357, 382 Lenka, D., 342,381 Leo, R., 249, 25 I , 269,314 Leone, 1. A., 112, 122, 128. 132,141, 143 Leslie, T. I., 5 5 , 86 Lessman, K. J., 35, 47 Letey, J., 160, 165, 231, 237 Levi, E., 93, 109 Levitt. J., 91, 109 Lewin, J., 304, 312 Lewis, D. E., Jr., 151, 231 Li, M.-Y., 166, 231 Li. P., 152, 229 Lian, S., 258, 259, 31 I Lichtenstein, E. P., 186, 187, 19 I , 192.2 12. 2 16, 229, 232, 233, 235 Liefstingh, G., 235 Lillah, M. T., 306, 310 Lindau, G., 112, 142 Linder. P. J., 93, 100, 109 Lindquist, D. A., 192, 231 Lindstrom, F. T., 159, 160, 236 Lindt, J. H., 313 Linke, H. A. B.. 203, 229, 236 Linzon, S. N., 112. 118, 133, 142, 143 Lipke, H., 183, 236 Lipton, G. R., 169, 238 Lisk, D. J., 191, 195, 229, 233 Littlefield, N., 135, 142 Liu, L. C., 219, 236 Lloyd, G. A., 172, 236 Lockard, R. G., 258. 312 Lockwood, J. L., 184,230 Loeffler, E. S., 176,232 Loehwing, W. F., 92, 109 Loeppky, C., 200, 2 15, 236, 239 Lofgren, C. S., 176, 230 Loft. B. C., 175, 238 Lojo, A. M., 352,379 Long, M. I. E., 360. 361, 379, 383 Loomis, H F., 12, 48 Loomis, R. S., 285, 313 Loomis, W. E., 321, 323, 335, 336 Loos, M. A.. 194, 195, 196, 218,233,236 Lopez-Gonzalez, J. D , 159, 176,236 Lotse, E. G., 149. 236 Loughman, B. C., 91, 101, 107

395

Lowe, R. H., 91, 94, 108 Lucas. R. L., 213. 240 Luckwill, L. C., 343, 344, 377 Ludwig, R. A., 173, 236 Luebs, R. E., 374, 376 Lundegardh, H., 107, 109, 319,335 Lunt, 0. R., 364, 370, 372, 374, 379, 380 Lynn, G. E., 164,229 Lyon. T. L., 92. 93. 109 M

Ma, P. C., 306, 311 McAlpine, V. W., 364, 379 McArthur, W. M., 55,87 McAuliffe, C., 174, 236 McBain, J. B., 178, 191, 236 McBeath, D. K., 348. 357, 379 McCall, W. W., 370, 379 McCallan, S. E. A., 206, 236 McCarty, M. K., 164, 238 McCarty, P. L., 160, 161, 184, 234, 235, 236 McClure, G. W., Jr., 205,232 McCollum, J. P., 198,238 McCormick, L. L., 18 I , 236 McCrory, S. A., 33,34,48 McCune, D.C., 119, 140,142,145 MacDonald, I. R.,91, 102,109 McDougall, B., 94,95,96,109 Macdowall, F. D. H., 123, 126, 127, 128, 130, 131, 132, 135, 143 McGahen, J. W., 199,234 Maciak, F., 345, 383 McKee, R., 29.48 McKeen, W. E., 92, 108 McKell, C. M., 348, 379 McKenzie, R. M., 5 5 , 88 MacLean, D. C., 118, 119, 144 McLean, J. D., 326,335 MacNamara, G. M., 151, 152, 236 MacRae, D. H., 179,240 MacRae, 1. C., 178, 190. 201, 236, 238, 340.379 Madison, J . H., 214, 236 Magnaye, C. P., 307,311 Magness, J. R., 48 Mahapatra, I. C., 342, 350, 379, 381 Maigninen, R., 55. 8 7 Malina, M. A., 175, 236

396

AUTHOR INDEX

Malkani, T. J., 258, 311 Malquori, A., 153, 236 Mamken, L. N., 374,378 Mandal, S. C., 303, 313 Manning, W. J., 133, 143 Manorik, A. V., 97, 109 Manzoorf, A. S., 305,312 Marbut, C. F., 54, 87 March, N. L., 5 5 , 88 Marckwordt, U., 102, 109 Market, S., 348, 376 Marshall, H. V., 78, 87 Marth, E. H., 216, 236 Martin. A. E., 338. 340, 379 Martin, J. H., 26,36,48,49 Martin, J. P., 165, 172, 213. 234, 236, 237, 339, 342, 343,379 Martin, W. S., 54, 87 Martini, M. L., 28, 48 Masahiko, O., 369,382,383 Matsuda, N., 379 Matsuguchi, T., 380 Matsui, M., 256, 257, 258, 311 Matsumura, F., 187, 188. 192. 236 Matsuo, T., 242, 282, 313 Matsushima, S., 270, 271, 277, 296, 297, 298.313 Matsushita, S., 29 I , 313 Matthews, S., 2 19, 233 Maud. R. R., 55,87 May, D S., 166, 234 Mays, D. A., 3 12, 372, 373,376, 380 Meagher, W. R., 222, 234 Meek, R. C , 220, 240 Meaitt, W. F., 151, 160, 206, 237, 238 Mehrotra, 0. N., 305. 313 Mehta, B. V., 345, 380 Mehta, V. S., 344, 382 Meidner, H., 335 Meikle, R. W., 354, 381 Mendel, J. L., 184, 236 Menges. R. M.. 166. 236 Menn, J. J., 178, 191, 236 Menser, H. A.. 123, 126, 127, 128, 129, 132, 136, 143 Menz, K. M., 328,335 Menzer, R. E., 218, 236 Menzie, C. M., 169, 184, 187,206,207,236 Mercer, F. V., 326,335

Merkle, M. G., 164, 165, 167,230,233,239 Mersereau, J . D., 144 Metcalf, R. L., 174, 230 Metzler, K., 366, 382 Middleboe, V , 341, 376 Middleton, J. T., 112, I 15, 120, 122, 123, 127, 128, 131, 132, 133, 134, 142, 143, 144, 145 Miears, R. J., 341, 381 Mikkelsen, D. S., 28, 47, 313, 341. 345, 376, 380 Miles, J. R. W.. 177, 187, 189, 236, 239 Millbank, J. W., 380 Miller, D. E., 201, 234 Miller. M. D., 28, 47, 242, 310 Miller, P. M., 214, 238 Miller, P. R., 112, 133, 143, 144 Miller, P. W., 133, 143 Miller, R. H.,91, 97, 99, 109 Miller, V. L., 112, 143, 207, 235 Mills, A. C., 149, 152, 153, 154, 157, 236 Milne, G., 54, 8 7 Miskin, K., 334. 335 Miskus, R. P., 185, 237 Mitchell, J. W., 93, 99, 100. 109 Mitchell, W. G., 187. 229 Mitsuhashi, N., 291, 311 Mitsui, S., 273, 304, 313, 350, 380 Miyake. K., 305.313 Miyasaka. A., 294, 310 Moberg, E. L., 364,380 Mohamed, A. H , 124, 143 Mohta, N. K , 342,377 Mollenhauer, H. H., 91, 93, 94, 109 Monteith. J. L., 285, 313 Moomaw, J C . , 246. 248, 298, 306, 313, 314, 315. 375,382 Moore, B., 172, 237 Moore, D. E., I5 I , 231 Mora, C. R., 352, 379 Moreland. W. B., 113. 114. 145 Morley, H. V., 187, 190, 240 Morooka, H., 303, 314 Morre, D. J., 91. 93, 94, 109 Morris, H J., 2 14, 237 Morrison, F. O., 184, 229 Morrison, R. B., 52. 87 Mortan, D. J., 352. 378 Mortensen, J. L , 343, 382

397

AUTHOR INDEX

Mortimer, C. H ,381 Mortland, M. M.. 149, 151, 1 5 2 , 155, 174, 179,237, 380 Morton, H. L., 165, 239 Moseman, J. G., 28, 48 MOSS. D. N., 3 18. 322. 323. 324, 326. 328, 332,335, 336 Moss. P., 196, 232 Moss, R. P.. 59, 87 Mountain, W. B., 345, 377 Muller. D., 279. 313 Mukammal. E. I.. 130, 143 Mukherjee, H. N., 303, 313 Mukherjee. P. N., 370, 380 Mulcahy, M. J., 52, 5 5 . 65, 66, 68, 78, 87, 88 Munck, L., 19.48 Munnecke, D. E., 172, 207,237, 239, 344, 345,380 Murakami. T., 310 Murata, Y., 279, 280, 185, 294. 310, 313, 325,336 Murayama. N.. 256. 270.313, 314 Murphy. R. T., 187,229, 237 Murray, D. S., 199. 237 Musgrdve. R. B., 322. 323, 335, 336 N

Nagai, I., 242, 313 Nagai, M., 269, 313 Nagarajah. S., 34 I , 380 Nagato. K., 270, 313 Nakata, K., 270, 313 Nakata. M., 345, 378 Nakaya, H., 313 Narashimha lyengar. B., 313 Narita, S., 272. 311 Nash. R. G.. 162, 163, 177. 198, 216. 222. 229, 233,235, 237 Navarrao. L., 176,231 Navasero. S. A.. 249, 251, 269. 305, 314, 315 Nearpass, D. C.. 149, 151. 153, 237 Neliubov, D., I 12. 143 Nelson. L. A., 76, 78, 80, 85. 86 Nelson. L. B., 358. 380 Ness, A. 0.. 5 5 , 87 Nettelton. W. D., 61, 76, 77, 86 Newbold. T. J., 53, 87

Newland. L. W., 149. 190. 236, 237 Nielsen. K. F., 348, 354, 380 Nimmo, W. B., 181, 204,239 Nishida, K., 294,313 Nishihara, N., 256, 257. 258, 311 Nishihara. T., 345, 351. 355, 357,378,380 Noble, W. M., 112, 118. 125, 126, 127, 129, 134, 142 Nobs. M. A., 328,335 Noguchi. Y., 301,313 Nommik. H.. 347, 356,380 Nomoto, K., 273,313 Northcote, K. H., 52, 5 5 , 61, 8 7 Norton. E. A., 8 7 Nowakowski, T. Z., 353. 354, 380 Nozaki, M., 270.314 Nye, P. H., 5 5 . 87 0

Oakes, A. J., 29, 48 Oakes. G., 33. 48 O'Bannon. J. H., 164,237 Obien. S. R., 159, 181, 220. 233, 237 O'Brien, D. G., 92, 93, 109 O'Brien, R. D., 170, 174, 231, 237 Obuchowski. I., 217. 237 Oddson, J. K , 160,237 Oertli. J. J.. 131. 143, 374, 379, 380 Oeser, A., 324, 336 Ogami, H., 291, 312 O'Gara. P. J., 136. 143 Ogata. T., 362, 363, 380 Ohira, K., 272, 311 Ohnishi. Y., 304, 305. 315 Oka. H., 282.313 Okajima. H., 270, 272, 273. 274,313, 314 Okamoto, Y., 270. 304. 313, 314 Okawa, K., 304, 313 Okuda. A., 304, 305.313, 340,380 Olien. C. R., 28, 48 Ollier, C. D., 5 5 , 61. 87, 88 Olson. F. R., 378 Ordin, L.. 133. 143 Osgerby. J. M., 152. 160. 217. 230, 232 Oshima, M.. 269, 270,313 Oshima, Y., 378 Ospenson. J. N., 150. 151. 239 Ost, H., I I I , 112, 143 Ota, Y., 271, 313

398

AUTHOR INDEX

Otsuka. H., 150. 229 Otsuki, K , 272, 311 Otten, R. J., 343, 344, 380 Otto, H W., 123, 124. 128, 141, 143 Otto, S., 172. 173. 231 Overqtreet, R., 108 Ozaki. K., 298, 313 P

Pack. D. E., 150, 15 I , 239 Pack, D. H., 114, 143 Pack. M. R., 118. 119, 142, 144 Palace, G . A., 252, 258, 314 Panse. V. G., 306,313 Pape. B. E., 167, 169, 237, 240 Papendick, R. I., 165. 240 Parameter, J. R., Jr., 112, 133, 143, 144 Pardue, J. R., 169, 237 Parish, D H , 352. 381 Park, C. S., 306, 313 Park, J. R., 306, 313 Park, Y D., 302, 313 Parker, B. L , I9 I . 231 Parkinson. D , 9 I , 95, 109 Parochetti. J . V.. 164, 168, 233, 237 Paw. J. F.. 165, 240, 342, 358, 366, 381, 382 Parsons. R. B., 5 5 . 86.87 Patchett, G. G., 178, 191, 236 Patel, G. J., 345.380 Patnaik, D., 306,310 Patnaik, S., 296,314, 341,376 Patrick, W. H ,Jr.. 340, 341, 350. 351,355, 356. 375,381 Patrick, Z. A., 123. 143 Pattanaik, S., 302, 303, 313 Paul, J., 313 Paulus, A. O., I IS, 143 Payne, P.. 341. 377 Payne. T. M. B., 105, 108 Payne, W. R., Jr., 151, 181, 237, 238 Peachey. J. E., 345,378 Pearce. R. E., 322. 328, 329, 334, 336 Pearsall, W. H., 340, 381 Pearson. G. A., 304, 313, 314 Pearson, R., 91, 95, 109 Pearson, R. W., 35 I , 377 Pease. H L.. 163. 203. 230, 238 Peck. D. R., 170,237

Peek. J. W., 334,336 Pencheva, L. A., 374. 381 Pendleton, R. L., 53, 88 Pendleton. J. W., 3 18, 333, 334. 336 Penny, A,, 339, 348. 349. 353, 361, 362. 364.378, 383 Perkins, I., 122, 133. 141, 143 Perry, P. W., 15 I , 220, 239 Pesek. J ., 340, 383 Peters, D. B.. 334, 336 Petersen, H. I., 378 Peterson, C. A,, I7 I , 237 Peterson, F. F., 74, 75, 76, 86 Peterson, F. J., 341, 351. 355, 356. 375, 381 Peterson, J. R., 220.237 Philen, 0. D., Jr., 150,237 Phillips, R. E., 159,238 Pieters, A. J., 29.48 Pillai, K. M., 306,314 Pinkerton. C., 166,231 Pires. E. G . , 117,142 Playford, P. E., 55.87 Plimmer,J. R., 166, 167, 168. 170, 178, 183, 186,198, 199,103,234,235,237 Polen. P. 6.. 175, 236 Ponnamperuma, F. N., 305,314, 340,381 Pope, J. D., Jr., 151, 181,238 Povilaitis. B., 124. 144 Powell, R., 358, 381 Powell, R. G., 93. 107 Powers, W. L., 159. 238 Pozin, M. E., 374, 381 Pramer, D., 203, 2 IS, 229, 237 Prasad, I., 215, 237 Prasad. R., 340, 350, 351, 352. 355, 356, 358,364,370,373,379,381 Pratt. P. F., 343, 374,376,382 Prentice, E. G., 92,93,109 Prescott, J. A., 53,55,87,88 Press, J. M., 176,238 Preston, W. H., Jr., 93, 99, 100, 109 Price. P. B.. 28-48 Priddle, W. E., 205,238 Priestly. J. H., I 12,142 Prill, R. C., 6 I , 88 Pristupa, N. A., 327,336 Probst. G . W., 168. 203, 206. 232, 238 Propst, B. E., 133, 143

399

AUTHOR INDEX

0

Quale, 0. R., I 5 5 , 238 Quastel, J. H., 340, 343, 357, 376, 379, 381 Quirk. W. A,, 381 R

Radaelli. L., 151,238 Radcliffe. E. B., 1 I , 48 Rademacher. B.. 2 18.234 152,238 Radke, R. 0.. Radwan, M. A., 345,381 Radwanski. S. A,. 55.88 Ragab. M. T. H., 198.238 Raghu. K., 190.236.238 Rajale, G. B.. 339, 340. 350. 351. 355, 356, 364. 365. 370, 373.381 Rajamannar. A,, 36 I, 378 Raman, K. V., 155, 179, 237 Ramand. E., 222.238 Ramchandra-Reddy, T. K., 92,93, 100,109 Ramiah, K., 241,306.3 14 Ramirez. E. A., 305.315 Raney. W. A,. 340,381 Rangaswami. G.. 92. 98, 101, 106, 107 Rasmusscn, D. C., 334. 336 Rasrnusson, H. P.. 326. 335 Ravinowitch, E. I . , 293. 314 Rawlins, W. A,, 187, 240 Raymond. L. W.. 54. 87 Reddy, G . R.. 356, 357. 381 Redemann, C. T., 354. 381 Reeve, W., 93. 99. 109 Reick, W. L.. 199. 237 Reid. D. A,. 28. 48 Reid, F. R., 368, 382 Reiman. B. E. F., 304. 312 Reinert, R. A., I 17. 123, I30.141, 142, 144 Reitz. L. P.. 19. 20. 27. 28. 48 Reuss. K.. 145 Rhodes, M. M.. 325. 336 Rhodes, R. C., 163, 200,205,231,232,238 Rich. S., 112, 133, 144, 214, 238 Richards, B. L.. 112. 144 Richardson. L. T., 2 13. 2 14, 238 Richter. M.. 91,93.96,98, 106, 109 Rieck. C. E.. 159. 160. 231 Riecken. F. F., 61. 88 Ries, S. K., 206, 235

Riggan, W. B., 134, 144 Rindt, D. W., 37 I , 381 Ripperton. L. A., 112. 141 Rishi, A. K , 361, 377, 378 Robbins. W. R., 112, 143 Roberts, J . L., 378 Roberts, R. N., 196, 236 Robertson. R. N.. 90, 108 Robinson. B.. 344. 382 Robinson. J. B., 344. 378 Roche, P., 306, 315 Rodrigo. D. M., 305, 314 Roeth. F. W.. 181, 218. 238 Romanowski, R. R., Jr., 222. 229 Rosefield, I., 178, 179, 232 Rosen, J. D.. 169. 203. 238 Rosenfield. C., 175, 238 Ross, J. A,, 200, 239 Ross, L., 352. 381 Ross, M., 214, 229 Ross, R. W., I I , 48 Ross. W. M., 27.49 Rothberg, T., 149, 150. 151, 156, 229 Rouatt, J. W., 105, 108 Rovira, A. D., 89. 90. 9 I , 92. 93, 96. 101, 102, 106, 108, 109 Rowe, P. R., I I , 48 Roy, R. N., 339. 381 Ruhe. R. V., 5 2 , 53, 5 5 , 58, 61, 62. 63, 65, 70. 7 1 . 72, 74, 7 5 , 76. 88 Runeckles, V C., 92, 96, 109, 123, 143 Runyan. R. L., 160,239 Russell. J. D., 151, 155, 181.238 Ryesson. K. A,. I ? , 48 Ryland. L. B.. 176, 232

S Sabey. B. R.. 348, 349, 355, 356. 381 Sahadevan, P. C., 310 Sahu. B. N., 342,381 Sakai. S., 379 Salandanan. S.. 340. 379 Salutsky, M. L.. 369. 376 Sanchez, P. A., 338, 339,381 Sandford, J. 0..341. 376 Santelmann. P. W., 159, 160, 230, 231 Santovich, S. A., 92. 109 Sarin, M. N., 2 5 2 , 310 Sasamoto, K.. 305, 314

400

AUTHOR INDEX

Saschenbrecker, P. W., 185, 231 Sato, K., 270, 314 Saunders, P. J. W., 133. 144 Sawyer, W. M.,176,232 Saxena, H K., 305,313 Scarbrook. C. E., 36 I, 381 Schecter, M. S., 176, 230 Schectman, J., 171, 230 Scheffer, F., 366, 381, 382 Scheffer, T. C., 133, 144 Schmidt, E. L., 91, 95, 98. 99, 109, 198, 230 Scholefield, P. G., 343, 357,376, 381 Scholl, W., 368, 382 Scholtes, W. H., 52, 53, 5 5 . 58. 63, 88 Schreiber, M. M.,343, 344, 380 Schroeder, M.,199, 238 Schroth, M. N., 9 I , 92. 104, 105, 109 Schubert, B. G., 35, 47 Schuetz, R. D., 169, 240 Schulz, K. R., 187, 191, 192. 235 Schulz-Schaeffer. J., IS, 43. 48 Schiitte, H. R.. 174, 238 Schwalm, H. W., 112, 143 Schwartz, H. G., Jr., 153, 238 Sciaroni, R. H., 373, 377 Scifres. C. J., 164, 238 Scott, D. C., 220, 238 Scott, G. D., 9 I , 109 Scott, H. D., 159,238 Scott. W. E., 112, 144 Seager, W. R., 7 I , 8 7 Seaholm, J . E., 34 I , 381 Seaton, G. A., 34. 49 Sechler, D., 122, 144 Segal, W.,377 Seif. R. D., 334, 336 Seigworth, K. J., 112, 144 Seliskar, C. E., 123, 141 Selman, F. L., 165, 239 Sen, G . , 93,107 Sen Gupta, A. K., 169, 235 Serratosa. J. M.,150. 238 Sethunathan, N., 178, 190, 238 Setterstrom, C., 126, 144 Shands, R. G., 28.48 Shanks, C. H., Jr.. 191, 232 Sharabi, N. El-D., 202, 238 Sharma, A. C., 342,379 Sharma, K. C., 342.382

Sharma, S. K., 342, 377 Shattuck, G. E., Jr., 346, 348, 382 Shaw, K., 340,376 Shaw. W. C., 28,47, 48 Shaw, W. M.,344.382 Shcheglova, G. M., 376 Sheets, T. J., 172, 198, 200, 204, 216, 219, 233, 234, 235, 238 Sheffer, F., 91,93,96,98, 106,109 Shepherd, L. N., 345,383 Shibles, R. M., 329, 335 Shiori, M., 302, 314 Shiraishi, K., 256, 314 Shrikhande, J. C., 344, 378 Shropshire. W., Jr., 125. 141 Siedman, G . , 131, 133, 134, 144 Siewierski, M., 203, 238 Silber, G., 133, 144 Sims, J. L., 252, 258,314 Simsiman. C. V ,375,382 Simsiman, G. V., 306,314 Sinclair, W. A., 128. 141 Singh, H., 344. 382 Sinha, M. N., 370, 381 Sinha, N. S., 344, 382 Sircar, S. M.,252. 314 Sister, H. D., 207, 234 Skinner. W. A., 205,238 Skipper, H. D., 198, 238 Skirde, W., 367, 382 Skogley. C. R., 382 Skrdla, W., 33. 48 Skyring. G. W., 338, 340,379, 382 Slack. A. V , 374,382 Slack, C. R., 294, 311, 325, 327, 335, 336 Slankis, V , 92, 96, 109 Slope. D. B.. 213, 238 Smale, B. C., 93. 100, 109 Smith, A. E., 168, 231, 238 Smith. D. T., 160, 206. 238 Smith, G. E.. 333, 336 Smith. J. B., 342. 382 Smith, J. W., 204, 238 Smith, N. R., 343, 382 Smith, R. J., Jr., 28, 47 Smith, R. S., 8 7 Smith, S., 165. 240 Smith, V K., 166. 238 Snelling, K W.. 159, 238 Soboczenski, E. J., 205,232

40 1

AUTHOR INDEX

Soga, Y.. 270.314 Solberg, R. A., 207. 239 Solomon, D. H., 175. 238 Soubies, L.. 356, 357. 382 Soundarajan. R., 36 I . 378 Sowell, G., Jr., I I . 48 Spanis. W. C., 207. 239 Speer, R. C., 362, 367, 370, 376 Spencer, E. Y., 171,239 Spencer. W. F . , 165.231, 234, 239 Sperber, J. I., 101. 109 Spratt, E. D., 353, 382 Spurr, A. M. M., 55.88 Sreenivasan. A., 340,382 Srivastava, S. P., 339, 382 Staccioli. G.. 153. 236 Stahlin, A., 382 Stallard, D. E., 205. 238 Stanford. G.. 36 I. 362, 377 Stanton, T. R., 28. 48 Stapp, C., 343, 382 Stark, F. L., 342. 382 Stark. R. W., 133, 144 Starkey. R. la.,377 Starostka, R. W., 369, 376 Steelink, C., 179, 239 Steggerda. J. J., 362. 377 Steinberg, R. A,. 92. 95. 109 Stenersen, J. H. V., 184. 239 Stenlid, G., 107. 109 Stephan. U.. 174, 238 Stephens, C. G.. 55,87, 88 Stephens. E. R., I 12. I 18, 144 Stephenson. H. F., 368. 378 Sterling, L. D.. 340, 376 Stern, A. C., 114. 144 Stetler. D. A., 326. 335 Stikler. R. L., 220. 239 Stinson, H. T.. 3 18, 336 Stojanovic, B. J., 340. 344, 376, 383 Stolzy. L. H., 132. 144 Stone. G. M.. 231 Stoner, W. N., 307. 311 Storrs. E. E., I8 I , 230 Stoy. v.. 294, 314 Strain, W. S., 7 I , 87 Stratrnann. H., I 15, 119, 126, 136. 141, 145 Street, H E., 92, 109 Streim, H. G., 173. 232

Stringer, A., 170. 240 Stringer. C. A.. 177, 189. 230 Subba Rao, N. S.,92, 102,109 Subrahrnanyam, V , 340, 382 Sugawara. K., 270. 313 Sullia, S. B., 92.93, 100,109 Sullivan, F., 122. 124, 141 Sun. Y. P., 176, 232 Suneson, C. A., 28.48 Sutcliffe, J. F., 90, 91, 109 Sutherland. D. J., 169. 238 Swain, F. G., 2 12, 230 Swaminathan. M. S., 340. 382 Swezey, A. W.. 352.382 Swift, J. D.. 175, 238 Swithenbank. C., 179, 240 Syers. J. K., 22 I , 234 Szabo, I., 382 Szuszkiewicz. T. E.. 132, 144 T

Tagawa. K.. 304,314 Tai, A.. 187, 188. 236 Tainton, N. M., 325, 335 Takagi, S., 270, 272, 314 Takagishi. H.. 360. 378, 382 Takahashi. E., 304, 305,313, 340, 380 Takahashi. J., 256, 307, 314 Takahashi, N., 270, 272, 314 Takato. H., 304, 313 Takeara, S., 270,313 Takeda, T., 279. 280,314 Takeyoshi, E., 241. 314 Talbert, R. E., 150, 160,239 Tanaka. A., 243, 244, 245, 247. 249, 251. 253. 254. 255. 256, 259, 260. 261. 262. 263. 264, 265. 266, 267, 269, 270. 282. 283, 288. 289, 290, 292, 293. 294. 296, 299, 300, 302, 303, 309. 312, 314, 315, 3 19,336 Tang, C.-S.. 167, 239 Taylor. A. W., 370. 382 Taylor, G. S., 131. 133, 143, 144 Taylor, H. F., 195, 239 Taylor, 0. C., 112. 117, 118. 119, 120. 123, 124, 125. 126. 132, 133. 134, 139, 141, 143, 144 Teasley. J. I., 151, 181, 238 Teater. R. W.. 343, 382 Tepe, J. B., 168. 203, 238

402

AUTHOR INDEX

Terasawa, S., 273, 313 Turner, N . J., 173, 239 Terman, G. L., 312, 338, 339, 362. 366, Turton. A. G., 55, 88 369, 370, 372, 373, 376, 377, 380, 382 Tweedy, B. G., 200, 215, 236, 239 Tewfik. M. S., 215, 233 Tysdal, H. M., 29, 48 Thomas, J. R., 374. 378 U Thomas, M. D , 112, 128, 144, 319. 321, 322.336 Uljee, A. H., 214, 239 Thompson, C. R., 117, 126, 134. 139, 141, Upchurch, R. P.. 155. 156, 165. 214, 239 144 Upliani, C., 356,382 Thompson, J. M , I8 I , 239 Ushioda, T., 360,382 Thorn, G. D., 173.236 V Thorne,G.,212.232 Thornton, R. H., 92, 94. 96, 98. 104, 107 Valezuela Calahorro, C., 159, 176. 236 Thorpe, J., 52.88 Vanachter, A., 2 IS, 239 Thysell, J. R., 28.47 Vancura, V., 91, 96, 98, 104, 105, 109 Tiedje,J. M , 177, 196,231,239 Van de Goor. G . A. W., 315 Tillett, E. R., 345, 382 Van Der Kerk, G. J. M., 206. 234 Ting, I. P., 125, 134, 135, 136. 139. 141, Van Dijk, D. C., 5 5 . 8 8 144 van Haut, H., 115, 119, 126. 136, 141, 144, Tingey, D. T., 117. 123, 130, 141, 144 145 Togari, Y.. 270, 314 Van Raalte, M. H., 273,315 Tokuoka. M.. 303.314 Van Valkenburg, J. W., 175, 238, 239 Tolbert, N . E., 324, 325, 336 Vavilov, N . I., 9. 25,28. 49 Tollen. G., 179, 239 Velasco. J. R., 306, 311 Tomerlin, A. T., 164, 237 Velly, J.. 306. 315 Tomlinson, T. E., 150, 151. 153, 168. 230, Venkateswarlu, J., 341, 377 235 Verduin, J., 32 I , 323, 336 Toth. S. J., 152,236 Vergara, B. S., 246. 248, 313, 314 Trademan, L., 175,236 Verloop. A., 18 I , 204. 239 Transtrum. L. G . , I 18,142 Verma, S. S., 306, 315 Tregunna, E. B., 294, 311, 325. 326, 327, Vernetti. J.. 154, 232 328. 334, 335 Viade, H. C., 219. 236 Treshow, M., 118, 119, 133, 142, 144 Viado, G . B., 174, 231 Trichell, D. W., 165. 239 Vickery, L. S., 123, 143 Trolldenier, G., 102, I09 Vinall, H. N., 29. 49 Trowbridge, A. C., 58, 88 Vlitos. A. J., 172. 239, 326. 335 Tseng, H. D.. 306,311 Voerman, S., 162, 239 Tsoy. C. T., 340.383 Voinov, M. I . , 96. 108 Tsuneyoshi, Y., 345, 351, 355, 357,380 Voitekhova, V A., 239 Tsunoda, S., 279, 280,314 Volk, G. M., 340, 342, 379, 382 Tu. C. M., 177, 187, 189, 236, 239 Volk, R. J., 293. 305. 312, 315, 324. 335 Tucker, B. M., 52, 61. 8 7 Volk,V. V., 151,235 Tucker, B. V., 150, I 5 I , 239 von Endt. D. W., 183, 201, 205, 234, 235, Tucker, W. P., 177, 230 237, 239 Tukey, H. B., Jr., 91. 109 von Schroeder, J.. 145 Turkhede, B. B., 340, 351. 352, 381 W Turner, B. C., 159, 160, 163. 167, 234 Turner, F. T., 351, 355. 356, 381 Waddington, D. V., 364, 380 Turner, G . 0..348. 352.382 Waggoner, P. E., I3 I , 144

AUTHOR INDEX

Wain, R. O., 195. 239 Wakabayashi, K., 369,382,383 Walker, A,, 152. 158, 159, 239 Walker, E. K., 133, 14.5 Walker, G. F., 175. 239 Walker, P. H., 5 5 , 88 Walker. W. W., 344, 383 Wall, J . S., 27, 4 9 Wallace, D. H.. 330. 335 Wallihan, E. F., 298. 315 Walling. C.. 175. 239 Wallnofer, P., 200. 239 Walsh, L. M.. 166, 221. 234 Walton, M. S., 184. 236 Wanta, R. C.. 113, 114. 133, 145 Ward, D. J., 20. 23, 48, 49 Ward, T. M.. 155. 156, 181. 239, 240 Ward, W. T., 55.88 Warder, F. G., 354, 380 Wardlaw. I . F.. 325. 335 Ware, J. H.. 358. 376 Warren,G. F., 152, 153, 164,220,231,233, 23 7 Warren. L. E., 348. 382 Watanabe. I., 350, 380 Watson, D. J . , 333. 336 Watson, G. A., 340, 383 Watson, J . P., 5 5 , 88 Wayne, L. G.. I 13, 142 Webb, B. D., 28. 47 Webb, R. E., 33, 49 Weber. J. B.. 150. 151, 156, 157, 181. 220, 237,238,239,240 Webley. D. M.. 101, 108, 195. 240 Webster. C. C., 113, 14.5 Wedemeyer, G., 185, 240 Weed. S. B., 150. 151, 156, 157, 181, 220, 237, 239, 240 Weeks. L. V , 160, 237 Weibel R. 0.. 3 18. 336 Weidensaul. T. C., 116. 143 Weierich. A. J., 163. 172. 232, 233 Weinhold, A. R.. 91, 92. 105. 109 Weinstein, L H , 119, 140, 142, 145 Weir, C. C.. 338, 339. 356. 383 Weiss. M. G.. 25. 49 Welch, L. F., 378 Wells, J. P., 307. 311, 315 Wen, H. P., 344. 383

403

Weng. W. P.. 340. 383 Wengel. M. E., 343, 382 Wenseley, R. N., 342,383 Went. F. W., 118. 125. 126, 127, 128, 131, 134, 135, 142, 143 West, P. M., 9 I , 93, 109 Westerman, R. L., 362, 383 Westlake, W. E., 169, 177. 229 Westover. H. L., 29, 4 8 Wetzel, R. G., 96. I 0 9 Whalley, R. D. B., 348, 3 7 9 Wheeler, W. H., 76, 77, 8 6 White, A. W., 165, 229 White, E. R., 17 I , 235 White, G. A., 35, 36, 47, 49 White, J. L.. 149, 150, 151. 152, 154. 155, 156, 161, 181,229,230,238 White, W. C., 340,383 Whitehead. D. R., 78,88 Whitehouse, W. E., 34,49 Whiteley. E. L., 36.49 Whiteman, P. T. S.. 375.376 Whitney, W. K., 191,240 Whittingham, W. F.. 186,229 Widdowson, F. V , 339. 353, 361. 383 Widofsky, J. G., 354, 381 Widtsoe, J . A,, 112, 145 Wiebe. G. A,, 28, 48 Wildung. R. E., 205, 240 Wilhour, R. G., 128. 145 Wilkinson, A. T. S., 187, 240 Wilkinson, V., 213, 240 Williams, C. H., 383 Williams, C. N., 325, 335 Williams. I. H., 180, 240 Williams, J. D. H., 152, 240 Williams, R. J. B., 339, 353, 361,383 Williams, W. A., 285, 313 Willis. G. H., 165, 240 Wilms, W., 91,93,96,98, 106, I09 Wilson, D., 329, 336 Wilson. J . K.. 92, 93. 109 Winfree. J . P., 345,383 Winnett, G., 203, 238 Winsor, G . W., 360, 361,379, 383 Winter, S. R., 333. 336 Winters, H. F., 35. 4 7 Wit, C. T., 306, 315 Witts, K. J., 333. 336

404

AUTHOR INDEX

Wittwer, H., 289, 311 Wolcott, A. R., 345, 380, 383 Wolff, I . A., 35, 4 8 Woltz, S., 91, 95, 109 Wong. N., 177,231 Wood, D. L., 133, 144 W o o d , F . A . , 112, 113, I 2 I , 1 4 5 Woodcock, D., 170, 195, 230, 232, 240 Woods, F. W., 92, 109 Wooldridge, S. W., 85, 88 Woolnough, W. G., 54, 88 Woolridge, W. R., 340. 377 Woolson, E. A., 162, 163, 186, 218, 221, 233,235, 237, 240 Worsham, A. D., 343, 383 Wright, A. N., 180, 192, 193, 205, 230 Wright. R. L., 5 5 . 60. 88 Wyatt, R.. 340, 381 Y

Yaalon, D. H., 62, 86 Yaffe, J., 175, 240 Yakobsin. G. A., 96. 105. 108 Yamada, N., 271,313 Yamaguchi, F. T., 370, 379 Yamaguchi, J., 249, 25 I , 269, 292, 294, 314, 315, 3 19,336 Yarnaguchi, S., 93, 99, 108 Yamaguchi, T., 315 Yamamoto, Y., 246, 312 Yamane, I., 340,383 Yamane, V. K., 149, 159. 233

Yamasaki, K., 269. 315 Yamasaki, T., 302. 315 Yamazaki, R. K., 324, 324,336 Yanai. T., 256, 314 Yang. S. C.. 311 Yarwood. C. E.. 133, 145 Yen, D. E., 17.49 Yeo, J. Y., 177,230, 368,377 Yih, R. Y.. 179, 240 Yoshida, M., 314 Yoshida, S., 304, 305. 312, 315 Yoshida. T., 190. 2 17. 238, 240 Yoshino. M., 256, 270, 313 Yoshinouchi. K., 363, 380 Yost, J. F., 175. 240 Young. H. C.. 177,230 Young. R. A., 2 13.231 Young, W. R., 187. 240 Youngson, C. R., 150. 152,233 Yount. J . B., 203. 237 Yuan. W. L.. 305.314 Yule, W. N., 190. 240

Z Zabik, M. J., 167, 169, 184, 230, 237, 240 Zahn. R., 126. 137, 145 Zahnley, J. W., 379 Zaitlin. M., 112. 129, 142 Zelitch, I., 324, 336 Zimmerman, P. W.. 112. 118. 119, 126. 142, 143, 144, 145

SUBJECT INDEX A

Crambe abyssinica, 36 Crested wheatgrass, 338 Crop ecology, rice, 246-252 Crotonylidenediurea, 366-367 Cucumber, 3 I Cyanoguanidine, 356

Acaricide, I79 Agropyron elongatum, 30 Air pollutants, plant response, I 1 1-145 Aldrin, 168, 186, 344 Alfalfa, 8, 22, 30. 32 I , 329 Algae, 2 I5 Amiben, 150, 205

D

2,4-D, 150, 151, 153, 167, 172, 194. 196, 2-Amino-4-chloro-6-methylpyrimidine, 213, 215, 343 355-356 Dalapon, 200, 2 13, 343 4-Amino-3,6-trichloropicolinic acid, I00 Damping-off, 2 14 Amitrole, I5 I , 344 Dazomet. 172, 213 Ammonia, 340, 35 1 DDT, 162, 166, 168,175. 182-186,222 Apple, 321 Desert soil, 70-76 Atrazine, 153, 180, 215. 220 Diazinon, 177, 178, 190 Dicamba, 100, 150, 165, 204 B Dichlobenil, 204 Barley, 18, 19, 23. 28, 213, 301, 329 Dichlone, 149 Bean, 31 2,4-Dichlorophenoxyaceticacid, 99 Binapacryl, I70 1,3-Dichloropropene, 179 Bluegrass, 125, 127 Dicyandiamide, 356-357 Boron, 303 Dieldrin, 162, 165, 166, 176, 186, 2 19, 222, Breeding, photosynthetic response, 327344 334 Digitaria, 29 Bromacil, 205 Dinitroanilines, 203 Bromegrass, 29, 338 Dioscorea spp., 17, 35 Bromus biebersteinii, 29 Dipropalin, 203 Buffelgrass, 12 Diquat, 150, 151, 152, 168, 204 Diuron, I8 I , 199, 343 C Carboxin, I74 Chlorarnben, 220 Chlordane, 176, 186 Chlorine, 304 Chloroneb, 207 2-Chloro-6-(trichloromethyl)pyridine,348354 Chrysanthemum, 95 Cocoa, 16 Coffee urabica, 1 I , 16 Copper, 302-303 Corn, 22, 372 see also maize Cotton, 361

E Endrin, 177, 186, 222 EPTC, 151, 172 F

Ferbarn, 206, 2 I5 Fluoride, I19 Formetanate, 179 Functional unit, plant, 263 Fungicides, 169, 174. 206-208,344-345 G

Geomorphology, 5 1-88 Germ plasm, plant, 1-49

405

406

SUBJECT INDEX

Gibberellic acid, 100 Growth analysis, 243-252 Growth efficiency, rice, 29 1-293 Guanylurea, 365-366 H

Heptachlor, 176, 186, I87,2 14,222,344 Herbicides, 97-101, 167-168, 193-206, 343-344 see also individual compounds Hibiscus cannabinus, 36

N

National Seed Storage Laboratory, 39-43 Nitralin, 203 Nitrification retarders, 337-358 Nitrogen, 101, 105. 118, 132. 215, 282. 295-298, 305 slow-release fertilizers, 337, 358-375 Nitrogen dioxide, 1 13. 1 19-1 20, I29 N-Serve, 348-354 Nutrient absorption, rice, 252-262 0

I

Imidan, 178 Insecticides, 168-169, 182-192, 344 see also individual compounds Ipomoea batatas, 17 Iron, 301-302 Isobutylidenediurea, 363-365

Oats, 18, 19, 23, 28, 122 Onion, 123 Oryza sativa, 28 1 Oxamide, 361-363 Ozone, 112, 117-118, 123, 128, 131, 132, I36 P

K Kaolinite, 150, 151, 153, 175, 176 Kenaf, 36 1

Laterite, 53-55, 65 ’ Lindane, 162, 165. 190 Linuron, 151, 152, 162, 181, 199, 222 Loess, 62-65 Lolium multiJorum, 29 Lolium perenne, 329 Lycopersicon esculentum, 32 M

MagAmp, 369 Maize, 8, 13. 25-26, 152. 177, 192, 318, 322-323. 324, 325 326, 330, 361, 374 Malathion, 152, 177, 192 Manganese, 302 MCPA, 213 Mercurials, 207-208 Metham, 172. 213 Microorganisms, pesticides, I8 1-208, 342345 Molybdenum, 303 Montmorillonite, 150, 151, 153, 156, 174 Monuron, 21 3, 343 Mycorrhiza, 208

PAN, 113, 118-1 19, 125. 134, 139 Paraquat, 150, I5 I , 152,204,2 I3 Parathion, 160, 162, 170, 190 PCNB, 206 Pennisetum, 29 Pennisetum ciliare, I2 Pentachloronitrobenzene, 206 Pepper, 1 1 Pesticides, soil behavior, 147-240 Phalarisgrass, 102 Phaseolus, 3 I , 45 Phenylcarbamates, 20 1 Phenylureas, 167, 199-200 Phorate, 191 Phosphate, 102 Phosphorus, 101, 298-301 Photodecomposition, pesticides, 166- 169 Photoperiod, 125 Photorespiration, 293 Photosynthesis, crop production, 3 17-336 Picloram, 100, 150, 153, 164, 165, 167 Picolinic acid, 100 Pine, 101 Pinto bean, 125. 126, 127, I3 I , 134, I36 Pinus strobus, I23 Pisum sativum, 32 Plant germ plasm, 1-49 Plinthite, 81-84 Ponderosa pine, 133

407

SUBJECT INDEX

Potato, 8, 15, 122, 321 Propanil, 202, 2 I5 Propham, 343 Proximpham, 17 I Pyrazon, 205 R

Rhizobium, 208, 2 10 Rhizosphere, 93, 273 Rice, 8, 18, 28, 43, 44, 202, 319, 333 338, 35 I, 357,361,364,366,373,374 physiology, 24 1-3 I5 Root exudation, 89- 109 Rye, 22. 28 Ryegrass, 29, 353, 362. 365. 366, 367

T

2,4,5-T, 150, 165, 194 Temperature, air pollutants, 127- I28 Terbacil, 205 Thiourea, 345. 348, 357-358 Tillers, 266, 267, 269-270 Tobacco, 95, 123, 124. 127, 128, 129, 131, 135, 136, 324 Tomato, 32, 102 Translocation, 267, 287-29 I Triazine, 99, 152, 153, 156, 167, 181, 198, 344, 345, 368-369 Trifluralin, 203 Toxaphene, 166, 176 U

S

Sesone, 172. 194 Silicon, 304-305 Simazine, 153 219, 344 Soil moisture, air pollutant interaction, I3 1-132 stress, 105 Soil morphology and genesis, 5 1-88 Soil, pesticides, 147-240 Solonetz, 65 Sorghum, 8, 22. 26-27, 323, 354 Soybean, 8, 130, 329 Subterranean clover, 3 I8 Sugar beet, 32 I , 326, 35 1 Sugarcane, 323, 324 Sulfur, 102 Sulfur dioxide, 112, 119, 123, 126, 129, 133 Sweet corn, 35 I Sweet potato 17

Urea, 340, 352, 357, 372, 374 Urea-acetaldehyde, 366 Urea-form, 358-361 V

Vermiculite, 150, I5 I Verononia anthelmintica, 35 W

Wheat, 8, I I , 18, 19, 23, 27-28, 321, 354. 367 WhIre pine, 123, 128 Y

Yam, 17 2

Zinc, 303 Ziram, 206

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