Salmon Lice

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Salmon Lice An Integrated Approach to Understanding Parasite Abundance and Distribution

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Salmon Lice An Integrated Approach to Understanding Parasite Abundance and Distribution Edited by

Simon Jones Richard Beamish

A John Wiley & Sons, Ltd., Publication

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This edition first published 2011, © 2011 by John Wiley & Sons, Inc. Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’s global Scientific, Technical and Medical business with Blackwell Publishing. Registered office:

John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK

Editorial offices:

2121 State Avenue, Ames, Iowa 50014-8300, USA The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK 9600 Garsington Road, Oxford, OX4 2DQ, UK

For details of our global editorial offices, for customer services and for information about how to apply for permission to reuse the copyright material in this book please see our website at www.wiley.com/wiley-blackwell. Authorization to photocopy items for internal or personal use, or the internal or personal use of specific clients, is granted by Blackwell Publishing, provided that the base fee is paid directly to the Copyright Clearance Center, 222 Rosewood Drive, Danvers, MA 01923. For those organizations that have been granted a photocopy license by CCC, a separate system of payments has been arranged. The fee codes for users of the Transactional Reporting Service are ISBN-13: 978-0-8138-1362-2/2011. Designations used by companies to distinguish their products are often claimed as trademarks. All brand names and product names used in this book are trade names, service marks, trademarks or registered trademarks of their respective owners. The publisher is not associated with any product or vendor mentioned in this book. This publication is designed to provide accurate and authoritative information in regard to the subject matter covered. It is sold on the understanding that the publisher is not engaged in rendering professional services. If professional advice or other expert assistance is required, the services of a competent professional should be sought. Library of Congress Cataloging-in-Publication Data Salmon lice : an integrated approach to understanding parasite abundance and distribution / edited by Richard Beamish, Simon Jones. p. cm. Includes bibliographical references and index. ISBN-13: 978-0-8138-1362-2 (hardcover : alk. paper) ISBN-10: 0-8138-1362-X 1. Lepeophtheirus salmonis. 2. Lepeophtheirus salmonis–Control. 3. Lepeophtheirus salmonis– Geographical distribution. I. Beamish, Richard. II. Jones, Simon. QL444.C79S25 2011 639.3 756–dc23 2011016564 A catalogue record for this book is available from the British Library. This book is published in the following electronic formats: ePDF 9780470961537; Wiley Online Library 9780470961568; ePub 9780470961544; Mobi 9780470961551 R Set in 10/12 pt Dutch801BT by Aptara Inc., New Delhi, India

Disclaimer The publisher and the author make no representations or warranties with respect to the accuracy or completeness of the contents of this work and specifically disclaim all warranties, including without limitation warranties of fitness for a particular purpose. No warranty may be created or extended by sales or promotional materials. The advice and strategies contained herein may not be suitable for every situation. This work is sold with the understanding that the publisher is not engaged in rendering legal, accounting, or other professional services. If professional assistance is required, the services of a competent professional person should be sought. Neither the publisher nor the author shall be liable for damages arising herefrom. The fact that an organization or Website is referred to in this work as a citation and/or a potential source of further information does not mean that the author or the publisher endorses the information the organization or Website may provide or recommendations it may make. Further, readers should be aware that Internet Websites listed in this work may have changed or disappeared between when this work was written and when it is read. 1

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Contents List of Contributors Foreword by Bob Kabata Preface Introduction: Lepeophtheirus salmonis—A Remarkable Success Story Craig J. Hayward, Melanie Andrews, and Barbara F. Nowak

vii xi xiii 1

Part I: The Distribution and Abundance of Planktonic Larval Stages of Lepeophtheirus salmonis: Surveillance and Modeling Chapter 1.

Chapter 2.

Chapter 3.

Chapter 4.

Modeling the Distribution and Abundance of Planktonic Larval Stages of Lepeophtheirus salmonis in Norway Lars Asplin, Karin K. Boxaspen, and Anne D. Sandvik Abundance and Distribution of Larval Sea Lice in Scottish Coastal Waters Alexander G. Murray, Trish L. Amundrud, Michael J. Penston, Campbell C. Pert, and Stuart J. Middlemas Sea Louse Abundance on Farmed Salmon in the Southwestern New Brunswick Area of the Bay of Fundy Blythe D. Chang, Fred H. Page, Michael J. Beattie, and Barry W.H. Hill Modeling Sea Lice Production and Concentrations in the Broughton Archipelago, British Columbia Dario J. Stucchi, Ming Guo, Michael G.G. Foreman, Piotr Czajko, Moira Galbraith, David L. Mackas, and Philip A. Gillibrand

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51

83

117

Part II: Salmon Louse Management on Farmed Salmon Chapter 5:

Salmon Louse Management on Farmed Salmon—Norway Gordon Ritchie and Karin K. Boxaspen

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Chapter 6:

Ireland: The Development of Sea Lice Management Methods David Jackson

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Chapter 7:

Salmon Louse Management on Farmed Salmon in Scotland Crawford W. Revie

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Chapter 8:

Sea Lice Management on Salmon Farms in British Columbia, Canada Sonja M. Saksida, Diane Morrison, Mark Sheppard, and Ian Keith

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Part III: Salmon Lice on Wild Salmonids in Coastal Zones: Present Status and Implications Chapter 9:

Present Status and Implications of Salmon Lice on Wild Salmonids in Norwegian Coastal Zones 281 Bengt Finstad and P˚ al Arne Bjørn

Chapter 10: Lepeophtheirus salmonis on Salmonids in the Northeast Pacific Ocean Simon R.M. Jones and Richard J. Beamish

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Index

331

Color plates appear between pages 50 and 51.

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List of Contributors Trish L. Amundrud Marine Scotland Science Marine Laboratory Aberdeen, Scotland, United Kingdom Melanie Andrews Kinki University Fisheries Research Laboratory Kushimoto, Wakayama, Japan Lars Asplin Institute of Marine Research Bergen, Norway Richard J. Beamish Pacific Biological Station Fisheries and Oceans Canada Nanaimo, British Columbia, Canada Michael J. Beattie New Brunswick Department of Agriculture, Aquaculture and Fisheries St. George, New Brunswick, Canada P˚ al Arne Bjørn Institute of Marine Research Bergen, Norway Karin K. Boxaspen Institute of Marine Research Bergen, Norway Blythe D. Chang St. Andrews Biological Station St. Andrews, New Brunswick, Canada Piotr Czajko Department of Mechanical Engineering University of Victoria Victoria, British Columbia, Canada

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List of Contributors

Bengt Finstad Norwegian Institute for Nature Research Trondheim, Norway Michael G.G. Foreman Institute of Ocean Sciences Fisheries and Oceans Canada Sidney, British Columbia, Canada Moira Galbraith Institute of Ocean Sciences Fisheries and Oceans Canada Sidney, British Columbia, Canada Philip A. Gillibrand National Institute for Water & Atmospheric Research Christchurch, New Zealand Ming Guo Institute of Ocean Sciences Fisheries and Oceans Canada Sidney, British Columbia, Canada Craig J. Hayward Tohoku University Institute for International Education Sendai, Miyagi, Japan Barry W.H. Hill New Brunswick Department of Agriculture and Aquaculture St. George, New Brunswick, Canada David Jackson Marine Institute Galway, Ireland Simon R.M. Jones Pacific Biological Station Fisheries and Oceans Canada Nanaimo, British Columbia, Canada Ian Keith Fisheries and Oceans Canada Courtenay, British Columbia, Canada

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David L. Mackas Institute of Ocean Sciences Fisheries and Oceans Canada Sidney, British Columbia, Canada Stuart J. Middlemas Marine Scotland Science Freshwater Laboratory Faskally, Pitlochry, Scotland Diane Morrison Marine Harvest Canada Campbell River, British Columbia, Canada Alexander G. Murray Marine Scotland Science Marine Laboratory Aberdeen, Scotland, United Kingdom Barbara F. Nowak University of Tasmania National Centre for Marine Conservation and Resources Sustainability Launceston, Tasmania, Australia Fred H. Page St. Andrews Biological Station St. Andrews, New Brunswick, Canada Michael J. Penston Marine Scotland Science Marine Laboratory Aberdeen, Scotland, United Kingdom Campbell C. Pert Marine Scotland Science Marine Laboratory Aberdeen, Scotland, United Kingdom Crawford W. Revie University of Strathclyde Glasgow, Scotland, United Kingdom Gordon Ritchie Marine Harvest Technical Centre Stavanger, Norway

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Sonja M. Saksida British Columbia Centre for Aquatic Health Sciences Campbell River, British Columbia, Canada Anne D. Sandvik Institute of Marine Research Bergen, Norway Mark Sheppard Fisheries and Oceans Canada Courtenay, British Columbia, Canada Dario J. Stucchi Institute of Ocean Sciences Sidney, British Columbia, Canada

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Foreword Ever since humans emerged in the primordial past as a distinct species, they sustained their populations in the manner that we referred to as hunter gatherers. In short, they lived as best they could, by utilizing what nature could provide. This was sufficient for as long as the human populations were small enough to survive on the stores of natural products, both plant and animal. As the populations increased in size, this way of providing the necessities of life was no longer satisfactory. The hunter gatherers slowly became farmers. Species of useful animals, too many to mention them all, were domesticated. Plants providing staple food were planted and harvested. Even some freshwater fish, able to be confined in small-scale environments, were cultivated. Only one branch of this general development remained outside the scope of change: marine fisheries. Let us face it: marine fishermen are the last survivors of the hunting gathering economy. Physically barred from the environment inhabited by the species they hunt and gather, faced with the enormous size of that environment, they pursue the object of their hunt in the manner still akin to the old hit-and-miss way of their ancestors. Their methods have vastly improved, and their hunts began to provide truly bountiful returns. Some Russian experts estimated that marine fisheries yielded annually as much as 100,000 tons of fish during the last few decades. This kind of drain on the resource could not continue indefinitely. It had to be reduced, if the stocks of marine fish were to survive. Slowly, the large, long-distance fishing fleets began to disappear, and restrictions on the size of catches had to be introduced. Finally, the inevitable happened. The first attempts at marine fish farming came into being. Salmon farms arrived at the scene. As might have been expected, the initiation of husbandry, in addition to obvious benefits, brought with it a range of problems and controversies. Husbandry creates high-density populations of the husbanded species. Interactions of individuals in such populations facilitate exchanges between them, including the spread of diseases and parasites. Such effects have not been unknown in dense populations of husbanded land animals. Salmon farms are not exempt. Dense populations of farmed salmon are plagued with a number of parasites, the most notorious of which is a so-called sea louse, a caligid copepod Lepeophtheirus salmonis, capable of reaching high intensity and prevalence of infection. The farms are not isolated. They occupy limited parts of the environment, which they share with the wild populations of the same species. Consequently, they inevitably pass on L. salmonis to the neighboring wild salmon. Since salmon constitutes the basis of a substantial and valuable fishery, it is not surprising that the imputed negative, even harmful, effects of salmon farms became a matter of bitter arguments. When a political party included in its program the abolition of these farms, the entire matter can be classified as biopolitics. Vast amounts of money are devoted to studies that may justify this attitude. And yet, the benefits that these farms provide in many areas of the world cannot be denied—both economic and social benefits. There are estimates of US$ 100 million losses annually, resulting from the damage caused by L. salmonis (farms by implication). At the same time, one comes across records showing that salmon farming has become the pillar of the economy of the coastal communities, not xi

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Foreword

only in the places where it is relatively small, as in Ireland, but also among producers of vast quantities of farmed salmon, as in Norway. The export value of the Norwegian farmed salmon brought in over 18 billion in local currency in the years 2006 and 2007. It cannot be denied that the salmon louse is harmful, sometimes very harmful to its salmon host, and that it would be much better to get rid of it. Since this is impossible, vigorous attempts are being made to reduce its numbers by all sorts of treatment, based on chemical medication, environmental manipulation, or both. So far, these attempts have met with limited success. It is important to keep in mind that salmon farming exists in two oceans, the Atlantic and the Pacific. The latter, specifically along the coast of British Columbia, is specific in that it takes place in the area inhabited by very large stocks of wild salmon. The species farmed there is largely the Atlantic salmon, more amenable to farming than the Pacific salmon. Here too, the greatest concern presents the sea louse, L. salmonis. However, the most recent investigations have shown that this sea louse is not genetically identical with the Atlantic sea louse known under the same name. It has been established that the sea lice from the farmed salmon are able to infect wild Pacific salmon. However, no evidence was found that this infection has very serious effects on the wild stocks. Indeed, the control measures in British Columbia aimed at curbing this infection proved to be more effective and required less effort than elsewhere. The concern exists that this might not continue and that the existing measures might cease to be effective. Research for alternative measures continues. Some investigations, which have already concluded that the deleterious effects of the sea louse are irredeemable and that curbing or completely removing salmon farming is the only acceptable measure, have not taken into account other factors that can adversely affect wild salmon stocks. There are many to be examined, to mention only the effects of spawning channels and other anthropomorphic artifacts known to have ill effects on the neighboring small wild stocks, the possible effects of the sea louse transmitted by nonsalmonid hosts, such as stickleback, herring, or even climatic fluctuations. After all, there are louse-infected wild salmon populations in the areas remote from the salmon farms. The advantages of the farm fallowing benefits have also been overestimated. Clearly, the last word in this matter has not been spoken. There is still a lot to be considered and thoroughgoing urgent investigations of the sea louse problem are in full swing. A substantial amount of them have about reached the publication stage and are collected in the voluminous typescript, which is hereby introduced. Bob Kabata

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Preface This book introduces the salmon louse, Lepeophtheirus salmonis, and summarizes its ecology defined by the biology of its hosts and the environment within which both the host and the parasite coexist. The chapters in the book describe the distribution of planktonic salmon lice larvae in the context of oceanographic models developed in geographically diverse regions and salmon biology. The role of open net pen salmon aquaculture in affecting the distribution and abundance of salmon lice is reviewed. In particular, common themes in parasite management such as the therapeutants used, Integrated Pest Management and Area Management Agreements are identified and discussed from regional perspectives to emphasize similarities and differences. Likewise, Scottish, Irish, Norwegian, and Canadian marine coastal habitats are described to emphasize unique and similar processes encountered in each region that are relevant to the distribution and survival of the parasite. Open net pen farming of Atlantic salmon in the Northern Hemisphere occurs in coastal areas that are the natural habitat of the salmon louse. Farmed salmon populations serve as hosts to parasitic salmon lice and there is a perceived risk that transfer of salmon lice from farmed salmon will adversely impact wild salmon. The biotic and abiotic factors regulating abundance and distribution of salmon lice in coastal areas are poorly understood. The factors that affect the early marine survival of salmon are also poorly understood. This poor understanding in association with a rapidly expanding salmon farming industry and unexplained declines in salmon abundances focused international attention on the salmon louse. The book provides an objective and global assessment of this controversial topic and as such, will be a valuable resource for fisheries biologists and managers. Simon Jones Richard Beamish Nanaimo, British Columbia

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Sognefjord

o r fj e g an d r Ha

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Figure 1.1. Norway with its 3000-km-long coastline and numerous fjords and islands suitable for fish farming. The two larger fjords Hardangerfjord and Sognefjord are shown inside the yellow square and the smaller picture.

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Figure 1.2. Vertical sections of salinity () and temperature (◦ C) along the Hardangerfjord for a summer situation with a distinct brackish layer in the inner part of the fjord. The fjord mouth to the right on the figures is indicated by a red arrow on the map. The red line on the map marks the section and the black arrow the start of the section. The positions of an observational buoy and a current meter mooring are marked by yellow dots for later references.

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Figure 1.7. Vertical long sections of salinity () in June for the years 2004–2010 showing the interannual difference in the extension of the brackish water layer. The fjord head is to the left and the mouth to the right in the figures. The location of the section corresponds to the red line in the map of Figure 1.2.

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Figure 1.10. Modeled spreading of salmon lice from a single source (blue arrow) and from three different release dates. Results after 12 hours (left panel) and 24 hours (right panel) are shown. The red-colored salmon lice were released on May 1, the green-colored salmon lice were released on May 5, and the blue-colored salmon lice were released on May 10 2007.

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Figure 1.11. Modeled spreading of salmon lice from a single source and from two different experiments. Results at the end of the simulated period between April 29 and May 18, 2007 are shown. The blue-colored lice correspond to a simulation with a batch of 800 lice released at the start of the simulation and the red-colored model lice correspond to a simulation where 5 lice are released every 3 hours for the whole period.

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Figure 1.13. Observations of salmon lice distribution and abundance from sentinel cages in the spring of 2001 and 2003 (upper panels) and salmon lice model results for the same period (lower panels). Blue dots in the upper panels show the positions of the cages. The large red dots in the lower panels mark the release position for the model salmon lice. The wind vectors represent the average wind for the simulated period May 8–28 in 2001 and 2003, respectively.

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Figure 3.14. Model-derived tidal excursion areas of finfish farms in southwestern New Brunswick in 2008, by farming area. Finfish farms are shown as small black polygons. (Modified from Chang et al. 2007.)

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Figure 3.15. Model-derived tidal excursion areas for finfish farms in the Letang area (Letang Harbour, Lime Kiln Bay, Bliss Harbour, and Back Bay) and adjacent farming areas in 2008. Finfish farms are shown as small black polygons. (Modified from Chang et al. 2005b.)

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Adult female salmon lice on an adult Atlantic salmon. (Photo: Bengt Finstad,

Figure 9.3. Sea trout infected with mobile salmon lice. (Photo: Bengt Finstad, NINA.)

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Introduction: Lepeophtheirus salmonis— A Remarkable Success Story Craig J. Hayward, Melanie Andrews, and Barbara F. Nowak

Introduction Lepeophtheirus salmonis, the salmon louse (Figure I.1), belongs to the Caligidae, a family of parasitic copepods collectively known as sea lice. Sea lice rank among the most notorious of parasites affecting cultured marine fish (Lester and Hayward 2006). L. salmonis is one of the most common species infesting Atlantic salmon (Salmo salar) in the Northern Hemisphere (Wootten et al. 1982; Pike 1989), and infection with this species is regarded as the most expensive health issue for the salmonid aquaculture industry (Boxaspen et al. 2007). The parasite also infects a range of other salmonid fish, both farmed and wild, as well as other unrelated fish such as the three-spined stickleback Gasterosteus aculeatus (see Jones et al. 2006), seabass Dicentrarchus labrax (see Pert et al. 2006), and saithe Pollachius virens (see Bruno and Stone 1990; Lyndon and Toovey 2001). Infestations can cause erosion of skin, most often on or near the head, with heavy infestations often resulting in host mortality (Finstad et al. 2000). L. salmonis is absent from sites with lowered salinity, and the most susceptible stage of the life cycle of salmon are smolts newly introduced to seawater (Wootten et al. 1982; Finstad et al. 2000). In recent years, comprehensive reviews of the growing body of literature available on L. salmonis and other species of sea lice affecting salmonids have been provided by Wagner et al. (2008), Boxaspen et al. (2007), Boxaspen (2006), Costello (2006), Lester and Hayward (2006), Heuch (2005), 2004, Johnson and Fast (2004), Tully and Nolan (2002), and Pike and Wadsworth (1999). For recent overviews of the prevention and control of L. salmonis and other sea lice infections in aquaculture, see Boxaspen et al. (2007) and Lester and Hayward (2006). Earlier discussions on this topic include those by Alderman (2002), Davies and Rodger (2000), Roth (2000), Pike and Wadsworth (1999), and Roth et al. (1993).

Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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Salmon Lice

Figure I.1. Adult salmon lice, L. salmonis, from the eastern North Pacific (redrawn from Kim 1998) and eastern North Atlantic (photographic credit: Craig Orr). (Data from Lester, R.J.G. and Hayward, C.J. 2006.)

Salmon Louse Biology Life Cycle The life cycle of L. salmonis (Figure I.2), as with most other parasitic copepods, is direct: it requires only one host for completion, although more than one host individual may be involved. L. salmonis also has the typical caligid complement of developmental stages (White 1942; Johannessen 1978; Schram 1993; Johnson and Albright 1991a, 1991b). After hatching out of eggs strings in the water column, there are two naupliar stages (designated “N1” and “N2”) that are free-living; next follows a copepodid stage (“C”) that must find and infect a fish; then follows four chalimus stages (“Ch1” to “Ch4”) that are tethered to a site on a host fish by a frontal filament; and then two preadult stages (“PA1” and “PA2”) and one adult stage (“A”) (Johnson and Albright 1991a, 1991b). The preadult and adult stages are also parasitic, but are mobile and can move over the surfaces of fish, and can also swim in the water column. Each stage is separated from the preceding stage by a molt (shedding of the outer cuticle, or “shell”), exposing

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Figure I.2. Life cycle of the salmon louse, L. salmonis (redrawn from Johnson 1998). (Data from Lester, R.J.G. and Hayward, C.J. 2006.)

a new cuticle underneath. The life cycle (whole or partial) was described previously (White 1942; Johannessen 1978; Schram 1993). Although only one host is required for completion of the life cycle, mobile stages of L. salmonis can readily transfer from one host fish to another. Ritchie (1997) removed various stages of L. salmonis from farmed salmon in Scotland, and found that over a 4-day period, 63% of male lice and 52% of female lice transferred to new hosts. Similarly, in aquarium experiments with na¨ıve salmon postsmolts and mobile stages of L. salmonis, 61% of males and 69% of females transferred to new hosts over a 4-day period (Ritchie 1997).

Temperature and Duration of Development Stages The duration of the different developmental stages is directly dependent on water temperature (Lester and Hayward 2006). For all stages, the reduction in minimum development time associated with increasing water temperature is well described by

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Belehr´adek’s function (Stien et al. 2005). The generation time for L. salmonis is 8–9 weeks at 6◦ C, 6 weeks at 9◦ C, and 4 weeks at 18◦ C (Wootten et al. 1982; Stuart 1990). In Scotland, up to four generations may occur between May and October with a summer water temperature of 9–14◦ C (Wootten et al. 1977; Wootten et al. 1982). In Ireland, Tully (1989) recorded a generation time (ovigerous female to ovigerous female) of 56 days at 13.6◦ C (males took 52 days) in an experimental cage; Johnson and Albright (1991a) reported a generation time of 7.5–8 weeks (at 10◦ C) in the laboratory for L. salmonis originating from Pacific Canada. Under laboratory conditions, females from Atlantic Canada lived for up to 210 days, indicating that they can overwinter on salmonid hosts in the open ocean and return to coastal areas when the host fish returns to spawn (Mustafa et al. 2000c). The lifespan of adults under natural conditions has not been determined (Pike and Wadsworth 1999). For the egg stage of L. salmonis, the duration varies from 17.5 days at 5◦ C, to 5.5 days at 15◦ C; at these respective temperatures, durations for the N1 stage is 52 hours and 9.2 hours, and for the N2 stage, 170 hours and 35.6 hours (Johnson and Albright 1991b). Durations reported for the other stages include the following: 10 days for the copepodid; 5 days for Chl; 5 days for Ch2; 9 days for Ch3; 6 days for CM; 10 days for PAl; and 12 days for PA2 (Johnson and Albright 1991b). Factors affecting female fecundity are poorly understood, with a level of unexplained variability in both average egg numbers per string and egg viability (Stien et al. 2005). Egg strings sampled at 12.2◦ C were shorter and contained fewer eggs than those collected at 7.1◦ C; those at this lower temperature were also smaller in diameter, and a higher percentage of them were nonviable (Heuch et al. 2000). Boxaspen and Naess (2000) found that the time to hatch ranged from 45.1 days at 2◦ C, to 8.7 days at 10◦ C. More successful hatching was reported at 22◦ C in ovigerous females acclimatized to 11.5◦ C than in females acclimatizated at a lower temperature (Johannessen 1978). Low water temperature promoted large body size, long developmental time, and greater fecundity (Tully 1989). The settlement and survival of copepodids at 10 days postinfection (pi) was significantly greater at 12◦ C than at 7◦ C, at a salinity of 34 ppt (Tucker et al. 2000b). Little information is available on mortality rates and distributions of developmental times after the initial minimum developmental times; data are also lacking on development times of parasitic stages at both low (<7◦ C) and high (>15◦ C) water temperatures (Stien et al. 2005). Boxaspen (2006) noted that during the summer of 1997, when water temperatures in Norwegian salmon farms exceeded 18◦ C, L. salmonis was absent.

Salinity Tolerance L. salmonis is absent from sites with low salinity (Pike and Wadsworth 1999). At one Scottish site, the free-swimming infectious copepodid stage of L. salmonis gather near river mouths to infect wild salmonid smolts as they enter the sea (Bricknell et al. 2006). In aquaria, the survival of free-swimming infectious copepodids of L. salmonis from Scotland is severely compromised at salinities below 29 ppt (Bricknell et al. 2006). In salinity gradients, copepodids of L. salmonis avoid salinities below 27 ppt, both by altering swimming behavior and changing the orientation of passive sinking (Bricknell et al. 2006). Reduced salinities also appear to reduce the ability of copepodids to attach

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to hosts, perhaps because their ability to sense or respond to the presence of hosts is compromised (Bricknell et al. 2006). The attachment of copepodids to host Atlantic salmon before exposure to low salinity does not aid survival (Bricknell et al. 2006). In contrast, Finstad et al. (1995) reported that attached stages of L. salmonis were able to survive in freshwater for up to 3 weeks, when attached to Arctic charr (Salvelinus alpinus).

Behavior and Dispersal of Larvae L. salmonis nauplii and copepodids are positively phototactic and exhibit a daily vertical migration, rising from the deeper waters to the surface during the day and sinking at night (Heuch et al. 1995). As salmon move downwards during daylight, this allows transmission to take place (Heuch et al. 1995). Aarseth and Schram (1999) noted that copepodids were photopositive in 1 m deep water columns when illuminated with visible light, but when this light was combined with ultraviolet light (with a spectral irradiance maximum at 313 nm), copepodids gathered significantly deeper in the water column. Although copepodids exhibit positive phototaxis, they are also able to infect fish in darkness (Boxaspen et al. 2007). Nauplii and copepodids swim upwards in response to pressure, and a change in water flow or a mechanical vibration induces a burst in swimming (Heuch et al. 1995). Heuch and Karlsen (1997) reported that copepodids are sensitive to low frequency water accelerations, such as those produced by a swimming fish. Heuch et al. (2007) subsequently confirmed that the approach of a silicone rubber fish mimic did attract copepodids of L. salmonis (65% of responses), whereas it led to an escape response in nonparasitic copepods (Acartia spp.) (87% of responses). Bailey et al. (2006) noted that copepodids display high activation and directional responses in Y-tube assays to salmon-conditioned water, to an extract of this water prepared by solid-phase extraction, and to a vacuum distillate of this extract. Bailey et al. (2006) also observed similar responses to two chemicals identified from salmonconditioned water by coupled gas chromatography–mass spectrometry: isophorone and 6-methyl-5-hepten-2-one. Bailey et al. (2006) isolated two such “semiochemicals” from a nonsalmonid fish as well, turbot (Scophthalmus maximus), which they identified as 2-aminoacetophenone and 4-methylquinazoline, yet when either of these were mixed into salmon-conditioned water, the activation and directional responses of larvae were eliminated. Electrophysiological recordings directly from the antennule also indicate that adult lice respond to an extract of whole fish (soaked in seawater) at a threshold sensitivity of a dilution of 10−4 ; when this extract was fractionated, greatest responses were shown to water soluble fractions containing compounds between 1 and 10 kDa (Fields et al. 2007). Although copepodids exhibit such attraction to host-derived substances, chemical stimulation seems to be unnecessary for initial settlement (Olsen 2001, cited by Heuch et al. 2007). Such molecules are probably most important during the final phase of infection, when the copepodids “taste” fish to determine whether the right host species has been settled upon (Boxaspen et al. 2007). The energy supply of copepodids of L. salmonis has been calculated to be 7800 calories per gram of dry weight, and this level declined sharply from 1–2 days to 7 days (Tucker et al. 2000a). Nevertheless, the age of copepodids did not significantly

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affect initial survival after attachment, or development, under experimental conditions (Tucker et al. 2000a). Costelloe et al. (1999) concluded that the concentration of larvae in seawater in Ireland is strongly affected by distance from salmon farms, as the concentration fell by two orders of magnitude within 100 m of farms. McKibben and Hay (2004) found that in Scotland, larvae in the intertidal zone were concentrated in river mouths, but only when gravid females were present on nearby fish farms. Penston et al. (2004) sampled offshore and sublittoral plankton in lochs and detected nauplii only next to fish farms, although copepodids were also detected in open water and at the head of a sea loch. Murray and Gillibrand (2006) used a particle-transport model to simulate the drift dispersal of larval stages of L. salmonis in currents in Loch Torridon, Scotland, and concluded that movements were very strongly influenced by prevailing winds.

Nutrition of L. salmonis Naupliar stages of L. salmonis lack a gut and anus, and do not feed; the copepodid has a mouth cone, but lacks a structure on the posterior lip of the mouth tube that is found in later stages, a dentigerous bar known as the strigil (Johnson and Albright 1991b). The first chalimus stage of L. salmonis has well-developed mouthparts and a functional alimentary canal, and is the first feeding stage in the life cycle (Jones et al. 1990; Bron et al. 1991). Feeding stages of L. salmonis scrape the skin of the host with the strigil; the mandibles aid the passage of food into the mouth tube (Kabata 1974). Host mucus and epidermis appear to be the main diet (Wootten et al. 1982). Blood was found in the gut of adult Lepeophtheirus spp. when blood vessels or hemorrhaging tissue occurred near the surface (Brandal et al. 1976). The midgut of L. salmonis is not divided into different zones as it is in other copepods (Nylund et al. 1992). L. salmonis has lower levels and a smaller diversity of proteases in the gut than does Caligus elongatus, a difference that was attributed to the wider host range of the latter (Ellis et al. 1990). Lipase was found in the gut of L. salmonis by Grayson et al. (1991). Kvamme et al. (2004) characterized five trypsin-like peptidase transcripts from L. salmonis, and found that their levels increased from planktonic to early hostattached stages and also from preadult to sexually mature stages. These authors also noted that the digestive functions of these five peptidases are indicated by their finding that they are all transcribed throughout the undifferentiated midgut. SkernMauritzen et al. (2007) characterized the molecular structure of a clip-domain containing seropeptidase of L. salmonis (the first to be documented for any copepod), which they designated LsCSP1. They noted that transcription appears to be upregulated during development, and that the peptidase was expressed in subcuticular tissue.

Epibionts on L. salmonis A number of species of epibionts (organisms living on the surface of other organisms) have been reported from L. salmonis, including the following: the alga Ulva spp.;

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ciliate suctorian protozoans (Ephelota gemmipara, Ephelota gigantea, and Epistylis spp., and the monogenean Udonella caligorum (see Treasurer 2002 and references therein; Fernandez-Leborans et al. 2005).

Morphology As in the majority of other caligids, adult L. salmonis exhibit sexual dimorphism; the female is larger than the male. As is also characteristic of most caligids, adult L. salmonis have a large, rounded, flat cephalothorax (Lester and Hayward 2006). L. salmonis and other members of the genus can be distinguished immediately from members of the genus Caligus in that only the latter, as fourth stage chalimi, preadults, and adults, have two rounded structures known as frontal lunules (Lester and Hayward 2006). Female L. salmonis are 10–18 mm long, and have a more prominent genital segment than males (5–7 mm long) (Kabata 1979; Figure I.1). Lice from wild fish are significantly larger than those from farmed fish, but when larvae from these two sources are raised on salmon at the same temperature, they have the same growth rate and morphology, indicating that louse size is plastic (Nordhagen et al. 2000). Adult females produce paired egg strings from the posterior end of the genital segment, which are up to 2 cm long and bear a total of up to 700 eggs (see Wootten et al. 1982; Costello 1993). The appendages are similar in both sexes, with the exception that the male has a striated ventral surface on the second antenna, to enhance attachment to the posterodorsal surface of the female during mating. Chalimus stages of L. salmonis also have a single eyespot as well as a relatively short frontal filament (Wootten et al. 1982). The copepodid has a single eye, located beneath the rostrum; this eye has two lenses, in addition to a lensless light-sensitive area (Boxaspen et al. 2007). The reproductive system and other aspects of the internal anatomy of the Caligidae has been described by Wilson (1905) and Ritchie et al. (1996). Bron et al. (1993) and Gresty et al.(1993) described the ultrastructure of sensory structures, and the frontal filament was described by Pike, Mackenzie, and Rowland (1993). Kabata and Hewitt (1971) described the locomotion of adult caligids.

Geographical Distribution L. salmonis occurs only in cold temperate waters of the Northern Hemisphere, where it has a circumpolar distribution (Lester and Hayward 2006; Boxaspen 2006).

Genetic Population Structure To help evaluate the claim that individuals of L. salmonis originating from farmed salmonids are responsible for the decline of populations of sea trout (Salmo trutta) since 1989 on the west coasts of both Scotland and Ireland, and of native salmonids (Oncorhynchus spp.) off Pacific Canada since 2001, a number of studies have examined

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the population structure of L. salmonis. However, as louse populations show varying degrees of polymorphism, there is currently still no consensus as to whether sea lice from farms are reducing numbers of wild salmonids (Lester and Hayward 2006). Due to the inclusion of the planktonic larval phase in the life cycle of L. salmonis, and also the high mobility of salmon, Todd et al. (1997) predicted that gene flow would be enhanced, and genetic differentiation of populations of L. salmonis would be precluded as a result of random drift alone. These authors then confirmed this in their analysis of allozyme variation in two polymorphic loci of female sea lice from sea trout, rainbow trout, and caged Atlantic salmon from around the Scottish coast. Allozyme data for L. salmonis in Norway was also examined by Isdal et al. (1997), but in contrast with Todd et al. (1997), these authors concluded that there were two distinct populations of L. salmonis in the north and south of the country. Patterns in randomly amplified polymorphic DNA (RAPD) were also examined by Todd et al. (1997) and, in contrast with their allozyme results, noted that there was some genetic differentiation of sea louse populations around the coasts of Scotland. In this study, populations of L. salmonis sampled from wild salmon and sea trout were genetically homogeneous, but samples taken from rainbow trout and farmed salmon showed significant genetic differentiation, both among the various farms and between wild and farmed salmonids. Evidence of high levels of small-scale spatial or temporal heterogeneity of RAPD marker band frequencies was also shown for the one farm from which repeat samples were analyzed. Putative “farm markers” were also detected in RAPD analysis in some individual parasites from west coast wild sea trout, indicating that they had probably originated from salmon farms. Todd et al. (1997) concluded that the observed range of phenotypes was produced by a combination of strong selection pressures (perhaps in reaction to chemotherapeutic treatments) and a founder effect on farms. Further analysis of RAPD fragments of L. salmonis from wild and cultured S. salar in Scotland was undertaken by Dixon et al. (2004). Even though distinct clusters of populations were discernible, these authors concluded that genetic differentiation did not fit any geographical pattern. Dixon et al. (2004) noted that this may indicate that selection for chemical resistance occurs after dispersal. Variation at six L. salmonis microsatellite loci was assessed by Todd et al. (2004); no significant differentiation was detected among lice from wild and farmed salmonids in Scotland, wild sea-run brown trout in Norway, and farmed Atlantic salmon in eastern Canada. It was concluded that larval interchange occurred between farmed and wild host stocks, and long distance oceanic migration of wild hosts are sufficient to prevent genetic divergence. However, L. salmonis from farmed Atlantic salmon in Pacific Canada showed significant but low differentiation from this Atlantic population. This result is consistent with the divergence of Pacific and Atlantic lineages as documented by Yazawa et al. (2008) (see section “Two Lineages: Atlantic and Pacific”).

Two Lineages: Atlantic and Pacific Based on morphological studies, L. salmonis has long been regarded as widespread in both the North Pacific and North Atlantic Oceans. Recent genetic evidence indicates that there are two populations in these oceans that do not interbreed, and in fact belong to different lineages (Yazawa et al. 2008). The level of divergence is consistent with the

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hypothesis that the Pacific form coevolved with Pacific salmon (Oncorhynchus spp.) and the Atlantic form coevolved with Atlantic salmonids (Salmo spp.) independently for the last 2.5–11 million years (Yazawa et al. 2008). As these two lineages probably belong to distinct species, but have yet to be distinguished formally and a new name assigned to the second species, the name “L. salmonis” will be used for reports of these species from both Atlantic and Pacific waters.

Relationships with Other Sea Lice, Detection, and Identification In 2000, the family Caligidae contained a total of 445 species in 33 genera; of these, 107 species belonged to the genus Lepeophtheirus (Ho 2000). Adult L. salmonis are usually readily visible to the naked eye on the head or body of infected fish, but confirmation of identification requires examination of the parasite under a microscope (Lester and Hayward 2006). The primary features used in identification are general body shape and relative size of body tagma, and patterns of setation (spines) or other morphological attributes on the legs and other appendages (Lester and Hayward 2006). Copepodids and chalimus larvae of L. salmonis are generally small (less than 4 mm long), and their detection requires at least the use of a magnifying glass (Johnson 1998). Larval stages attached to host fish, and larval stages in the water column, are relatively difficult to identify by their morphology alone. Accordingly, molecular methods have now been developed in a number of studies, both to confirm the identity of attached larval L. salmonis where there had been some doubt (Jones et al. 2006), and to quantify the numbers of free swimming larvae collected in plankton samples by the use of real-time PCR (McBeath et al. 2006).

Host–Parasite Relationships Site and Host Selection On contacting a host, the copepodid grips the skin with its clawed antennae and examines the surface using the antennules, which bear high-threshold contact chemoreceptors (Bron et al. 1993). Copepodids usually reject nonsalmonid hosts and reenter the water column (Bron et al. 1993). Once a suitable salmonid host is found, the copepodid penetrates host’s skin using antennae, and the anterior end of the cephalothoracic shield is pushed into the epidermis, causing it to separate from the basement membrane. A frontal filament (Figure I.1) is formed through production of an adhesive secretion, which quickly hardens. The larva then molts into the first chalimus stage (Jones et al. 1990; Bron et al. 1991). The typical attachment sites for the chalimus stage are the dorsal and pectoral fins and around the anus of wild and caged fish (Wootten et al. 1982; Tucker et al. 2002), but under the confines of experimental conditions, the chalimus can also attach to the buccal cavity and gills (Bron et al. 1991; Johnson and Albright 1991b; Genna et al. 2005). Genna et al. (2005) found that, under controlled conditions in a flume, three variables (light, salinity, and host velocity) independently and interactively determined the distribution and number of copepodids settling on hosts; the highest settlement occurred when salmon swam at slow speeds.

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Preadult and adult stages of L. salmonis attach by suction, which is generated by the cephalothorax, and sealed by its marginal membrane and the expanded base of the third pair of legs (Kabata and Hewitt 1971). Individuals can also move freely over the surface of the host. These stages are most abundant on the head and dorsal surfaces of hosts and, especially in Oncorhynchus gorbuscha and Oncorhynchus nerka, on the posterior ventral surface (White 1940; Wootten et al. 1982; Nagasawa 1987).

Pathogenicity In most cases, the effects on the host are directly related to the physical damage caused by the parasite through its attachment and feeding activities (Pike and Wadsworth 1999). The feeding activity of the parasite is the primary cause of pathology associated with adult caligid copepods; the extent of host skin damage depends on the number of parasites. In contrast, the pathology caused by the chalimus stages results from the attachment by the frontal filament and consequently the limited feeding radius (as reported by Boxshall 1977 for a related species of Lepeophtheirus). If salmon with heavy infections of L. salmonis die, the main cause of death appears to be osmoregulatory failure through extensive skin damage, though secondary bacterial infection has also been suggested in some cases (Wootten et al. 1982). Small host fish can die very rapidly when infected with sea lice without any appreciable disease signs (Ho 2000). This sudden mortality, without any development of open lesions has been compared to toxic shock in mammals and is possibly mediated by prostaglandin E2 (PGE2), which is secreted by L. salmonis and detected in blood of the host (Fast et al. 2004; Fast et al. 2006a). Direct blood feeding can result in the development of anemia. Based on Wagner and McKinley’s (2004) predictive feeding-rate model 15–25% of the tissue consumed by L. salmonis is blood. At higher infection levels (>0.5 sea lice/g), this level of blood consumption may cause anemia, and this would compound problems with osmotic balance (Wagner and McKinley 2004). The effects on host are related to the host factors, in particular host species as well as the number of the parasites present on the host and their developmental stages. Five adult L. salmonis cause skin erosion on salmon smolts. Finstad et al. (2000) estimated from laboratory dose-response studies that wild smolts would die at 0.75 adult lice per gram of body weight. A total of 11 attached individuals is regarded as a lethal load for Atlantic salmon smolts (Heuch 2005; Heuch et al. 2005). However, up to 2000 of the parasites have been recorded on a farmed fish (Brandal and Egidius 1977), possibly indicating that if the salmon is sufficiently large, it can withstand significant skin erosion (Lester and Hayward 2006). These discrepancies in the numbers of parasites causing morbidity may be due to the fact that the estimates are based on incorrect assumptions. These estimates have been extrapolated from laboratory studies and limited field studies and suffer from inconsistency, in particular with regard to life stage of the parasite and the host species (Wagner et al. 2008).

Clinical Signs and Pathology Clinical signs of sea lice infection include skin erosion, initially only at the point of attachment (Bron et al. 1991; Johnson and Albright 1992a). At higher levels of

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infection, when preadult and adult stages are involved, these become skin lesions and then large open wounds; there may be subepidermal hemorrhaging and erosion of the skin, which appear as grey patches, these wounds can expose the cranial bones (Wootten et al. 1982). These open lesions usually occur on the head and back of the fish, behind the dorsal fin (Jðnsdðttir et al. 1992; Johnson et al. 1996). The large open wounds may be associated with secondary bacterial infections (Egidius 1985). Secondary fungal infections may ensue if fish with exposed wounds are returned to freshwater (H˚astein and Bergsjo 1976). Edema, hyperplasia, sloughing of epidermal cells, and inflammation are caused by attachment and feeding of preadult and adult L. salmonis (Jðnsdðttir et al. 1992). Chinook and coho salmon are more resistant to L. salmonis than Atlantic salmon and respond to infection by extensive epithelial hyperplasia and inflammation (Johnson and Albright 1992a). Jones et al. (1990) described the histopathology associated with early developmental stages of L. salmonis. Initial mechanical damage caused by copepodid attachment and feeding by Ch1 and Ch2 causes a mild epidermal hyperplasia. Later stages cause damage by feeding, with a focus of irritation around the periphery of the lesion associated with the frontal filament. The greatest damage is associated with the remnant of the frontal filament following detachment by the Ch4 stage. Lesions, 0.5 cm in diameter, have an outer ring of heavily pigmented tissue and a depressed core of white skin. The basement membrane is reorganized over the remains of the filament and there is dermal fibrosis with inflammatory infiltration. Infection of Atlantic salmon with low level of preadult and adult sea lice (0.04 lice/g of fish) resulted in increased apoptosis and necrosis of epithelial cells and a decrease in the numbers of mucous cells (Nolan et al. 1999). This tissue response is host specific and ranges from almost nonexistent at the site of attachment on Atlantic salmon to a strong response with epithelial hyperplasia and inflammation at the site of sea louse attachment on coho salmon (Johnson and Albright 1992a).

Pathophysiology Sublethal infection by L. salmonis compromises the overall fitness of Atlantic salmon. Even when sea lice are not feeding, they cling to the host by digging into the epidermis, using claw-like antennae and maxillipeds (Lester and Hayward 2006). Hence, the mere presence of sea lice on the skin is enough to cause stress to fish (Ho 2000). A number of studies demonstrate that experimental infection of Atlantic salmon with L. salmonis elevates levels of cortisol significantly compared with those in controls (e.g., Bowers et al. 2000; Mustafa et al. 2000a; Finstad et al. 2000). Additionally, Bowers et al. (2000) reported elevated plasma glucose; and Finstad et al. (2000) noted that after preadult stages of L. salmonis appeared, a secondary alteration to host physiology occurred, in the form of elevated plasma chloride levels, and that salmon with the highest lice infections died throughout the experiment. Infection of Atlantic salmon with low levels of preadult and adult sea lice (0.04 lice/g of fish) resulted in an increased gill Na/K-ATPase activity and an increased Na:Cl ratio in blood serum (Nolan et al. 1999). Jones et al. (2007) noted a transient cortisol response in juvenile chum salmon 21 days after exposure to low numbers of L. salmonis copepodids; hematocrit of exposed chum salmon was also significantly lower than that of unexposed chum. Coho salmon implanted with hydrocortisone (0.5 mg/g body weight) produced a diminished

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epithelial hyperplasia and inflammation and were more susceptible to infection by L. salmonis than were control coho salmon (Johnson and Albright 1992b). For wild sea trout (Salmo trutta) smolts transferred to seawater in experimental conditions, L. salmonis did not show consistent effects on physiological stress markers until the lice developed to the mobile preadult and adult stages (Wells et al. 2006). Preadult L. salmonis caused significant increases in plasma chloride, osmolality, glucose, lactate, and cortisol, and a significant reduction in hematocrit (Wells et al. 2006). Critical swimming speeds in Atlantic salmon infected in the laboratory with high numbers of L. salmonis were significantly lower than both control salmon and salmon with low numbers of sea lice (Wagner et al. 2003). In addition, after swimming, plasma chloride levels in salmon with higher sea louse numbers were significantly increased compared with those in uninfected salmon and those with low numbers of sea lice (Wagner et al. 2003). Webster et al. (2007) quantified the energetic cost of different salinities on pink salmon (both infected with L. salmonis and in control pink salmon), and confirmed that infection changes the salinity preference from saltwater to freshwater. These authors also recorded a 14-fold increase in the frequency of jumping in infected fish, and a decrease in foraging between 13 and 33 days postinfection. Todd et al. (2007) noted that among wild, one sea-winter salmon returning to Scotland, those individuals in poor condition were no more likely to carry high infestations than were those in good condition. Finally, in three-spined sticklebacks off British Columbia there was no significant relationship between the intensity of L. salmonis and condition factor (Jones et al. 2006).

Immune Response Salmon naturally infected with L. salmonis produce only very low levels of specific antibodies (Grayson et al. 1991). This is most likely due to the fact that for most of the life cycle, the sea lice are not in intimate, fixed contact with host surfaces (Pike and Wadsworth 1999). Even chalimi, which attach to a fixed position on hosts, are distanced from the skin (except when feeding) by the inanimate frontal filament (Lester and Hayward 2006). A serum antibody response to an antigen (>200 kDa), associated with the apices of gut epithelium folds in L. salmonis, was found in naturally infected Atlantic salmon (Grayson et al. 1991). Different antigens in adult and chalimus stages of L. salmonis were identified. Atlantic salmon immunized with crude extracts of either adult L. salmonis or another sea louse species, C. elongatus, produced humoral antibodies that reacted with antigens in these extracts, as well as fewer antigens from crude extracts of chalimus stages and eggs (Reilly and Mulcahy 1993). As yet, none of these antigens have been shown to produce protective immunity in the salmon. Fast et al. (2004) detected PGE2, a potent vasodilator that is thought to aid in parasite evasion of the host immune response, in secretions of L. salmonis; concentrations ranged from 0.2 to 12.3 ng per individual and varied with incubation temperature and time kept off the host. PGE2 downregulates Atlantic salmon inflammatory gene expression (Fast et al. 2004; Fast et al. 2006b). Trypsin is another sea lice secretion that can aid feeding and avoid host immune responses (Johnson et al. 2002).

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Macrophage function (as measured by respiratory burst activity and phagocytosis rate) was significantly impaired in Atlantic salmon experimentally infected with preadult L. salmonis (Mustafa et al. 2000). In a series of experiments, Fast et al. (2006a) twice exposed Atlantic salmon to L. salmonis from Pacific Canada and monitored the stress and immunological responses. These authors found that the expression of nearly all six of the immune-related genes they studied increased following initial infection, but that the immunological stimulation did not reduce parasite numbers, nor protect against reinfection. Lice counts increased from a mean of 16.3 per fish at 9 days pi up to 142.8 per fish at 26 days pi. Plasma cortisol levels were significantly increased over those in control fish on days 26, 33, and 40 days pi; similarly, plasma PGE2 levels were significantly higher in infected fish at 9, 33, and 40 days pi (Fast et al. 2006a). In infected fish at 9 days pi, expression of interleukin-1 beta, tumor necrosis factor alpha-like cytokine, major histocompatibility class II, transforming growth factor-beta-like cytokine and cytooxygenase-2 genes were increased; expression of most of these returned to control levels 21 days pi (Fast et al. 2006a). The expression of the major histocompatibility class I gene was 2–10 times lower in head kidneys of infected salmon than in uninfected salmon at 21 days pi (Fast et al. 2006). Conversely, by 14 and 21 days pi, major histocompatibility class II expression was significantly increased (more than 10 times) in infected salmon. Finally, expression of interleukin-1 beta also increased by three times in head kidneys of infected salmon by 21 days pi, but no differences were observed in cyclooxygenase-2 expression over the course of the infection. Fast et al. (2007) concluded that in addition to PGE2 and trypsin, L. salmonis secreted other immunomodulatory compounds that inhibited the expression of immunerelated genes (interleukin-1 beta and major histocompatibility class I) of Atlantic salmon in vitro. The immunosuppression caused by sea lice infections can make the host more susceptible to other infections. Two-year old rainbow trout challenged with the microsporidian Loma salmonae 28 days after exposure to sea lice developed 2.5 times the number of xenomas than control trout not exposed to sea lice (Mustafa et al. 2000). This increase was observed to correspond with the suppressed macrophage function noted above.

Host Susceptibility MacKinnon (1998) noted that a host’s susceptibility to infestation of L. salmonis can be influenced by several interacting factors, including the host’s stress and nutritional status, the effectiveness of the host’s immune system, and the genetically determined susceptibility of the host. Dawson et al. (1997) determined that the attachment and survival of chalimus stages were significantly lower on Atlantic salmon than on sea trout because of nonselective settlement of the copepodids, followed by differential mortality. These authors also found that the survival of preadult and adult sea lice declined more rapidly on sea trout than on Atlantic salmon, but that Atlantic salmon ultimately had a lower abundance of lice. According to Fast et al. (2003), the high susceptibilities of Atlantic salmon and rainbow trout to infection with L. salmonis may be related to characteristics of the

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host mucus and the high degree at which the mucus of each stimulates the production of low-molecular-weight proteases in the sea lice. These authors found variation in the release of respective proteases and alkaline phosphatases in sea lice in response to mucus from these two species and the mucus of two others (coho salmon and winter flounder). In Pacific Canada, Jones et al. (2007) exposed juvenile pink and chum salmon to high and low numbers of L. salmonis copepodids (735 and 243 per fish, respectively), and found that the fin and head kidney of pink salmon expressed three proinflammatory genes (interleukin-8, tumor necrosis factor alpha-1, and interleukin-1 beta) earlier and at higher levels than in chum salmon. These authors suggested that this may be evidence of a mechanism by which the pink salmon more rapidly reject lice. The strain of host Atlantic salmon also influences louse burdens. Individuals of the wild Dale strain, when kept in tanks with four other stocks and then challenged with L. salmonis, had significantly lower louse density than did two other stocks (wild Vosso and Farm 2 strains) (Glover et al. 2004). Glover et al. (2007) provided evidence of a link between major histocompatibility complex (MHC) class II and susceptibility to L. salmonis. Within one salmon family, fish with the MHC genotype Sasa-DAA3UTR 208/258 displayed a significantly lower abundance of lice compared to those possessing the MHC genotype Sasa-DAA-3UTR 248/278. Glover and Skaala (2006) tagged and reared wild and farmed smolts of Atlantic salmon, and their hybrids, in a sea cage for 8 months and found that, on all three sampling dates over this period, farmed individuals displayed the highest abundances of L. salmonis, with no significant differences between hybrid and wild individuals. Interestingly, they also found that an individual’s level of infection at one time was only a weak predictor of the level of infection at another time. Kolstad et al. (2005) studied genetic variation in resistance of Atlantic salmon to L. salmonis and concluded that the potential for improving resistance by selective breeding was high. These authors also recommended challenge tests during selective breeding to increase resistance.

Occurrence on Wild Salmonid Fish L. salmonis most commonly infects the Salmonidae, especially the genera Salmo, Salvelinus, and Oncorhynchus (see Kabata 1979; Egidius 1985). On wild, river-bound Atlantic salmon, a few L. salmonis per fish was regarded as a common sight (Brandal and Egidius 1977). The prevalence and intensity of infection of L. salmonis on such wild fish is also occasionally high (Johnson et al. 1996). For example, grilse of S. salar entering the estuary of the Moser River, Nova Scotia, were found to be heavily infected with hundreds of L. salmonis and exhibited severe lesions (White 1940). Berland (1993) found the prevalence and intensity of L. salmonis (and another sea louse species, C. elongatus) on wild salmon in west Norway to be low in 1973 and 1988, but high in 1992 (mean intensities of 11.7 and 7.44 per fish, compared with 20.18), and noted that this increase may perhaps have been attributable to the presence of salmon farms. In the North Pacific Ocean and Bering Sea, 78% of L. salmonis were documented to infect wild pink salmon (Oncorhynchus gorbuscha), 15% infected chinook salmon

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(O. tschawytscha), and the remainder infected steelhead trout (O. mykiss), coho (O. kisutch), chum (O. keta), and sockeye (O. nerka) salmon (Nagasawa et al. 1993). In the northeast Pacific, Beamish et al. (2007) proposed that transportation of L. salmonis into coastal areas increased the transmission potential of their infectious stage at a time when host densities increased in these areas and decreased in the open ocean.

Occurrence on Farmed Salmonid Fish Severe outbreaks of L. salmonis in aquaculture first occurred within a few years of the establishment of salmon farms in the North Atlantic Ocean in Norway, in the 1960s; outbreaks on farms in Scotland were recorded a decade later (Wootten et al. 1982). Farms in Norway are located on sites with a consistently higher salinity than in Scotland, and accordingly have more severe L. salmonis infections (Pike 1989). Salmon farms in the Bay of Fundy, Atlantic Canada, are also subject to outbreaks of L. salmonis, but are unusual in that they are less adversely affected by L. salmonis than by C. elongatus (Hogans and Trudeau 1989a, 1989b). Although more recently, infestations with L. salmonis on farmed salmon in the Bay of Fundy have increased in frequency and economic significance (see Chapter 3 contributed by Chang et al.). In the Pacific Ocean, L. salmonis has also caused lesions to pen-cultured salmonids (Atlantic salmon, Salmo salar) in British Columbia (Pike and Wadsworth 1999) and in Japan (chum salmon, O. keta, pink salmon, O. gorbuscha, and masu salmon, Oncorhynchus masou) (Urawa 1998; Nagasawa 2004). Nevertheless, L. salmonis is not regarded as a major problem in the farming of coho salmon in Japan (Ho and Nagasawa 2001). This is likely to be because of the farmers’ practice of rearing only young fish, and only over an 8-month period, followed by an annual period of fallowing (Ho and Nagasawa 2001). Additionally, coho salmon were found not to host chalimus stages, only the adults and preadults, indicating that the life cycle is not completed on this host. However, in contrast, another salmonid farmed in Japan—rainbow trout, O. mykiss—is highly susceptible to L. salmonis (Ho and Nagasawa 2001). In the Southern Hemisphere, L. salmonis has never been recorded on any salmonids introduced for farming to Australian, New Zealand, and Chilean waters, nor has the parasite been recorded on any local wild fish in these regions. Undoubtedly, this is because these species were introduced in their freshwater stage (usually eggs) and thus could not result in an accidental introduction of L. salmonis. Additionally, the geographical remoteness of these regions from the native range of salmonid fish ensures that there is practically no chance for the natural dispersal of the salmon louse to these southerly regions. However, there has been a case of live sea lice present on a consignment of fresh Atlantic salmon imported from the Northern Hemisphere at the Sydney Fish Market in Australia in 2003 (Green 2003), suggesting that there is a risk of introduction of L. salmonis to the Southern Hemisphere.

Occurrence on Nonsalmonid Fish Most authors originally considered L. salmonis to be more or less specific to salmonid fish, and thus to have a higher specificity for hosts than most other sea lice species.

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However, a range of nonsalmonid hosts has now been documented. Other known hosts of L. salmonis include three-spined sticklebacks (Gasterosteus aculeatus), white sturgeon (Acipenser transmontanus), Pacific sand lance (Ammodytes hexapterus), lingcod (Ophiodon elongatus), flag rockfish (Sebastes rubrivinctus), and Pacific redfin (Tribolodon brandtii) in the North Pacific Ocean; and saithe (Pollachius virens) and sea bass (Dicentrarchus labrax) in the North Atlantic Ocean (Bruno and Stone 1990; Jones et al. 2006; Lyndon and Toovey 2001; Margolis and Arthur 1979 (and references therein); Pert et al. 2006 (and references therein)). The synopsis of parasites of Canada published by Margolis and Arthur (1979) did not list three-spined sticklebacks as a host of L. salmonis, nor of any other species of Lepeophtheirus. Since then, Kabata (1988) reported chalimus stages of an unidentified species of Lepeophtheirus from stickleback, but did not provide quantitative data; Rohde et al. (1995) also recorded unidentified Lepeophtheirus on sticklebacks off Pacific Canada, but in this case, they noted that 20 of these hosts were infected by just two individuals; these may well have been chalimi of L. salmonis. However, more recently, Jones et al. (2006) confirmed the presence of L. salmonis on threespined sticklebacks in Pacific Canada for the first time, using both morphological and molecular data. Interestingly, these authors also recorded relatively high numbers, with an overall prevalence of 83.6%, a mean intensity of 18.3 lice per fish, and a maximum intensity of 290 lice (in a sample size of 1309 sticklebacks). The majority of the individuals (over 97%) were copepodid and chalimus stages (Jones et al. 2006). Only five adults (0.03%) were collected, and as none of these were gravid females, it appears that this fish species serves only as a temporary host, and that the life cycle cannot be completed. However, this does not diminish the potential role of this host species as a reservoir host, and in the dispersal of L. salmonis. Jones et al. (2006) confirmed in the laboratory that L. salmonis did not develop beyond the preadult stage on sticklebacks; interestingly, these authors found that development up to this stage was just as rapid on sticklebacks as it was on pink and chum salmon. Since L. salmonis was not among the more than 70 different taxa of parasites that had been recorded on or in sticklebacks up to 1979 (see the checklist of Margolis and Arthur 1979), and as the life cycle of L. salmonis probably cannot be completed on three-spined sticklebacks, this would seem to indicate that sticklebacks have been acquiring high levels of infections of L. salmonis in British Columbia only in recent years. However, it has not yet been resolved whether this is simply a natural phenomenon, or whether it is associated with the development of salmonid aquaculture. In contrast with infections of L. salmonis on three-spined sticklebacks, gravid female L. salmonis have been recorded from two of the other two known nonsalmonid host fish of L. salmonis, saithe, and sea bass, which were both collected in or near salmon farms in Scotland (Lyndon and Toovey 2001; Pert et al. 2006). However, Ritchie’s (1997) experimental results indicate that mobile stages of L. salmonis can readily transfer from one host individual to another (for a summary of these data, see section “Life Cycle”). Hence, is not yet certain that female L. salmonis did in fact become gravid after infecting saithe and sea bass, as they could have become gravid on farmed salmon some time before transferring to these other nonsalmonid hosts. This question could be resolved with aquarium experiments.

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Interactions between Wild and Farmed Fish Salmon farms are considered a significant risk factor for the presence of L. salmonis on wild salmonid fish in the northeast Atlantic Ocean (Butler 2002; Heuch et al. 2005). Boxaspen (1997) placed lice-free salmon in cages at three sites chosen at varying distances from salmonid fish farms off Bergen, Norway, and found that lice abundance was negatively correlated with distance to farms during the highest temperatures of the study, whereas during colder temperatures (<6◦ C), lice abundance was positively correlated with distance to farms. Bjørn et al. (2001) reported that lice burdens of sea trout and Arctic charr in areas with intensive farming in Norway were significantly higher than at other localities without farms. These authors noted that the burdens of lice on wild salmonids around farms were around ten times higher than those on salmonids away from farms, and also that the most heavily infected fish in farm areas returned to freshwaters prematurely. In addition, 47% of fish caught in freshwater and 32% of those captured at sea carried lice at intensities above the level shown to induce mortality in laboratory experiments. Accordingly, Bjørn et al. (2001) concluded that high lice numbers may have a profound negative effect on wild populations of sea trout. Also in Norway, Birkeland (1996) observed that early-returning sea trout postsmolts trapped at the mouth of one river had a median infestation intensity of 206 lice, and noted that these fish experienced a median decrease of 23.5% in body mass. Hatton-Ellis et al. (2006) similarly concluded that in Scotland over a 5-year period, when the levels of ovigerous lice on local salmon farms were elevated, sea trout smolts in a loch were rapidly infested and returned early. Nevertheless, Boxaspen et al. (2007) concluded that wild and farmed salmon are capable of coexisting, as long as the total number of louse larvae is adapted to local hydrodynamic conditions and the characteristics of wild salmonid populations. Since salmon populations on the western coast of Norway may experience both infection by L. salmonis and moderately acidified rivers due to acid rain, Finstad et al. (2007) undertook experiments that indicated that mortality was highest in those lice-infected salmon exposed to the lowest pH; they concluded that lice densities and acidification pressure in combination can explain some of the annual variation in postsmolt survival. No general consensus has yet been reached as to whether the offspring of sea lice infecting farmed salmonids reduce the numbers of migrating wild salmonids in all regions where L. salmonis occurs and salmonids are farmed. In Pacific Canada, e.g., Morton and Routledge (2005) reported an increase in mortality among wild juvenile pink and chum salmon in the Broughton Archipelago that were naturally infected with 1–3 sea lice. However, Brooks (2005) affirmed that reduced salinities in the region from June through to November most years provided a natural control of infective copepodids, and that currents in locations where salmon farms occur flush the free-swimming nauplii larvae at least 7.3–10.0 km downcurrent and out of the archipelago, before the larvae become infective. Krkoˇsek et al. (2006) countered that Brooks (2005) misinterpreted how salinity affects louse development, misread the timing of seasonal salinity changes in relation to migration of juvenile salmon, and used models that overestimated the distance that louse larvae are flushed. Beamish et al. (2006) subsequently suggested that wild Pacific salmon can, in fact, coexist successfully with farmed Atlantic salmon on the Pacific coast of Canada, since they documented

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exceptional returns of pink salmon in an environment with farmed Atlantic salmon and L. salmonis. This topic remains controversial, and is still debated vigorously at this time (e.g., see Brooks and Jones (2008) and the response by Krkoˇsek et al. (2008).

Economic Significance Infestations of L. salmonis and other sea lice in salmon farms in Norway and Scotland were estimated to have cost over 70 million ecu in 1997 alone (Costello and Boxshall 2000). In 1995 in Canada, infestations were estimated to have cost CAN$20 million (Pike and Wadsworth 1999). Johnson et al. (2004) concluded that the annual cost of sea lice infections globally exceeds US$100 million. Due to the economic importance of L. salmonis and other species of sea lice, a series of international conferences have been held, the proceedings of which have been published in two edited books (Boxshall and Defaye 1993; Sayer et al. 1996), in special issues of international journals (Contributions to Zoology 69 (1/2) 2000); Aquaculture Research 31 (11) 2000; Pest Management Science 58 (6) 2002; Aquaculture Research 35 (8) 2004; Journal of Fish Diseases 32 (1) 2009), and also in a newsletter devoted to sea lice, “Caligus.”

Seasonality and Epizootiology Recent epizootiological studies have increased the data available for understanding the population dynamics of sea lice in aquaculture and in wild fisheries. In northwest and northeast Ireland, all L. salmonis larvae were from wild stocks of S. trutta; however, in the west, 94% of L. salmonis larvae originated from farmed salmon (Tully and Whelan 1992). It has been estimated that between 1 and 38 million larvae were produced per day from single salmon farms in Ireland (Tully and Whelan 1992). Orr (2007) estimated that the 12 active salmon farms in Broughton Archipelago, Pacific Canada hosted over 6 million gravid L. salmonis, which in turn produced 1.6 × 109 eggs during 2 weeks in the winter of 2003–2004. Krkoˇsek et al. (2006) stated that the presence of farms and the practice of maintaining adult salmon infected with L. salmonis in coastal waters exposed wild juvenile salmonids in these coastal areas to lice that they would not otherwise encounter, as they were no longer spatially segregated. Gravid females and other stages of L. salmonis occur year-round on salmon farms in northern Europe, with a succession of generations during the year (Wootten et al. 1982). L. salmonis occur in the greatest numbers in late summer and autumn, and this could be due to an accumulation of the parasite from successive generations. However, Tully (1989) noted that because mature lice disappeared from fish before maturation of the next generation was complete, the total intensity of infection did not rise cumulatively. Additionally, high summer temperatures may have an adverse effect on the parasite. For example, Tully (1989) noted that there was little reproduction in Ireland until the onset of winter, because high water temperatures adversely affected the parasite. Revie et al. (2002) examined the epizootiology of L. salmonis (and C. elongatus) in the west of Scotland over 4 years, and determined that infections of L. salmonis were

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less common in the first year of production than in the second. Using statistical regression six variables were identified as significant in explaining patterns of abundance of mobile L. salmonis across 40 salmon farms in Scotland: level of treatment; type of treatment; cage volume; current speed; loch flushing time; and sea louse abundance in the preceding 6 months. Factors that had been assumed to be critical, including stocking density, site biomass, water temperature, and the presence of neighbors, were not found to be significant in this model (Revie et al. 2002). Revie et al. (2005) developed a mathematical model to describe patterns of sea lice infection on salmon farms in Scotland and to predict the likely effect of treatment strategies, after taking into account development rates and mortality using compartments representing life history stages and external infection pressure. The model demonstrated that the timing of treatments is critical if sea lice are to be effectively controlled. Revie et al. (2007) measured the clustering of L. salmonis in salmon in cages in Norway and Scotland using an interclass correlation coefficient, and confirmed that significant clustering occurs within cages for the stages considered (chalimus and mobiles). As a result, they concluded that the “few fish from many cages” approach results in a marked improvement in precision. Comparison of epizootiological patterns of L. salmonis infections in farmed Atlantic salmon in Norway and Scotland over several years showed that infection levels of both chalimus and mobile stages were consistently higher in Scotland than in Norway (Heuch et al. 2003). These authors noted that this could be because the water bodies used for farming in Scotland are shallower and more enclosed; because pens are shallower and smaller; because seawater temperatures are higher; and because access to medications differ. In western Canada, Saksida et al. (2007) used a generalized linear model to examine several years of data they collected on sea lice in the Broughton Archipelago, and determined that water temperature and salinity had no effect on the abundance of mobile stages of L. salmonis, whereas location of farms and time of year were among factors that did significantly affect louse abundance. These authors concluded that effective management programs for L. salmonis should be based not only on geographical location, but also on these other factors. Predictive models of sea lice population dynamics could assist in salmon health management on a farm and improved louse control. A simple mathematical model of a single cohort in the life cycle of L. salmonis based on laboratory trials successfully predicted the timing and numbers of parasites present on laboratory salmon (Tucker et al. 2002). Interestingly, this study also showed that the death rates of postsettlement stages of lice in experimental tanks were highly variable, despite the lack of variations in environmental conditions in a controlled laboratory environment.

Infections Related to the Presence of L. salmonis Unidentified bacteria found in the gut of L. salmonis have been proposed as a source of disease in caged salmonids (Nylund et al. 1991; Nylund et al. 1992). L. salmonis may act as a vector for Aeromonas salmonicida and infectious salmon anemia virus (Nylund et al. 1993). Furthermore, the skin damage caused by L. salmonis can result in secondary bacterial and fungal infections.

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Summary L. salmonis, the salmon louse, is a notorious parasite of salmonids and other fish. This chapter summarizes aspects of the biology of this sea louse, including geographical distribution; the existence of two distinct lineages in the Atlantic and Pacific; salinity tolerance; range of hosts and economic importance; occurrence on nonsalmonid hosts; morphology, epibionts and life cycle; temperature and duration of developmental stages; behavior and dispersal of larvae; host and site selection; parasite nutrition; and interactions with hosts, including pathogenicity; clinical signs and pathology; pathophysiology; immune response; host susceptibility; infections related to presence of L. salmonis; seasonality and epizootiology; and genetic population structure.

References Aarseth, K.A. and Schram, T.A. 1999. Wavelength-specific behaviour in Lepeophtheirus salmonis and Calanus finmarchicus to ultraviolet and visible light in laboratory experiments. Marine Ecology Progress Series 186: 211–217. Alderman, D. 2002. Trends in therapy and prophylaxis. Bulletin of the European Association of Fish Pathologists 22: 117–125. Bailey, R.J.E., Birkett, M.A., Ingvarsdðttir, A., Mordue, A.J., Mordue, W., O’Shea, B., Pickett, J.A., and Wadhams, L.J. 2006. The role of semiochemicals in host location and non-host avoidance by salmon louse (Lepeophtheirus salmonis) copepodids. Canadian Journal of Fisheries and Aquatic Sciences 63: 448–456. Beamish, R.J., Jones, S., Neville, C.E., Sweeting, R., Karreman, G., Saksida, S., and Gordon, E. 2006. Exceptional marine survival of pink salmon that entered the marine environment in 2003 suggests that farmed Atlantic salmon can coexist successfully in a marine ecosystem on the Pacific coast of Canada. ICES Journal of Marine Sciences 63: 1326–1337. Beamish, R.J., Neville, C.M., Sweeting, R.M., Jones, S.R.M., Ambers, N., Gordon, E.K., Hunter, K.L., and McDonald, T.E. 2007. A proposed life history strategy for the salmon louse, Lepeophtheirus salmonis in the subarctic Pacific. Aquaculture 264: 428–440. Berland, B. 1993. Salmon lice on wild salmon (Salmo salar L.) in western Norway. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. DeFaye), pp. 179–187. Ellis Horwood, New York. Birkeland, K. 1996. Consequences of premature return by sea trout (Salmo trutta) infested with the salmon louse (Lepeophtheirus salmonis Krøyer): migration, growth, and mortality. Canadian Journal of Fisheries and Aquatic Sciences 53: 2808–2813. Bjørn, P.A., Finstad, B., and Kristoffersen, R. 2001. Salmon lice infections of wild sea trout and Arctic char in marine and freshwaters: the effects of salmon farms. Aquaculture Research 32: 947–962. Bowers, J., Mustafa, A., Speare, D.J., Conboy, G.A., Brimacombe, M., Sims, D.E., and Burka, J.F. 2000. The physiological response of Atlantic salmon, Salmo salar L., to a single experimental challenge with sea lice, Lepeophtheirus salmonis. Journal of Fish Diseases 23: 165–172. Boxaspen, K. 1997. Geographical and temporal variation in abundance of salmon lice (Lepeophtheirus salmonis) on salmon (Salmo salar L.). ICES Journal of Marine Science 54: 1144–1147. Boxaspen, K. 2006. A review of the biology and genetics of sea lice. ICES Journal of Marine Science 63: 1304–1316. Boxaspen, K. and Naess, T. 2000. Development of eggs and the planktonic stages of salmon lice (Lepeophtheirus salmonis) at low temperatures. Contributions to Zoology 69: 51–55. Boxaspen, K., Heuch, P.A., Bjørn, P.A., Finstad, B., Frost, P., and Glover, K. 2007. Salmon lice: Importance, problem and treatment. In: Aquaculture Research, From Cage to Consumption

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(eds M. Thomassen, R. Gudding, B. Norberg, and L. Jørgensen), pp. 322–366. Norwegian Research Council, Oslo. Boxshall, G.A. 1977. The histopathology of infection by Lepeophtheirus pectoralis (M¨ uller) (Copepoda: Caligidae). Journal of Fish Biology 10: 411–415. Boxshall, G.A. and Defaye, D. (eds.). 1993. Pathogens of Wild and Farmed Fish: Sea Lice. Ellis Horwood, London. Brandal, P.O. and Egidius, E. 1977. Preliminary report on oral treatment against sea lice, Lepeophtheirus salmonis with Neguvon. Aquaculture 10: 177–178. Brandal, P.O., Egidius, E., and Romslo, I. 1976. Host blood: a major food component for the parasitic copepod Lepeophtheirus salmonis Krøyer, 1838 (Crustacea: Caligidae). Norwegian Journal of Zoology 24: 341–343. Bricknell, I.R., Dalesman, S.J., O’Shea B., Pert, C.C., and Luntz, A.J.M. 2006. Effect of environmental salinity on sea lice Lepeophtheirus salmonis settlement success. Diseases of Aquatic Organisms 71: 201–212. Bron, J.E., Sommerville, C., and Rae, G.H. 1993. Aspects of the behaviour of copepodid larvae of the salmon louse Lepeophtheirus salmonis (Krøyer, 1837). In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. DeFaye), pp. 125–142. Ellis Horwood, New York. Bron, J.E., Sommerville, C., Jones, M., and Rae, G.H. 1991. The settlement and attachment of early stages of the salmon louse, Lepeophtheirus salmonis (Copepoda: Caligidae) on the salmon host, Salmo salar. Journal of Zoology 224: 201–212. Brooks, K.M. 2005. The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada. Reviews in Fisheries Science 13: 177–204. Brooks, K.M. and Jones, S.R.M. 2008. Perspectives on pink salmon and sea lice: scientific evidence fails to support the extinction hypothesis. Reviews in Fisheries Science 16: 403–412. Bruno, D.W. and Stone, J. 1990. The role of saithe, Pollachius virens L., as a host for the sea lice, Lepeophtheirus salmonis and Caligus elongatus Nordmann. Aquaculture 89: 201–207. Butler, J.R.A. 2002. Wild salmonids and sea louse infestations on the west coast of Scotland: sources of infection and implications for the management of marine salmon farms. Pest Management Science 58: 595–608. Costello, M.J. 1993. Review of methods of control of sea lice (Caligidae: Crustacea) infestation on salmon (Salmo salar) farms. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall, and D. DeFaye), pp. 219–252. Ellis Horwood, New York. Costello, M.J. 2006. Ecology of sea lice parasitic on farmed and wild fish. Trends in Parasitology 2210: 475–483. Costello, M. and Boxshall, G.A. 2000. Editorial. Aquaculture Research 31: 793–794. Costelloe, M., Costelloe, J., O’Donohoe, G., Coghlan, N., and O’Connor, B. 1999. A review of field studies on the sea louse, Lepeophtheirus salmonis Krøyer, on the west coast of Ireland. Bulletin of the European Association of Fish Pathologists 19: 260–264. Davies, I. and Rodger, G. 2000. A review of the use of ivermectin as a treatment for sea lice [Lepeophtheirus salmonis (Krøyer) and Caligus elongatus Nordmann] infestation in farmed Atlantic salmon (Salmo salar L.). Aquaculture Research 31: 869–883. Dawson, L.H.J., Pike, A.W., Houlihan, D.F., and McVicar, A.H. 1997. Comparison of the susceptibility of sea trout (Salmo trutta L.) and Atlantic salmon (Salmo salar L.) to sea lice (Lepeophtheirus salmonis)(Krøyer, 1837) infections. ICES Journal of Marine Science 54: 1129–1139. Dixon, B., Shinn, A., and Sommerville, C. 2004. Genetic characterisation of populations of the ectoparasitic caligid, Lepeophtheirus salmonis (Krøyer, 1837) using randomly amplified polymorphic DNA. Aquaculture Research 35: 730–741. Egidius, E. 1985 Salmon lice, Lepeophtheirus salmonis. Journal of Animal Morphology and Physiology leaflet 26: 1–4.

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Tucker, C., Norman, R., Shinn, A.P., Bron, J.E., Sommerville, C., and Wootten, R. 2002. A single cohort time delay model of the life-cycle of the salmon louse Lepeophtheirus salmonis on Atlantic salmon Salmo salar. Fish Pathology 37: 107–118. Tully, O. 1989. The succession of generations and growth of the caligoid copepods Caligus elongatus and Leopeoptheirus salmonis parasitising farmed Atlantic salmon smolts (Salmo salar L.). Journal of the Marine Biological Association of the United Kingdom 69: 279–287. Tully, O. and Whelan, K.F. 1992. The impact of sea lice (Lepeophtheirus salmonis) infestation of sea trout (Salmo trutta L.) along the west coast of Ireland, 1989–1991. Paper presented at the Conference on Pathological Conditions of Wild Salmonids SOAFD Marine Laboratory, Aberdeen, Scotland, UK. Tully, O. and Nolan, D.T. 2002. A review of the population biology and host-parasite interactions of the sea louse Lepeophtheirus salmonis (Copepoda Caligidae). Parasitology 124: s165–s182. Urawa, S. 1998. A study of Lepeophtheirus salmonis (Copepoda, Caligidae) on sea watercultured coho salmon (Oncorhynchus kisutch) and rainbow trout (O. mykiss) in Japan. Bulletin of the National Salmon Resources Centre 1: 35–38. Wagner, G.N. and McKinley, R.S. 2004. Anaemia and salmonid swimming performance: the potential effects of sub-lethal sea lice infection. Journal of Fish Biology 64: 1027–1038. Wagner, G.N., Fast, M.D., and Johnson, S.C. 2008. Physiology and immunology of Lepeophtheirus salmonis infections of salmonids. Trends in Parasitology 24: 176–183. Wagner, G., McKinley, R., Bjørn, P.A., and Finstad, B. 2003. Physiological impact of sea lice on swimming performance of Atlantic salmon. Journal of Fish Biology 62: 1000–1009. Webster, S.J., Dill, L.M., and Butterworth, K. 2007. The effect of sea lice infestation on the salinity preference and energetic expenditure of juvenile pink salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Sciences 64: 672–680. Wells, A., Grierson, C.E., MacKenzie, M., Russon, I.J., Reinardy, H., Middlemiss, C., Bjørn, P.A., Finstad, B., Wendelaar Bonga, S.E., Todd, C.D., Hazon, N., and Nazon, N. 2006. Physiological effects of simultaneous, abrupt seawater entry and sea lice (Lepeophtheirus salmonis) infestation of wild, sea-run brown trout (Salmo trutta) smolts. Canadian Journal of Fisheries and Aquatic Sciences 63: 2809–2821. White, H.C. 1940. “Sea lice” (Lepeophtheirus) and death of salmon. Canadian Journal of Fisheries and Aquatic Sciences 5: 172–175. White, H.C. 1942. Life history of Lepeophtheirus salmonis. Journal of the Fisheries Research Board of Canada 6: 24–29. Wilson, C.B. 1905. North American parasitic copepods belonging to the family Caligidae. Pt 1. The Caliginae. Proceedings of the US National Museum 28: 479–672. Wootten, R., Smith, J.W., and Needham, E.A. 1977. Studies on the salmon louse, Lepeophtheirus. Bulletin de l’Office International des Epizooties 87: 521–522. Wootten, R., Smith, J.W., and Needham, E.A. 1982. Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus. Proceedings of the Royal Society of Edinburgh 81B: 185–197. Yazawa, R., Yasuike, M., Leong, J., von Schalburg, K., Cooper, G., Beetz-Sargent, M., Robb, A., Davidson, W., Jones, S., and Koop, B. 2008. EST and mitochondrial DNA sequences support a distinct Pacific form of salmon louse, Lepeophtheirus salmonis. Marine Biotechnology.

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Part I The Distribution and Abundance of Planktonic Larval Stages of Lepeophtheirus salmonis: Surveillance and Modeling

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Modeling the Distribution and Abundance of Planktonic Larval Stages of Lepeophtheirus salmonis in Norway Lars Asplin, Karin K. Boxaspen, and Anne D. Sandvik

Introduction Norway spans from a latitude of 58◦ N to 71◦ N and has a long coastline of about 3000 km (Figure 1.1). The coast has numerous islands and fjords of various sizes, and the topography is frequently complicated. Some general features exist for the Norwegian fjords and usually they are much longer than they are wide. Fjord lengths can be several tens of kilometers, and the longest fjord, the Sognefjord, is more than 200 km long with a width between 2 and 5 km. Fjords are often several hundreds of meters deep, and deeper than the outside coastal ocean. Steep mountains surrounding the fjords influence the atmospheric conditions by channeling the winds along the fjord axis, which provides shelter and reduced possibilities for long wave fetches. The oceanography of fjords is complicated by winds, freshwater runoff, tides, and internal wave interaction with the coastal ocean (Farmer and Freeland 1983; Dyer 1997). The topography of the fjords further complicates the dynamics. For example, in a narrow fjord, less than about 1 km, the hydrodynamics will be unaffected by the rotation of the earth. In a fjord wider than 1–2 km, the earth’s rotation hydrodynamics must be considered, and the difference between nonrotating and rotating dynamics is large. In nonrotating dynamics, the equilibrium state, or the path of least resistance, is one of stable water masses and no motion or surface elevation. In rotating dynamics, the rotation of the earth, the Coriolis acceleration, must be balanced by the other forces. The equilibrium state is one of motion, the geostrophic current, and horizontal pressure forces. In the rotating system, energy needs to be supplied to the water masses to slow them down toward a state of no motion. Interestingly, little is known about the transition between nonrotating and rotating dynamics. The water masses are relatively cold and have strong upper layer stratification. Temperatures in the upper 10–20-m depths range between 0 and 5◦ C during winter and can exceed 20◦ C at the surface during summer. Below the pycnocline at 30–50-m depth, the mean temperature is between 7 and 8◦ C. Seasonal temperature variation is much lower, lagging temperatures in the surface layer by several months. This temperature range is favorable for the farming of Atlantic salmon. The water stratification is Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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Figure 1.1. Norway with its 3000-km-long coastline and numerous fjords and islands suitable for fish farming. The two larger fjords, Hardangerfjord and Sognefjord, are shown inside the yellow square and the smaller picture. (See also color plate section.)

weakest during the cold season when the precipitation accumulates as snow in the mountains. During the spring and through to the end of the fall, river runoff and precipitation create a distinct surface brackish layer in the fjords. Such a layer is typically strongest in the inner part, as seen from a long section of hydrography in the Hardangerfjord from July 2008 (Figure 1.2). The brackish layer is gradually mixed with the deeper fjord water toward the coast. The brackish layer depth depends on the amount of discharged freshwater and fjord topography, and is typically between 1

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and 10 m for Norwegian fjords. The presence of the brackish layer, and the downward mixing of buoyant water, create a strong vertical gradient in temperature and salinity in the upper 10–20 m of the fjord water. Many of the numerous rivers along the Norwegian coast contain Atlantic salmon and other salmonids. In an assessment report of a working group reporting to the Directorate for Nature Management, 452 salmon rivers were identified (Hansen et al. 2008). Almost half of these rivers have been negatively altered by human activities. The estimated number of wild Atlantic salmon returning from the ocean in 2007 was 470,000, which is the second lowest from 1983 to 2007 (Hansen et al. 2008). Norwegian coastal waters and fjords are suitable for farming of Atlantic salmon not only due to the natural water quality conditions but also due to the large relatively sheltered areas. Since its beginning around 1970, salmon farming has increased enormously and today produces more than 800,000 tons (see Chapter 5 contributed by Ritchie and Boxaspen). This represents an abundance of approximately 300 million individuals in almost 1000 licensed sites (see also Chapter 5 contributed by Ritchie and Boxaspen; statistics from the Directorate of Fisheries, http://www.fdir.no). Thus, the number of farmed salmon is between 500 and 1000 times larger than that of the wild salmon. Just one licensed site potentially holds almost as many fish as the number of all wild stocks. The salmon louse (Lepeophtheirus salmonis) is the main parasite on the Atlantic salmon in Norway. Salmon lice are mostly a threat to the welfare and existence of wild salmon stocks and are considered to be partly responsible for the observed wild stock decline (Hansen et al. 2008; Heuch et al. 2005). The salmon louse has ten stages, where the first three are planktonic (see the introductory chapter contributed by Hayward et al.). Environmental conditions of the water are critical for the growth and distribution of these planktonic stages. The abundance and distribution of salmon lice in the fjord and coastal waters can be critical for the production of Atlantic salmon stocks. Strong variability of the environmental conditions will lead to variability of the abundance and distribution of the salmon lice in the fjord and coastal waters. Factors influencing this variability are the production of salmon lice eggs (mostly from the farmed fish; Heuch et al. 2005), the water current that determines the spreading of the planktonic salmon lice, the water temperature determining the growth rates of eggs and the larval stages, and the salinity influencing the salmon lice survival and behavior (Heuch 1995). This chapter considers aspects of the salmon lice distribution and abundance in Norwegian fjord and coastal waters. Although we show results from two large fjord systems at the western coast, the Hardangerfjord and the Sognefjord, the results mostly apply to the whole Norwegian coast. We identify typical variability of the environmental conditions as current and hydrography and present model results and observations of salmon lice distribution. We do not consider production of lice from farms as a source of variability to planktonic salmon lice.

Methods to Determine Planktonic Louse Distribution and Abundance A broad range of methods are needed for the collection of information that can be used to understand the dynamics of fjord areas. The spatial and temporal variability is sufficiently complex that there needs to be a massive observational system or a

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combination of a few central observations and numerical modeling. Thus, we use a combined approach of both observations and numerical modeling as scientific methods. The use of numerical models has the extra advantage that the results can be used for hindcasts and forecasts, as well as to run applications such as the salmon lice growth and distribution model. The numerical modeling approach we use is similar to models used in weather predictions. As we all know, the weather is a highly chaotic and a relatively unpredictable system on time scales more than a few days. The situation is slightly better in the ocean, as the evolution of the system is much slower and the predictable period longer. For weather predictions and ocean predictions, reliable results depend on a good initial state and, most importantly, on good forcing. Thus, we have spent much effort to optimize the forcing and have established an approach to simulate the spreading of the salmon lice. First, we needed detailed information of the winds and the atmospheric conditions to run a mesoscale atmospheric model. Second, we needed detailed information on the conditions in the coastal ocean outside the fjord to run a system consisting of an ocean and a nested coastal model. Then, we could run the fjord model and, finally, the salmon lice growth and advection model. Observations were needed for model validation and for the construction of initial model fields. Quantifying the uncertainty of the model results identifies the limitations. However, this is not a trivial task, even with numerous observations. Dee (1995) describes a pragmatic approach to model validation. He proposed the following definition: Validation of a computational model is the process of formulating and substantiating explicit claims about the applicability and accuracy of computational results, with reference to the intended purpose of the model as well as to the natural system it represents. Thus, a validated model is not necessarily “correct,” but it has been subjected to a variety of validation activities that indicate the expected accuracy of model predictions. Model validation for generic numerical ocean models is an ongoing process. The described methods are generic in the sense that they can be applied to all areas of the Norwegian coast. Model implementations already exist for several fjord and coastal areas of Norway.

Observation of the Environmental Conditions Measurements of salinity and temperature were made either with a CTD-sonde (SAIV SD204, http://www.saivas.no) or with sensors for conductivity and temperature from Aanderaa Instruments (http://www.aadi.no) attached to an observational buoy. Collectively, these instruments measure conductivity, temperature, and depth. The measuring interval of 1 second for the CTD-sonde was appropriate for making vertical profiles at various locations. The sensors of the observational buoy produced 10-minute averages of salinity, temperature, and density. Current measurements were made from either a vertical profiler, measuring flow in 1-m bins with a range of 30–50 m (the Nortek Aquadopp Profiler, http://www.nortek-as.com), or an Aanderaa Instruments Doppler current sensor 4100 (http://www.aadi.no) that measured the

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current close to an observational buoy. The positions of the observational buoy and the current meter mooring are shown in Figure 1.2.

Observation of Salmon Lice—Sentinel Cages Direct observations of free-living planktonic salmon lice stages are difficult. Some success has been achieved in Scottish lochs using a small plankton net (Penston et al. 2004). In Norwegian fjords, a similar approach has so far not experienced similar success. Instead, we have developed, over a 10-year period, an indirect method for assessing planktonic salmon lice abundance using small cages stocked with Atlantic salmon smolts as sentinels (see also Chapter 5 contributed by Ritchie and Boxaspen, and Chapter 2 contributed by Murray et al.). Each cage has a volume of approximately 1 m3 holding 20–30 fish of 80–100 g (Figure 1.3). After 3-week deployment, the fish are recovered and the attached salmon lice are counted. We are working on an assessment of the accuracy of the sentinel cage method for estimating salmon lice infection and, especially, how to transfer these numbers to the infection pressure on the wild fish stock.

Figure 1.3. The layout of the sentinel cage being moored to a larger surface buoy attached to a ∼100-kg anchor. Typically, the moorings are deployed at depths between 50 and 150 m.

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The Coastal Ocean Model We used a coastal ocean model system consisting of a North Sea model with 20-km horizontal grid resolution and a Western Norwegian coast model with 4-km horizontal resolution nested in the North Sea model to model explicitly the open boundary conditions toward the coast for the fjord model. The Princeton Ocean Model (Blumberg and Mellor 1987) is the main engine for the implementation of both the North Sea model and the Western Norwegian coast model. The Princeton Ocean Model is a primitive-equation, free-surface, three-dimensional, σ -coordinate ocean model. This model has been used for many years at the Institute of Marine Research and is named the Norwegian Ecological Model System (NORWECOM; Skogen and Søiland 1998). Initial values as well as boundary conditions for the North Sea model were taken from climatologies (Martinsen et al. 1992). The model system was forced by atmospheric fields from the hindcast archive of the Norwegian Meteorological Institute (Reistad and Iden 1998) and river data from a multitude of sources. Boundary values for the fjord model were written every 30 minutes.

The Atmospheric Model The MM5 mesoscale atmospheric model is a nonhydrostatic σ -coordinate model developed at the Pennsylvania State University and the National Center for Atmospheric Research in the United States (Dudhia 1993). For the present study, MM5 was configured with two domains with horizontal grid resolutions of 9 km and 3 km. The innermost nest covered the western part of Norway including both the Sognefjord and the Hardangerfjord. In the vertical, 23 σ -coordinates were used where the lower level was approximately 38 m above the surface and the upper level at 15-km height. The MM5 contains parameterizations and submodels for turbulence, radiation, and cloud physics. Initial conditions were taken from the analyzed atmospheric fields of the European Centre for Medium Range Weather Forecasts, as well as boundary conditions every 6 hours. Results from the MM5 model were interpolated onto the fjord model grid as 6 hourly snapshot values.

The Fjord Model The Bergen Ocean Model is a three-dimensional σ -coordinate numerical model solving the so-called primitive equations (i.e., conservation of momentum, mass, salt, and temperature). The Bergen Ocean Model is developed at the University of Bergen and the Institute of Marine Research by Berntsen et al. (1996) on the basis of the Princeton Ocean Model. The prognostic variables are three-dimensional current, hydrography, water level, turbulent length scale, and turbulent kinetic energy. The Bergen Ocean Model has an embedded turbulence model (Mellor and Yamada 1982). The equations were solved using finite difference techniques on a staggered Arakawa C-grid. The time step was explicit. For the fjords in western Norway, the Cartesian horizontal grid consisted of 800 × 800 m2 (Figure 1.4). In the vertical, 21 levels were used with the highest resolution in the upper few meters where grid cells can only be a few

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decimeters deep in order to resolve vertical gradients caused by wind and freshwater runoff. Maximum depth was set to 400 m for technical reasons, but this will not critically affect the results for the upper 50 m, which is the region of interest for salmon lice. The details of the bottom topography below 400 m will only slightly affect the phase velocity of the tides (Asplin et al. 1999). The initial model values contained static stable conditions without any flow or water elevation and a typical vertical stratification for the simulated period. Every 30 minutes, the values at the open boundary were updated from the results of the coastal model using a flow relaxation scheme—boundary condition (Martinsen and Engedahl 1987). Every 6 hours, the wind forcing was updated from the MM5 model. River runoff was included from 62 separate rivers, on the basis of a few measurements and/or interpolations from the Norwegian Water Resources and Energy Directorate and Statkraft.

The Salmon Lice Growth and Advection Model The growth and advection in three dimensions of the first three planktonic stages of salmon lice have been modeled. The tricky part of this modeling is to incorporate

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the lice behavior, which is virtually impossible to observe other than in controlled laboratory experiments. Such models have been developed by Gillibrand and Willis (2007), Gillibrand and Amundrud (2007), and Amundrud and Murray (2007). Water current advection of salmon lice was measured using a standard particle-transport model with hourly current values from the fjord model and a random walk diffusion ˚ (Adlandsvik and Sundby 1994). At each 6-minute step, the particles were given an axisymmetric Gaussian random velocity. Typically, a diffusion coefficient in the range 1–10 m2 s−1 was used. For this advectional part of the salmon lice model, the quality of the fjord current model is believed to be most critical. For the growth of the salmon louse, we used empirical data from laboratory experiments (Boxaspen, unpublished data) and numbers reported by Stien et al. (2005). These results indicated that the salmon louse copepodid was infectious between 50 and 150 degree days after hatching. Salmon lice behavior in the model is based on the following assumptions: (1) The salmon louse has a diel migration, i.e., it swims toward the surface during daytime and downward during nighttime (Heuch et al. 1995; Hevrøy et al. 2003). (2) Salmon lice are limited to depths above 10 m since this is where wild salmon smolts reside (Davidsen et al. 2008). (3) Salmon lice avoid water of salinity <20 by swimming downward (Heuch 1995). By excluding salmon lice below 10-m depth, we only model the proportion of the planktonic population with the best chance to encounter a wild salmon smolt. The quality of the salmon lice growth and advection model might be improved by improving the louse behavior, although we need to model the mean behavior of “super particles,” i.e., model particles representing a large number or certain representative or only the successful lice.

Model Results of the Distribution and Abundance of Planktonic Salmon Lice We present examples from the variable environmental conditions and salmon lice distribution supporting the following general features of planktonic salmon lice found in Norwegian waters (1) Planktonic salmon lice can spread quickly. (2) Salmon lice can spread over large areas, although the majority of the salmon lice generally do not move very far from a given source. (3) The variability of salmon lice spreading is large. Results that we have gathered during recent years from different locations in Norwegian fjords and coastal waters indicate that the distribution and abundance of planktonic salmon lice vary substantially in a relatively unpredictable manner. This variability is related to high variability of fjord environmental conditions. Most of our sample results are from the fjords in the western part of Norway (the Hardangerfjord and the Sognefjord), but the results can typically be generalized to any fjord area along the Norwegian coast.

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Variability of the Fjord Hydrography The time variability of the hydrography in the surface waters of a fjord spans from a few hours up to seasonal and interannual scales. Temperature measurements from the observational buoy in the Hardangerfjord (its position is marked by “buoy” in Figure 1.2) at 3-m depth between July and December 2008 illustrate this variability (Figure 1.5). The seasonal signal is obvious with a high summer value and a gradual cooling through the fall. Superimposed on this trend are fluctuations of many periods and some with large amplitudes. These measurements are from the main fjord, and horizontal advection of water of different temperature is likely to occur. Frequent episodes of wind mixing the water both horizontally and vertically also occur. Thus, the temperature variability might be less in more sheltered areas such as in smaller fjords and fjord arms. We found that a change in temperature of 2–4◦ C can happen within days, e.g., around day 220 or 330 (Figure 1.5). Variability of salinity in the surface waters is associated with the variability of temperature. The lowest salinity values are in the summer, and a gradual increase occurs during the fall as illustrated from the Hardangerfjord buoy measurements at 3-m depth in June to December 2008 (Figure 1.6). Variable runoff, as well as episodes of strong winds and horizontal advection of water masses of different salinity, produces occasionally large fluctuations in the long term. Oscillations produced by internal waves occur because the density of the cooler water is mostly determined by salinity. As long as the salinity is higher than 20, its variability in the surface layer will probably not affect the salmon lice, other than the inhibiting effect of the pycnocline to vertical motion and the vertical swimming of the salmon lice. Rapid changes in salinity can occur within only a few days, e.g., around day 220 with an increase of 4–5 and around day 300 with a drop of 5–6 (Figure 1.6). In the summer period, between day 190 and 240, large oscillations of a short duration appear. This is probably when the vertical position of the halocline is in the proximity of the sensor Temperature at 3-m depth in the Hardangerfjord for 2008 22 20 18

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(at 3-m depth) and only small vertical shifts of water create large variations in the measured salinity. Because of interannual differences in regional precipitation and melting conditions, the horizontal extension of the brackish layer in the fjords will also vary interannually. We found large variations of the brackish water horizontal extension in the Hardangerfjord for June 2004–2010 (Figure 1.7). The thickness of the brackish layer was similar between the years, approximately 5–10 m, but the salinity varied significantly. The year of lowest salinity was 2005 with values <15–20 outside the fjord. The highest salinities of the brackish layer occurred in 2004, 2006, and 2009 when the measured values were mostly above 20. The horizontal extent of the brackish layer varies as well. Using a salinity of 25 as a measure, we found this isohaline farthest out of the fjord in 2007, followed by the years 2005 and 2008 with a brackish layer extension far out of the fjord. In 2004, 2006, and 2010, the horizontal extension of the measured brackish layer in June was much shorter and 50–80 km less than that for 2007 (Figure 1.7).

Variability of the Fjord Current Many factors affect the variability of the currents within a fjord. The brackish layer flow is typically strongest during the spring and summer when river runoff is at its highest. The wind-driven flow is usually stronger during the winter, although strong local wind episodes can occur year round. The tides vary between spring and neap phase, and the tidal wave propagating into the fjord from a water level change at the mouth will create stronger currents in areas of narrow and restricted topography (Farmer and Freeland 1983). In other seasons, the tidal flow inside the fjords is usually modest as it often will be part of a standing wave. The stratification of the water masses in the coastal water outside the fjords can produce internal pressure gradients into the fjords and create internal waves in wide fjords, i.e., larger than 2–3 km (Asplin et al.

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1999; Sundfjord 2010). These waves propagate at a modest speed of 0.5–1 m s−1 and can last for several days. The associated current, which can be directed both into and out of the fjord, can move large amounts of water in the upper 50–100 m of the fjords. As an illustration of currents in a large fjord, measurements from the buoy in the Hardangerfjord at 11-m depth for the period June–December 2008 showed significant fluctuations in velocity (Figure 1.8). The buoy position is marked in Figure 1.2. The flow component along the fjord axis is shown, and mean values exceeded 0.5 m s−1 on several occasions. The measurements identify a modest tidal flow of less than 0.1 m s−1 of amplitude, which is to be expected at this location where the fjord is several kilometers wide and more than 500 m deep. Other variability included rapid episodes of a strong current lasting for only a few days, probably due to strong winds (single peaks, e.g., around day 170 or 330) and episodes of relatively high mean currents lasting for many days, probably induced by internal waves propagating into the fjord from the coast (e.g., between day 180 and 200).

Fjord Model Current Validation A good representation of the current and current dispersion is important for the fjord model of salmon lice advection. In April–May 2007, there was a reasonable

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Along-fjord current component at 11 m for the Hardangerfjord East buoy in 2008 0.8

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Figure 1.8. Time series of along-fjord current (m s−1 ) at 11-m depth from the Hardangerfjord buoy as 10-minute measurements from June to December 2008. Positive values are shown into the fjord.

comparison between the numerical model results and a central current observation. The current measurement was taken farther out of the fjord (at the position marked “mooring” on Figure 1.2), and the daily mean values at 5-m depth describe a typical period of shifting conditions and large episodes of inflow or outflow to the fjord, each lasting several days (Figure 1.9). The observation is compared with the numerical model results for the same period (red line). Obviously, the fit between the observed and modeled current is not perfect, but the results are sufficient to confidently force

Along-fjord current at 5-m depth, 2007 Observation Model result

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Table 1.1. Statistics of the numerical model results and the current meter mooring at the position in the middle of the Hardangerfjord in May 2007. The currents are along the main fjord axis decomposed onto inward and outward directions.

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Depth (m)

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SD current inward (m s−1 )

Mean current outward (m s−1 )

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the salmon lice growth and advection model with the model current. Looking closer at the numbers, it is possible to identify a reasonable match between mean flow and the standard deviation when separating the current into inward and outward flow (Table 1.1).

Results of the Salmon Lice Model Spread Quickly The salmon lice model shows that salmon lice can spread quickly within the fjord. This depends on the variable current in the fjord, and the spread will be slow if released in a period of slack current. An example of rapid and rather unpredictable spreading of salmon lice is given in the results of a model simulation from May 2007 (i.e., from a period where the fjord model current compares favorable with observations, as shown in the section “Fjord Model Current Validation”). Only 24 hours are simulated using the salmon lice growth and advection model and realistic currents from the fjord model. Three batches of 200 model lice were released on May 1, May 5, and May 10, respectively (Figure 1.10). After 12 hours, the model salmon lice in the three batches were localized relatively close, but the batches did not overlap. Twelve hours later, the batch of May 5 (green colored) moved approximately 30 km into the fjord, which corresponded to a speed of 0.7 m s−1 . This is considered rapid, but according to the current observations, such current speeds are not unrealistic for shorter periods. The batch released on May 1 (red colored) moved 20 km out of the fjord between 12 and 24 hours corresponding to a speed of almost 0.5 m s−1 . The model salmon lice of the batch released on May 10 (blue colored) were no longer localized together but had spread out in most of the outer fjord system. This occurred during only 12 hours, and the speed of the individual salmon lice ranged from zero to more than 1 m s−1 .

Spread over Large Areas Another important result is that during their lifespan (up to about 150 degree days, typically 2–3 weeks for water temperatures in the range 7–14◦ C), salmon lice can spread over a large area. This is illustrated by two model simulations, which only differ in how the salmon lice were released. Both simulations were from April 29 to May 18

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Source

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36′

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Figure 1.10. Modeled spreading of salmon lice from a single source (blue arrow) and from three different release dates. Results after 12 hours (left panel) and 24 hours (right panel) are shown. The red-colored salmon lice were released on May 1, the green-colored salmon lice were released on May 5, and the blue-colored salmon lice were released on May 10, 2007. (See also color plate section.)

in 2007. A total of 800 model salmon lice were released for both simulations from only one source. For the first simulation, all 800 model salmon lice were released at the start on April 29. For the second simulation, 5 model lice were released every 3 hours throughout the period. The results from both simulations showed a distribution over a large area, covering most of the fjord system (Figure 1.11). The two different ways of releasing model salmon lice apparently do not influence the distribution in a significant manner. The distribution of the maximum distance traveled by the individual model salmon louse for a 10-day period in May 2007 showed that most of the salmon lice did not move very far from the source, i.e., typically less than 25 km (Figure 1.12). However, we did find a small number of salmon lice were able to travel more than 200 km in this 10-day period.

Large Variability The variability of planktonic salmon lice distribution depends mostly on the variable number of hatched eggs and variability of the currents. The salmon lice advection model can only quantify the variability of the currents, as the number of salmon lice modeled must be specified a priori. The currents vary in the range from hours up to interannually, and we expected to find that the variability of the salmon lice spreading is a reflection of the scale of current variability. We have seen in the previous model example that a batch of model salmon lice released only 5 days prior to another moved in a totally different direction (Figure 1.10). This serves as an example of the variability of spreading on a short time scale (hours).

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Figure 1.11. Modeled spreading of salmon lice from a single source and from two different experiments. Results at the end of the simulated period between April 29 and May 18, 2007, are shown. The blue-colored lice correspond to a simulation with a batch of 800 lice released at the start of the simulation and the red-colored model lice correspond to a simulation where 5 lice are released every 3 hours for the whole period. (See also color plate section.)

By performing sufficient model experiments, it is possible to illustrate variability on many time scales. An example of interannual variability of salmon lice distribution is from the outer part of the Sognefjord where we measured the distribution of planktonic salmon lice from an array of sentinel cages in May 2001 and May 2003. We modeled salmon lice distribution for the same periods (Figure 1.13). Both the distribution from the observations and the model results indicate that in May 2001 salmon lice spread into the fjord and in 2003 the spreading was out of the fjord and to the north. The only difference in the model results from 2001 and 2003 is the environmental conditions

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Figure 1.12. Distribution of the distance traveled in 10 days for salmon lice particles from the release position marked by source in Figure 1.11.

(the number and release of the salmon lice are identical), and the reason for the different distribution is the integrated effect of the current variability over the simulated period (May 8–28). The mean wind vector clearly indicates a more inward current system in 2001 compared to 2003. The difference in abundance (10 times more lice in 2001 than in 2003) cannot be explained by environmental variability. This can only be due to the number of hatched eggs produced between the 2 years. There were either fewer salmon farms in operation in 2003 compared to 2001 or the farmers improved their delousing skills.

Concluding Remarks The variation in the distribution of the planktonic salmon lice relates directly to the environmental variability. This variability is from hours to years and from hundreds of meters to the fjord scale. Variable currents will affect the distribution of the planktonic salmon lice, possibly moving them more than 100 km from their source (although the majority of the salmon lice move much less). Water temperature has an important influence on the growth of the salmon louse and the evolution of their populations. Salmon lice growth and egg hatching times are particularly sensitive in the temperature range between 5 and 15◦ C, temperatures typical of the spring in Norwegian fjords. It will be of crucial importance to be able to quantify the effects of environmental variability on the abundance and distribution of planktonic salmon lice. This will necessarily be related to the production of salmon lice for a region. Other factors, and possibly more important for such an estimate, will be the number and size of the fish as well as the delousing treatment success for a salmon lice population on farmed fish.

48 20'

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6°E 18'

> 250 200 - 250 150 - 200

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Figure 1.13. Observations of salmon lice distribution and abundance from sentinel cages in the spring of 2001 and 2003 (upper panels) and salmon lice model results for the same period (lower panels). Blue dots in the upper panels show the positions of the cages. The large red dots in the lower panels mark the release position for the model salmon lice. The wind vectors represent the average wind for the simulated period May 8–28 in 2001 and 2003, respectively. (See also color plate section.)

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An approach using a population dynamics model for salmon lice coupled to an advection and growth model might quantify the appropriate capacity of a region to contain salmon lice from aquaculture. Maintaining aquaculture and the sea trout stocks residing within fjords is challenging from the management standpoint. A modeling approach will possibly be a way to manage fish farms such that there will be capacity for both the wild fish and an aquaculture industry.

References ˚ Adlandsvik, B. and Sundby, S. 1994. Modelling the transport of cod larvae from the Lofoten area. ICES Journal of Marine Science Symposium 198: 379–392. Amundrud, T.L. and Murray, A.G. 2007. Validating particle tracking models of sea lice dispersion in Scottish sea lochs. ICES CM 2007/B:05,12 p. Asplin, L., Salvanes, A.G.V., and Kristoffersen, J.B. 1999. Non-local wind-driven fjord-coast advection and its potential effect on plankton and fish recruitment. Fisheries Oceanography 8: 255–263. Berntsen, J., Skogen, M.D., and Espelid, T.O. 1996. Description of a sigma-coordinate ocean model. Fisken og havet, Institute of Marine Research, Norway, 12, 33 p. Blumberg, A.F. and Mellor, G.L. 1987. A description of a three-dimensional coastal ocean circulation model. In: Three-Dimensional Coastal Ocean Models (ed. N. Heaps), Vol. 4, pp. 1–16. American Geophysical Union, Washington, DC. Davidsen, J.G., Plantalech Manel-la, N., Økland, F., Diserud, O.H., Thorstad, E.B., Finstad, B., Sivertsg˚ard, R., McKinley, R.S., and Rikardsen, A.H. 2008. Changes in swimming depths of Atlantic salmon Salmo salar post-smolts relative to light intensity. Journal of Fish Biology 73: 1065–1074. Dee, D.P. 1995. A pragmatic approach to model validation. In: Quantitative Skill Assessment for Coastal Ocean Models (eds D.R. Lynch and A.M. Davies), pp. 1–13. American Geophysical Union, Washington, DC. Dudhia, J. 1993. A nonhydrostatic version of the Penn State-NCAR mesoscale model: validation tests and simulation of an Atlantic cyclone and cold front. Monthly Weather Review 121: 1493–1513. Dyer, K.R. 1997. Estuaries: A Physical Introduction. John Wiley & Sons, Ltd., Chichester, 195 p. Farmer, D.M. and Freeland, H.J. 1983. The physical oceanography of fjords. Progress in Oceanography 12(2): 147–220. Gillibrand, P.A. and Amundrud, T.L. 2007. A numerical study of the tidal circulation and buoyancy effects in a Scottish fjord. Journal of Geophysical Research (Oceans) 112: C05030. Gillibrand, P.A. and Willis K. 2007. Dispersal of sea louse larvae from salmon farms: modelling the influence of environmental conditions and larval behaviour. Aquatic Biology 1: 63–75. Hansen, L.P., Fiske, P., Holm, M., Jensen, A.J., and Sægrov, H. 2008. Bestandsstatus for laks i Norge. Prognoser for 2008. Rapport fra arbeidsgruppe. Utredning for DN 2008-5, 66 p. (In Norwegian.) Heuch, P.A. 1995. Experimental evidence for aggregation of salmon louse copepodids, Lepeophtheirus salmonis, in step salinity gradients. Journal of the Marine Biological Association of the United Kingdom 75: 927–939. Heuch, P.A., Bjørn, P.A., Finstad, B., Holst, J.C., Asplin, L., and Nilsen, F. 2005. A review of the Norwegian National Action Plan Against Salmon Lice on Salmonids: the effect on wild salmonids. Aquaculture 246: 79–92. Heuch, P.A., Parsons, A., and Boxaspen, K. 1995. Diel vertical migration: a possible hostfinding mechanism in salmon louse (Lepeophtheirus salmonis) copepodids? Canadian Journal of Fisheries and Aquatic Sciences 52: 681–689.

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Hevrøy, E.M., Boxaspen, K.K., Oppedal, F., Taranger, G.L., and Holm, J.C. 2003. The effect of artificial light treatment and depth on the infestation of the sea louse Lepeophtheirus salmonis on Atlantic salmon (Salmo salar L.) culture. Aquaculture 220: 1–14. Martinsen, E.A. and Engedahl, H. 1987. Implementation and testing of a lateral boundary scheme as an open boundary condition for a barotropic model. Coastal Engineering 11: 603–637. ˚ Martinsen, E.A., Engedahl, H., Ottersen, G., Adlandsvik, B., Loeng, H., and Bali˜ no, B. 1992. MetOcean MOdeling Project, Climatological and hydrographical data for hindcast of ocean currents. Technical report 100. The Norwegian Meteorological Institute, Oslo, Norway, 93 p. Mellor, G.L. and Yamada, T. 1982. Development of a turbulence closure model for geophysical fluid problems. Reviews of Geophysics and Space Physics 20: 851–875. Penston, M.J., McKibben, M.A., Hay, D.W., and Gillibrand, P.A. 2004. Observations on openwater densities of sea lice larvae in Loch Shieldaig, Western Scotland. Aquaculture Research 35: 793–805. Reistad, M. and Iden, K.A. 1998. Updating, correction and evaluation of a hindcast data base of air pressure, winds and waves for the North Sea, Norwegian Sea and the Barents Sea. Technical report 9. Det Norske Meteorologiske Institutt, Oslo, Norway, 42 p. Skogen, M.D. and Søiland, H. 1998. A user’s guide to NORWECOM v2.0. The NORWegian ECOlogical Model system. Technical report. Fisken og havet 18/98, Institute of Marine Research, Pb. 1870, N-5024 Bergen, Norway, 42 p. Stien, A., Bjorn, P.A., Heuch, P.A., and Elston, D.A. 2005. Population dynamics of salmon lice Lepeophtheirus salmonis on Atlantic salmon and sea trout. Marine Ecology Progress Series, 290: 263–275. Sundfjord, V.N. 2010. Volume transport due to coastal wind-driven internal pulses in the Hardangerfjord. Master’s thesis, Department of Geosciences, MetOs section, University of Oslo, Norway, 62 p.

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Chapter 2

Abundance and Distribution of Larval Sea Lice in Scottish Coastal Waters Alexander G. Murray, Trish L. Amundrud, Michael J. Penston, Campbell C. Pert, and Stuart J. Middlemas

Scotland’s Coastal Waters Scotland sits in the Northern Hemisphere between the North Sea to the east, and the Atlantic to the west at latitudes of approximately 55◦ N to 60◦ N. The east coast is relatively smooth and dominated by large firths (large sea bays), while the western coast and island regions contain more than 100 distinct sea lochs or voes. Many of these sea lochs or voes are fjordic, others take the form of drowned river valleys and the range of size and circulation characteristics is very broad. The term “sea loch” is used to describe estuaries on Scotland’s mainland and western islands, while “voes” are estuaries in the northern island groups of Orkney and Shetland. As the terminology is geographical, rather than indicative of water-body characteristics, hereafter both are referred to inclusively as sea lochs. It is primarily in Scotland’s sea lochs that the aquaculture industry interacts with the natural ecosystem, including wild fish populations. Small amounts of salmonid aquaculture previously existed in east coast firths, but current marine production is located solely to the west and north of the country with more than 250 finfish farms currently licensed (Smith 2007) in nearly 50 different hydrographically defined management areas (Anon. 2000). Most lochs contain five or fewer farms, while 20% of larger sea lochs scattered around Scotland contain more than 15 farms each. The sea lochs that contain finfish farms and/or wild fish populations vary wildly in characteristics, which are likely to impact the way sea lice behave and interact with wild salmonids. From the largest of these (Loch Fyne) with a surface area of 183.7 km2 to the smallest (Northra Voe) at 0.2 km2 , sea lochs vary in size, depth, freshwater input, circulation, and tidal range. Therefore, we present only a very brief summary of their characteristics.

Temperature and Salinity Located on the northeast edge of the North Atlantic, Scotland benefits from the warm oceanic currents extending up from the Gulf Stream, with surface temperatures in February averaging 7◦ C in the Hebrides, 6◦ C in Orkney, and 4◦ C in closer inshore Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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waters on the west coast of the mainland. In July, temperatures range from 13◦ C in the Hebrides and Orkney Islands, to 16◦ C in more inshore areas. Surface salinities in coastal waters tend to be slightly higher in summer due to lower freshwater input, but this difference is relatively small (Craig 1959). Due to climate change, temperatures of Scottish waters have been elevated in recent years (Hughes 2007).

Sea Loch Circulation Many of the sea lochs in Scotland are fjordic, with steep sides and deep basins cut off from coastal waters by shallow sills at the loch mouth. Sea loch sills have an average mean depth of 20 m and an average maximum depth of 34 m. Mean sill depths range from a maximum mean depth of 78 m (Loch Dunvegan, on the Isle of Skye) to a minimum mean depth of 1 m or less (multiple lochs). These sills have the potential for limited mixing between bottom water and outside oceanic coastal waters. Scotland also has a smaller number of sea lochs without sills. Here, oceanic water will be able to easily mix with the bottom sea loch water through the traditional two-layer flow associated with estuarine circulation (Dyer 1973). Freshwater flows generally play a relatively minor role in circulation in Scottish sea lochs, which is often dominated by tidal and wind-driven circulation. Most of Scotland’s larger rivers flow to the east coast, so freshwater input into most west-coast sea lochs is small relative to their total volume. Scotland’s temperate climate results in a lack of seasonality in rainfall and a lack of significant winter snow accumulation. This ensures a steady flow of freshwater input to sea lochs throughout the year with any seasonal variation smaller than variation due to short-term weather events. However, freshwater input does drive net seaward surface flows. Freshwater inputs potentially play an important role in sea lice viability. Reduced salinities strongly reduce sea lice survival, which would be of relevance for many river mouths within lochs. Colder freshwater input during the winter months could have an influence on lice life spans and maturation rates during the winter season. Tidal mixing and transport contribute significantly to the circulation in Scottish sea lochs. Scotland’s tides vary with location, but tidal range often exceeds 4 m and can reach as much as 5 m in some locations. Reflecting this tidal prism, calculations are often used as a simple estimate of water exchange processes in a sea loch for management purposes (i.e., Gillibrand and Turrell 1997). Tidal flows also lead to complex three-dimensional surface circulation patterns in enclosed areas, such as sea lochs, creating strong tidal gyres that can dominate local circulation (see section “Hydrodynamics and the Physical Environment”). This complex flow is important for understanding the transport of parasites such as sea lice between salmonid populations (whether farmed or wild). However, not all of Scottish sea lochs experience these high tidal regimes. The Shetland Islands have considerably lower tides of approximately 1 m in range, whilst the lowest tidal range recorded in the sea loch catalogue (Edwards and Sharples 1986) is at Caolisport, opening into the Sound of Jura, in the southwest corner of the Scottish mainland. It is therefore overly simplistic to categorize all sea loch circulation as dominated by tidal forcing and more sophisticated models of circulation and mixing (similar to FJORDENV; Stigebrandt 2001) are under development for aiding in the management of Scotland’s coastal waters.

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Wind is an important, often dominant, contributor to the surface circulation in sea lochs, and therefore to the transport of sea lice. Extensive fieldwork and modeling in Loch Torridon (Amundrud et al. 2006; Gillibrand and Amundrud 2007; Amundrud and Murray 2009) highlights the importance of wind-driven transport to the patterns of lice dispersion. Transport dominated by wind direction, rather than tidal cycles or freshwater input, varies greatly with short-term weather events in this system. Many Scottish sea lochs (including Loch Torridon) are surrounded by steep, mountainous terrain that will funnel winds preferentially in certain directions. Understanding local sea lice transport will therefore require observations of local rather than regional wind patterns.

Coastal Transport Scottish sea lochs are relatively small enclosed basins with an average length of 8.4 km (Edwards and Sharples 1986), contrasting with the large fjordic systems of western Canada and Norway. Sea loch lengths vary from <1 km to 60.5 km (Loch Fyne); only 28 lochs exceed 10 km and only 9 lochs exceed 20 km in length. The small size of the lochs, combined with the known long-distance transport of sea lice larvae (Brooks 2005; Amundrud and Murray 2009) suggests that planktonic sea lice are regularly exported from some sea lochs into coastal waters. These may then be transported between the many sea lochs whose mouths are directly adjacent to each other (Figure 2.1). This suggests that management of sea lice may be more effective on regional rather than individual loch scales. Research to address this potential coastal connectivity in Scotland is now underway by the authors but as the impact will vary around the coastline, the total potential will likely remain unclear for the near future.

Sea Lice in Scotland Interaction of Lepeophtheirus Salmonis with Wild and Farmed Salmonids (See also Introduction) Atlantic salmon (Salmo salar L.) and sea trout (an anadromous form of brown trout (Salmo trutta L.)) have life strategies that include migration to the marine environment for varying periods before returning to spawn in their native rivers. There is a high chance of contact and subsequent infection with Lepeophtheirus salmonis (Pike and Wadsworth 1999). Indeed, several studies have found that Atlantic salmon and sea trout can rapidly become infected upon migrating to sea (Tully et al. 1993a; Birkeland and Jakobsen 1997; MacKenzie et al. 1998; Finstad et al. 2000; Hatton-Ellis et al. 2006). Atlantic salmon undertake lengthy migrations, often traveling long distances in the oceanic environment for considerable periods of their lives. In contrast, sea trout usually remain in shallow coastal waters (Pemberton 1976; Jarrams 1987; Potter 1990; Middlemas et al. 2009), although some sea trout can migrate considerable distances at sea (Potter 1990). Atlantic salmon are commonly infected with sea lice at a high prevalence although returning adults rarely have the larval chalimus stages attached (Todd et al. 2000). The prevalence and intensity of L. salmonis infections on Atlantic

54 2

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Figure 2.1. Positions of the Atlantic salmon farms (boxed numbers), plankton samples stations (underlined letters), and sentinel cages (crossed circles) in the Loch Torridon system. The inserts show the position of the study area in relation to (i) the British Isles and (ii) Scotland.

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salmon increases with time at sea. Jacobsen and Gaard (1997) reported that two sea winter (SW) fish typically had a higher abundance of mobile L. salmonis than one SW fish (see also Chapter 7 contributed by Revie). With the development of intensive marine salmonid farms that provide a high population of hosts in condensed inshore areas, the potential for farmed/wild fish interactions of sea lice are high (Pike and Wadsworth 1999; Johnson et al. 2004; Heuch et al. 2005). The quantitative risk of cultured salmonids infecting wild stocks is difficult to determine and will vary depending on the degree of overlap between cage sites and migratory routes, the dispersion and survival rates of copepodids emanating from the farmed salmonids, and the behavior of potential hosts and copepodids in the marine environment (Pike and Wadsworth 1999). Stocks of Atlantic salmon and sea trout have experienced serious declines in many areas, particularly the west coast of Scotland and Ireland (Vøllestad et al. 2009). Sea lice populations associated with aquaculture activities have been implicated as an important threat to wild salmonids (Anon. 1993, 2002; Butler 2002; Ford and Myers 2008; Revie et al. 2009, Costello 2009b). During the initial marine phase of their life cycle, sea trout may be more vulnerable to sea lice infestation than Atlantic salmon because they are more likely to remain in coastal areas, which are also utilized for Atlantic salmon aquaculture. Sea trout often migrate to sea only to return to freshwater early and it has been suggested that this may be an attempt by the fish to rid themselves of sea lice (Birkeland and Jakobsen 1997; Hatton-Ellis et al. 2006) that cannot tolerate extended periods at low salinities (McLean et al. 1990; Bricknell et al. 2006; Wells et al. 2007). L. salmonis epidemics on farmed Atlantic salmon have chronologically followed the pattern of the rapid development of the Atlantic salmon farming industry (MacKinnon 1997). Even if lice abundance on farms is well controlled, the large numbers of fish on farms means these populations contribute disproportionately to larval production (Heuch and Mo 2001; Butler 2002; Penston and Davies 2009). These high lice numbers on farms have been linked to elevated lice levels on wild salmonids off the west coast of Scotland (Butler 2002; Hatton-Ellis et al. 2006) although a study by Marshall (2003) on the northwest of Scotland found no correlation between larval L. salmonis abundance on sea trout and the number of ovigerous lice on neighboring farms. The possibility that marine salmonid farming may directly or indirectly have an effect on declining wild salmonid populations is still debated, as populations have also declined in regions where no farming exists, e.g., southwest Scotland and England (McGeorge and Sommerville 1996). Nonetheless, the studies have shown that sea lice of farm origin can present, in some locations, a significant threat to wild salmonids (Anon. 2002; Revie et al. 2009; Costello 2009b). L. salmonis feed upon the mucus, skin (White 1942; Jones et al. 1990; Jonsdottir et al. 1992), and blood (Brandal et al. 1976) of the host, and infestations of this parasite can have deleterious effects on salmonids (Brandal and Egidius 1979; Wootten et al. 1982; Grimnes and Jakobsen 1996; Finstad et al. 2000). Atlantic salmon farms represent a large but variable source of infective stages available for transmission to both farmed Atlantic salmon and potentially wild salmonids (Pike and Wadsworth 1999). Therefore, the recovery of heavily infested sea trout (Tully et al. 1993a, 1993b; Hatton-Ellis et al. 2006) prompted investigations into possible interactions between L. salmonis on farmed Atlantic salmon and wild salmonids (Anon. 1993; Costelloe et al. 1998a, 1998b; Tully et al. 1999; Krkoˇsek et al. 2005).

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The dispersal and behavior of L. salmonis larvae in the natural environment remains an area of ongoing research in Scotland (Penston et al. 2008a, 2008b; Amundrud and Murray 2009; Costello 2009b). There is a geographical overlap between the environments utilized by wild salmonids and Atlantic salmon farms (Heuch et al. 2005), therefore establishing the dispersion and behavior of L. salmonis copepodids is of prime interest to better understand interactions between sea lice on farmed and wild fish.

L. salmonis Infection on Atypical Hosts Although L. salmonis is largely thought to be salmonid specific, there are reports of L. salmonis on nonsalmonid hosts. These alternative hosts might act as vectors or reservoirs when salmonids are absent from the local environment or if farmed salmon are undergoing treatment for lice (see the introductory chapter contributed by Hayward et al.). Species that have been reported in Scotland as infected with L. salmonis include sea bass (Pert et al. 2006) and saithe (Pollachius virens) (Lyndon and Toovey 2001; Bruno and Stone 1990). Three-spined sticklebacks (Gasterosteus aculeatus) may be a particularly important secondary host for Lepeophtheirus spp. in Canada (Kabata 1973; Beamish et al. 2005), subsequently identified as L. salmonis (Jones et al. 2006); however, field surveillance and laboratory studies indicated lice were prey rather than parasites and suggests three-spined sticklebacks are not an important L. salmonis host in Scotland (C. Pert, personal observations). The presence of other species of parasitic copepods has been reported from a large number of nonsalmonid species cultured in the marine environment although there are few well-documented cases of disease (Johnson et al. 2004). Johnson et al. (2004) reported damage to cultured cod in Norway caused by Caligus elongatus von Nordmann, 1832 and Caligus curtus M¨ uller O.F., 1785.

Statistical Description of Loads on Wild Salmonids Parasite loads are typically overdispersed, with a few individual hosts having loads much higher than the mean, while many have zero or very low loads. This has important implication for population-level effects on hosts; even at low mean loads some individuals may have damagingly large loads. Mortality of parasites associated with parasite-induced mortality of hosts is likely to affect a disproportionate number of parasites. Variance is associated with mean load for parasite in general, as can be shown in the following expression (Shaw and Dobson 1995): log variance = 1.551 log (mean load) + 1.098. A meta-analysis of data sets on lice loads on sea trout (Murray 2002) found a very similar expression: log variance = 1.6 log (mean load) + 0.6.

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And for lice on wild salmon from the River North Esk in eastern Scotland (Murray and Simpson 2006) is also similar: log variance = 1.35 log (mean load) + 0.51. Thus, sea lice loads on sea trout and salmon show patterns that are typical of parasites, although variance at low loads is lower than for average variance from a large range of parasite species. This reflects high prevalence even at low loads. Bakke and Harris (1998) noted there was evidence for a decline in the rate of increase in variance at higher loads, possibly because mortality was higher for fish with very high lice loads, hence limiting the upper boundary of lice loads when the mean was high.

Control of Lice in Scottish Aquaculture (See also Chapter 5 for Sea Lice Control in Other Jurisdictions) To mitigate any impact sea lice on farmed salmon may have on wild salmonids, measures are taken to prevent and/or control sea louse infestations. The prevention of louse infestations at Atlantic salmon farms is extremely difficult and antilouse treatments, often just termed lice treatments, are commonly employed in order to control such infestations (Wootten et al. 1982; Grant 2002; Revie et al. 2005, 2009). Indeed, without treatment, Revie et al. (2002a) suggested that levels of L. salmonis on Scottish farmed Atlantic salmon in the second year of production would rapidly reach levels that would threaten the sustainability of the industry and the welfare of the fish. However, reduced sensitivity of L. salmonis to the chemotherapeutants can occur, especially if they are misused (Jones et al. 1992; Lees et al. 2008b). Historically, lice on Atlantic salmon farms have been controlled using topical/bath treatments in which the net of the pen to be treated is raised up and surrounded by a tarpaulin to temporarily provide a reduced and enclosed volume (Roth 1993). R ) is added to the pen to achieve the target The chemical treatment (e.g., Excis concentration for the specified duration. After the treatment (usually 1 hour), the tarpaulin is removed and the chemical disperses into the sea (Roth 1993). Several chemicals have been used to treat lice, e.g., organophosphates, but as with this example, reduced sensitivity of L. salmonis to the chemical can occur (Jones et al. 1992; Grant 2002), so care must be taken to maintain the effectiveness of the R (emamectin benzoate), provide an medicines. In-feed treatments, such as SLICE alternative method of treating for sea lice. Oral delivery has several advantages over topical application, e.g., administration is easy and less stressful for the fish, and entire farms can be treated synchronously (Grant 2002). However, in-feed treatments cannot be used effectively if the fish are not feeding (Costello 2006). The target dose of the chemotherapeutant is applied for 7 consecutive days and confers a protective effect for approximately 10 weeks posttreatment (Stone et al. 2000; Treasurer et al. 2002). The R (cypermain chemotherapeutants currently used in Scottish aquaculture are Excis  R methrin) and SLICE (Lees et al. 2008a). The direct costs of sea louse medicines and their application, and indirect costs such as lost growth of stressed infected fish

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and downgraded carcass value, were most recently estimated to be approximately €33 million in the United Kingdom (Costello 2009a). In 1999, the Tripartite Working Group was established to address problems common to wild salmonid fisheries and Atlantic salmon farming, with an emphasis on sea lice (see www.tripartiteworkinggroup.com). The Members of the Tripartite Working Group are Marine Scotland, Scottish Natural Heritage, Scottish Environment Protection Agency, the Crown Estate, Highlands and Islands Enterprise, Highland Council, Association of Salmon Fishery Boards, Rivers and Fisheries Trust Scotland, Scottish Anglers National Association, Atlantic Salmon Trust, and Scottish Salmon Producers Organisation. The objectives of the Tripartite Working Group are to develop and promote the implementation of measures for the restoration and maintenance of healthy stocks of wild and farmed fish; to develop and promote the initiation of measures for the regeneration of wild salmon and sea trout stocks; and to propose arrangements at a local and national level for taking forward the foregoing and to ensure that the results of this work are reflected in the development of Local Authority fish farm planning guidelines and Framework Plans (Anon. 2004). The Tripartite Working Group Concordat argued for cooperation at a local level between the interests of wild and farmed salmonids and encouraged the development of Area Management Agreements (AMAs) to be run by Area Management Groups (AMGs). The role of the AMAs is “to ensure that the potential impact of aquaculture on wild fish, with particular regard to sea lice production, is minimized to create conditions in which wild fish populations could successfully co-exist with a viable aquaculture industry” (Anon. 2004). AMAs are being developed between local industry and wild fisheries interests throughout the west coast and Western Isles. To date, 18 AMAs have been implemented. These cover a range of objectives, including single-year class management and synchronized production/fallowing cycles, synchronized lice treatments, zero ovigerous salmon lice, particularly during the critical wild smolt migration period (Feb–June), and regular provision of sea louse data. The Tripartite Working Group process, previously funded by Highlands and Islands Enterprise, is now funded by the Scottish Government and will receive approximately £350,000 for each year between 2008 and 2011. This provision covers the ongoing running costs of a project manager, four Regional Development Officers (RDOs), and the cost of Tripartite Working Group meetings. Regional Development Officers liaise directly with the Tripartite Working Group Project Manager and report to the Regional Steering Committee and the Tripartite Working Group Plenary and Management Groups. RDOs facilitate the formation of AMGs, develop, deliver, and monitor the AMA process. A significant proportion of the RDO’s time is spent on field operations, such as river and farm site visits and in developing trusted working relationships between AMG partners. Time is also allocated to providing secretariat services to AMGs, liaising with other RDOs to identify common problems and potential solutions, attending meetings with the TWG Management Group and Plenary Group, and assisting in the delivery of a public relations strategy. A program was set up with the objectives of informing fish farmers and wild fish interests of the benefits of involvement in the Tripartite Working Group process and to encourage positive political and regulatory endorsement of the TWG process at both local and national levels. It also aimed to generate positive media coverage of the

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Tripartite Working Group process and to encourage new participation in Tripartite Working Group as a result of media and political endorsement for the process.

Case Study: The Loch Torridon System The Loch Torridon AMA and AMG were established in 2001. The AMG circulates information on matters of relevance to local wild and farmed salmonids, e.g., farm louse counts, and meets for discussions biannually. The Torridon AMG is joint-chaired by a wild fisheries representative and an aquaculture representative, with chairmanship alternating between each meeting. Research into sea lice interactions between wild and farmed salmonids on the Scottish west coast has benefitted from participation in the AMA process. Evidence of decline in sea lice populations has been found at both the local (Penston et al. 2008b) and national level (Lees et al. 2008a), although the efficacy of lice control chemotheraputants may be in decline (Lees et al. 2008b).

Hydrodynamics and the Physical Environment The Loch Torridon sea loch system is located on the northwest coast of Scotland (Figure 2.2). Similar to many lochs, Torridon resembles a miniature Norwegian or

A

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Figure 2.2. View from Shieldaig River (sample station S) looking in a northwesterly direction, past sample station A, toward station C, and adjacent salmon farm 1 (see Figure 2.1).

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Canadian fjord, with silled regions blocking the flow of deep water to the coastal ocean. Specifically, Loch Torridon can be described as a three-basin system, with the inner basins (Upper Loch Torridon and Loch Shieldaig) separated from the outer basin (Loch Torridon) by a series of sills. Loch Torridon itself has a low freshwater input flow, even relative to other Scottish lochs (Edwards and Sharples 1986), with annual freshwater input equaling only 10% of the volume of the loch. This low input may increase the viability of sea lice larvae within the basins, as surface salinities remain high throughout most of the loch. Freshwater input into Loch Torridon is via six small rivers located around the basin. Due to their sea trout populations, the Rivers Shieldaig and Balgy have been the subjects of sampling and modeling efforts. Much of the work described in this section is focused on Loch Shieldaig and the potential for transport of larval lice toward populations of sea trout located in the vicinity of the River Sheildaig (Figure 2.2).

Host Populations, Including Farmed and Wild Research into sea lice has been carried out in Loch Torridon (specifically in the Loch Shieldaig basin) by both the Freshwater Laboratory and Marine Laboratory of Marine Scotland since 1999 (then called FRS). Initially, there were five fish farm sites in the sea lochs, operated by two companies, with capacities of 600 to 1000 tons operating on a 2-year production cycle with synchronized fallowing. In 2006, one of the operators rationalized production of its two farms by closing the Diabaig site (farm 2) and combined their production at a single site (farm 3) in Upper Loch Torridon. Wild sea trout populations spawn in the Shieldaig, Balgy, and Torridon rivers, and salmon are found in the Balgy and to a much lesser extent, the Torridon. On going to sea, sea trout postsmolts tended to remain near their natal river for the first 14 days and thereafter undertook more extensive movements with 37% of fish detected >6 km from their natal rivers (Middlemas et al. 2009). In the River Balgy, the maximum recorded annual catch of sea trout was 394 in 1975. The maximum recorded annual catch of Atlantic salmon was just under 70 in 1987. Between 2002 and 2006, the mean annual catch of sea trout and Atlantic salmon was approximately 30 for each. There are grounds to suspect that some of the Atlantic salmon in the River Balgy are escapees from an upstream freshwater hatchery (Middlemas and Stewart 2008). Applying a rod and line exploitation rate of 15% for both salmon (Kettlewhite 2000) and sea trout (Butler 2002) to annual catches on the River Balgy between 2002 and 2006 provides an estimate of approximately 200 sea trout and 200 Atlantic salmon returning to this river. The rod and line exploitation rate applied here is likely not absolutely correct, but it serves to provide perspective of the size of the salmonid population in the River Balgy. The River Torridon is believed to have smaller populations of Atlantic salmon and sea trout than the River Balgy. A maximum catch of 60 sea trouts was reported but no fishing has taken place in the River Torridon in recent years. Atlantic salmon catches are not recorded, but very low. The River Shieldaig sea trout population has been monitored by Marine Scotland scientists since 1999 using both upstream and downstream fish traps. Historically, the

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maximum catch of sea trout was 60 but catches have declined to zero in recent years. There are no Atlantic salmons in the River Shieldaig. In late spring 2006, elevated sea lice levels were detected on postsmolt sea trout, at a time when fish farm lice levels were close to zero (Raffell et al. 2007). In late 2006, lice levels rose on the fish farms and this is reflected in the elevated larval sea lice population found during the 2006–2007 production cycle using the open-water (see section on “Offshore Sampling of Larval Lice”), shoreline (see section on “Coastal Sampling of Larval Lice”), and sentinel cage data (see section on “Sentinel Cages”).

Plankton Sampling for Larval Lice The predominant species of louse larvae recovered was L. salmonis, with very few C. elongatus being recovered (McKibben and Hay 2004a; Penston et al. 2008a, 2008b; Penston and Davies 2009). The methods of identification of louse larvae based both on morphology and a specially developed q-PCR are described in McBeath et al. (2006). Briefly, copepodids were identified morphologically based on size, the armature of the maxilliped and morphology of the prosome, and the second segment of the urosome (Schram 2004). The proximal segment of the maxilliped of L. salmonis has no process and the distal segment has a process with 3–5 “fingers.” The proximal segment of the maxilliped of C. elongatus has a medial process and the distal segment has two diverging processes originating from a common base. Almost all larvae identified from Loch Torridon were L. salmonis.

Coastal Sampling of Larval Lice McKibben and Hay (2004a) only recovered copepodids near the shoreline of Loch Shieldaig and Upper Loch Torridon when the two local Atlantic salmon farms (farms 1 and 3; Figure 2.1) were in second year of their production cycle and gravid L. salmonis were present on the farmed fish; this association is detailed in the following sections. Larval louse densities at the shoreline have shown a pattern whereby high counts are only obtained in years in which Atlantic salmon farms are in their second year of a production cycle (McKibben and Hay 2004a; Raffell et al. 2007; Figure 2.3), a time when louse loads are typically elevated at Scottish Atlantic salmon farms (Revie et al. 2002b). However, high larval counts were not obtained in 2005, in spite of this being the second year of production cycle. By this stage, all farms in Loch Torridon R . had formed an AMA and were performing synchronous treatments using SLICE An increase occurred again in 2007, possibly due to nonsynchronous application of treatments during that year or a possible reduction in the sensitivity of lice to the medication (Penston and Davies 2009).

Offshore Sampling of Larval Lice Planktonic louse data collected in the open waters of Loch Shieldaig supported the link between gravid L. salmonis on the local farm (farm 1) in Loch Shieldaig and the L. salmonis copepodids recovered at the shoreline near the mouth of the River Shieldaig (Penston et al. 2004). Copepodid densities collected at sample station A peaked approximately 2 weeks after estimated numbers of gravid L. salmonis at farm

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Figure 2.3. Larval louse counts obtained from samples station S (from 1999) and sample station A (from 2002), locations shown in Figure 2.2; note that the axis for shoreline S is 40 times that for offshore A. Y1/Y2 = first/second year of production cycle for local farms 1 and 3 (Figure 2.2).

1 peaked; and 1 week later copepodid density peaked at the shoreline. Penston et al. (2004) indicated that onshore winds may play a role in transporting planktonic larvae toward the head of Loch Shieldaig. This was supported by a cross-correlation analysis which found a significant (p-value < 0.05) relationship between the densities of copepodids at sample station A and onshore winds (Penston 2009). This finding is consistent with Costello (2006) who suggested that planktonic louse larvae in coastal waters might be transported toward estuaries by onshore winds. The larval lice formed clear spatial patterns (Penston et al. 2008a, 2008b). Sample station A (in the vicinity of the River Shieldaig) was one of the open-water sample stations where greatest densities of copepodids and lowest densities of nauplii were collected. Nauplii were recovered in greatest densities at sample stations near farms, e.g., C and G, indicating recent release near those locations. Nauplii were present in greater densities at 5 m than at 0 m depth and copepodid densities were greater at 0 m than at 5 m depth. Copepodids were more widespread than nauplii. Shoreline copepodid concentrations were an order of magnitude greater than those at offshore stations. In a study that investigated L. salmonis planktonic larval densities during three successive Atlantic salmon farm production cycles, from 2002 to 2007, temporal patterns in planktonic louse larvae densities were also evident. Densities of nauplii and copepodids were consistently low during three farm fallow periods and the first few weeks after Atlantic salmon farms stocked with louse-free smolts (Penston and Davies 2009). This pattern is consistent with the observations of Bron et al. (1993a) who suggested that fallow periods result in the minimization of numbers of farm-generated lice. Increases in nauplius and copepodid densities occurred around October of 2001 and 2002, respectively (Penston et al. 2004, 2008a). These periods coincided with the first winter of the local farming production cycle and this has been shown to be a time

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of the production cycle when numbers of mature L. salmonis increased on farmed Atlantic salmon in Scottish waters (Revie et al. 2002b). This increase in L. salmonis numbers at Atlantic salmon farms during the early winter probably results from salmonids with gravid L. salmonis returning in the late summer months initializing infections on farmed Atlantic salmon. Copepodid densities peaked in the second year of all three cycles: (1) in March and October 2003 during the 2002–2003 cycle, (2) in September 2005 during the 2004–2005 cycle, and (3) in March 2007 in the 2006–2007 cycle (Penston and Davies 2009). This pattern observed at the open-water stations is consistent with the recovery of louse larvae at the shoreline described in section “Coastal Sampling of Larval Lice” as only when farms are in their second year of production (McKibben and Hay 2004a; Figure 2.3). The peak in copepodid densities in 2005 was small in comparison to that of other second years (Figure 2.3). The comparatively low abundance of larvae in 2005 was attributed to effective lice management at the local Atlantic salmon farms (Penston et al. 2008b) and possibly explains why no larvae were recovered at the shoreline in 2005 (Figure 2.3). Of the larval densities recovered during the three production cycles (albeit the third cycle was not sampled to completion), greatest densities were recovered in March of 2003 and 2007 (Penston and Davies 2009). Atlantic salmon farms apply strategic treatments in February/March to minimize numbers of adult L. salmonis on farmed Atlantic salmon when the wild salmonids would be migrating to sea (Anon. 2006). L. salmonis counts increase at farms during the first winter (Revie et al. 2002a); therefore, a peak in L. salmonis on farmed Atlantic salmon could be expected around the time of the strategic treatments. Peaks in L. salmonis counts on Scottish Atlantic salmon farms around this time of year have also been reported elsewhere (Revie et al. 2002b; Treasurer et al. 2002). Peaks in L. salmonis on farmed Atlantic salmon corresponded with peaks in L. salmonis larval density in the water column (Penston et al. 2004, 2008b; Penston and Davies 2009). R was only used at one farm in the Loch Torridon management In 2002, SLICE area, but as the medicine became more available; by 2004, it was used to treat all of the farmed Atlantic salmon in the Loch Torridon management area. The synchronized R in the 2004–2005 production cycle achieved effective lice control use of SLICE at the Atlantic salmon farms that lasted for approximately 10 weeks (Stone et al. 2000; Treasurer et al. 2002) and this appeared to lead to conditions of low L. salmonis densities in the water column (Penston et al. 2008b; Penston and Davies 2009). During these periods, which included the summer months when wild salmonids would be most abundant, larval densities were low: the mean larval density was 0.015 ± 0.049 larvae m−3 (Penston et al. 2008b). In these instances, some of the larvae recovered in Loch Shieldaig could have been transported there from other active farms in the Torridon management area or elsewhere; however, Penston and Davies (2009) showed that the numbers of L. salmonis at all the farms in the management area were comparatively low at these times and any contributions from remote farms is unknown. The larval densities observed nonetheless point toward a low background signal of L. salmonis larvae from wild fish. The sum total number of gravid L. salmonis on farmed Atlantic salmon within Loch Torridon between January 2002 and June 2007 was estimated to be 1.2 × 107 and the upper and lower range on gravid L. salmonis on wild salmonids was estimated to be 4.18 × 105 and 1.67 × 105 , respectively. The contribution of larvae from gravid L. salmonis on wild salmonids in Loch Torridon was estimated to be smaller than that

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from farmed Atlantic salmon by an estimated factor of 29–72 (Penston and Davies 2009), and this was largely as a result of the comparatively small number of wild salmonids in the Loch Torridon system compared to the number of farmed Atlantic salmon. The small numbers of wild salmonids compared to farmed Atlantic salmon is not unique to Loch Torridon. Todd et al. (2004) stated that the numbers of wild salmonids migrating through Scottish coastal waters are extremely low compared with the numbers of Atlantic salmon held almost year-round in pens. In related studies elsewhere, larval lice from wild sources were also found to be minor in comparison to farmed sources due to the numerical dominance of farmed hosts over wild hosts (Tully and Whelan 1993; Heuch and Mo 2001; Butler 2002; Krkoˇsek et al. 2005; Costello 2006). No correlation was found between mean copepodid densities in the water column and the numbers of gravid L. salmonis on wild salmonids either with the upper estimate (p-value = 0.79) or the lower estimate (p-value = 0.43). Penston and Davies (2009) concluded that gravid L. salmonis on farmed Atlantic salmon were the most important sources of L. salmonis larvae in the Loch Torridon system. This conclusion is consistent with those from Ireland (Tully and Whelan 1993), Norway (Heuch and Mo 2001), Pacific Canada (Krkoˇsek et al. 2005), and an earlier study in Scotland (Butler 2002). The mean monthly copepodid densities at the sample stations A, C, and E correlated significantly (p< 0.001) with the monthly estimated numbers of gravid L. salmonis on combined farmed Atlantic salmon, and with the numbers on individual farms, except for farm 2. The strongest correlation between the number of gravid L. salmonis present at individual farms and the mean densities of louse copepodids was with data from farm 3. The significant relationship between mean larval densities and numbers of gravid L. salmonis at farms 1, 3, 4, and 5 generally spread from lags of ±3 months, but extended to ±5 months at farm 3. The production cycle at farm 2 was not synchronized with that at the other farms. The contributions of L. salmonis larvae from a single farm running asynchronously to the bulk of the farmed Atlantic salmon in Loch Torridon would tend to be masked by the larval output from gravid L. salmonis on the bulk of the farmed Atlantic salmon in the area. Hence, gravid numbers on farm 2 might be expected to have a low correlation, if any, with L. salmonis copepodid densities in the water column. Additionally, farm 2 is located in a sheltered, steepsided basin, seaward of the sample stations, so the local hydrography might limit the dispersal of louse larvae (section on “Sea Loch Circulation”) and may influence any relationship between the numbers of gravid L. salmonis at this farm and L. salmonis copepodid densities in the water column of the wider loch. Furthermore, farm 2 ceased production in January 2006. In contrast, the correlation coefficients of numbers of gravid L. salmonis at farms 4 and 5 with L. salmonis copepodid densities were relatively high even though they were also located seaward of the sampling stations, and had low proportions of the total numbers of farmed Atlantic salmon and gravid L. salmonis. The production cycles at farms 4 and 5 were synchronous with those of farms 1 and 3 during the first cycle. Farms 4 and 5 were only stocked in the second half of the following two cycles; but the production was essentially synchronous, as they were fallow when farms 1 and 3 were fallow. The synchronicity with the production cycles of these farms and farms 1 and 3 potentially makes it difficult to separate any correlation between the numbers of gravid L. salmonis at these small farms and the recovered copepodid densities. The correlation analysis used was potentially dominated by the largest

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contributor of L. salmonis copepodids. This may limit further interpretation of the relative significance of individual farms when production is synchronized. However, synchronization will potentially emphasize variations in gravid louse numbers arising from management strategies such as loch-wide fallowing. The significant correlations (p-value < 0.001) between the numbers of gravid L. salmonis on Atlantic salmon at farms 1, 3, 4, and 5 with the mean densities of L. salmonis copepodids recovered from the water column across sample stations supports the contention that gravid L. salmonis on farmed Atlantic salmon represented the major source of L. salmonis copepodids in Loch Torridon. An observed trend in the results suggested that the greater the biomass at a farm, the greater the number of gravid L. salmonis, and the greater the correlation with copepodid densities in the water column (with the exception of farm 2). An increase in the consented biomass at farm 3 in 2006, from 800 to 1767 tons, made this farm the largest in Loch Torridon. The number of farmed Atlantic salmon at individual farms may be a better predictor than maximum consented biomass or the total number of gravid L. salmonis at individual farms. Heuch and Mo (2001) assumed that the numbers of gravid L. salmonis on farmed Atlantic salmon were the maximum level officially permissible, and this approach would naturally lead to the conclusion that the farms with greater numbers of fish have greater numbers of gravid L. salmonis. However, in Penston and Davies (2009), the gravid burdens at each individual farm were based upon the louse counts taken at each respective farm, and yet the overall result was the same; the farms with the greatest numbers of fish during the study period had greatest numbers of gravid L. salmonis. The farms with the greatest percentage of the total number of farmed Atlantic salmon were generally estimated to have the greatest numbers of gravid L. salmonis. Atlantic salmon farms elsewhere have been indicated to be major sources of L. salmonis larvae (Tully and Whelan 1993; Heuch and Mo 2001; Butler 2002). The relationship established in Penston and Davies (2009) emphasize the importance of effective control of L. salmonis at Atlantic salmon farms.

Lice Counts from Wild Fish Lice on wild sea trout also showed a pattern of higher prevalence in the second year of farm production than in the first (Hatton-Ellis et al. 2006; Middlemas et al. 2010). There is both a higher number of sea trout returning early and a higher prevalence of sea lice infestation on these fish in years when local farms are in their second year of production (Figure 2.4). These counts were obtained by electrofishing in May and June in the first 120 m above tide line of the Shieldaig River (Hatton-Ellis et al. 2006). Only fish <198 mm were included in the data used by Middlemas et al. (2010), and presented here in Figure 2.4, because this enabled an estimate of the numbers of trout with lice intensity above a threshold for damage; this threshold was also exceeded more commonly in the second year of farm production (Middlemas et al. 2010). However, the pattern of higher loads in the second year of production is the same when all trout are included (Hatton-Ellis et al. 2006). There appeared to be a reduced load in 2003, which was before the pelagic larval densities decreased in 2004–2005 (Figure 2.3). No lice were found on the trout sampled in this cycle, which agrees with the openwater and shoreline larval lice observations. However, in the subsequent 2006–2007 and 2008–2009 cycles, lice returned to wild sea trout in the second year of local farm

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Figure 2.4. Numbers of lice-free (white) and lice-infested (black) sea trout <198 mm long returning to the Shieldaig River. This is a stocked river; hence, numbers of fish returning may vary depending on stocking policy. Numbers are prevalence of infestation. Also shown is the year of local farm production. (Data from Middlemas et al. 1999, 2010; calculated by Middlemas from Hatton-Ellis et al. 2006.)

production again in agreement with observations of plankton sampling and laterally sentinel cages. The association of elevated loads of lice on wild sea trout with the second year of production seems to be widespread. A survey of loads on wild sea trout from the Scottish west coast found a significant increase in the sea lice burdens on sea trout from 10 of 11 sites when local farms were in the second year of a production cycle (McKibben and Hay 2004b; Middlemas et al. 2010).

Sentinel Cages (See also Chapter 5) To determine the viability of the larval sea lice obtained through plankton tows, the Scottish Government commissioned Marine Scotland to carry out a 2.5-year survey determining the monthly infection pressure on wild salmonids within Loch Shieldaig. The main aim of the study was to investigate spatial and monthly infection pressure and determine if there are any “hotspots” of infection within the loch system. Between April 2006 and September 2008, three sentinel cages, each containing 50 Atlantic salmon, were located in Loch Shieldaig for 1 week per month. This time period covered a complete production cycle of two local Atlantic salmon farms including a fallow period within the loch system. Each station was positioned to correspond to the expected migration patterns of salmonids and to allow for investigation of spatial gradients in infection pressure due to surface circulation. After exposure to lice infection pressure in the loch, the fish were removed, euthanized, and the number and developmental stage of any lice on each recorded. Cage, month, and salmon length all had a significant effect on the abundance of lice on the sentinel fish (p = 0.003, <0.0001, and <0.0001, respectively). The fish in cage 3

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had more lice than those in cages 1 and 2 (p = 0.009 and 0.025, respectively), but there was no significant difference in abundance between cages 1 and 2 (p = 0.44). Cage 3 had an estimated 68% more lice than cage 1 (95% confidence interval of 21–133%) and 48% more than cage 2 (95% confidence interval of 8–103%). Lice abundance was low until December 2006; it began to increase in January 2007. Lice abundance remained relatively high until October 2007, and then dropped markedly. Lice abundance was approximately proportional to fish length squared (the estimated coefficient was 1.87 with a 95% confidence interval of 1.45–2.29), suggesting abundance was proportional to fish surface area. Lice abundances on the sentinel fish were correlated with those on the farmed fish across a wide range of time lags (pointwise, 5% significance level). This reflects the common trend in abundance at both the farms and the sentinel cages, with greater abundances in 2007 compared to 2006. The detrended data show only a few significant correlations at lags of 2 or more months; these are hard to interpret and probably spurious due to the large number of correlations made. In particular, there is no statistical evidence that higher numbers of lice on farms led to higher numbers of lice on the sentinel fish either in the same month or 1 month later. The cage data would suggest that L. salmonis infection is spread not only by the infective copepodids but also by preadult stages (Pert et al. 2008). These mobile preadults may play a role as pioneers in establishing infection more rapidly than copepodids. Since they can survive for longer periods and can be transported on wandering salmonids and nonsalmonids (Pert et al. 2006), this may be of particular importance in reestablishing infection after an area has been fallowed. Infection rates were highest near the Shieldaig River (Pert et al. 2008). This study has also shown that L. salmonis are present, albeit in low numbers, within the loch throughout the year.

A Summary of Observations on Lice in Loch Torridon Larval lice have been observed repeatedly to exist at high levels both through direct shoreline and offshore counts of pelagic larvae, infection rates in sentinel cages, and observed numbers on wild fish. These independently obtained data all support a greatly elevated infection pressure when local farms are in their second year of salmon production. Even in these years of high infection pressure the infection pressure is variable in space and time and can be elevated at locations that are remote from the putative source farms. Nauplii were found close to farms, while older copepodids dominated the concentrations remote from farms, indicating farms were a source of larvae. These observations are strong evidence that farms magnify lice infection pressure as a result of the very large biomass of fish on these farms. Although these farms are emptied, fallowed, and then stocked with lice-free fish, the infection of lice on these farms is probably initiated from wild fish (Bron et al. 1993a), either from larvae produced by ovigerous females on these wild fish or direct colonization by mobile stages. It is also possible that infection was imported from neighboring management areas with different production cycles. Only low levels of input are required to initiate an on-farm infection that can then reach high abundance (Revie et al. 2005). Coordinated treatment of lice on farms in Loch Torridon resulted in effective control and so infection pressure was low in 2005, the second year of a production cycle.

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Modeling Sea Lice Dispersal in Loch Torridon Coupled models hydrodynamic-particle models have been developed for the Loch Torridon system (Amundrud and Murray 2009). Such models consist of a hydrodynamic model that derives current velocities and directions, and a particle-tracking model that uses the currents to calculate the movements of particles representing lice. The particle model also handles the biology of production, maturation, and survival of the lice represented by the particles. Outputs from the model are used to identify areas in which high larval lice concentrations may be created, and hence infection risk is elevated. This coupled particle–hydrodynamic modeling approach is widely used to simulate planktonic dispersal, e.g., the dispersal of crab larvae in Delaware Bay (Tilburg et al. 2006) or Calanus finmarchicus over the North Atlantic (Speirs et al. 2006).

Hydrodynamic Modeling The hydrodynamics of Loch Torridon have been modeled by Gillibrand and Amundrud (2007) and Amundrud and Murray (2009). The circulation model used is the three-dimensional baroclinic coastal ocean model GF8. This model was developed based on techniques used for modeling the North Sea (Backhaus 1985), which were modified for the tidal Strait of Georgia (Stronach et al. 1993) before being further changed to describe the St. Lawrence Estuary and the Gulf of St. Lawrence (Saucier et al. 2003). The model used here resembles that of Saucier et al. (2003). Full details of the model are described in Gillibrand and Amundrud (2007) and are not repeated here. The model is based on a hydrostatic solution with the Bousinesq approximation to the equations of mass, momentum, and density conservation first developed by Backhaus (1985). The equations are solved on an Arakawa-C grid with a horizontal grid spacing of x = y = 100 m, while the domain is rotated counterclockwise 49◦ for numerical efficiency such that the x-axis points to the southeast. Vertically, the model contains 15 discrete layers with the top five layers set at 4 m intervals. The thickness of the surface layer varies with the displacement of the sea surface from its mean height such that during spring tides the surface layer ranges from approximately 2 to 6 m in depth. The model is forced by tides, winds, freshwater inputs, and the density of offshore coastal waters. Tidal elevations were obtained from output of the POLCOMS model run at a resolution of 1.8 km (personal Communication, J. Holt) and validated against UK Hydrographic Office (UKHO) tide charts. Earlier modeling (Gillibrand and Amundrud 2007) used benthic pressure at a location 9 km west of Loch Torridon to derive a tidal signal. Winds were derived from a buoy moor near the center of Loch Shieldaig; this is a major improvement from earlier estimates in which winds were derived from Glascarnoch, tens of kilometers distant from Loch Torridon. Freshwater input from rivers was estimated using the gauged river flow provided by the Scottish Environmental Protection Agency at the River Carron (20 km south), scaled for the relative catchment areas. These inputs were applied to the surface cells corresponding to each of the six river mouths in the model (Figure 2.1). Rainfall has not been included to date as it was found to be insignificant during preliminary trials. The density of offshore coastal waters is approximated from a conductivity–temperature–depth

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profile collected on July 17, 2001, from a local offshore station. Offshore densities have therefore only been derived for summer conditions within Loch Torridon and care should be taken before extrapolating to the winter months. The modeled currents were tested using drifter buoys whose movements were followed using a global positioning system. Unfortunately, there were major discrepancies with observed movements 2.5 times faster than simulated motion. However, the simulation did not allow for wind drag on the buoys and when a direct wind-driven component (1.2% of wind speed) was added to the drifter’s velocities, the result was a reasonably accurate simulation of observed drifter movements (Amundrud and Murray 2009). The larval sea lice are not affected by direct wind effects, so this is a case of observations being less accurate than the model! More correctly, the observations were inappropriate as a test of the model. Having verified the hydrodynamic model, its output was saved at 10-minute intervals on the 100-m grid structure of the model. This output field was used to drive movements of simulated particles representing larval lice. These are biological particles whose properties alter the simple transport behavior of the particles.

Biological Particle Modeling The particle-tracking model calculates the movements, maturation, and mortality of particles representing larval lice (Amundrud and Murray 2009). The number of lice each particle initially represents (P0 ) is the total number of larvae produced divided by the number of simulated particles, which is 1500. However, for calculation of relative concentration distributions, actual larval production need not be calculated. Particles are released in batches of ten every 10 minutes over a period of 25 hours to cover two tidal cycles. Enough simulated particles must be released to generate a smooth distribution field, but without unmanageable computational overheads. The model simulates distributions of relative, not absolute, levels of infection risk, so the number of lice represented by each particle is not specified. Simulation of absolute concentrations would depend on viable egg production on farms, which could be incorporated into the model.

Maturation Time Sea lice larvae pass through two nauplii phases and the duration of these phases depends on temperature. A number of different models that describe this function have been developed (Boxaspen and Naess 2000; Brooks 2005). However, the model adopted for Loch Torridon was that of Stein et al. (2005); this model fitted the data over the range of temperatures found in Loch Shieldaig. The time T from egg hatching to copepodid emerging (through the two nauplii stages) is: τ = [24.79/(T − 10 + 24.79 × 0.525)]2 . The model gives a maturation time that initially declines rapidly as temperature rises from near freezing, but this rate falls off rapidly as temperature rises further. At 2◦ C maturation takes 24.4 days, by 5◦ C it is down to 9.6 days, at 10◦ C 3.6 days are required, and at 15◦ C maturation occurs after only 1.9 days by this

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formula. Thus, low temperatures lead to very prolonged time before the larvae become infectious, allowing much potential for dispersal. Small differences at low temperatures have large effects. This sensitivity may be most important at low spring temperatures. Currently, the model assumes a single uniform temperature across the loch for the duration of scenarios of a few days length. Hence, a single maturation time applies for each scenario investigated. Slow temperature changes and limited spatial variation within the loch mean that this approach is appropriate, at least within the Loch Shieldaig basin. However, the formula selected allows for temperature variation in longer term runs or in environments with greater spatial variation in temperature. Having reached the age determined as maturation time, the larvae can become infectious copepodids. This may be simulated under the assumption that they all mature instantly or maturation might be simulated as a probability of occurring, so the different particles mature over a period of time. A sensitivity analysis has been carried out allowing maturation to occur instantaneously or at rates of 50 to 1% h–1 (Murray and Amundrud 2007). The effect of varying this parameter was very limited and a default 10% h–1 is used (Amundrud and Murray 2009).

Larval Survival and Senescence To become infectious, larvae must survive the maturation processes, and having matured, the time they will remain an infection risk depends on survival and also senescence. Relative infection risk is not affected by mortality prior to time T, since all larvae are equally affected. However, mortality of copepodids, or of nauplii after T, does determine where the relative infection risk is concentrated. Mortality rate is strongly dependent on salinity with a rapid drop in survival, if salinity falls below about 29 ppt (Johnson and Albright 1991; Bricknell et al. 2006). However, salinity over most of Loch Shieldaig is generally close to full seawater. The rate of mortality in pure seawater is uncertain, with Johnson and Albright (1991) giving 1% h−1 (Stein et al. 2005) and Bricknell et al. (2006) 50% mortality in 24 hours or 2.9% h–1 . We have therefore investigated mortality rates of 1 and 3% h–1 and 6% h–1 (representing reduced salinity) as a sensitivity analysis for this parameter (Murray and Amundrud 2007). Following Stein et al. (2005), we assume the same mortality rates for nauplii and copepodids. That is, Pt = P0 e−at . Even if larvae survive, they may become senescent and unable, or with reduced ability, to infect hosts. This factor too must be included in the decay rate as it controls the louse’s ability to contribute to infection pressure even if it survives. The importance of senescence depends on survival rates; if mortality is 3% h−1 , <0.6% will be alive after a week, and so even if lice become senescent this will have little effect on infection total pressure. However, if mortality is 1% h−1 , then 18% will still be alive after a week; and if a significant proportion of these are senescent, this will affect infection pressure at the margins. Senescence is highly uncertain, but senescent lice will sink (Bricknell et al. 2006) and so observed lice are likely to be vital.

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Particle-Movement Modeling Horizontal Movement of Particles We have developed a coupled model for dispersal of sea lice in Loch Torridon (Murray and Gillibrand 2006; Amundrud and Murray 2007; Murray and Amundrud 2007; Amundrud and Murray 2009). The particle-transport model accounts for biology in a simple manner; it retains the particles in the surface layer of the loch. This is achieved by only using surface currents and excluding vertical currents. Currents are downloaded from the hydrodynamic model at 10-minute intervals on a 100-m grid square. Particles representing larval lice are moved by currents determined by these outputs from the hydrodynamic model and interpolated linearly in time and with the inverse square of distance from the nearest four grid square centers (Amundrud and Murray 2009). A stochastic diffusion term is added so that each individual particle follows a unique trajectory even with respect to particles released at the same place and time: p (x n+1 , y n+1 ) = p (x n + y n ) + u (x , y) +



6RDh t ,

where p(xn , yn ) is the location of the particle at time n, u is the velocity, Dh is the diffusion coefficient, t is the time step, and R is a random variable distributed evenly from −1 to +1. The model uses a fixed 10-minute time step t for solving biological equations (Amundrud and Murray 2009) and in this it simplifies on earlier versions that used variable time steps (Murray and Gillibrand 2006). The potential for overshoot onto land is dealt with using “sticky” boundary conditions such that should their trajectory carry them into a part of the model deemed “land” (where current velocity always is zero) the particle is held at its previous position for that time step. This process is described in more detail in Amundrud and Murray (2009). The factors in lice biology that affect their transport are their movement relative to the water and the time over which they are available to be transported. This time consists of the period required for larvae to mature through two noninfectious nauplii stages and the duration of the infectious copepodid stage. This is also controlled by the survival of larvae during these stages. All these factors are affected by environmental conditions and so a model is developed that replicates these features for the environment of Loch Shieldaig.

Vertical Movement of Particles Larval lice have only limited swimming ability; however, this may be enough to control the depth of the larvae and so select between currents. Larval lice in Loch Shieldaig have been shown to maintain themselves near the surface (Penston et al. 2008a) with copepodids strongly concentrated near the surface and nauplii spread over a wider range of depths in the top few meters of water. This concentration at the surface is also supported by the observation from Norway that salmon held below the top 4 m of the water column are strongly protected against lice infestation (Hervoy et al. 2003). Lice have the capacity to migrate vertically in response to light (Heuch et al. 1995), and have the ability to sense incoming tides (Bron et al. 1993b), and to accumulate in haloclines (Heuch 1995). Diurnal migration has been simulated by Gillibrand and Willis (2007) in an idealized coastal system. Vertical migration has not been

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explicitly included in the Torridon model, but experiments with transport of larval lice at different depths has shown that, so long as part of the time of dispersal is in the surface layer, the pattern of concentration of copepodids is similar (Amundrud and Murray 2009). Copepodids sink when dead (Bricknell et al. 2006)—this means that larvae found in surface layers or dispersing by surface water movement are likely to be viable. So, the concentrations of larvae found away from farms are likely to be infectious, at least at the time the larvae were moved there.

Modeling Results The principal output of model scenarios is maps of infection pressure. The units of infection pressure are described as “particle-hours.” The number of particles (weighted for survival, Pt ) that are in each grid square of the model, as a result of the movement of particles, is recorded for each time step. These sums may be mapped as a “snapshot” or summed in each grid square over the entire run of a specific scenario. A grid square in which ten particles were present for one time-step would have the same value as one in which one particle remained for ten time-steps (ignoring particle decay). These values are a substitute for infection pressure, the rate at which a fish becomes infested with lice, which depends on the concentration of infectious particles and the time for which fish are exposed. Logarithms of particle-hour values are taken to clearly identify areas in which fish are at relatively high risk of infection in different scenarios. The model results allow assessment of patterns in the distribution of infection risk, as measured in particle-hours. Example scenarios are illustrated in Figures 2.5 and 2.6. General properties of the distributions are discussed first and specific scenarios detailed later. A key feature of the distributions generated in all scenarios investigated is the formation of localized concentrations that are several orders of magnitude higher than background concentrations over the rest of Loch Shieldaig (Murray and Gillibrand 2006; Amundrud and Murray 2009). The location of these concentrations can vary substantially between scenarios, and also with time within individual scenarios (not shown). Ovigerous lice on farms in inner, but not outer, Loch Torridon resulted in infection pressure in Loch Shieldaig (Amundrud and Murray 2009). However, several scenarios generated concentrations within the vicinity of the Shieldaig River. This river supports a population of wild sea trout and the location therefore represents a potential for infection greatly in excess of that which would occur under random dispersal of larvae. The locations of the concentrations of risk are driven by environmental factors. Wind, freshwater inputs and tides, and the location of release and depth of the larvae determine the hydrodynamics of the currents for which the larvae are exposed (Amundrud and Murray 2009), while temperature and salinity determine the period over which the larvae are exposed to these currents (Murray and Amundrud 2007). The single most important environmental factor determining distributions is the direction of the wind (Figure 2.5). When winds are from the west, especially the northwest, larvae accumulate in the upper part of loch Shieldaig, where, as described, they may represent a risk to wild sea trout. Only 0.2% or 6.9% of larvae are exported

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Influence of wind: 7-day simulations a) NW wind

b) SE wind

c) NE wind

d) S wind

e) NW2 wind

0.1

1

10

100

1000

Figure 2.5. Results of the coupled hydrodynamic–particle-tracking model in log (particlehours) summed over scenario runs for a variety of realistic wind fields. (See also color plate section.)

from the Loch Torridon system under two scenarios based on realistic northwesterly winds (Amundrud and Murray 2009). However, southeasterly winds result in larvae accumulating on the opposite shore, and indeed with a substantial 91.6% of larvae being exported entirely from the Loch Torridon system (Amundrud and Murray 2009). Westerly winds represent the prevailing direction in western Scotland and, therefore, the tendency to accumulate around the River Shieldaig. Other lochs, with different bathymetries are liable to have higher rates of export than Loch Torridon. Freshwater flows into Loch Shieldaig are relatively small because the drainage basin is small; the terrestrial area of drainage is about the same area as that of the loch itself. Flows do affect distributions in the immediate vicinity of the river and explain the inability of larvae to move through the narrows into landward basins. Tidal flows drive advection currents; these include large-scale circulation patterns and large velocity short-term currents. However, there are no large differences between larval distribution under spring and neap tidal conditions (Amundrud and Murray 2009) scenarios and so no tidal scenarios are shown. Water temperature determines the time required for larvae to mature from newly hatched nauplii I to infectious copepodids. At low temperatures, the maturation period is prolonged and the effect of low temperatures on distribution is substantial, with significant differences between 5 and 10◦ C. However, the effect on distribution when

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Influence of temperature and mortality a) Mortality 1%

b) Mortality 0.05%

c) Mortality 3%

d) Mortality 6%

0.1

1

10

100

Figure 2.6. Results of the coupled hydrodynamic–particle-tracking model in log (particlehours) summed over scenario runs for a range of hourly mortality rate scenarios. (See also color plate section.)

temperatures are raised from 10 to 15◦ C is relatively small which reflects the tailing off of change in maturation time at higher temperatures (Murray and Amundrud 2007). Because runs of sea trout and salmon smolts occur in spring (Butler 2002) when temperatures are low, this effect may be of considerable importance. The effect of different levels of salinity on larval survival has been simulated by a simple constant mortality rate (Figure 2.6). The effect on absolute concentrations is very large, but there is little effect on the relative distribution of larvae. As discussed, more information is required on mortality rate and salinity. Salinity is clearly important in terms of larval survival when salinity is <29 ppt (Johnson and Albright 1991; Bricknell et al. 2006) and while depressed salinity is not significant in Loch Torridon, especially the Shieldaig basin, it is of significance in other Scottish sea lochs and especially in estuaries with large rivers. An example is the Firth of Tay that receives the water from Scotland’s largest river and for which there is a large decline in sea lice loads on fish relative to nearby coastal water (Todd et al. 2000). In summary, the model generates localized high concentrations of risk. The locations of these concentrations vary greatly between scenarios, although there is a tendency to accumulate near the Shieldaig River. The largest single factor behind variation is wind, but temperature and salinity can also influence the location and intensity of these concentrations.

Conclusions Scottish coastal waters are an environment on a smaller scale than those of Norway or Canada. The lochs and voes are smaller than the fjords of those two countries, and

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lack features such as spring snow melt. These smaller environments can allow for the practical management of lice at the loch scale, although exchange between lochs may have to be considered. Much study has been concentrated on the Loch Torridon system and especially the Loch Shieldaig basin of this system. A clear association has been demonstrated in this system between concentrations of pelagic lice in the marine environment and the local salmon farms production cycle. Modeling demonstrates the development of spatial gradients in pelagic lice densities due to simple mechanisms; high concentrations may often be formed several kilometers from their source. The formation of these patches is dependent on environmental conditions, especially local wind and its interaction with the bathymetry of the loch. Initial infection comes from wild fish or from farmed fish on different production cycles, as farmed fish are free of lice when initially put to sea, and preadult lice may play a role in initiation of this, but salmon farms then magnify the infection pressure.

Summary In this chapter, the unique characteristics of the Scottish coastal environment (section “Scotland’s Coastal Waters”) are related to the biology of lice and the interaction with their salmonid hosts in this environment (section “Sea Lice in Scotland”), including the steps taken to manage lice loads in Scottish salmon aquaculture. These general discussions are followed by a detailed description of the environment and sea lice distribution in a small, but intensively studied, sea loch (small fjord): Loch Torridon (section “Case Study: The Loch Torridon System”). Scottish researchers have collected extensive biological and physical data focusing on larval lice dispersal throughout Loch Torridon (and especially the Loch Shieldaig basin within this system). To predict the observed accumulation at coastlines, coupled biophysical models are used on a loch-wide scale (section “Modeling Sea Lice Dispersal in Loch Torridon”). Observations and model results can be used to support sustainable aquaculture and promote healthy wild salmonid populations.

References Amundrud, T.L. and Murray, A.G. 2007. Validating particle tracking models of sea lice dispersion in Scottish Sea Lochs. ICES CM 2007/B:05, 12 p. Amundrud, T.L and Murray A.G. 2009. Modelling of sea lice dispersion under varying environmental forcing in loch torridon, a Scottish sea loch. Journal of Fish Diseases 32: 27–44. Amundrud, T.L., Penston M.J., and Murray A.G. 2006. A Summary of the Effects of Environmental Factors on the Simulated Dispersal of Sea Lice Larvae and the Findings of the 04/05 Plankton Survey in the Loch Torridon System, Western Scotland. Fisheries Research Services Internal Report, No 15/06. Anon. 1993. Report of the Sea Trout Working Group 1993. Department of the Marine, Ireland, 127 p. Anon. 2000. Final Report of the Joint Government/Industry Working Group on Infectious Salmon Anaemia (ISA), The Scottish Executive, Aberdeen, Scotland, UK, 136 p. Anon. 2002. Review and Synthesis of the Environmental Impacts of Aquaculture. The Scottish Executive, Edinburgh, 62 p.

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Anon. 2004. Tripartite Working Group Concordat and Report; Wild and Farmed Salmonids, Ensuring a Better Future. Scottish Executive, Edinburgh, 18 p. Anon. 2006. A Code of Good Practice for Scottish Finfish Aquaculture. Scottish Salmon Producers’ Organisation, Perth, 122 p. Backhaus, J.O. 1985. A three-dimensional model for the simulation of shelf sea dynamics. Deutsche Hydrographische Zeitschrift 38: 165–187. Bakke, T.A. and Harris, P.D. 1998. Diseases and parasite in wild Atlantic salmon (Salmo salar) populations. Canadian Journal of Fisheries and Aquatic Sciences 55(Suppl. 1): 247–266. Beamish, R.J., Neville C.M., Sweeting R.M., and Ambers, N. 2005. Sea lice on adult Pacific salmon in the coastal waters of Central British Columbia, Canada. Fisheries Research 76: 198–208. Birkeland, K. and Jakobsen, P. 1997. Salmon lice, Lepoephtheirus salmonis, infestation as a casual agent of premature return to rivers and estuaries by sea trout (Salmo trutta L.) juveniles. Environmental Biology of Fishes 49: 129–137. Boxaspen, K. and Næss, T. 2000. Development of eggs and planktonic stages of salmon lice (Leophtheirus salmonis) at low temperature. Contributions to Zoology 69: 51–55. Brandal, P.O. and Egidius, E. 1979. Treatment of salmon lice (Lepeophtheirus salmonis Krøyer, 1838) with Neguvon—description of method and equipment. Aquaculture 18: 183–188. Brandal, P.O., Egidius, E., and Romslo, I. 1976. Host Blood: a major food component for the parasitic copepod Lepeophtheirus salmonis, Krøyer, 1838 (Crustacea: Caligidae). Norwegian Journal of Zoology 24: 341–343. Bricknell, I.R., Dalesman, S., O’Shea, B., Pert, C.C., and Mordue, J. 2006. The effect of environmental salinity on sea lice (Lepeophtheirus salmonis) settlement success. Diseases of Aquatic Organisms 71: 201–212. Bron, J.E., Sommeville, C., and Rae, G.H. 1993b. Aspects of the behaviour of copepodid larvae of the salmon louse Lepeophtheirus salmonis (Krøyer, 1837). In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 125–142. Ellis Horwood, New York. Bron, J.E., Sommerville, C., Wootten, R., and Rae, G.H. 1993a. Fallowing of marine Atlantic salmon, Salmo salar L., farms as a method for the control of sea lice, Lepeophtheirus salmonis (Krøyer, 1837). Journal of Fish Diseases 16: 487–493. Brooks, K.M. 2005. The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada. Reviews in Fisheries Science 13: 177–204. Bruno, D.W. and Stone, J. 1990. The role of saithe, Pollachius virens L., as a host for the sea lice, Lepeoptheirus salmonis Krøyer and Caligus elongatus Nordmann. Aquaculture 89: 201–207. Butler, J.R.A. 2002. Wild salmonids and sea louse infestations on the west coast of Scotland: sources of infection and implications for the management of marine salmon farms. Pest Management Science 58: 595–608. Costello, M.J. 2006. Ecology of sea lice parasitic on farmed and wild fish. Trends in Parasitology 22: 475–483. Costello, M.J. 2009a. The global economic cost of sea lice to the salmonid farming industry. Journal of Fish Diseases 32: 115–118. Costello, M.J. 2009b. How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere. Proceedings of the Royal Society Series B. 276: 3385–3394. Costelloe, M., Costelloe, J., Coghlan, N., O’Donohoe, G., and O’Connor, B. 1998a. Distribution of the larval stages of Lepeophtheirus salmonis in three bays on the west coast of Ireland. ICES Journal of Marine Science 55: 181–187. Costelloe, M., Costelloe, J., O’Donohoe, G., Coghlan, N.J., Oonk, M., and Heijden, Y. 1998b. Planktonic distribution of sea lice larvae, Lepeophtheirus salmonis, in Killary Harbour, west

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coast of Ireland. Journal of the Marine Biological Association of the United Kingdom 78: 853–874. Craig, R.E. 1959. Hydrography of Scottish coastal waters. Marine Research Series No. 2. HMSO, London. Dyer, K.R. 1973. Estuaries: A Physical Introduction. John Wiley & Sons, London. Edwards, A. and Sharples, F. 1986. Scottish Sea Lochs: A Catalogue. Scottish Marine Biological Association/Nature Conservancy council, 110 p., revised 1991. Finstad, B., Bjørn, P.A., Grimnes, A., and Hvidsten, N.A. 2000. Laboratory and field investigations of salmon lice [Lepeophtheirus salmonis (Krøyer)] infestation on Atlantic salmon (Salmo salar L.) post-smolts. Aquaculture Research 31: 795–803. Ford, J.S. and Myers, R.A. 2008. A global assessment of salmon aquaculture impacts on wild salmonids. Public Library of Science Biology 6(2): e33. Gillibrand, P. and Turrell, W. 1997. The use of simple models in the regulation of the impact of fish farms on water quality in Scottish sea lochs. Aquaculture 159: 33–46. Gillibrand, P.A. and Amundrud, T.L. 2007. A numerical study of the tidal circulation and buoyancy effects in a Scottish fjord: Loch Torridon. Journal of Geophysical Research 112: C05030. Gillibrand, P.A. and Willis, K.J. 2007. Dispersal of sea louse larvae from salmon farms: modelling the influence of environmental conditions and larval behaviour. Aquatic Biology 1: 63–85. Grant, A.N. 2002. Medicines for sea lice. Pest Management Science 58: 521–527. Grimnes, K. and Jakobsen, A. 1996. The physiological effects of salmon lice infection on postsmolt of Atlantic salmon. Journal of Fish Biology 48: 1179–1194. Hatton-Ellis, M., Hay, D., Walker, A.F., and Northcott, S.J. 2006. Sea lice Lepeophtheirus salmonis infestations of post-smolt sea trout in Loch Shieldaig, Wester Ross, 1999–2003. In: Sea Trout: Biology, Conservation and Management (eds G.S. Harris and N.J. Milner), pp. 372–376. Blackwell Publishing, Oxford. Hervoy, E.M., Boxaspen, K., Oppedal, F., Taranger, G.L., and Holm, J.C. 2003. The effect of artificial light treatment and depth on the infestation of the sea louse Lepeophtheirus salmonis on Atlantic salmon (Salmo salar L.) culture. Aquaculture 220: 1–14. Heuch, P.A. 1995. Experimental evidence for aggregation of salmon louse copepodids (Lepeophtherius salmonis) in step salinity gradients. Journal of the Marine Biological Association of the UK 75: 927–939. Heuch, P.A. and Mo, T.A. 2001. A model of salmon louse production in Norway: effects of increasing salmon production and public management measures. Diseases of Aquatic Organism 45: 145–152. Heuch, P.A., Bjorn, P.A., Finstad, B., Holst, J.C., Asplin, L., and Nilsen, F. 2005. A review of the Norwegian ‘National Action Plan against Salmon Lice on Salmonids’: the effect on wild salmonids. Aquaculture 246: 79–92. Heuch, P.A., Parsons, A., and Boxaspen, K. 1995. Diel vertical migration: a possible host-finding mechanism in the salmon louse (Leopeophtheirus salmonis) copepodids? Canadian Journal of Fisheries and Aquatic Sciences 52: 681–689. Hughes, S.L. 2007. Scottish Ocean Climate Status Report 2004 and 2005. Fisheries Research Services, Aberdeen. Jacobsen, J.A. and Gaard, E. 1997. Open-ocean infestation by salmon lice (Lepeophtheirus salmonis): comparison of wild and escaped farmed Atlantic salmon (Salmo salar L.). ICES Journal of Marine Science 54: 1113–1119. Jarrams, P. 1987. Sea Trout Run. A & C Black (Publishers), London. Johnson, S.C. and Albright, L.J. 1991. Development, growth, and survival of Leopeophtheirus salmonis (copepoda: caligidae) under laboratory conditions. Journal of the Marine Biological Association of the United Kingdom 71: 425–463.

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Johnson, S.C., Treasurer, J.W., Bravo, S., Nagasawa K., and Kabata, Z. 2004. A review of the impact of parasitic copepods on marine aquaculture. Zoological Studies 43: 229–243. Jones, M.W., Sommerville, C., and Bron, J. 1990. The histopathology associated with the juvenile stages of Lepeophtheirus salmonis on the Atlantic salmon, Salmo salar L. Journal of Fish Diseases 13: 303–310. Jones, M.W., Sommerville, C., and Wootten, R. 1992. Reduced sensitivity of the salmon louse, Lepeophtheirus salmonis, to the organophosphate dichlorvos. Journal of Fish Diseases 15: 197–202. Jones, S.R.M., Prosperi-Porta, G., Kim, E., Callow, P., and Hargreaves, N.B. 2006. The occurrence of Lepeophtheirus salmonis and Caligus clemensi (Copepoda: Caligidae) on three-spine stickleback Gastrosteus aculeatus in coastal British Columbia. Journal of Parasitology 92: 473–480. Jonsdottir, H., Bron, J.E., Wootten, R., and Turnbull, J.T. 1992. The histopathology associated with the preadult and adult stages of Lepeophtheirus salmonis on the Atlantic salmon, Salmo salar L. Journal of Fish Diseases 15: 521–527. Kabata, Z. 1973. Copepoda and branchiura. In: Guide to the Parasites of Fishes of Canada. Part II-Crustacea (eds Margolis and Z. Kabata), pp. 3–127. Canadian Special publications of Fisheries and Aquatic Sciences 101, Ottawa. Kettlewhite, A. 2000. Awe Fisheries Trust Annual Report 1999. Awe Fisheries Trust, Argyll. Krkoˇsek, M, Lewis, M.A., and Volpe, J.P. 2005. Transmission dynamics of parasitic sea lice from farm to wild salmon. Proceedings of the Royal Society B, 1–8. Lees, F., Gettinby, G., and Revie, C.W. 2008a. Changes in epidemiological patterns of sea lice infestation on farmed Atlantic salmon, Salmo salar L., in Scotland between 1996 and 2006. Journal of Fish Diseases 31: 259–268. Lees, F. Baillie, M., Gettinby. G., and Revie, C.W. 2008b. The efficacy of emamectin benzoate against infestations of Lepeophtheirius salmonis on farmed Atlantic salmon (Salmo salar L.) in Scotland, 2002–2006. Public Library of Science One 3: e1549. Lyndon, A.R. and Toovey, J.P.G. 2001. Occurrence of gravid salmon lice (Lepeophtheirus salmonis (Krøyer)) on saithe (Pollachius virens (L.)) from salmon farm cages. Bulletin of the European Association of Fish Pathologists 21: 84–85. MacKenzie, K., Longshaw, M., Beggs, G.S., and McVicar, A.H. 1998. Sea lice (Copepoda: Caligidae) on wild sea trout (Salmo trutta L.) in Scotland. ICES Journal of Marine Science 55: 151–162. MacKinnon, B.M. 1997. Sea lice: a review. World Aquaculture 28: 5–10. Marshall, S. 2003. The incidence of sea lice infestations on wild sea trout compared to farmed salmon. Bulletin of the European Association of Fish Pathologists 23: 72–79. McBeath, A.J.A., Penston, M.J., Snow, M., Cook, P.F., Bricknell I.R., and Cunningham, C. 2006. Development and application of real-time PCR for the specific detection of Lepeophtheirus salmonis and Caligus elongatus larvae in Scottish plankton samples. Diseases of Aquatic Organisms 73: 141–150. McGeorge, J. and Sommerville, C. 1996. The potential for interaction between the parasites of wild salmonids, non-salmonids and farmed Atlantic salmon in Scottish sea lochs. In: Aquaculture and Sea Lochs (ed K.D. Black), pp. 59–71. Harlequin Press, Oban. McKibben, M.A. and Hay, D.W. 2004a. Distributions of planktonic sea lice larvae Lepeoptheirus salmonis in the inter-tidal zone in Loch Torridon, Western Scotland in relation to salmon farm production cycles. Aquaculture Research 35: 742–750. McKibben, M.A. and Hay, D.W. 2004b. Larval sea lice densities and sea lice levels on postsmolt sea trout in western Scotland, 2002–2003. Joint AWCFT/FRS Research Project Final Report. McLean, P.H., Smith, G.W., and Wilson, M.J. 1990. Residence time of the sea louse, Lepeophtheirus salmonis K., on Atlantic salmon, Salmo salar L., after immersion in fresh water. Journal of Fish Biology 37: 311–314.

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Middlemas, S.J and Stewart, D.C. 2008. Unusually High Incidence of Large One-Year-Old Salmon Smolts Trapped on a Small West Coast. Scottish river Fisheries Research Services report No. 69. Middlemas, S.J., Stewart, D.C., Mackay, S., and Armstrong, J.D. 2009. Habitat use and dispersal of post smolt sea trout Salmo trutta in a Scottish sea loch system. Journal of Fish Biology 74: 639–651. Middlemas, S.J., Raffell, J.A., Hay, D.W., Hatton-Ellis, M., and Armstrong, J.D. 2010. Temporal and spatial patterns in sea lice levels on sea trout in Western Scotland in relation to fish farm production cycles. Biology Letters 6: 317–323. Murray, A.G. 2002. Using observed load distributions with a simple model to analyse the epidemiological patterns of sea lice (Lepeophtheirus salmonis) on sea trout (Salmo trutta). Pest Management Science 58: 585–594. Murray, A.G. and Amundrud, T.L. 2007. Using coupled biophysical–particle tracking models of sea lice in Loch Torridon. Proceedings of the International Congress on Modelling and Simulation. Christchurch, New Zealand, December 2007, 2848–2853. Murray, A.G. and Gillibrand, P.A. 2006. Modelling dispersal of larval salmon lice in Loch Torridon, Scotland. Marine Pollution Bulletin 53: 128–135. Murray, A.G. and Simpson, I. 2006. Patterns in Sea Lice Infestation on Wild Atlantic Salmon Returning to the North Esk River in Eastern Scotland 2001–2003. Fisheries Research Services Report 20/06, Aberdeen, Scotland, UK. Pemberton, R. 1976. Sea trout in North Argyll sea lochs, population, distribution and movements. Journal of Fish Biology 9: 157–179. Penston, M.J. 2009. Dynamics of planktonic larval sea louse distribution in relation to Atlantic salmon (Salmo salar L.) farms in a Scottish sea loch. PhD thesis, University of Aberdeen, Scotland, UK. Penston, M.J. and Davies, I.M. 2009. An assessment of salmon farms and wild salmonids as sources of Lepeophtheirus salmonis (Krøyer) copepodids in the water column in Loch Torridon, Scotland. Journal of Fish Diseases 32: 75–88. Penston, M.J., McKibben, M.A., Hay, D.W., and Gillibrand, P.A. 2004. Observations on openwater densities of sea lice larvae in Loch Shieldaig, Western Scotland. Aquaculture Research 35: 793–805. Penston, M.J., Millar, C.P., Zuur, A., and Davies, I.M. 2008a. Spatial and temporal distribution of Lepeophtheirus salmonis (Krøyer) larvae in a sea loch containing Atlantic salmon, Salmo salar (L.), farms on the north-west coast of Scotland. Journal of Fish Diseases 31: 361– 371. Penston, M.J., Millar, C.P., and Davies, I.M. 2008b. Reduced Lepeophtheirus salmonis larval abundance in a sea loch on the west coast of Scotland, 2002–2006. Diseases of Aquatic Organisms 81: 109–117. Pert, C.C., Urquhart, K., and Bricknell, I.R. 2006. The sea bass (Dicentrarchus labrax L.): a peripatetic host of Lepeophtheirus salmonis (Copepoda: Caligidae)? Bulletin of the European Association of Fish Pathologists 26: 163–165. Pert, C.C., Kilburn, R., Cook, P., McCarthy, U., Urquhart, K., McBeath, S., Weir, S., McBeath, A., and Bricknell, I.R. 2008. Monitoring the Infection Pressure from Sea Lice on Wild Salmonids. In a Scottish west coast Sea Loch. Oral Presentation. 10th International Meeting on Copepoda, Pattaya, Thailand. Pike, A.W. and Wadsworth, S. 1999. Sealice on salmonids: their biology and control. Advances in Parasitology 44: 233–337. Potter, E.C.E. 1990. Movements of sea trout (Salmo trutta L.) in the central and southern North Sea. In The Sea Trout in Scotland (ed M.J. Picken and W.M. Shearer), pp. 47–52. Scottish Marine Biological Association, Oban. Raffell, J., Buttle, S., and Hay, D.W. 2007. Shieldaig project review June 2006-June 2007. Internal Report. Fisheries Research Services, Pitlochry.

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Revie, C., Dill, L., Finstad, B., and Todd, C. 2009. “ Salmon Aquaculture Dialogue Working Group Report on Sea Lice” commissioned by the Salmon Aquaculture Dialogue available at http://www.worldwildlife.org/site/PageNavigator/SalmonSOIForm. (Last accessed date July 2009). Revie, C.W., Gettinby, G., Treasurer J.W., Grant A.N., and Reid, S.W. 2002a. Sea lice infestations on farmed Atlantic salmon in Scotland and the use of ectoparasitic treatments. The Veterinary Record 151: 753–757. Revie, C.W., Gettinby, G., Treasurer, J.W., Rae, G.H., and Clark, N. 2002b. Temporal, environmental and management factors influencing the epidemiology of sea lice (Lepeophtheirus salmonis) infestations on farmed Atlantic salmon (Salmo salar) in Scotland. Pest Management Science 58: 576–584. Revie, C.W., Robbins, C., Gettinby, G., Kelly, L., and Treasurer, J.W. 2005. A mathematical model of the growth of sea lice, Lepeophtheirus salmonis, populations on farmed Atlantic salmon, Salmo salar L., in Scotland and its use in the assessment of treatment strategies. Journal of Fish Diseases 28: 603–613. Roth, M. 1993. Current practices in the chemotherapeutic control of sea lice infestations in aquaculture: a review. Journal of Fish Diseases 16: 1–26. Saucier, F.J., Roy, F., Gilbert, D., Pellerin, P., and Ritchie, H. 2003. Modeling the formation and circulation processes of water masses and sea ice in the Gulf of St. Lawrence, Canada. Journal of Geophysical Research 108(C8): 3269. Schram, T.A. 2004. Practical identification of pelagic sea lice larvae. Journal of the Marine Biological Association of the United Kingdom 84: 103–110. Shaw, D.J. and Dobson, A.P. 1995. Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111: S111–S135. Smith, R.J. 2007. Scottish Fish Farm Annual Production Survey 2006. Fisheries Research Services, Aberdeen, Scotland, UK, 53 p. Speirs, D.C., Gurney, W.S.C., Heath, M.R., Horbelt, W., Wood, S.N., and de Ceuvas, B.A. 2006. Ocean-scale modelling of the distribution, abundance, and seasonal dynamics of the copepod Calanus finmarchicus. Marine Ecology Progress Series 313: 173– 192. Stein, A., Bjørn, P.A., Heuch, P.A., and Elston, D.A. 2005. Population dynamics of salmon lice Lepeophtheirus salmonis on Atlantic salmon and sea trout. Marine Ecology Progress Series 290: 263–275. Stigebrandt, A. 2001. FJORDENV–A water quality model for fjords and other inshore waters. G¨ oteborg University, G¨ oteborg, Sweden 44 p. Stone, J., Sutherland, I.H., Sommerville, C., Richards, R.H., and Endris, R.G. 2000. The duration of efficacy following oral treatment with emamectin benzoate against infestations of sea lice, Lepeophtheirus salmonis (Krøyer), in Atlantic salmon Salmo salar L. Journal of Fish Diseases 23: 185–192. Stronach, J.A., Backhaus, J.O., and Murty, T.S. 1993. An update on the numerical simulation of oceanographic processes in the waters between Vancouver Island and the mainland: the GF8 model. Oceanography and Marine Biology Annual Review 31: 1–86. Tilburg, C.E., Houser, L.T., Steppe, C.N., Garvine, R.W., and Epifanio, C.E. 2006. Effects of coastal transport on larval patches: models and observations. Estuarine Coastal and Shelf Science 67: 145–160. Todd, C.D., Walker, A.M., Hoyle, J.E., Northcott, S.J., Walker, A.F., and Ritchie, M.G. 2000. Infestations of wild adult Atlantic salmon (Salmo salar L.) by the ectoparasitic copepod sea louse Lepeophtheirus salmonis Krøyer: prevalence, intensity and the spatial distribution of males and females on the host fish. Hydrobiology 429: 181–196. Todd, C.D., Walker, A.M., Ritchie, M.G., Graves, J.A., and Walker, A.F. 2004. Population genetic differentiation of sea lice (Lepeophtheirus salmonis) parasitic on Atlantic and Pacific

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salmonids: analyses of microsatellite DNA variation among wild and farmed hosts. Canadian Journal of Fisheries and Aquatic Sciences 61: 1176–1190. Treasurer, J.W., Wallace, C., and Dear, G. 2002. Control of sea lice on farmed Atlantic salmon, S. salar L. with the oral treatment emamectin benzoate (SLICE). Bulletin of the European Association of Fish Pathologists 22: 375–380. Tully, O. and Whelan, K.F. 1993. Production of nauplii of Leopepotheirus salmonis (Krøyer) (Copepoda: Caligidae) from farmed and wild salmon and its relation to the infestation of wild sea trout (Salmo trutta L.) off the west coast of Ireland in 1991. Fisheries Research 17: 187–200. Tully, O., Poole, W.R., and Whelan, K.F. 1993b. Infestation parameters for Leopepotheirus salmonis (Krøyer) (Copepoda: Caligidae) parasitic on sea trout (Salmo trutta L.) post smolts on the west coast of Ireland during 1990 and 1991. Aquaculture and Fisheries Management 24: 520–529. Tully, O., Poole, W.R., and Whelan, K.F. 1999. Spatial and temporal variation in the infestation of sea trout (Salmo trutta L.) by the caligid copepod Lepeophtheirus salmonis (Krøyer) in relation to sources of infection in Ireland. Parasitology 119: 41–51. Tully, O., Poole, W.R., Whelan, K.F., and Merigoux, S. 1993a. Parameters and possible causes of epizootics of Lepeophtheirus salmonis (Krøyer) in relation to origin and water temperature. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 202–213. Ellis Horwood, Chichester. Vøllestad, L.A., Hirst, D., L’Ab´ee-Lund J.H., Armstrong, J.D., McLean, J.C., Youngson, A.F., and Stentseth, N.C. 2009. Divergent trends in anadromous salmonid populations in Norwegian and Scottish rivers. Proceedings of the Royal Society 276: 1021–1027. Wells, A., Grierson, C.E., Marshall, L., MacKenzie, M., Russon, I.J., Reinardy, H., Sivertsgard, R., Bjorn, P.A., Finstad, B., Bonga, S.E.W., Todd, C.D., and Hazon, N. 2007. Physiological consequences of “premature freshwater return” for wild sea-run brown trout (Salmo trutta) postsmolts infested with sea lice (Lepeophtheirus salmonis). Canadian Journal of Fisheries and Aquatic Science 64: 1360–1369. White, H.C. 1942. Life history of Lepeophtheirus salmonis. Journal of the Fisheries Research Board of Canada 6: 24–29. Wootten, R., Smith, J.W., and Needham, E.A. 1982. Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids, and their treatment. Proceedings of the Royal Society of Edinburgh (B) 81: 185–197.

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Chapter 3

Sea Louse Abundance on Farmed Salmon in the Southwestern New Brunswick Area of the Bay of Fundy Blythe D. Chang, Fred H. Page, Michael J. Beattie, and Barry W.H. Hill

Introduction Atlantic salmon (Salmo salar) have been farmed in floating net cages in the southwestern New Brunswick portion of the Bay of Fundy (Figure 3.1) since 1978. The first harvest was 6 tons from one farm in 1979. The largest production level was an estimated 41,000 tons in 2006 (Figure 3.2). Production decreased slightly in recent years, largely due to the introduction of a new Aquaculture Bay Management Area framework in 2006. Production in 2008 was 26,000 tons (Statistics Canada 2009). There are currently more than 90 licensed finfish farms, of which approximately 70 are actively growing Atlantic salmon. These farms are located in an area approximately 60 × 60 km2 . There are also several farms located in adjacent waters of Cobscook Bay, Maine, United States. The first farm in southwestern New Brunswick was started in 1978 at Lords Cove, Deer Island, and the second farm at Dark Harbour, Grand Manan Island, started in 1980 (Figure 3.3). In the mid-1980s, the industry grew rapidly, especially in the Letang area (Letang Harbour, Lime Kiln Bay, Bliss Harbour, and Back Bay) and around Deer and Campobello islands. In the 1990s, the industry expanded into Passamaquoddy Bay and along the eastern and southern shores of Grand Manan Island. In the early 2000s, the industry expanded into the Maces Bay area. Sea lice have been observed on wild salmon in Atlantic Canada, including the Bay of Fundy, long before the start of salmon farming. Bere (1930) reported the salmon louse, Lepeophtheirus salmonis, on Atlantic salmon from the Passamaquoddy Bay area in 1928, although she did not include any data on prevalence or abundance. White (1940, 1942) observed small numbers of L. salmonis on adult Atlantic salmon in the Apple River at the head of the Bay of Fundy and in the Margaree River, Cape Breton Island, in the 1930s, but the lice caused no appreciable damage to the fish in these rivers. He also reported heavy infestations on salmon grilse entering the Moser River on the Atlantic coast of Nova Scotia in 1939 and 1940. Largest abundances of grilses

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Figure 3.1. Map of the salmon farming area in southwestern New Brunswick and Cobscook Bay, Maine, showing finfish farms in 2008 (small black polygons) and the former commercial salmon fishing area.

Figure 3.2. Total production of farmed Atlantic salmon in southwestern New Brunswick from 1979 to 2008, and the number of licensed marine finfish farms in each year. (Data sources: Statistics Canada (2009); New Brunswick Department of Agriculture, Aquaculture and Fisheries (unpublished data).)

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Figure 3.3. Locations of finfish farms in southwestern New Brunswick (full circles) and adjacent Maine (open circles), 1980–2005.

were in mid-August 1939 when hundreds of sea lice were observed per fish, resulting in mortalities. Templeman (1967a, 1967b) sampled salmon in the Labrador Sea, off the west coast of Greenland, and east and southeast of Newfoundland in 1965 and 1966. L. salmonis occurred on 70–93% of salmon sampled from the different areas and the average number of lice per fish varied from 2.7–7.5. Sea lice were probably present in low numbers on farmed salmon in southwestern New Brunswick during the earliest years of the industry, although the first reported outbreak was in 1984 at one salmon farm in Dark Harbour, Grand Manan Island (L’Aventure 1987; Stuart 1990). That outbreak was confined to the one farm, which was located far from other farms. The next large outbreak began in the fall of 1994 in the Letang area (Hogans 1995) and quickly spread throughout the industry.

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Various chemical treatments have been the main method of controlling sea lice on farmed salmon in southwestern New Brunswick. In the first reported outbreak at R ), an organophosDark Harbour in 1984, bath treatments with dichlorvos (Nuvan phate that was used to control sea lice on farmed salmon in Europe, were found to be effective (L’Aventure 1987). In 1994 and 1995, emergency permits were granted allowing the use of hydrogen peroxide and pyrethrin bath treatments at some farms (O’Halloran and Hogans 1996). Feed treated with ivermectin was also used. This drug has regulatory status in Canada, but is not specifically labeled for sea louse treatment. It has been used as an “off-label” drug treatment, under veterinary prescription R ), another organophosphate, was first (Burridge 2003). Azamethiphos (Salmosan used in southwestern New Brunswick in October 1995 and became the main antilouse chemical used for the next few years. An initial field trial with farmed Atlantic salmon in Atlantic Canada showed that bath treatment with azamethiphos resulted in reductions of L. salmonis numbers by 100% for gravid females, 98.3% for preadults, and 68% R ) for chalimus larvae (O’Halloran and Hogans 1996). Emamectin benzoate (SLICE became available under Health Canada’s Emergency Drug Release program as a dietary treatment starting in 1999. The first field trial of emamectin benzoate in Atlantic Canada demonstrated that it was effective against all life stages of sea lice on farmed Atlantic salmon (Armstrong et al. 2000) and it became the only antilouse treatment used in southwestern New Brunswick during most of the last decade (Burridge 2003; Westcott et al. 2004; MacPhee and Moore 2007).

Sea Louse Abundance on Farmed Salmon in Southwestern New Brunswick The most common sea louse species affecting farmed salmon in southwestern New Brunswick and throughout the Northern Hemisphere are L. salmonis (commonly called the salmon louse) and Caligus elongatus (Hogans and Trudeau 1989b). L. salmonis is considered to be limited mainly to salmonids, while C. elongatus can infect a wide variety of fish species (Kabata 1979). A third species, Caligus curtus, has also been reported in southwestern New Brunswick, but is not common (Hogans and Trudeau 1989b). Available data on sea louse abundance on farmed salmon in southwestern New Brunswick are limited. Much of the sea louse monitoring was conducted by veterinarians working for fish farm companies and those data were generally not available. Furthermore, analysis and interpretation of the available data are often difficult because of the chemical treatments used to control sea louse abundance. Nevertheless, some general trends can be discerned from the available data. In the early years of farming in southwestern New Brunswick, sea lice, especially C. elongatus, were observed at salmon farms, generally in low numbers (Hogans and Trudeau 1989a; Hogans 1995). An exception was the large outbreak of L. salmonis reported at Dark Harbour, Grand Manan Island, in 1984, in which up to 100 sea lice per fish were reported (L’Aventure 1987; Stuart 1990). In a study at one salmon farm in Lime Kiln Bay in July 1988, C. elongatus was the only sea louse species found. The prevalence was 55% on both smolts and market-size salmon with intensities of 2.6 lice per smolt and 2.4 lice per market-size fish (Hogans and Trudeau 1989a). A follow-up study was conducted in southwestern New Brunswick in 1988–1989 (Hogans and Trudeau 1989b) at an experimental site near St. Andrews, one farm in

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Lime Kiln Bay and one farm at Campobello Island. Three species of sea lice were found on farmed salmon: C. elongatus, C. curtus, and L. salmonis. C. elongatus was by far the most abundant of these species, accounting for 97% of the lice recovered. Prevalence and intensity of C. elongatus on farmed salmon showed strong seasonal variations. Prevalence, that was about 50% in July, reached 100% in September–October and declined to about 60% by February. The intensity averaged one louse per infected fish in July, peaked to 19 lice per fish in October and was <2 lice per fish in January–February. The trends appeared to be correlated with temperature. C. curtus was the least abundant, comprising just 0.7% of specimens recovered. L. salmonis comprised only 2% of the lice recovered. Its prevalence and intensity showed similar seasonal trends to C. elongatus with a prevalence of 1% in July, a maximum of 8% in October, declining to <4% in November, and 0% in December–February. Intensity was one louse per fish in July and August, with a maximum of about three lice per fish in October. Intensity declined to one louse per fish in November and zero in December–February. None of the sea louse species appeared to cause mortalities of cultured salmon during the study period. During the mid-1990s, sea lice became more prevalent throughout the rapidly expanding southwestern New Brunswick salmon farming industry. Large numbers of L. salmonis began infecting farmed salmon in the Letang area in the fall of 1994 (Hogans 1995). L. salmonis has been the main species of concern in southwestern New Brunswick since then. Hogans (1995) collected sea louse data from 16 farms in southwestern New Brunswick from August 1994 to early 1995. The abundance of L. salmonis at six Letang area farms increased from 2–3 lice per infected fish in August–September 1994 to 84 per infected fish in late October 1994. Infection rates on market-size fish were 1.7 times that of spring smolts. Treatment of smolts with ivermectin and hydrogen peroxide in November–December 1994 reduced the mean intensity to <30 lice per infected fish in January–March 1995. The intensity of infection in the winter of 1994–1995 at farms in Passamaquoddy Bay, Deer Island, Campobello Island, Beaver Harbour, and Cobscook Bay (i.e., outside of the initial sea louse outbreak area) varied from 2.9–9.1 lice per fish, much lower than in the Letang area. As in the Letang area, infection rates were higher on market-size fish than on smolts. Hogans (1995) also observed changes in sea louse abundance at three farms in the Letang area during January–March 1995. The lowest numbers of mature stages were found in mid-February (when the water temperature was lowest, reaching 0.8◦ C) and numbers began to increase at the end of February and March 1995 (when the temperature began to rise). By late 1995, the outbreak of L. salmonis had spread to all operating salmon farms in southwestern New Brunswick (Hogans 1997). In response to the outbreak, the New Brunswick government conducted a monitoring program for sea louse abundance on farmed fish in southwestern New Brunswick from October 1994 to August 1996. The salmon farming area was divided into ten Sea Louse Management Zones with the goal to sample at least one farm per zone each month. It was proposed to sample three or more cages per farm and ten fish per cage; however, this level of sampling was not achieved in any of the ten zones. Sampling of at least one farm per month was achieved in the Letang area. Sampling was conducted at farms on a semivoluntary basis, so some farms were sampled more than others. In 1994, sampling occurred only in farms in the northern Passamaquoddy Bay and Letang areas. Sampling increased in 1995 and 1996 with ≥90% of operating farms in southwestern New Brunswick being sampled at least once each year.

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14

50 L Ha eta rb ng ou r

L. salmonis

45

C. elongatus Temperature: Lime Kiln Bay

Lime Kiln Bay

12

Temperature: SWNB farms

35

10

Bliss Harbour

30

8

25 6

20 15

Temperature (°C)

Ba

ck

Ba y

40

4

10 2 5

Jul-96

Aug-96

Jun-96

Apr-96

May-96

Mar-96

Jan-96

Feb-96

Dec-95

Oct-95

Nov-95

0 Sep-95

Jul-95

Jun-95

Apr-95

May-95

Feb-95

Mar-95

Jan-95

Dec-94

Oct-94

Aug-95

ND

0 Nov-94

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Average number of Iice (all stages) per fish

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Figure 3.4. Abundance of L. salmonis and C. elongatus on farmed salmon in southwestern New Brunswick, 1994–1996. Data are monthly averages of all louse stages on all fish sampled; 4–58 farms were sampled in any one month, with the highest numbers of farms sampled in 1996. Temperature data are monthly means at 5 m below the water surface, from 20 farms in southwestern New Brunswick (see Figure 3.10) and data from Martin et al. (1999) at a location in Lime Kiln Bay (black dot on inset map). ND, insufficient data (only one farm sampled). (Previously unpublished data provided by the New Brunswick Department of Agriculture, Aquaculture and Fisheries.)

The 1994–1996 data showed that L. salmonis was present on farmed salmon throughout the year (Figure 3.4). Overall abundance showed a strong seasonal trend: the highest abundance was observed in summer and fall and the lowest in late winter and spring, although there was considerable variation among individual farms (an opposite seasonal trend was reported for British Columbia in Chapter 8 contributed by Saksida et al.). Seasonal trends in sea louse abundance at individual farms were affected by the use of antilouse chemicals (hydrogen peroxide, pyrethrin, ivermectin, azamethiphos). Unfortunately, adequate information on the types, dates, and efficacy of chemical treatments during this period were not available. Chalimus larvae were present throughout the year, but were generally more abundant in summer and fall (Figure 3.5). There were sufficient data to compare sea louse abundance on smolts with premarket and market-size fish only for the period June–December 1995. During this period, the average sea louse abundance was higher on premarket and market-size fish, compared to smolts (Figure 3.6). In September, sea louse abundance on premarket and market-size fish was twice that on smolts, similar to what Hogans (1995) observed in the fall of 1994 in the Letang area. The abundance of L. salmonis appeared to be slightly higher in the fall of 1994, reaching an average abundance of 47.5 lice per fish for all samples in November. This

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14

50 Chalimus All other stages of L. salmonis Temperature: SWNB farms Temperature: Lime Kiln Bay

45

12

40

30

8

25 6

20 15

Temperature (°C)

10

35

4

10 2 5

Jul-96

Aug-96

Jun-96

Apr-96

May-96

Mar-96

Jan-96

Feb-96

Dec-95

Oct-95

Nov-95

0 Sep-95

Jul-95

Jun-95

Apr-95

May-95

Mar-95

Jan-95

Feb-95

Dec-94

Oct-94

Aug-95

ND

0 Nov-94

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Figure 3.5. Abundance of chalimus larvae and all other stages of L. salmonis on farmed salmon in southwestern New Brunswick, 1994–1996. The abundance of chalimus larvae is used as an indicator of recruitment onto salmon hosts. Data are monthly averages of all fish sampled. From 4 to 58 farms were sampled in any one month, with the highest numbers in 1996 Temperature data are as in Figure 3.4. ND, insufficient data (only one farm sampled). (Previously unpublished data provided by the New Brunswick Department of Agriculture, Aquaculture and Fisheries.)

compared to the fall of 1995 with an average of 34.2 lice per fish in September. The apparent difference may result from most sampling in 1994 being confined to the Letang area, where the outbreak was occurring, while in 1995, sampling was throughout the southwestern New Brunswick farming area. The maximum abundances of L. salmonis observed at individual farms were similar in 1994 and 1995. In 1994, the highest average abundance was 110 lice per fish at a farm in Back Bay in November, while in 1995, the highest value was 107 lice per fish at a farm in northern Passamaquoddy Bay in October. C. elongatus was much less abundant than L. salmonis (Figure 3.4). The abundance of C. elongatus was highest in the fall of 1994 and remained low after January 1995, but nevertheless showed a similar seasonal trend as L. salmonis. Data for January–August 1996 indicate that abundance was lower than in the same months of 1995 (Figure 3.5). Unfortunately, this monitoring program was terminated after August 1996, preventing a comparison of the abundance during the peak sea louse periods in the fall of 1996 with previous years. However, Hogans (1997) studied L. salmonis at three farms in southwestern New Brunswick (two in Lime Kiln Bay and near northern Deer Island) from August 1996 to March 1997. The prevalence in the fall of 1996 was similar to the previous year and the intensity of infection in 1996 was about 40% of that in 1995. He indicated that the main reason for this decrease was the increased use of azamethiphos (starting in late 1995).

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70 Smolts

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Temperature: SWNB farms

12 50 10 40 8 30

6

20

Temperature (°C)

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10

2 ND

0 Jun-95

Jul-95

Aug-95

0 Sep-95

Oct-95

Nov-95

Dec-95

Figure 3.6. Average abundance of L. salmonis (all stages) on smolts and premarket/marketsize fish in southwestern New Brunswick salmon farms in June–December 1995. Temperature data are monthly means at 5 m below the water surface, from 20 farms in southwestern New Brunswick (see Figure 3.10). ND, insufficient data (only one farm sampled). (Abundance data provided by the New Brunswick Department of Agriculture, Aquaculture and Fisheries.)

A more recent study was conducted at salmon farms in Passamaquoddy Bay (including the northwest shore of Deer Island) in May–December 2006 (MacPhee and Moore 2007). Eight of 11 active farms were monitored; seven had 2006 year-class smolts and one had 2005 year-class market fish. Most of the farms had introduced smolts in the spring of 2006, presumably louse-free, and no sea lice were found in May. There was a maximum abundance of sea lice in mid-September (Figure 3.7). The temporal trends at individual farms did not always reflect the overall trend. Numbers at individual farms were affected by treatments with emamectin benzoate, which were not synchronized among farms. Salmon on all of the eight participating farms were treated with emamectin benzoate; those on seven of the farms treated twice between July and December, and those on the other farms treated three times during this period. The first chalimus larvae of L. salmonis were found on farmed salmon in early June and chalimus larvae were present until the end of the study period in December, with highest abundance in September (Figure 3.8). L. salmonis was much more abundant than C. elongatus in the 2006 study, as in the 1994–1996 studies (Figure 3.7). The abundance of L. salmonis in Passamaquoddy Bay in May–December 2006 was much lower than in the same months in 1995 (Figure 3.9). The maximum monthly average abundance of L. salmonis for all Passamaquoddy Bay farms sampled in 2006 was 3.3 per fish in September, compared to 38.6 in September 1995. For C. elongatus, the difference between these 2 years was not as great (Figure 3.9) with a maximum in 2006 of 0.7 lice per fish in September, compared

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16 Lepeophtheirus Caligus Temperature BB Temperature PB

dd yB ay

BB

14

PB

Deer Island

10

2 8 6

Temperature (°C)

12

sa

ma q

uo

3

Pa s

Average number of Iice (all stages) per fish

1 4 2

0

0 May-06

Jun-06

Jul-06

Aug-06

Sep-06

Oct-06

Nov-06

Dec-06

Figure 3.7. Abundance of L. salmonis and C. elongatus on farmed salmon in Passamaquoddy Bay, May–June 2006. Data are monthly averages of all louse stages on all fish sampled; eight of 11 active salmon farms in the area were sampled. No lice were found in May. Temperature data are monthly averages at two locations within Passamaquoddy Bay (see inset map) at 5 m below the water surface (1–5 records per month). (From MacPhee and Moore 2007.) 16 Chalimus All other stages of L. salmonis Temperature BB Temperature PB

3

14

12

10 2 8 6

Temperature (°C)

BLBS084-03

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1 4 2

0

0 May-06

Jun-06

Jul-06

Aug-06

Sep-06

Oct-06

Nov-06

Dec-06

Figure 3.8. Abundance of chalimus larvae and all other stages of L. salmonis on farmed salmon in Passamaquoddy Bay, May–June 2006. The abundance of chalimus larvae is used as an indicator of recruitment onto salmon hosts. Data are monthly averages of all fish sampled; eight of 11 active salmon farms in the area were sampled. No lice were found in May. Temperature data are as in Figure 3.7. (From MacPhee and Moore 2007.)

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Figure 3.9. Comparison of abundance of L. salmonis (top) and C. elongatus (bottom) on farmed salmon in Passamaquoddy Bay in May–December of 1995 and 2006. Temperature data are monthly averages from two locations in each year (see inset maps) at 5 m below the water surface. ND, insufficient data (only one farm sampled). (Abundance data for 1995 provided by the New Brunswick Department of Agriculture, Aquaculture and Fisheries; 2006 data from MacPhee and Moore (2007).)

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to 1.1 lice per fish in November 1995. The lower overall sea louse abundance in 2006 was probably due to the use of emamectin benzoate. The pattern of initial infestation by C. elongatus, followed by L. salmonis, observed in southwestern New Brunswick has also been observed in Ireland (Jackson and Minchin 1992). Some European studies have also shown similar seasonal trends to that observed in southwestern New Brunswick. In Scotland and Ireland, L. salmonis abundance on farmed salmon was observed to be highest in late summer and fall (Wootten et al. 1982; Jackson and Minchin 1993). However, other European studies have shown different seasonal trends. In a later Scottish study (Wootten 1985), L. salmonis was most abundant on farmed salmon in December–March. Tully (1989) found that sea louse abundance on Atlantic salmon in an untreated cage in Ireland was variable through the summer and increased in December–January. Boxaspen (1997) recorded a large increase in the abundance of L. salmonis on farmed Atlantic salmon at sites near Bergen, Norway between May and June and massive settling of lice on salmon in November–March. At salmon farms in the Broughton Archipelago in the central coast area of British Columbia, sea louse abundance also showed strong seasonal trends, with Caligus clemensi most abundant in the spring and L. salmonis most abundant in the fall (Brooks 2005).

Effects of Temperature Water temperatures were recorded at 5-m depth at 30-minute intervals at 20 salmon farms in southwestern New Brunswick from April 1995 to October 1997 (Figure 3.10) as part of a study by Peterson et al. (2001). During this period, the highest temperature recorded was 16.1◦ C in August 1995 at a site in northern Passamaquoddy Bay, and the lowest was 0.1◦ C in February 1996 at the same site. The seasonal range in daily average temperature at farms varied from 10.5◦ C at a farm in the southern Deer Island area to 14.7◦ C at the northern Passamaquoddy Bay farm. The range in daily average temperatures among sites varied seasonally, with lowest ranges (usually <1◦ C) in spring and fall and highest ranges (usually >2◦ C, maximum 5.7◦ C) in summer. Studies in southwestern New Brunswick indicated that seasonal trends in sea louse abundance on farmed salmon were related to water temperature, with the highest numbers of both L. salmonis and C. elongatus in fall (September–November) when water temperature was highest, and lowest numbers in winter (January–February; Figures 3.4 and 3.7; Hogans and Trudeau 1989b; Hogans 1995). In contrast, seasonal trends at some locations in Scotland, Ireland, and Norway have shown increases in abundance in winter when temperatures were low (Wootten 1985; Tully 1989; Boxaspen 1997). The minimum winter temperatures in those areas, about 3–5◦ C, were considerably higher than typical minimum winter temperatures of less than 2◦ C in southwestern New Brunswick. In Scotland, where the normal water temperature range is 3.5–14◦ C, L. salmonis reproduces on farmed salmon throughout the year (Wootten et al. 1982; Wootten 1985). Hogans (1995) observed that newly hatched L. salmonis nauplii were observed during the coldest winter months in southwestern New Brunswick, but very few nauplii successfully molted to the copopodid stage at 2–3◦ C. He reported that the production of infective copepodids was limited or nonexistent at <3◦ C and that chalimus stages appeared to not molt, or molt very slowly, at <2.5◦ C. He also noted that the numbers

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14 12 10

sa m Ba aqu y od

dy

8

6

Pa s

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4

Deer I. Campobello I. Bay of Fundy

2

0 01/01/1995

Grand Mannan I.

01/01/1996

01/01/1997

01/01/1998

Figure 3.10. Temperatures at 5-m depth at salmon farms in southwestern New Brunswick, April 1995 to October 1997. Points represent daily averages of data recorded at 30-minute intervals at up to 20 farms each day (see Peterson et al. 2001). Inset map shows data collection locations (black dots).

of gravid females, the production of egg strings, and the infection rate by copepodids increased as the water temperature rose in late February–March. The 1994–1996 and 2006 data from southwestern New Brunswick suggest that recruitment of L. salmonis onto farmed salmon (as estimated by the abundance of chalimus larvae) was low when the water temperature was <7–8◦ C (Figures 3.5 and 3.8). Ritchie et al. (1993) found that adult female L. salmonis in Scottish salmon farms produced more, but smaller, eggs in winter, compared to in summer, due to temperature and photoperiod effects. Hogans (1995) also observed that the number of eggs and the length of egg strings of L. salmonis increased as temperature decreased from 3◦ C to 1◦ C in laboratory studies, while field observations in southwestern New Brunswick indicated that the number of lice with egg strings increased as the temperature increased in late winter. Estimates of the generation time for L. salmonis vary considerably and are highly correlated with temperature, as reviewed in the introductory chapter contributed by Hayward et al. and in Pike and Wadsworth (1999). The potential number of L. salmonis generations on southwestern New Brunswick salmon farms was estimated using water temperatures recorded during the Peterson et al. (2001) study (Figure 3.10). The generation times and number of generations were estimated following the approach of Tully (1992), using the daily mean, minimum, and maximum water temperatures from the time series records. The cumulative number of generations was estimated by inverting the generation time to give an estimate of the proportion of the development

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cycle that would occur on each day and then calculating the cumulative sum of these proportions. When a start date of January 1st is assumed, the number of potential generations in 1996 is estimated to be 3.6. If we assume a start date of March 31st, the number of potential generations is 3.3. This delayed start date (Figure 3.11) is the date at which water temperature exceeds 3◦ C, the temperature below which Hogans (1995) suggests successful larval development does not occur. This latter cumulative generation curve is shown in Figure 3.11.

Effects of Salinity Various studies have shown that L. salmonis cannot tolerate low salinities, as reviewed in the introductory chapter contributed by Hayward et al. Salinity data collected from three locations within the southwestern New Brunswick salmon farming area (two in Passamaquoddy Bay and one in Lime Kiln Bay) from 1999 to 2008 indicated that the surface (1-m depth) salinity never dropped below 18 psu and was mostly 25–33 psu, while at 5-m depth the salinity varied from 27 to 33 psu (Figure 3.12). This suggests that low salinity is probably not a limiting factor for L. salmonis in southwestern New Brunswick. In areas with a greater salinity range, salinity may have a greater influence on sea lice. In the central coast area of British Columbia, where the salinity typically varies from 15 to 30 psu during the year, Brooks (2005) indicated that seasonal trends in the abundance of L. salmonis on farmed salmon may be at least partly related to seasonal salinity variations.

Effects of Water Circulation Pike and Wadsworth (1999) noted that water currents are recognized as important in the transmission of sea lice between salmon farms, because good flushing will minimize reinfection. In a study of epidemiological factors affecting sea louse abundance on Scottish salmon farms, Revie et al. (2003) reported that, of the factors outside of farm management control, only current speed and flushing time had a significant effect on the abundance of L. salmonis; sea louse abundance was lower where current speeds were high and flushing times short (i.e., short residence time). Because dispersal of sea lice apparently occurs mostly during the planktonic naupliar and copepodid stages (Costello 2006) and is therefore influenced by water currents, the risk of transmission between farms would be greatest where there are several farms that are connected by water circulation. This suggests that the best scenario for minimizing reinfection and transmission among farms would be where there are strong currents and large distances separating farms. In southwestern New Brunswick, many farms are located in close proximity to another farm. More than one-third of farms have a neighboring farm <300 m away and three-quarters of farms have a neighboring farm <1 km away (Figure 3.13). The salmon farming area with the shortest separation distances between neighboring farms is the Letang area (Letang Harbour, Lime Kiln Bay, Bliss Harbour, and Back Bay) where 19 of the 23 farms have a nearest neighbor <300 m away. This is also the area where the outbreak of L. salmonis started in the fall of 1994.

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Daily water temperature statistics 5 m below the surface for 1996

16

14 12 Temperature (°C)

10 8

6 Daily max Daily avg

4

Daily min 2 Daily range

11/1/96

9/1/96

7/1/96

5/1/96

3/1/96

1/1/96

0

Date (mm/d/yy)

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600

4

3 Cumulative generation number Instanteous generation times

400

2

11/1/96

9/1/96

0 7/1/96

0 5/1/96

1

3/1/96

200

Cumulative generation number

Potential generation times and number based on Tully (1992) and SWNB daily water temperature statistics for 1996

1/1/96

BLBS084-03

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Date (mm/d/yy)

Figure 3.11. Water temperature summary statistics for 1996 (top panel), potential sea louse generation times (bottom panel) calculated from the water temperatures based on the approach of Tully (1992), and the cumulative number of generations assuming a starting date of March 31, the date when the daily mean water temperature exceeded 3◦ C in 1996 (bottom panel).

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Figure 3.12. Salinities at three locations in the salmon farming area of southwestern New Brunswick at 1-m depth (top) and 5-m depth (bottom). Data were recorded one to five times per month (see Martin et al. 1999). Locations are shown on inset maps in Figures 3.4 and 3.7.

As an indicator of the relative flushing rates at each farm, we can use the size of the tidal excursion area of each farm, as estimated using a tidal circulation model (Greenberg et al. 2005). We used the model to estimate the tidal excursion areas of farms in southwestern New Brunswick, with forcing by the principal lunar semidiurnal tidal constituent (M2 ), which is the predominant tidal component in southwestern New Brunswick (Figure 3.14). Maps of estimated tidal excursion areas of individual farms and details on the methodology can be found in Page et al. (2005); Chang et al. (2005a, 2005b, 2006a, 2006b, 2007). Using the sizes of the model-derived tidal excursion areas as indicators of flushing rates, we predicted that farms in Beaver Harbour and northern Passamaquoddy Bay would have the lowest average flushing rates, while farms in Letete Passage and eastern Grand Manan Island would have the highest flushing rates (Table 3.1). To estimate the amount of interaction due to water circulation between farms, we determined the overlaps between tidal excursion areas and farm sites (Table 3.1). The percentage of farm tidal excursion areas that overlapped at least one other farm site varied from 0% for farms in Beaver Harbour to 100% for farms in the Letang area. The maximum number of farm sites overlapped by a farm tidal excursion area was 9, for a farm in the Letang area. The farming area with

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Figure 3.13. Frequency distribution of distances between each finfish farm in southwestern New Brunswick and its nearest neighboring farm, 2008. Top graph is for all farms in southwestern New Brunswick. Remaining graphs are for subareas. The distances are the shortest distances through water between farm site boundaries.

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Figure 3.14. Model-derived tidal excursion areas of finfish farms in southwestern New Brunswick in 2008, by farming area. Finfish farms are shown as small black polygons. (Modified from Chang et al. 2007.) (See also color plate section.)

the highest average number of overlaps between farm tidal excursion areas and farm sites is the Letang area (Figure 3.15) and the lowest is in the Beaver Harbour/Maces Bay area (Table 3.1). The data from the period of maximum sea louse abundance in 1995 (July–October) showed that the highest average abundance of L. salmonis was in northern Passamaquoddy Bay and the Letang area (Figure 3.16). The Letang area had the highest density of farms, the highest number of predicted overlaps of farm sites by tidal excursion areas, as well as relatively low current speeds. Together, these factors would suggest a greater risk of sea louse infection. The northern Passamaquoddy Bay area had the greatest separation distances between farms and a low average number of overlaps between tidal excursion areas and farm sites, which would indicate a smaller risk of sea lice spreading between farms. However, this area also had the lowest current speeds (apart from the two farms in Beaver Harbour), which would indicate a higher

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Table 3.1. Average sizes of model-derived tidal excursion areas and the average number of farm sites overlapped by tidal excursion areas of farms in each farming area in southwestern New Brunswick in 1996 and 2008. There were no farms in the Maces Bay area until 1998.

Farming area 1996 Passamaquoddy Bay north Deer and Campobello Islands Letete Passage Letang area Beaver Harbour Grand Manan Island east Grand Manan Island south 2008 Passamaquoddy Bay north Deer and Campobello Islands Letete Passage Letang area Beaver Harbour and Maces Bay area Grand Manan Island east Grand Manan Island south

ABMA 1(north)

Number of farms

Average size of tidal excursion area (km2 )

Average number of farms overlapped by tidal excursion areas

5

0.8

0.4

1(south) + 4

24

9.9

1.5

6 2a 3a 2b

4 25 2 6

11.3 2.6 0.2 14.6

2.8 4.0 0.0 1.0

3b

4

4.4

0.8

1(north)

9

1.0

0.2

1(south)+4

28

7.4

1.3

6 2a 3a

3 23 11

10.3 2.8 5.6

2.0 3.9 0.2

2b

11

16.3

1.9

3b

9

9.8

1.1

ABMA, Aquaculture Bay Management Area (2006 framework).

risk of reinfection. Grand Manan Island farms, which had the lowest abundance of sea lice, had relatively large tidal excursion areas, and low to moderate numbers of overlaps of farm sites by tidal excursion areas. The abundance of C. elongatus, which was much lower overall than that of L. salmonis, showed a different distribution among farming areas, with low abundance in the northern Passamaquoddy Bay and Letang areas and less variability among areas than was seen for L. salmonis (Figure 3.16). Hogans (1997) conducted plankton tows in and near salmon cages at three farms in southwestern New Brunswick from August 1996 to March 1997. The densities of nauplii and copepodids were low in all samples. Sea louse larvae were found inside cages only during August–November. Outside of the cages (10–20 m away), larvae were extremely rare. He concluded that overall larval density was low in 1996, which

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Figure 3.15. Model-derived tidal excursion areas for finfish farms in the Letang area (Letang Harbour, Lime Kiln Bay, Bliss Harbour, and Back Bay) and adjacent farming areas in 2008. Finfish farms are shown as small black polygons. (Modified from Chang et al. 2005b.) (See also color plate section.)

he related to the low abundance of sea lice on farmed salmon at these sites in that year. He also concluded that larval abundance and density were greatest at the infection site and decreased away from the site.The low numbers of larvae outside of cages indicated that, at least in 1996, most of the sea louse infections were due to reinfection within cages, rather than dispersal of lice between cages and farms. He also noted that the cages had moderately to heavily fouled nets which helped to retain larvae within the cages. At the time of his study, there were no available circulation models with which to predict larval transport. The information we now have on water circulation in southwestern New Brunswick suggests that there is the potential for transport of sea louse larvae among farms, especially where there are many farms within a bay and where sea louse numbers are high. In western Ireland, Costelloe et al. (1996) also found highest densities of L. salmonis larvae within a cage which had fouled nets. Densities in tows outside the cage were <10% of the densities inside and a model predicted that very few larvae would be recovered >2 km away from the farm. In a Scottish loch, Penston et al. (2008) found that L. salmonis nauplii were more abundant in plankton tows close to salmon farms. They also found that copepodids were more widely distributed than nauplii, indicating that the larvae can be transported several kilometers away from where hatching occurs. Particle-tracking models of sea louse dispersal have predicted dispersal distances of

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35 Average number of Iice (all stages) per fish

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5

0 Passama- Deer and Letete quoddy Campobello Passage Bay north Islands

Letang area

Beaver Harbour

Grand Grand Grand Manan I. Manan I. Manan I. east south Dark Harbour

Figure 3.16. Average abundance of L. salmonis and C. elongatus (all stages) on salmon in farming areas of southwestern New Brunswick, during the peak period of louse abundance in 1995 (July–October). (Data provided by the New Brunswick Department of Agriculture, Aquaculture and Fisheries.)

several kilometers in a Scottish loch (Murray and Gillibrand 2006), up to 100 km in a larger Norwegian fjord (Asplin et al. 2004), and up to 40 km in the Broughton Archipelago, British Columbia (Brooks 2005). Model predictions of tidal mixing in the Passamaquoddy Bay and Letang areas indicate that some particles released in these areas could be transported several kilometers, but others would remain near their point of origin after ten tidal cycles (Thompson et al. 2002). It should be noted that since our tidal excursion estimates are based on just the M2 tide, they probably underestimate the actual tidal excursions that would include other tidal components, as well as wind and freshwater input. Furthermore, our tidal excursion estimates represent water movement over just one tidal cycle (12.4 h), while sea louse larvae may be in the sea for several days. Hence, the tidal excursion areas shown in Table 3.1 and Figures 3.14 and 3.15 would likely underestimate the potential area of dispersion of sea lice due to water currents.

Management Actions to Control Sea Lice in southwestern New Brunswick The spread of sea lice among fish appears to occur mainly during the planktonic larval stages through a combination of passive transport and active movement (Johnson 1998; Costello 2006). Direct transfer of mobile stages (preadults and adults) of sea lice between fish hosts may also occur when fish are situated in close proximity. Transfer of mobile stages of L. salmonis between salmon hosts has been observed in

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the laboratory and in a sea cage (Bruno and Stone 1990; Hogans 1995; Ritchie 1997). Transfer of mobile stages of C. elongatus among salmon hosts has also been reported (Hogans and Trudeau 1989a; Bruno and Stone 1990). Saksida et al. (2007) noted that the possibility that mobile sea lice could be directly transferred between wild and farmed salmon could not be discounted, especially in British Columbia where salmon farming occurs in the presence of large wild salmon populations. The experience in Scotland and Ireland indicated that chemical treatment was the main effective sea louse control method available. The effectiveness of chemical treatments could be increased (and the overall use of chemicals reduced) through the organization of farms into management areas, within which sea louse populations would be monitored and chemical treatments coordinated. Sea louse abundances could be reduced by practicing single-year-class farming, because lice are easily transferred between generations at multiyear-class farms. Sea louse abundance could be further reduced through fallowing at individual farms and synchronized fallowing of all farms in the same management area (Bron et al. 1993; Grant and Treasurer 1993; Jackson and Minchin 1993). Bron et al. (1993) reported that longer fallow periods (16–17 weeks) were more effective than shorter periods (9 weeks), but Revie et al. (2003) found no significant effect of longer (10–12 weeks) versus shorter (6–7 weeks) fallow periods. Costello (2006) recommended a fallow period of 4–6 weeks. Revie et al. (2003) also found that stocking density, site biomass, and the presence of neighboring farms within 5 km with whom there is no working management agreement, were not important factors. In 1995, ten Sea Louse Management Zones were created in the southwestern New Brunswick farming area to allow for better coordination of actions to deal with the sea louse problem. The delineation of the zones (Figure 3.17) was based mainly on local knowledge of water currents and site interactions. At the time, there were little data on water circulation in southwestern New Brunswick at the scale needed to predict between-farm interactions. Within each zone, antilouse treatments were to be coordinated. However, the conversion of farms to single-year-class operations, with fallowing between successive year-classes and synchronized fallowing of farms within these management zones, were not implemented throughout the industry because it was felt at the time that the negative economic impacts of such practices would be too large. In 1996, more than 60% of salmon farms in southwestern New Brunswick were multiyear-class operations (McGeachy and Moore 2003). Management actions related specifically to sea louse control were relegated to secondary importance with the start of an outbreak of infectious salmon anemia (ISA) among salmon farms in southwestern New Brunswick in 1996. However, it was recognized that management actions to control ISA would also be beneficial in the control of sea lice. Research by Nylund et al. (1993) indicated the possible role of sea lice in the spread of ISA, thus controlling sea lice would also likely be beneficial to the management of ISA. A new site allocation policy for southwestern New Brunswick was introduced in 2000, largely to deal with the management of ISA (NBDAFA 2000). Because there were no available chemical or drug treatments for ISA, the only option was to implement some of the management actions that were previously rejected as impractical for the management of sea lice. The southwestern New Brunswick salmon farming area was divided into 21 Aquaculture Bay Management Areas (ABMAs), encompassing all farms operating at the time. The ABMA boundaries were based on a combination

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Figure 3.17. Ten sea louse management areas in the southwestern New Brunswick salmon farming area, 1995. Finfish farms in southwestern New Brunswick and adjacent Maine in 1995 are shown as small black polygons.

of fish health, oceanographic, and business considerations, although knowledge of local water currents was still quite limited at the time. Both industry and government understood that the number of ABMAs would probably need to be reduced. Farms were required to become single-year-class operations, operating on a 2-year rotation system with smolt entries in either odd or even years. All farms in the same ABMA (with a few exceptions) would have fish of the same year-class. However, up to 20% of market fish could be held over at the time of the next smolt entry. As a result of the implementation of the new site allocation policy, all salmon farms in southwestern New Brunswick had become single-year-class operations by the end of 2002 (McGeachy and Moore 2003). Despite the new policy and the associated management changes, ISA continued to infect farms in southwestern New Brunswick and adjacent Maine after 2000. Among the probable factors contributing to the continued spread of ISA were the large number of ABMAs, which were not sufficiently isolated oceanographically and the 2-year rotation system that allowed for up to 20% holdovers. Thus, there was not a mandatory fallowing between successive year-classes. In order to address these issues, a new ABMA framework was implemented starting in 2006. This new framework included fewer, but larger, ABMAs, which had a stronger oceanographic basis, and

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Figure 3.18. Aquaculture Bay Management Areas (ABMAs) for the southwestern New Brunswick salmon farming area, implemented starting in 2006. ABMA 4 (dashed line) was incorporated into ABMA 1 in 2010. Finfish farms in southwestern New Brunswick and adjacent Maine in 2006 are shown as small black polygons.

a 3-year rotation system, with mandatory fallowing (4 months per site, 2 months per ABMA) between successive year-classes (Figure 3.18). In addition to facilitating better management of ISA, the new ABMA framework was expected to assist in the management of other fish health issues, such as sea lice. The volume of emamectin benzoate used in southwestern New Brunswick decreased by about 50% from 2002 to 2008, indicating that sea louse abundance had also decreased. A major challenge now facing the salmon farming industry is the development of resistance to this chemical by sea lice. Reduced sensitivity to emamectin benzoate has been recently reported in L. salmonis in Scotland (Lees et al. 2008) and in Caligus rogercresseyi in Chile (Bravo et al. 2008). The first indications of possible resistance to this chemical in L. salmonis in southwestern New Brunswick were reported in the summer of 2008 in the Letang area. However, at the time, the data were inconclusive. By the summer of 2009, emamectin benzoate had become ineffective in the Letang area and was showing decreased effectiveness in other areas of southwestern New Brunswick. Consequently, sea louse abundance increased on farmed salmon in southwestern New Brunswick and farmers requested emergency authorizations for

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R other chemical treatments. Bath treatments using deltamethrin (ALPHA MAX ) were allowed in the Letang area from May 2009 to May 2010. Bath treatments using azamethiphos were permitted in all areas of southwestern New Brunswick from R ), added to feed, was also October 2009 to October 2010. Teflubenzuron (Calicide made available under an Emergency Drug Release. Continued effective management of sea lice will require the use of various chemical treatments rotated according to an Integrated Pest Management Program, thus reducing the risk of the lice developing tolerance to a single product. Other management options, such as nonchemical treatment methods and reevaluation of the ABMA framework in the context of sea lice, should also be investigated.

Sea Louse Interactions between Farmed Salmon and Wild Fish in southwestern New Brunswick Lice infecting fish farms can originate from wild fish that occur in the vicinity of farms or from infected farmed fish. The risk of sea louse transfer between wild and farmed fish is a function of the distance between fish farms and wild salmon migration pathways, as well as the abundance of lice on the “donor” fish. As mentioned previously, most dispersal appears to happen during early sea louse development when stages occur in the plankton and are subject to transport by water currents (Costello 2006). The possibility that mobile stages (preadults and adults) could also transfer between wild and farmed fish located in close proximity cannot be discounted (Saksida et al. 2007). Atlantic salmon have historically inhabited seven major rivers in the outer Bay of Fundy area (southwestern New Brunswick) and 32–42 rivers in the inner Bay of Fundy area (east of Saint John). The Bay of Fundy once supported an important commercial salmon fishery with about two-thirds of the catch in most years returning to the Saint John River system. Data for commercial salmon catches in the Bay of Fundy are available from 1870. Since that time, the largest reported catch was 470 tons in 1873 (Huntsman 1931a), which would be in the order of 100,000 fish. Catches dropped sharply in the late 1870s, before increasing again in 1906 to 440 tons. Catches then experienced a general decline (although with large interannual fluctuations) until the fishery was permanently closed in 1985 due to the low abundance of stocks. Inner Bay of Fundy stocks are currently considered to be endangered, while outer Bay of Fundy stocks are not meeting conservation requirements (Jones et al. 2006). The total number of adult salmon returning to Bay of Fundy rivers in recent years is estimated to be about 5000 per year, of which >90% are Saint John River fish and about onequarter of these are hatchery fish (Jones et al. 2006). The historic abundance of adult salmon returning to inner Bay of Fundy rivers was estimated to have been >40,000, but the abundance had fallen to as few as 250 by 1999 (DFO 2008). In comparison, there are about 15,000,000 farmed salmon in sea cages in southwestern New Brunswick at present. The migration routes of adult Atlantic salmon can be estimated from commercial catches. The most important component of the commercial salmon fishery was a drift net fishery for salmon returning to spawning grounds in the Saint John River system. This fishery took place off the mainland coast of New Brunswick, mainly between Saint John Harbour (at the mouth of the Saint John River) and Point Lepreau (Perley 1852;

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Huntsman 1931a). Huntsman (1931b) reported that the fishery for returning Saint John River salmon “. . . extends from the harbour out into the bay to the southwest nearly to Grand Manan in a strip of water roughly between one mile and eight miles off the coast” (Figure 3.1). He also noted that returning salmon were relatively scarce nearshore, as evidenced by the scarcity of salmon caught in herring weirs located along the mainland coast and the very rare occurrences in weirs on the northern end of Grand Manan Island (Huntsman 1936). He suggested that the salmon were following the lower salinity outflow water from the Saint John River. This route would not take them into the area where most salmon farming now occurs. There is the possibility that migrating adult salmon could come near some of the new farms that have been located east of Point Lepreau since 2003, as well as farms located off the east coast of Grand Manan Island. However, even in these areas, the probability of sea louse transfers between migrating and farmed fish is likely to be low because the migrating salmon are mostly staying some distance offshore. However, predicted tidal excursion areas of some farms in the southeastern Grand Manan Island area do extend several kilometers offshore (Figure 3.12) and drifters released off the coast near Musquash Harbour have sometimes moved several kilometers offshore within 1 d (Page et al. 2009), indicating the possibility that planktonic sea louse stages could be transported some distance offshore. The commercial fishery for Saint John River Atlantic salmon occurred mostly between May and September, with the largest catches in most years in June or July (May and Lear 1971). This means that the seasonal timing of the returning adult migration overlapped with the period of high sea louse abundance on farmed salmon, although the largest catches were earlier than the peak in sea louse abundance on farmed salmon (usually in September or later). There was also a small commercial salmon fishery in some years in Charlotte County (west of Point Lepreau to the United States border), which is the area where most salmon farming now occurs. The salmon caught by this fishery were from rivers within the local area and not the Saint John River (Huntsman 1931a). The most important salmon rivers in this area are the St. Croix and Magaguadavic Rivers. Perley (1852) reported that in the early 19th century, there were up to 18,000 salmon returning to the St. Croix River per year, but by the mid-19th century, there were <200. The decline was attributed to dam construction. Returns of adult Atlantic salmon to the St. Croix River in the 1980s and 1990s were <400 per year, with highest returns in 1987 and 1988 (Jones et al. 2006). In the Magaguadavic River, a return of 940 salmon in 1983 was reported as being double the highest previous number three decades earlier (Martin 1984). The number of salmon returning to the Magaguadavic River has declined since then. The reasons for the decline are unknown, but it corresponds with the development of salmon aquaculture in the area. The St. Croix and Magaguadavic Rivers have both experienced near zero returns in recent years (Jones et al. 2006). There is the potential for sea louse transfer between wild salmon postsmolts and farmed salmon where there is spatial overlap in their distributions. Ultrasonic tagging studies on postsmolts migrating from the Saint John River system and inner Bay of Fundy rivers in 2001 and 2002 found that few of these fish entered the salmon farming area of southwestern New Brunswick (Lacroix 2008). However, surface trawl sampling indicated there was the possibility that some postsmolts could move into the vicinity of salmon farms along the eastern shore of Grand Manan Island (Lacroix and Knox 2005). Earlier reports indicated that many postsmolts from the Saint John River and

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the Big Salmon River (an inner Bay of Fundy river) did enter the Passamaquoddy Bay area (Huntsman 1936; Jessop 1976) where there are now several salmon farms. Ultrasonic tagging studies on postsmolts from the St. Croix and Magaguadavic Rivers show that their migration routes bring them into the vicinity of several salmon farms (Lacroix et al. 2004). The preceding information suggests that the risk of transfer of sea lice between wild salmon of the most important river, the Saint John River and farmed salmon in southwestern New Brunswick is relatively low because the spatial overlap of wild postsmolts and adults of this river with farmed salmon is relatively small. For salmon of the Magaguadavic and St. Croix Rivers, whose migration routes pass near salmon farms, both as postsmolts and adults, their numbers are currently very low, so the risk of large-scale transfer of sea lice from wild to farmed salmon would be expected to be low. However, the potential for sea louse transfer from farmed salmon to wild salmon of these rivers would be high, especially if there are high sea louse numbers on fish in salmon farms located near the wild salmon migration routes. The available data on sea louse abundance on wild salmon suggests that large-scale transfers of lice from farmed to wild salmon have not occurred in southwestern New Brunswick. Captures of postsmolts in the Bay of Fundy and Gulf of Maine in 2001–2003 indicated that the outmigrating fish were healthy with no sea lice (Lacroix and Knox 2005). However, Carr and Whoriskey (2004) found that two of 23 “landlocked” Magaguadavic River salmon, which had emigrated from freshwater into Passamaquoddy Bay in 2002, returned to the river in less than 2 months with significant dermal damage due to sea lice. They suggested that postsmolts migrating from the Magaguadavic River may be susceptible to sea louse infestations when they pass near fish farms and this could cause higher mortality. However, they also reported that wild adult salmon returning to the river during 1992–2002 were not severely damaged by sea lice. Adult salmon returning to inner Bay of Fundy rivers have also been found to be relatively free of sea lice (DFO 2008). The situation in southwestern New Brunswick with respect to the transfer of sea lice between farmed and wild salmon is in contrast with the situation in an area of coastal British Columbia referred to as the Broughton Archipelago, where Krkoˇsek et al. (2005) concluded that large-scale transfer of L. salmonis from farmed to wild pink salmon (Oncorhynchus gorbuscha) had occurred, although there has been considerable debate over this issue (Brooks 2005; Krkoˇsek et al. 2006; Brooks and Stucchi 2006). There is also evidence that sea louse infestations of wild Atlantic salmon and other salmonids in some areas of Europe were at least partly due to louse larvae originating from salmon farms (Tully and Whelan 1993; Tully et al. 1993; Bjørn and Finstad 2002; Heuch et al. 2005; Penston and Davies 2009). In southwestern New Brunswick, the available information indicates that it is unlikely that wild salmon are a major source of L. salmonis infecting farmed salmon, due to the small numbers of wild salmon and the relatively small spatial overlap between farmed salmon and the major runs of wild salmon. At some sites, infected farmed salmon from the same farm or neighboring farms are likely serving as reservoirs. The potential for the water-borne transport and dispersal of sea lice between salmon farms and bays was discussed previously. However, where farms are isolated from wild salmon migration routes and from neighboring active farms, it would appear that there must be other sources of sea lice. For C. elongatus, which is known to infect

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many fish species, it is probable that pollock (Pollachius virens), which are often found in and around salmon cages in southwestern New Brunswick, act as a reservoir (Wootten et al. 1982). Anecdotal information provided by salmon farmers indicates that even when entire bays have been fallowed of farmed salmon for several months, sea louse infestations can occur shortly after farmed salmon have been reintroduced. In such cases, water-borne movement of larvae from other infected farms seems unlikely, but cannot be entirely discounted. In the absence of water-borne movement of larvae, this suggests that the sea lice may have been transferred from nonsalmonid wild fish. L. salmonis is considered to be a parasite of salmonids and occurrence on other species is considered unusual (Kabata 1979). However, L. salmonis have been found on several other species of marine fish (see the introductory chapter contributed by Hayward et al.), many of which are found in southwestern New Brunswick marine waters (Macdonald et al. 1984). If L. salmonis is found to occur on nonsalmonid species in coastal southwestern New Brunswick, this may help explain the reinfection of farms in isolated bays or where fallowing has occurred and wild salmon are rare.

Summary The southwestern New Brunswick salmon farming industry started in 1978 and now has over 90 farms located within a relatively small area. Sea lice were present in the early years of the industry, but generally in small numbers. An outbreak of L. salmonis started in the fall of 1994, and quickly spread throughout the salmon farming area of southwestern New Brunswick. There are only limited data available on sea louse abundance on farmed salmon in southwestern New Brunswick, and the use of chemical treatments makes this data difficult to interpret. The data indicate that sea lice are present on farmed salmon throughout the year, with highest abundances in late summer and fall. Because winter and summer water temperatures are lower than in other salmon farming areas, the number of generations of L. salmonis per year in southwestern New Brunswick is estimated to be only about 3–4, which is 2–3 generations fewer than in other major salmon aquaculture areas. Salinity is generally >28 psu in the salmon farming area in southwestern New Brunswick, so sea louse abundance is unlikely to be limited by salinity. There were geographic differences in the intensity of sea louse infestations in southwestern New Brunswick. The highest abundance of sea lice was in the Letang area, which had the highest density of farms and small tidal excursion areas. A tidal circulation model can be used to predict the connectivity among farms due to water circulation. The greatest connectivity occurs at farms with large tidal excursion areas and many close neighboring farms. Sea lice, especially L. salmonis, will likely continue to infect farmed salmon as long as salmon farming continues. Information on water currents in southwestern New Brunswick indicates that where sea louse larvae are present, they can be transported between farms, especially where farms are located close together. This indicates the need for a coordinated sea louse control strategy among farms. Chemical treatments, especially emamectin benzoate, have been effective in controlling sea louse numbers up until recently. However, sea lice are developing resistance to this chemical.

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Therefore, other chemical treatments will have to be used in order to control sea louse numbers so that salmon farming can remain economically sustainable and wild salmon are protected. Research on other chemical and nonchemical treatments will be required to assess their effectiveness in controlling sea lice on farmed fish in southwestern New Brunswick, as well as to determine their potential impacts on nontarget species and the environment. An Aquaculture Bay Management Area framework was implemented in 2000, largely to manage an outbreak of infectious salmon anemia. This framework included single-year-class farming on a 2-year rotation system. However, farms were allowed to keep some market fish on site at the time of the subsequent smolt entry, so fallowing was not mandatory. A revised Aquaculture Bay Management Area framework was introduced in 2006. This new framework includes fewer Aquaculture Bay Management Areas, single-year-class farming on a 3-year crop rotation, and mandatory fallowing of farms and Aquaculture Bay Management Areas between successive smolt entries. Other options for managing sea lice should be investigated. More research on how sea lice spread would be beneficial, including fieldwork and modeling of the role of water currents in the spread of sea lice. This would assist in determining where to locate new farms to ensure that they do not increase the likelihood of sea louse infestations. Such work would also help in the designation of Aquaculture Bay Management Areas or the readjustment of existing Aquaculture Bay Management Area boundaries. Other issues that should be investigated include determining the most effective fallow length for controlling sea lice in southwestern New Brunswick and the role of nonsalmonid hosts for L. salmonis in the spread of sea lice and reinfection of farms in southwestern New Brunswick. Evidence available to date suggests that there have been no large-scale transfers of sea lice from farmed salmon to wild salmon. Nevertheless, most wild salmon stocks in the Bay of Fundy are in low abundance and at least some of these stocks spatially overlap for part of their lives with the salmon farms of southwestern New Brunswick. Therefore, it is important that there be close monitoring of sea louse abundance and proper treatment and management of sea lice to ensure that numbers remain low. This will ensure that there is no large production of sea louse larvae by farmed salmon that could infect wild salmon in the Bay of Fundy, thus decreasing their prospects for recovery.

Acknowledgments We thank the New Brunswick Department of Agriculture, Aquaculture, and Fisheries (NBDAAF) for making available unpublished data from 1994 to 1996 and R. Pitre for collecting the data. Tidal circulation model research was conducted in collaboration with D.A. Greenberg and J.D. Chaffey (Bedford Institute of Oceanography), and funded by the Fisheries and Oceans Canada Aquaculture Collaborative Research and Development Program, with contributions from the New Brunswick Salmon Growers’ Association and NBDAAF. Water temperature data during 2006 were collected by M. LeGresley and P. McCurdy (St. Andrews Biological Station) from the CCGS Pandalus III (Captain W. Miner and deckhand D. Loveless). We also thank K. BrewerDalton (NBDAAF) for providing information on recent treatment issues.

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References Armstrong, R., MacPhee, D., Katz, T., and Endris, R. 2000. A field efficacy evaluation of emamectin benzoate for the control of sea lice on Atlantic salmon. Canadian Veterinary Journal 41: 607–612. Asplin, L., Boxaspen, K., and Sandvik, A.D. 2004. Modelled distribution of salmon lice in a Norwegian fjord. ICES CM 2004/P:11, 12 p. Bere, R. 1930. The parasitic copepods of the fish of the Passamaquoddy region. Contributions to Canadian Biology and Fisheries New Series 5: 423–430. Bjørn, P.A. and Finstad, B. 2002. Salmon lice, Lepeophtheirus salmonis (Krøyer), infestation in sympatric populations of Arctic char, Salvelinus alpinus (L.), and sea trout, Salmo trutta (L.), in areas near and distant from salmon farms. ICES Journal of Marine Science 59: 131–139. Boxaspen, K. 1997. Geographical and temporal variation in abundance of salmon lice (Lepeophtheirus salmonis) on salmon (Salmo salar L.). ICES Journal of Marine Science 54: 1144–1147. Bravo, S., Sevatdal, S., and Horsberg, T.E. 2008. Sensitivity assessment of Caligus rogercresseyi to emamectin benzoate in Chile. Aquaculture 282: 7–12. Bron, J.E., Sommerville, C., Wootten, R., and Rae, G.H. 1993. Fallowing of marine Atlantic salmon, Salmo salar L., farms as a method for the control of sea lice, Lepeophtheirus salmonis (Krøyer, 1837). Journal of Fish Diseases 16: 487–493. Brooks, K.M. 2005. The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada. Reviews in Fisheries Science 13: 177–204. Brooks, K.M. and Stucchi, D. 2006. The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada (Brooks, 2005)—a response to the rebuttal of Krkoˇsek et al. (2005a). Reviews in Fisheries Science 14: 13–23. Bruno, D.W. and Stone, J. 1990. The role of saithe, Pollachius virens L., as a host for the sea lice, Lepeoptheirus salmonis Krøyer and Caligus elongatus Nordmann. Aquaculture 89: 201–207. Burridge, L.E. 2003. Chemical use in marine finfish aquaculture in Canada: a review of current practices and possible environmental effects. Canadian Technical Report of Fisheries and Aquatic Sciences 2450 1: 97–131. Carr, J. and Whoriskey, F. 2004. Sea lice infestation rates on wild and escaped farmed Atlantic salmon (Salmo salar L.) entering the Magaguadavic River, New Brunswick. Aquaculture Research 35: 723–729. Chang, B.D., Page, F.H., Losier, R.J., Greenberg, D.A., Chaffey, J.D., and McCurdy, E.P. 2005a. Water circulation and management of infectious salmon anemia in the salmon aquaculture industry of Cobscook Bay, Maine and adjacent southwestern New Brunswick. Canadian Technical Report of Fisheries and Aquatic Sciences 2598: 54 p. Chang, B.D., Page, F.H., Losier, R.J., Greenberg, D.A., Chaffey, J.D., and McCurdy, E.P. 2005b. Water circulation and management of infectious salmon anemia in the salmon aquaculture industry of Letete Passage, Back Bay, Bliss Harbour, and Lime Kiln Bay in southwestern New Brunswick. Canadian Technical Report of Fisheries and Aquatic Sciences 2599: 55 p. Chang, B.D., Page, F.H., Losier, R.J., Greenberg, D.A., Chaffey, J.D., and McCurdy, E.P. 2006a. Water circulation and management of infectious salmon anemia in the salmon aquaculture industry of eastern Grand Manan Island, Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Sciences 2621: 34 p. Chang, B.D., Page, F.H., Losier, R.J., Greenberg, D.A., Chaffey, J.D., and McCurdy, E.P. 2006b. Water circulation and management of infectious salmon anemia in the salmon aquaculture industry of Passamaquoddy Bay, southwestern New Brunswick. Canadian Technical Report of Fisheries and Aquatic Sciences 2622: 46 p.

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Chang, B.D., Page, F.H., Losier, R.J., Lawton, P., Singh, R., and Greenberg, D. 2007. Evaluation of Bay Management Area scenarios for the southwestern New Brunswick salmon aquaculture industry: Aquaculture Collaborative Research and Development Program final report. Canadian Technical Report of Fisheries and Aquatic Sciences 2722: 69 p. Costello, M.J. 2006. Ecology of sea lice parasitic on farmed and wild fish. Trends in Parasitology 22: 475–483. Costelloe, M., Costelloe, J., and Roche, N. 1996. Planktonic dispersion of larval salmon-lice Lepeophtheirus salmonis, associated with cultured salmon, Salmo salar, in western Ireland. Journal of the Marine Biological Association of the United Kingdom 76: 141–149. DFO (Department of Fisheries and Oceans Canada). 2008. Recovery potential assessment for inner Bay of Fundy Atlantic salmon. DFO Canadian Scientific Advisory Secretariat Science Advisory Report 2008/050: 34 p. Grant, A.N. and Treasurer, J.W. 1993. The effects of fallowing on caligid infestations on farmed Atlantic salmon (Salmo salar L.) in Scotland. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 255–260. Ellis Horwood, New York. Greenberg, D.A., Shore, J.A., Page, F.H., and Dowd, M. 2005. A finite element circulation model for embayments with drying intertidal areas and its application to the Quoddy Region of the Bay of Fundy. Ocean Modelling 10: 211–231. Heuch, P.A., Bjørn, P.A., Finstad, B., Holst, J.C., Asplin, L., and Nilsen, F. 2005. A review of the Norwegian ‘National Action Plan Against Sea Lice on Salmonids’: the effect on wild salmonids. Aquaculture 246: 79–92. Hogans, W.E. 1995. Infection dynamics of sea lice, Lepeophtheirus salmonis (Copepoda: Caligidae) parasitic on Atlantic salmon (Salmo salar) cultured in marine waters of the lower Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Sciences 2067: 10 p. Hogans, W.E. 1997. Planktonic density and dispersion of larval sea lice (Lepeophtheirus salmonis) (Copepoda: Caligidae) and its relationship to infection dynamics and sea cage site location in the lower Bay of Fundy. Report to the Department of Fisheries and Oceans Canada, St. Andrews, NB, 17 p. Hogans, W.E. and Trudeau, D.J. 1989a. Caligus elongatus (Copepoda: Caligoida) from Atlantic salmon (Salmo salar) cultured in marine waters of the lower Bay of Fundy. Canadian Journal of Zoology 67: 1080–1082. Hogans, W.E. and Trudeau, D.J. 1989b. Preliminary studies on the biology of sea lice, Caligus elongatus, Caligus curtus and Lepeophtheirus salmonis (Copepoda: Caligoida) parasitic on cage-cultured salmonids in the lower Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Sciences 1715: 14 p. Huntsman, A.G. 1931a. The Maritime salmon of Canada. Bulletin of the Biological Board of Canada 21: 99 p. Huntsman, A.G. 1931b. Fundy survey —the salmon fishery. Report of the Atlantic Biological Station for 1931 (Biological Board of Canada, Toronto, ON), Appendix 45, 2 p. Huntsman, A.G. 1936. Return of salmon from the sea. Bulletin of the Biological Board of Canada 51: 20 p. Jackson, D. and Minchin, D. 1992. Aspects of the reproductive output of two caligid copepod species parasitic on cultivated salmon. Invertebrate Reproduction and Development 22: 87–90. Jackson, D. and Minchin, D. 1993. Lice infestations of farmed salmon in Ireland. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 188–201. Ellis Horwood, New York. Jessop, B.M. 1976. Distribution and timing of tag recoveries from native and nonnative Atlantic salmon (Salmo salar) released into Big Salmon River, New Brunswick. Journal of the Fisheries Research Board of Canada 33: 829–833. Johnson, S.C. 1998. Crustacean parasites. In: Diseases of Seawater Netpen-reared Salmonid Fishes (eds M.L. Kent and T.T. Poppe), pp. 80–90. Fisheries and Oceans Canada, Pacific Biological Station, Nanaimo, BC.

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Jones, R.A., Anderson, L., Flanagan, J.J., and Goff, T. 2006. Assessments of Atlantic salmon stocks in southern and western New Brunswick (SFA 23), an update to 2005. Fisheries and Oceans Canada. Canadian Scientific Advisory Secretariat Research Document 2006/025: 82 pp. Kabata, Z. 1979. Parasitic Copepoda of British Fishes. The Ray Society, London, UK, 468 p. Krkoˇsek, M., Lewis, M.A., and Volpe, J.P. 2005. Transmission dynamics of parasitic sea lice from farm to wild salmon. Proceedings of the Royal Society B 272: 689–696. Krkoˇsek, M., Lewis, M.A., Volpe, J.P., and Morton, A. 2006. Fish farms and sea lice infestations of wild juvenile salmon in the Broughton Archipelago—a rebuttal to Brooks (2005). Reviews in Fisheries Science 14: 1–11. Lacroix, G.L. 2008. Influence of origin on migration and survival of Atlantic salmon (Salmo salar) in the Bay of Fundy, Canada. Canadian Journal of Fisheries and Aquatic Sciences 65: 2063–2079. Lacroix, G.L. and Knox, D. 2005. Distribution of Atlantic salmon (Salmo salar) postsmolts of different origins in the Bay of Fundy and Gulf of Maine and evaluation of factors affecting migration, growth, and survival. Canadian Journal of Fisheries and Aquatic Sciences 62: 1363–1376. Lacroix, G.L., McCurdy, P., and Knox, D. 2004. Migration of Atlantic salmon postsmolts in relation to habitat use in a coastal system. Transactions of the American Fisheries Society 133: 1455–1471. L’Aventure, J. 1987. The case history of an Atlantic salmon farm. In: Atlantic Canada Aquaculture Workshop—Proceedings, Volume II (Salmonids) (ed J.F. Roache), pp. 28–34. Canada Department of Fisheries and Oceans, Atlantic Fisheries Technology Program (AFTP), General Education Series. No. 5. Lees, F., Baillie, M., Gettinby, G., and Revie, C.W. 2008. Factors associated with changing efficacy of emamectin benzoate against infestations of Lepeophtheirus salmonis on Scottish salmon farms. Journal of Fish Diseases 31: 947–951. Macdonald, J.S., Dadswell, M.J., Appy, R.G., Melvin, G.D., and Methven, D.A. 1984. Fishes, fish assemblages, and their seasonal movements in the lower Bay of Fundy and Passamaquoddy Bay, Canada. Fisheries Bulletin 82: 121–139. MacPhee, D. and Moore, M. 2007. A retrospective study of sea lice dynamics and treatments on aquaculture sites in Passamaquoddy Bay, New Brunswick in 2006. Report for the New Brunswick Department of Agriculture and Aquaculture, St. George, NB, 20 p. Martin, J.D. 1984. Atlantic salmon and alewife passage through a pool and weir fishway on the Magaguadavic River, New Brunswick, during 1983. Canadian Manuscript Report of Fisheries and Aquatic Sciences 1776: 11 p. Martin, J.L., LeGresley, M.M., Strain, P.M., and Clement, P. 1999. Phytoplankton monitoring in the southwest Bay of Fundy during 1993–96. Canadian Technical Report of Fisheries and Aquatic Sciences 2265: 132 p. May, A.W. and Lear, W.H. 1971. Digest of Canadian Atlantic salmon catch statistics. Fisheries Research Board of Canada Technical Report 270: 106 p. McGeachy, S.M. and Moore, M.J. 2003. Infectious salmon anemia in New Brunswick: an historical perspective and update on control and management practices (1997–2002). In: International Response to Infectious Salmon Anemia: Prevention, Control, and Eradication: Proceedings of a Symposium; September 3–4, 2002; New Orleans, LA. Technical coordinators: O. Miller. and R.C. Cipriano. Technical Bulletin 1902. U.S. Department of Agriculture, Animal and Plant Health Inspection Service; U.S. Department of the Interior, U.S. Geological Survey; U.S. Department of Commerce, National Marine Fisheries Service; Washington, DC, pp. 145–153. Murray, A.G. and Gillibrand, P.A. 2006. Modelling salmon lice dispersal in Loch Torridon, Scotland. Marine Pollution Bulletin 53: 128–135. NBDAFA (New Brunswick Department of Agriculture, Fisheries and Aquaculture). 2000. Bay

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of Fundy marine aquaculture site allocation policy. New Brunswick Department of Agriculture, Fisheries and Aquaculture, Fredericton, NB, 22 p. Nylund, A., Wallace, C., and Hovland, T. 1993. The possible role of Lepeophtheirus salmonis (Krøyer) in the transmission of infectious salmon anaemia. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 367–373. Ellis Horwood, New York. O’Halloran, J. and Hogans, W.E. 1996. First use in North America of azamethiphos to treat Atlantic salmon for sea lice infestation: procedures and efficacy. Canadian Veterinary Journal 37: 610–611. Page, F.H., Chang, B.D., Losier, R.J., Greenberg, D.A., Chaffey, J.D., and McCurdy, E.P. 2005. Water circulation and management of infectious salmon anemia in the salmon aquaculture industry of southern Grand Manan Island, Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Sciences 2595: 78 p. Page, F.H., Chang, B., Losier, R., and McCurdy, P. 2009. Water currents, drifter trajectories, and the estimated potential for organic particles released from a proposed salmon farm operation in Little Musquash Cove, southern New Brunswick to enter the Musquash Marine Protected Area. Fisheries and Oceans Canada. Canadian Science Advisory Secretariat Research Document 2009/003: 41 p. Penston, M.J. and Davies, I.M. 2009. An assessment of salmon farms and wild salmonids as sources of Lepeophtheirus salmonis (Krøyer) copepodids in the water column in Loch Torridon, Scotland. Journal of Fish Diseases 32: 75–88. Penston, M.J., Millar, C.P., Zuur, A., and Davies, I.M. 2008. Spatial and temporal distribution of Lepeophtheirus salmonis (Krøyer) larvae in a sea loch containing Atlantic salmon, Salmo salar L., farms on the north-west coast of Scotland. Journal of Fish Diseases 31: 361–371. Perley, M.H. 1852. Reports on the Sea and River Fisheries of New Brunswick, 2nd ed. Queen’s Printer, Fredericton, NB, 294 p. Peterson, R.H., Page, F., Steeves, G.D., Wildish, D.J., Harmon, P., and Losier, R. 2001. A survey of 20 Atlantic salmon farms in the Bay of Fundy: influence of environmental and husbandry variables on performance. Canadian Technical Report of Fisheries and Aquatic Sciences 2337: 117 p. Pike, A.W. and Wadsworth, S.L. 1999. Sea lice on salmonids: their biology and control. Advances in Parasitology 44: 233–337. Revie, C.W., Gettinby, G., Treasurer, J.W., and Wallace, C. 2003. Identifying epidemiological factors affecting sea lice Lepeophtheirus salmonis abundance on Scottish salmon farms using general linear models. Diseases of Aquatic Organisms 57: 85–95. Ritchie, G. 1997. The host transfer ability of Lepeophtheirus salmonis (Copepoda: Caligidae) from farmed Atlantic salmon, Salmo salar L. Journal of Fish Diseases 20: 153–157. Ritchie, G., Mordue (Luntz), A.J., Pike, A.W., and Rae, G.H. 1993. The reproductive output of Lepeophtheirus salmonis adult females in relation to seasonal variability of temperature and photoperiod. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 153–165. Ellis Horwood, New York. Saksida, S., Karreman, G.A., Constantine, J., and Donald, A. 2007. Differences in Lepeophtheirus salmonis abundance levels on Atlantic salmon farms in the Broughton Archipelago, British Columbia, Canada. Journal of Fish Diseases 30: 357–366. Statistics Canada. 2009. Aquaculture Statistics 2008. Catalogue no. 23–222-X. Statistics Canada, Ottawa, ON, 37 p. Stuart, R. 1990. Sea lice, a maritime perspective. Bulletin of the Aquaculture Association of Canada 90: 18–24. Templeman, W. 1967a. Atlantic salmon from the Labrador Sea and off West Greenland, taken during A.T. Cameron cruise, July-August 1965. International Commission on Northwest Atlantic Fisheries Research Bulletin 4: 5–40. Templeman, W. 1967b. Distribution and characteristics of Atlantic salmon over oceanic depths and on the bank and shelf slope areas off Newfoundland, March-May, 1966. International

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Commission on Northwest Atlantic Fisheries Research Document 67–54(Series No. 1856): 39 p. Thompson, K.R., Dowd, M., Shen, Y., and Greenberg, D.A. 2002. Probabilistic characterization of tidal mixing in a coastal embayment: a Markov Chain approach. Continental Shelf Research 22: 1603–1614. Tully, O. 1989. The succession of generations and growth of the caligid copepod Caligus elongatus and Lepeophtheirus salmonis parasitising farmed Atlantic salmon smolts (Salmo salar L.). Journal of the Marine Biological Association United Kingdom 69: 279–287. Tully, O. 1992. Predicting infestation parameters and impacts of caligid copepods in wild and cultured fish populations. Invertebrate Reproduction and Development 22: 91–102. Tully, O. and Whelan, K.F. 1993. Production of nauplii of Lepeophtheirus salmonis (Krøyer) (Copepoda: Caligidae) from farmed and wild salmon and its relation to the infestation of wild sea trout (Salmo trutta L.) off the west coast of Ireland in 1991. Fisheries Research 17: 187–200. Tully, O., Poole, W.R., Whelan, K.F., and Merigoux, S. 1993. Parameters and possible causes of epizootics of Lepeophtheirus salmonis (Krøyer) infesting sea trout (Salmo trutta L.) off the west coast of Ireland. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 202–213. Ellis Horwood, New York. Westcott, J.D., Hammell, K.L., and Burka, J.F. 2004. Sea lice treatments, management practices and sea lice sampling methods on Atlantic salmon farms in the Bay of Fundy, New Brunswick, Canada. Aquaculture Research 35: 784–792. White, H.C. 1940. “ Sea lice” (Lepeophtheirus) and death of salmon. Journal of the Fisheries Research Board of Canada 5: 172–175. White, H.C. 1942. Life history of Lepeophtheirus salmonis. Journal of the Fisheries Research Board of Canada 6: 24–29. Wootten, R. 1985. Experience of sea lice infestation in Scottish salmon farms. ICES CM 1985/F: 7/Ref.M. Wootten, R., Smith, J.W., and Needham, E.A. 1977. Studies on the salmon louse, Lepeophtheirus. Bulletin—Office international ´epizooties 87: 521–522. Wootten, R., Smith, J.W., and Needham, E.A. 1982. Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids and their treatment. Proceedings of the Royal Society Edinburgh 81B: 185–197.

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Chapter 4

Modeling Sea Lice Production and Concentrations in the Broughton Archipelago, British Columbia Dario J. Stucchi, Ming Guo, Michael G.G. Foreman, Piotr Czajko, Moira Galbraith, David L. Mackas, and Philip A. Gillibrand

Introduction The region of central British Columbia referred to as the Broughton Archipelago is located off the mainland coast and to the east of Queen Charlotte Strait (Figure 4.1). The waters of the Broughton Archipelago and adjoining fjords and watersheds of the region support the production of all native species of Pacific salmon (Oncorhynchus spp.), except for sockeye (Morton and Williams 2003). The Broughton Archipelago is also a major Atlantic salmon farming area. In recent years, reports (Morton et al. 2004) of high infestation levels of sea lice on outmigrating juvenile pink (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) in the Broughton Archipelago in 2001 together with the large decline in pink salmon returns in 2002 (Pacific Fisheries Research Conservation Council 2002) have generated considerable public debate, media attention, and research activity. The controversy is rooted in the conflicting views of the causative links between salmon farms as reservoirs of sea lice, the increased infestation levels on the juvenile salmon, and variable pink salmon abundance in the Broughton region. Several studies have investigated the interactions between farmed and juvenile wild salmon with regard to sea lice (Morton and Williams 2003; Morton et al. 2004; Krkoˇsek et al. 2005; Brooks 2005; Brooks and Stucchi 2006), and more recent studies (Krkoˇsek et al. 2007, 2008; Brooks and Jones 2008; Riddell et al. 2008) addressed the sustainability of pink and chum populations in the region and surrounding regions. Monitoring programs were initiated in 2003 to determine the distribution of juvenile Pacific salmon and their sea lice loads in the Broughton and to document the year-to-year variations in sea lice abundance (Jones and Nemec 2004; Jones and Hargreaves 2007, 2009). The physical oceanography (circulation, temperature, and salinity conditions) of the Broughton Archipelago and surrounding region plays a contributing role in the life history and transport of sea lice and their hosts. Our description of the physical environment and understanding of the oceanographic processes have improved Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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substantially as we have expanded our observational database and developed circulation models for the region (Foreman et al. 2006). Understanding the biology of the salmon louse Lepeophtheirus salmonis and the environmental factors affecting its life history have also improved in recent years (Heuch et al. 2000; Stien et al. 2005; Bricknell et al. 2006). The combination of improved numerical circulation modeling methods and advances in the understanding of the biology of sea lice have stimulated the application of coupled physical and biological models (Asplin et al. 2004; Murray and Gillibrand 2006; Gillibrand and Willis 2007; Amundrud and Murray 2009; see Chapters 1 and 2 contributed by Asplin et al. and Murray et al., respectively) to simulate the transport and dispersal of sea lice larvae in coastal waters. In this chapter, we describe and use physical and biological models to predict the water column concentrations of the planktonic larval stages of L. salmonis and to estimate the production of sea lice eggs from salmon farms in the region. We compare model results with observations to identify areas of agreement and areas that require further study or improvements. We identify and discuss limitations of the models that arise from assumptions, initial conditions, parameter settings, and from our understanding of the relevant physical and biological processes. Our goal is to develop and evaluate credible models of the sea lice interactions between farmed and wild salmon and to describe the limitations and inaccuracies in these models. Predictions from such models could lead to a better understanding of the temporal and spatial distribution of the infective pressure from sea lice of farm origins. The model predictions could be used to manage the salmon farms of the Broughton Archipelago by identifying the zones and time periods where sea lice on farms should be reduced.

Numerical Circulation Model The Finite Volume Coastal Ocean Model (FVCOM) developed by Chen et al. (2003, 2006) was used to model the three-dimensional circulation, the salinity, and temperature fields in the Broughton Archipelago and adjacent fjords and channels we have used. A more complete description of the Finite Volume Coastal Ocean Model, its application to the Broughton Archipelago and comparisons of its results with observations are detailed in Foreman et al. (2009). The geographic area modeled is essentially the same as that used in Foreman et al. (2006) from the open boundary at the northern end of Queen Charlotte Strait to the southern boundary in Johnstone Strait (Figure 4.1). The model domain is represented by an irregular triangular grid consisting of 42,682 nodes and 74,774 triangles. The triangle sides vary in length from approximately 2.3 km in Queen Charlotte Strait to less than 50 m in some of the narrow passages. The variable grid element size allows a better representation of the complicated coastline and bathymetry in the Broughton Archipelago than the uniform rectangles that are often required by other numerical model methods. The grid was constructed with an updated version of the software package TRIGRID (Henry and Walters 1993). A σ -coordinate system having 21 layers represented the vertical dimension. The interlayer spacing was variable, with the highest resolution near the surface and bottom. Model bathymetry and coastline were obtained from Canadian Hydrographic Service digital charts and from some recent multibeam survey data. Water depths in the region range from 0 to 520 m. However, we have specified a minimum depth of 3 m to eliminate the need to create “mud flats” and extensive intertidal areas and thus

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reduced model run times. Given the generally steep sided topography of the region, the small intertidal areas are not expected to have a significant effect on the overall circulation dynamics. To avoid “hydrostatic inconsistency” associated with a σ -coordinate system, model bathymetry was smoothed with a volume preserving technique (Foreman et al. 2006). Insufficient bathymetric smoothing produces noisy currents and exaggerated vertical mixing of temperature and salinity in areas of steep topography. Model bathymetry was smoothed such that within each triangle h/h < 0.3, where h is the depth range and h the average depth. Based on tests covering a range of settings for the smoothing parameter, the particular choice of 0.3 resulted in relatively accurate representations of bathymetry and inhibited excessive mixing.

Tidal Forcing Tidal currents account for the majority of the energy in the currents measured in the region (Foreman et al. 2006). To represent the tidal forcing and ensure that nonlinear interactions would be approximated, six tidal constituents (M2 , S2, N2 , K1 , P1 , and O1 ) were used to force our application of FVCOM in the Broughton Archipelago. At Alert Bay, these six constituents account for 84% of the tidal elevation change. Tidal elevations approximated from tidal constituents determined from a combination of tide gauge records and the North Pacific model of Foreman et al. (2000) were specified along the open boundaries in Queen Charlotte Strait and Johnstone Strait. Boundary conditions for the tidal and subtidal currents are zero flow normal to the coast, along with a free slip condition that restricts the currents to be tangential along the coast.

Freshwater The large freshwater discharge into the region drives a conspicuous estuarine circulation and influences the salinities throughout the region (Thomson 1981; Foreman et al. 2006). Knight Inlet, in particular, has been the subject of many studies (Pickard and Rogers 1959; Freeland and Farmer 1980; Farmer and Freeland 1983; Baker and Pond 1995) on the influence of freshwater discharge on the circulation, mixing, and water property variations. To accurately model the estuarine circulation we have forced the Finite Volume Coastal Ocean Model of the Broughton region with freshwater discharge observations (www.wsc.ec.gc.ca/products) from the six major rivers in the region, namely (1) the Klinaklini, (2) Kingcome, (3) Wakeman, (4) Salmon, (5) Nimpkish, and (6) Tsitika Rivers (Figure 4.1). Discharges from several other smaller yet significant rivers (Glendale, Kakweiken, and Ahta Rivers) have been estimated by using the discharge data from the gauged rivers but scaled by relative watershed areas. The discharge data from the gauged rivers used to force the model are shown in Figure 4.2.

Winds Winds also influence the surface circulation in fjords, and Baker and Pond (1995) have shown that in Knight Inlet the winds were the main factor driving surface

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Figure 4.2. Discharge from gauged rivers entering the model domain from July 2007 to July 2008. (See also color plate section.)

layer flow. They demonstrated with short-term wind and current measurements (36 day record in March–April 1988 and 37 day record in June–July 1989) taken near the junction of Tribune Channel and Knight Inlet, that up-inlet wind events reversed the estuarine seaward surface flow for 1 or 2 days at a time. In previous models of the region, Foreman et al. (2006) did not include wind forcing because of the scarcity of long-term local wind measurements. The only routinely monitored winds in the region are from the Port Hardy airport, which is about 80 km to the west of the Broughton Archipelago. To rectify this lack of wind observations in the Broughton Archipelago and Knight Inlet, a network of nine, shore-based Davis Instruments’ weather stations was installed (Figure 4.3) in May 2007 and operated until the fall of 2008. To force the circulation model with winds it was necessary to interpolate/extrapolate the observed winds to all regions of the model such that the topographic steering by the steep sided mountainous terrain was taken into account. An assimilation technique based on Bennett’s (1992, 2002) representer approach was used. Representers for each wind velocity component at each of the ten observational sites were computed and a least squares best fit to all available wind observations determined the wind field throughout the model domain. Further details of this technique are described in Foreman et al. (2009).

Climatology The climatology (January to March) of all temperature and salinity profiles obtained from 1955 to 2008 was used to specify the initial conditions for the three-dimensional temperature and salinity fields in the model domain. Questionable data were

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eliminated by discarding those lying beyond two standard deviations of the mean. The temperature and salinity fields were interpolated to the nodes of the model grid and then further smoothing was applied. In the absence of detailed time series of observations and to maintain background estuarine flow in Johnstone and Queen Charlotte Straits, the salinity and temperature conditions at the open boundaries were nudged back toward their initial conditions. January to March is generally the time of minimum river discharge and well before the onset of the summer freshet, which begins in May (Figure 4.2) (Foreman et al. 2009). During these winter months, surface salinities are generally high (∼30 psu), surface temperatures are at their lowest (6–7◦ C), and vertical stratification of the surface waters is the weakest (Brooks 2005).

Evaluation of the Model Accurate model flow, temperature, and salinity fields are needed to accurately simulate sea lice development, dispersion, and transport in complex hydrodynamic environments. Herein, we present comparisons with observations from the model run period, March 15 to April 3, 2008. Furthermore, we confine our comparisons to the near surface zone since this appears to be the habitat for the planktonic larval stages of L. salmonis and its juvenile pink salmon hosts (Heard 1991). Detailed and comprehensive comparisons of the Finite Volume Coastal Ocean Model generated currents, temperature, and salinity fields with concurrent observations and also with historic observations are presented in Foreman et al. (2009).

Currents The average surface flow between March 15 and April 3, 2008, highlights a conspicuous feature of the circulation of this region, namely the estuarine flow (Figure 4.3). The estuarine, seaward surface flow is evident throughout the model domain and especially prominent in the fjords (Knight and Kingcome Inlets) and Johnstone Strait. In Tribune Channel, the seaward flow is mostly northward and westward from Thompson Sound. The general circulation pattern in the surface flows is consistent with results from an earlier model, ELCIRC, and with observations from key passages in the region (Foreman et al. 2006). However, there is a notable difference at the junction of Knight Inlet with Tribune Channel. There does not appear to be any surface flow from Knight Inlet turning northward into Tribune Channel, and there is a southward flow in Tribune Channel from Thompson Sound that disappears before reaching Knight Inlet. This is contrary to the results from the ELCIRC model simulations. It appears that, at least for this short simulation period, some of the freshwater from the Kakweikan River has moved into the southern portion of Tribune Channel. This different circulation pattern may have implications for the transport of lice larvae at this critical junction because most of the pink salmon produced in the region, i.e., Glendale River pinks (Riddell et al. 2008), travel through this junction. Furthermore, these outmigrating salmon first encounter salmon farms at this junction when they are relatively small (< 0.7 g) in size. A summary of the instrumentation, sampling strategy, and timing of the current meter data sets is presented to provide the necessary background for the subsequent comparisons between the model and observed currents. More completed and

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Figure 4.3. Model mean surface flows as computed by a harmonic analysis over the period of March 15 to April 3, 2008. Only vectors separated by a minimum of 500 m are shown. Also shown are the locations of the weather stations (black triangles). (Adapted from Foreman et al. 2009.)

detailed information are provided in Foreman et al. (2009). Current meter moorings were deployed in Knight Inlet (KIW05, 06) and Tribune Channel (TCS05, 06) from September 2007 to September 2008 (Figure 4.4). Near the end of March 2008 the moorings were recovered and then redeployed. In Knight Inlet, KIW05 was replaced with three separate moorings (KIW06 Mid, N, and S) deployed 4 km to the east and spaced across the inlet, one centered in the channel and one each on the north and south sides. All moorings included an upward looking RD Instruments acoustic Doppler current profiler (ADCP) at a nominal depth of 40 m plus several conventional Aanderaa Instruments RCM current meters equally spaced in the water column below the ADCP. The ADCP measured the near-surface current profile in 0.5 m bins but because of side lobe reflection from the surface the shallowest useable bin was located at about 4 to 5 m below the surface. Figure 4.5 compares the observed and modeled along-channel currents at KIW05 and includes the along-channel winds from the weather station at Hoeya Head to demonstrate the influence of wind in the surface circulation. The model currents are generally coherent with the observations. The mean seaward surface estuarine flow (∼0.2 m s−1 ) and the tidal currents (∼0.2 m s−1 ) are both well-reproduced in the model. The large eastward (+ve) wind-driven current event on March 15th is reproduced by the model, but weaker eastward wind events later in the data record are not captured.

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Glacier Falls Sir Edmond Bay 50.8

Weather Station Salmon Farm Current Meter Mooring

Cliffe Bay

Tribune Channel

Burdwood

Gilford I. TCS05-06 50.7

Humphrey Rks.

Port Elizabeth

Doctor Islets

Bennett Pt.

Hoeya Head

Sargeaunt Pass. KIW06-N KIW06-Mid KIW05 KIW06-S Shewell I.

Knight Inlet

Chatham Channel

50.6 Clio Channel 126.6

126.3

126.0

Longitude (°W)

Figure 4.4. Map of the southern Broughton Archipelago showing the Knight Inlet–Tribune Channel junction. Locations of weather stations, salmon farms, and current meter moorings are shown.

Model currents ADCP currents Hoeya winds

0.6

8

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21

22

23

24

25

26

27

March 2008 Figure 4.5. Along-channel modeled and observed currents at 4.5 m for the March 15 to April 3, 2008, period from the mooring site KIW05. Also shown are the along-channel winds from Hoeya Head. (Adapted from Foreman et al. 2009.)

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Table 4.1. Observed and model mean flows, along with correlation coefficients (R) between model and observed along-channel currents, at various depths at mooring KIW05 over the period of 1:00 GMT March 15 to 14:00 GMT March 26. Depth (m)

R

Observed mean (m/s)

Model mean (m/s)

4.5 9.5 14.5 19.5 24.5 29.5 34.5 95.0 130.0

0.74 0.78 0.77 0.84 0.86 0.89 0.87 0.95 0.94

−0.18 −0.11 −0.07 −0.03 −0.01 0.01 0.02 0.02 0.02

−0.19 −0.05 0.03 0.05 0.08 0.08 0.08 0.01 −0.02

The correlation between observed and model currents at 4.5 m was 0.74, and the strength of the correlation improved (maximum of 0.95) as depth increased (Table 4.1). Agreement between observed and model mean along-channel velocity was excellent at the surface (4.5 m). However, at 9.5 m the model underpredicted the strength of the seaward flow, and it overpredicted the strength of the deeper return flow. The model did not reproduce the depth of the reversal in the estuarine flow; the model currents reversed direction at about 12 m versus the 27 m depth for the reversal in the observations. Similar analyses for the observations from the KIW06 moorings for the period from March 27 to April 3, 2008, generally show lower correlations (Table 4.2). In the top 10 m of the water column, correlations between observations and model alongchannel currents range from a low of 0.55 (10 m at KIW06-N) to a high of 0.77 (10 m for KIW06-S). The observations from the three KIW06 current meter mooring placed across the inlet reveal significant differences in the structure of the mean along-channel flow from the north to south side. On the north side of the inlet, the Table 4.2. Observed and model mean flows, along with correlation coefficients (R) between model and observed along-channel currents, versus depth at the KIW06 moorings over the period of 3:00 GMT March 27 to 24:00 GMT April 3. KIW06-North

Depth (m) 5 10 15 20 25 30

KIW06-Mid

KIW06-South

R

Observed Model mean mean (m/s) (m/s)

0.67 0.77 0.62 0.55 0.61 0.67

0.022 0.018 0.010 0.009 −0.009 −0.017

R

Observed Model mean mean (m/s) (m/s)

R

Observed Model mean mean (m/s) (m/s)

0.55 0.59 0.67 0.65 0.62

−0.076 −0.073 −0.065 −0.063 −0.061

0.68 0.60 0.48 0.48 0.63 0.79

0.053 0.048 0.030 0.012 −0.002 −0.010

−0.042 −0.043 −0.036 −0.030 −0.020

0.009 0.017 0.001 −0.009 −0.004 0.005

0.049 0.018 0.013 0.009 0.008 0.008

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mean along-channel flow is seaward (westward) down to 60 m while in the middle and southern side of the inlet the mean flow in the top 23 m is eastward or toward the head of the inlet. The model captures most of this cross-channel structure in the observed mean along-channel flow (Table 4.2). At the southern mooring, the model matches the magnitude of the mean flow at 10 and 15 m but overestimates it at 5 m. At the other two mooring sites, the model underestimates the observed mean along-channel flow. The influence of the winds at the Tribune Channel mooring (TCS06), as represented by the weather station at Shewell Island (Figure 4.4), can be seen in the ADCP currents at 5 m (Figure 4.6). In the upper 20 m of the water column there is reasonable agreement between observed and modeled currents: correlation coefficients range from 0.53 at 10 m to 0.73 at 20 m. The model tidal currents are smaller and lag the measured currents (Figure 4.6, Table 4.3). The highest correlation (0.65) between observed currents and model currents occurs at a lag of 2 hours. Harmonic analysis of the observed and modeled currents at 5 m confirms that the M2 tidal constituent is underestimated by the model, 0.17 m s−1 observed versus 0.12 m s−1 modeled. For the mean along-channel flow, the model reproduces the observed reversal in flow direction between 20 and 50 m and shows good agreement with observations at 10 and 15 m. At 5 and 20 m, the model underestimates observed mean flow by 0.03 m s−1 and 0.02 m s−1 , respectively. Overall, the model does a reasonable job representing 15 10 0.4

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29

30 March

31

1

2008

2

3

4

April

Figure 4.6. Along-channel modeled and observed currents at 5-m depth from the mooring site TCS06 for the March 28 to April 3, 2008, period. Also shown are the along-channel winds at the Shewell weather station. Positive winds and currents are directed 35◦ north of eastward. (Adapted from Foreman et al. 2009.)

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Table 4.3. Observed and model along-channel mean flows, along with correlation coefficients (R) between the model and observed currents, versus depth at mooring TCS06 over the period of 0:00 GMT March 28 to 24:00 GMT April 3. Positive flows are directed 15◦ north of eastward. Depth (m)

R

Observed mean (m/s)

Model mean (m/s)

5 10 15 20 50 85 130

0.65 0.53 0.70 0.73 0.76 0.72 0.84

0.058 0.067 0.066 0.061 −0.022 −0.066 −0.019

0.028 0.058 0.057 0.044 −0.009 −0.039 −0.059

the currents in this region, and the simulation of surface currents is much improved over earlier modeling efforts (Foreman et al. 2006) now that wind forcing has been included.

Temperature and Salinity As mentioned earlier, the model was initialized with the climatology for this time period—a climatology that included observations from 2008. Salmon farms in production routinely monitor daily profiles of temperature, salinity, and dissolved oxygen down to 15 or 20 m. Though the temperature measurements were usually accurate enough (±0.1◦ C) for comparison with our model result, only a few farms in the Broughton Archipelago used instruments capable of measuring salinity with sufficient accuracy (±0.5 psu) to permit comparison with our model results. We compared data from the Humphrey Rock site (Figure 4.4) with our model results. Apart from the March 16 to 17 surface-cooling event in the farm data, both the observed and modeled temperature data sets exhibit small temperature (<1◦ C) variations over the mid-March to early April 2008 period (Figure 4.7). Given that we have not implemented surface heat flux forcing in our application of FVCOM the agreement in overall temperature conditions indicates that our climatology provides a reasonably accurate representation of the temperature conditions. The relatively small temperature variations observed at this time of the year will have a minimal effect on the biological model that will be presented in a later section of this chapter. However, if we are to model the late spring and summer conditions when solar heating becomes important surface heat flux forcing will be required in our model. Comparison of salinity data from the farm site and modeled salinity generally show less variation both in time and depth in the observed salinities than in the model (Figure 4.8). However, salinities in both data sets are mostly in the 28 to 30 psu range with some notable exceptions. The model shows a distinct surface freshening in the later half of the model run period. The model surface salinity decreases from 28 psu to about 25 psu with little change occurring at depths below 5 m. The salinities from Humphrey Rock do not show this surface freshening. The causes for this freshening event in the model results are not clear but may be due to a combination of inaccurate winds and estimates of the Kakweiken River discharge. The surface salinity will not

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0

Figure 7.

7.30

Model

7.25

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7.20

7.20

10

Depth (m)

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7.20

7.20

15 0

6.5

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7.1

Observations

7.0

5

7.0 10

7.1

7.1 7.1 7.1 March 15

March 20

March 25

March 30

April 3

2008

Figure 4.7. Depth–time contour diagrams of modeled (top) and observed (bottom) temperature conditions from the Humphrey Rocks farm site.

have a large influence on the lice production estimates (discussed later in the chapter) as salinity effects on egg viability become significant at salinities below 25 psu. However, a slight decrease in the survival of nauplii is expected below 30 psu (discussed later in the chapter). Improved modeling of the temperature and salinity fields will require the inclusion of surface heat transfers and testing different schemes representing internal mixing. Observational data (wind and river discharge) will also be required to accurately force the model. From March to April, temperature and salinity variations are generally muted as surface heating is minimal and run-off is low; thus, the effects of these environmental variables on the production and development of L. salmonis will be minimal. The stronger influence of temperature and salinity conditions will be exerted later in the spring and summer as surface temperatures rise and the freshets significantly reduce surface salinities.

Particle Tracking To estimate the transport and dispersal of sea lice larvae, some modifications to the Finite Volume Coastal Ocean Model were required, e.g., the three-dimensional Lagrangian particle-tracking code provided in the Finite Volume Coastal Ocean Modeling suite. In addition, biological characteristics (developmental stage, mortality, and behavior) were assigned to the particles in order to better simulate the planktonic

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0

29.0

27.0 28.0

29.5 5

30.0

10

Depth (m)

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Model 15 0

29.0

29.5

29.5

29.5

5

30.0

30.0

30.0

10

Observations 15 March 15

March 20

March 25

March 30

April 3

2008

Figure 4.8. Depth–time contour diagrams of modeled (top) and observed (bottom) salinity conditions from the Humphrey Rocks farm site.

larval stages of L. salmonis. For efficient use of computer resources and time, the particles’ three-dimensional Lagrangian trajectories were computed after the Finite Volume Coastal Ocean Model runs were completed using saved model output fields (circulation, temperature, and salinity) subsampled hourly. Tracking the particle trajectories using the saved Finite Volume Coastal Ocean Model outputs permitted simulations with large numbers of particles and the efficient development and testing of a range of biological characteristics and release scenarios. The particle’s three-dimensional positions were computed by the following equation, which in addition to the advective components includes random walk components to describe horizontal and vertical diffusion of the particles:

Lt (x , y, z) = Lt−t (x , y, z) + t [U (x , y, z) + W(z)] + δ H (x , y) + δz (z), where Lt (x, y, z) is the location of a particle at time t, t is the time step of particletracking algorithm, U(x, y, z) is the velocity from circulation model, W is the vertical swimming speed of the organism, and δ H and δ z represent the horizontal and vertical random walk adjustments to the particle position. Model velocities were linearly interpolated in space and time and the particle’s advection was calculated using a 4th order Runge–Kutta algorithm.

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Similar to the procedure in Gillibrand and Willis (2007), the calculation of the horizontal random walk component is given by δ H (x , y) = γ [6 K H • t]1/2 , where the horizontal eddy diffusivity KH is set to 0.1 m2 s−1 and γ is a random number ranging between −1 and 1. From Ross and Sharples (2004) , the random walk adjustment to the vertical position zp is given by  1/2 δz (z) = γ 6 K V (z p + 0.5 K V (z p )t) + K V (z p )t, where KV is the vertical eddy diffusivity from FVCOM and K V its first derivative. The application of the above equation requires a stability criterion (Ross and Sharples 2004) for the minimum time step in the particle-tracking algorithms such that 

 1 t  min    , K  V where K V is the second derivative of the vertical eddy diffusivity. To satisfy the stability criterion above, we used a particle-tracking algorithm time step of 60 seconds. The rules governing the behavior of particles that encounter the shoreline in the model may have important implications for the transport and distribution of those particles throughout the model domain. For the present study, planktonic larval stages of L. salmonis were assumed to behave more like water particles than rigid physical objects that can become grounded at the shoreline. Following Gillibrand and Willis (2007) and Amundrud and Murray (2009), in our particle-tracking algorithm, a particle is not permitted to run into the shoreline and become stranded. Instead, if a particle is projected to hit a coastal boundary in the next time step it is held at its current position. The particle will not move from that position until the advective flow or the random walk component in a subsequent time step moves the particle away from the coastal boundary.

Sea Lice Modeling The biology of L. salmonis and its interactions with its hosts have been reviewed in the introductory chapter contributed by Hayward et al. and in several earlier reviews (Pike and Wadsworth 1999; Tully and Nolan 2002; Costelloe 2006; Boxaspen 2006). Other studies have concentrated on the parasite’s development and growth (Johnson and Albright 1991; Boxaspen and Naess 2000), its mating and reproductive capacity (Ritchie et al. 1993; Hull et al. 1998; Heuch et al. 2000; Mustafa et al. 2000), and population dynamics (Stien et al. 2005). The number of sea louse eggs produced from salmon farms in Ireland, Norway (Heuch and Mo 2001), and British Columbia, Canada (Orr 2007), has been estimated (Tully and Whelan 1993). In this section, we describe our models of (a) the production rate of sea lice eggs from salmon farms, and (b) the development and mortality of the planktonic larval stages (nauplii I and

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II and copepodid). An egg production-rate model is required to estimate the number of nauplii produced at individual farm sites. The development and mortality model estimates the fate of this parasite in its free swimming or planktonic state as it is transported by the ocean currents and affected by the temperature and salinity of the marine environment.

Farm Production of Sea Lice Eggs An important aspect of the fecundity of the female louse is that once the spermatophore has been successfully placed and attached, the louse is capable of producing multiple-egg string pairs. Ritchie et al. (1993) suggest that up to six egg string pairs may be produced by a single-mated female. In their studies of the egg production of L. salmonis, Heuch et al. (2000) reported that adult females reared at 7◦ C in the laboratory survived for up to 191 days and produced as many as 11 successive pairs of egg strings. Mustafa et al. (2000) reported that female lice produced as many as 10 successive pairs of egg strings in their laboratory trials (see also chapter the introductory chapter contributed by Hayward et al.). No similar data from field observations are available. The fecundity or rate of viable egg production, PE , of a mated adult female louse is represented by PE =

1 τS

•

ES • ρ E ,

(4.1)

where τ S is the minimum egg development period (time to hatch of the first egg on the string) or egg string replacement time, ES is the number of eggs in a pair of egg strings, and ρ E is the proportion of the eggs that hatch and develop into actively swimming nauplii. In the following section we discuss the environmental factors affecting the terms on the RHS of Equation 4.1 and the functional relationships and parameter settings used in our model. Several researchers (Heuch et al. 2000; Johnson and Albright 1991; Boxaspen and Naess 2000; Tucker et al. 2000) have conducted laboratory-rearing experiments to determine the effect of temperature on egg development time and reported significantly longer egg string development times at lower temperatures than at higher temperatures. Stien et al. (2005) summarized the data on the effect of temperature on egg development time and modeled the relationship using a simplified Belehradek function, which has the form  τS =

β1 T − 10 + β1 β2

2 ,

(4.2)

where T is temperature in degree Celsius and β 1 and β 2 are parameters. Stien et al. (2005) used a least square procedure to fit Equation 4.2 to the experimental data and computed the value of β 1 and β 2 as 41.98◦ C d−0.5 and 0.338◦ C d−0.5 , respectively. The temperature of the surface waters of the Broughton Archipelago from late winter to early summer ranges from about 7 to 10◦ C that corresponds with minimum egg

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string development times of 14.1 and 8.7 days, respectively. Because Stien et al. (2005) used minimum egg development times (i.e., time to first hatch) to compute their least squares fit, we have slightly modified the egg development time in Equation 4.1 by adding a small time increment to take into account the hatching period, i.e., the time from first to last egg hatched on an egg string pair. Johnson and Albright (1991) report that at 10◦ C the average hatching period is 37.7 hours (1.32 days). The number of eggs, ES , per pair of egg strings or sacs carried by a female louse is highly variable and dependent on several factors such as temperature, photoperiod effect, host species, farmed or wild fish, or exposure to therapeutants. On farmed Atlantic salmon, the number of eggs ranges from 214 to 758 per louse (Pike and Wadsworth 1999). Tully and Whelan (1993) reported that the number of eggs on lice collected at several farm sites in Ireland varied both spatially and temporally ranging from 251 to 715 (mean of 465). Heuch et al. (2000) found that there were no significant differences in the number of eggs between lice from wild (320 to 748) and farmed fish (152 to 462). There is little information on the number of eggs in a pair of egg strings produced by L. salmonis on farmed fish in British Columbia. However, Marine Harvest Canada has provided adult females from one farm site in the Broughton Archipelago. Several specimens were sent to the Institute of Ocean Sciences for identification and examination. All specimens were identified as adult female L. salmonis, and except for a few, all were carrying egg strings. Calculations of the number of eggs carried by individual female lice were accomplished by measuring the length of the left and right egg strings and then multiplying by the size of a representative egg in the respective eggs strings. The representative size of the eggs was determined by counting the number of eggs in short segments of the egg string. The number of eggs per string varied from 150 to 500 but the size of eggs was remarkably uniform at 0.067 mm (Figure 4.9), and the average number of eggs was 580 (σ = 192, n = 19). For calculation of louse production, we used these data to set the value of ES to a constant 580 eggs per louse. The limited and sometimes contradictory data on the factors that control the number of eggs carried by a female preclude the specification of a functional relationship for ES . Clearly, a better understanding of the factors that influence the number of eggs produced per female is required to improve the accuracy of egg production estimates for British Columbia farm sites (see the introductory chapter contributed by Hayward et al.). Not all salmon louse eggs will hatch and become actively swimming nauplii. The factors affecting the viability of the eggs are not completely understood, but it is clear that salinity is an important determinant. In experiments conducted at 10◦ C, Johnson and Albright (1991) showed that at salinities of 15 psu or lower none of the eggs developed into actively swimming nauplii. At salinities of 20, 25, and 30 psu, all or most of the eggs will hatch but on average only 20%, 51%, and 55%, respectively, of the eggs will develop into active nauplii (Johnson and Albright 1991). Above 20 psu, the percentage of active nauplii ranges from about 10 to 90%. Accordingly, we have implemented a salinity dependent egg viability coefficient, ρ E (Table 4.4) based on the experimental work of Johnson and Albright (1991). The total daily production rate of active nauplii, TN , from an operational salmon farm is given by TN = PE • C AF

•

NFish ,

(4.3)

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600

y = 14.969x R 2 = 0.9654 400

Eggs/String

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0 10

15

20

25

30

35

String length (mm)

Figure 4.9. Relationship between egg string length and number of eggs in the string from samples of gravid female sea lice (L. salmonis) collected at a salmon farm in the Broughton Archipelago. The reciprocal of the slope of the curve corresponds to size of the egg.

where PE is the rate of viable egg production (i.e., active nauplii) for an adult female louse (eggs/female-day), CAF is the average number of adult females lice per farm fish, and N Fish is the number of fish on the farm. Most if not all adult females will be inseminated and produce a series of egg strings. After mating, the time for an adult female to mature and extrude its first egg string pair was about 6 days (Hull et al. 1998). Therefore, in the egg production model, we assume that all adult females are capable of producing egg strings. Hull et al. (1998) presented observations of a cohort of sea lice on laboratory-maintained salmon in which the first adult females appeared on day 16 postinfection and that by day 25 no unmated adult females remained. In different trials of postponed mating, adult males were introduced to a population of unmated preadult II females. After 24 hours of the terminal molt, no females remained unmated (Hull et al. 1998). In rearing experiments, Heuch et al. (2000) monitored the time from infection to production of first and subsequent egg string pairs of L. salmonis females. By the time some females Table 4.4. Salinity effect on the egg viability, ρ E . Salinity (psu) 15 or less 20 25 30

ρE 0 0.2 0.51 0.55

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were producing their second pair of egg strings, all females had produced at least one pair of egg strings. In British Columbia, all salmon farm operators are required as a term and condition of their aquaculture license to have an up-to-date Fish Health Management Plan specific to each of their farm sites. In 2004, the Sea Lice Management Strategy was integrated into the farm’s Fish Health Management Plan. A component of the Sea Lice Management Strategy requires farm operators to monitor and report sea lice abundance on their farmed salmon (BCMAL 2008). For an operational salmon farm, the Fish Health Management Plan requires monthly sampling of 60 fish (20 from each of three net pens) and that the lice on the fish be enumerated and classified according to species, life stage, and gender (Saksida et al. 2007; see Chapter 8 contributed by Saksida et al.). For L. salmonis, enumerated life stages include adult females (with or without egg strings) and motiles (adult and preadult males and females). For Caligus clemensi, total motiles are counted. The counts of the chalimus life stages of both species of lice are combined. Farm companies operating in the Broughton Archipelago provided us with their monthly lice data from September 2007 to July 2008 and the corresponding fish inventory data. The temperature data from several farm sites were also provided and used to determine the egg string development time, τ S (Equation 4.2). We calculated daily egg production from all farms in the Broughton from September 2007 to July 2008 but did not include the effect of salinity on viable egg production. The salinity dependent viability factor was implemented later in the particle-tracking simulations using FVCOM salinities. The temporal pattern of total egg production from all farms in the Broughton shows (Figure 4.10) high production rates in the fall and winter followed by a rapid 5.0

4.0

Eggs × 109/month

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3.0

2.0

1.0

0.0 Sep

Oct

Nov

2007

Dec

Jan

Feb

Mar

Apr

May

Jun

Jul

2008

Figure 4.10. Total monthly L. salmonis egg production from all active salmon farms in the Broughton Archipelago. Effects of salinity on viability of eggs have not been included in these estimates.

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decline from February to April and then generally low levels into the summer of 2008. The rapid decline in lice production from February to April 2008 resulted from the coordinated actions of the farm companies to either fallow or treat their R , so that lice levels would be low during the juvenile salmon salmon with SLICE outmigration period. Individual farm sites deviate from this overall pattern depending R had been applied. upon production schedule and when whether SLICE

Planktonic Larval Development, Mortality, and Behavior The temperature dependence of the development times of the naupliar stages I and II has been investigated by several researchers (Heuch et al. 2000; Johnson and Albright 1991; Boxaspen and Naess 2000; Tucker et al. 2000; see the introductory chapter contributed by Hayward et al.). Stien et al. (2005) then modeled the relationship between the naupliar development times τ (T) and temperature using a simplified Belehradek function: 

β1 τ (T) = T − 10 + β1 β2

2 .

(4.4)

Values of β 1 and β 2 are 24.79◦ C d−0.5 and 0.525◦ C d−0.5 , respectively, for the least squares fit to minimum development times from egg hatching to the copepodid stage. At temperatures of 7 and 10◦ C, the periods from egg hatching to molting of a nauplius into a copepodid are 6.1 and 3.6 days, respectively. It is noteworthy that the developmental data for the preinfective stages of L. salmonis of Pacific origin (Johnson and Albright 1991) fit well with those data for L. salmonis of Atlantic origin (see Figure 3 in Stien et al. 2005). Copepod survival from egg to copepodid has been estimated from laboratory studies. Data were provided on the number of active copepodids resulting from rearing at 10◦ C and ∼30 psu of eggs strings collected from both wild salmon and farmed salmon. On average, about 9% of the eggs produced active copepodids and this ranged widely from 2 to 19% (S. Jones, personal communication). We model the time rate of change in abundance of a cohort of nauplii Npi (t) using a first order rate function: d Npi (t) = μ pi Npi (t), dt

(4.5)

where the mortality coefficient μpi and t is the time from hatching. The solution to the above equation is the exponential decay function: Npi (t) = Npi (0) exp(−μ pi t),

(4.6)

where Npi (0) is the abundance of the active nauplii at time of hatching (t = 0) and can be restated in terms of the number of viable eggs as ES ·ρ E. Averaging the survival data of Johnson and Albright (1991) and those collected by S. Jones (personal communication) yields a value of 18% for the proportion of eggs that that become active copepodids in full strength seawater (∼30 psu) at 10◦ C. Using

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Equation 4.6 together with the naupliar development time of 3.6 days, as given by Equation 4.4, yields a mortality coefficient μpi of 0.31 d−1 for the preinfective naupliar stages. At a salinity of 25 psu only 0.9% of the eggs developed to the copepodid stage (Johnson and Albright 1991), yielding a mortality coefficient of 1.11 d−1 . The dependence of the mortality coefficient on salinity in the range from 25 to 30 psu is calculated from linear interpolation between 30 and 25 psu and expressed by μ pi (S) = 0.16 • S − 5.11.

(4.7)

At salinities higher than 30 psu, the mortality coefficient was held constant at 0.31 d−1 . Although specific data on the survival of nauplii at salinities lower than 20 psu are lacking, the experiments of Johnson and Albright (1991) suggest that survival is severely compromised. Consequently, we extrapolated to salinities lower than 25 psu using Equation 4.7 as this resulted in very low survival rates for the naupliar stages (Figure 4.11). At 30 psu, our salinity-dependent mortality coefficient is about three times larger than that used by Gillibrand and Willis (2007) and about two times larger that calculated by Stien et al. (2005). The value used by Gillibrand and Willis (2007) was based on mortality rates typical for copepods in general whereas the value calculated by Stien et al. (2005) used the Johnson and Albright (1991) data. In our calculation, the inclusion of the S. Jones (personal communication) data produced an even higher mortality rate at 30 psu. In contrast, at salinities lower than 28 psu, the functional 1.00

10 ° C

7° C 0.5

0.75

0.4

Gillibrand and Willis (2007) = 0.1 d -1

= 0.32 d-1

0.3

0.50

S = 25 psu = 1.11 d-1

0.2

Proportion of total eggs

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0.00 0

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0.0 13

Time from hatching (days) Figure 4.11. Mortality curves for nauplii and copepodids used in our particle-tracking simulations. Also shown are the mortality curves from Gillibrand and Willis (2007) for S > 30 psu. Solid curves represent the naupliar stage and dashed curves the copepodid stage.

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relationship used by Gillibrand and Willis (2007) generally produces much larger mortality coefficients. For the age-independent natural mortality coefficient of copepodids, we used the Stien et al. (2005) value of 0.22 d−1 , which was based on mean survival time in rearing experiments conducted at 30 psu by Johnson and Albright (1991). Johnson and Albright (1991) found optimal survival of copepodids at 25 psu, while Bricknell et al. (2006) found reduced survival at salinities lower than 29 psu. Given the ambiguous experimental results we have not implemented a salinity dependent mortality coefficient for the infective stage. Instead, we have adopted a constant mortality of 0.22 d−1 . At salinities lower than 20 psu, survival of the copepodids is compromised, but the parasite appears to have developed a range of behaviors to avoid these suboptimal salinity environments: Bricknell et al. (2006) observed active swimming away from extremely low salinity waters (< 12 psu) to passive sinking to avoid higher but still suboptimal salinities. The infectivity of the copepodid or its ability to find, settle, and attach successfully to the host is also a relevant characteristic of the model. The planktonic larvae of L. salmonis are nonfeeding, surviving on the finite energy reserves of their yolk sac. As the copepodid ages, its energy reserves become depleted (Tucker et al. 2000). Consequently, a free-swimming copepodid may survive for many days but its ability to infect a host will likely be reduced over time. Tucker et al. (2000) found that the energy reserves declined sharply in copepodids 5 and 7 days postmolt when compared to those aged 1 and 2 days. Furthermore, successful attachment to hosts was significantly reduced in copepodids aged 7 days when compared to copepodids 1 and 3 days postmolt (Tucker et al. 2000). In experiments where L. salmonis eggs were reared to the copepodid stage for infection trials, copepodids aged 7 days or more have not been used as their ability to infect the host is significantly diminished (C. Pert personal communication). Consequently, we have implemented a finite lifetime of 7 days for the copepodids to reflect the diminished ability to infect a host. After 7 days postmolt we no longer track particles representing copepodids in our simulations.

Diel Vertical Migration The planktonic larval stages of L. salmonis are reported from laboratory studies to perform diel vertical migrations (Pike and Wadsworth 1999; see the introductory chapter contributed by Hayward et al.). In the real ocean environment, the depth range of diel vertical migration is unknown. Given that the planktonic copepodid’s survival is limited by its energy reserves and that its host location behavior is energetically demanding, Brooks (2005) suggested that the depth range of the diel migrations may be limited and that the planktonic copepodid will occupy the near surface waters. Where there have been extensive sampling programs (Costelloe et al. 1998 in Ireland and McKibben and Hay 2004 in Scotland) planktonic sea lice larvae were captured near the surface. Plankton sampling in the Broughton Archipelago also indicated larvae occurred mostly in the surface layer (M. Galbraith, personal communication). Recent studies carried out in the Broughton Archipelago with a 10 m vertical column suspended in the ocean showed that the copepodids did not exhibit any depth preference during the day- or nighttime (A. Lewis, personal communication).

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We have ascribed two behavioral patterns to the copepodids. In one pattern, the copepodids perform positively phototactic diel vertical migration with the maximum vertical extent of the migration set to a depth of 10 m. The swimming speed set for this migration follows Gillibrand and Willis (2007), 5.5 m h−1 (upward) for daylight hours and −5.5 m h−1 (downward) for nighttime hours. In addition, the copepodids are constrained to remain within the top 10 m of the water column. Also, there is a salinity avoidance behavior that overrides the diel vertical migration such that if the copepodids encounter salinities less than 20 psu they will actively swim away (downward) until more suitable salinities are encountered. In the second behavioral pattern, copepodids do not perform diel vertical migration but maintain their low salinity avoidance behavior described above.

Maturation As the nauplii are advected and dispersed through the marine environment, they will experience a temperature and salinity field that varies in time and space. The development of the nauplii is temperature dependent and to account for the maturation of the nauplii in a varying temperature field, we introduce a new variable, the maturation level M. The maturation level M is calculated in Equation 8 and assigned to the particle being tracked Mt = Mt−1 + t/τ (T),

(4.8)

where τ (T) is the temperature development time described earlier. At t = 0, when the egg hatches M = 0, and when M = 1, the nauplius molts into a copepodid.

Simulations We combined the three-dimensional Lagrangian particle-tracking techniques with the biological models of egg production and planktonic larval stage survival to estimate the spatial and temporal concentrations of the L. salmonis copepodid in the surface waters of the Broughton Archipelago. The particle-tracking simulations used the Finite Volume Coastal Ocean Model circulation to transport and disperse the lice larvae, and the Finite Volume Coastal Ocean Model temperature and salinity fields were used to calculate egg production and to control the development and behavior of the planktonic larval stages. The model of lice egg production from the farms was used to set the strength of the source or assign weights to the particles in the simulations. The time period for our simulation was from March 15 to April 3, 2008, coincident with the early outmigration period for juvenile pink (Beamish et al. 2006) and chum salmon (Heard 1991). The juvenile pink and chum are very small (< 0.7 g) at this time of year and most vulnerable to lice infections (Jones and Hargreaves 2009). This time period also coincided with the start of the Department of Fisheries and Oceans’ (DFO) juvenile Pacific salmon monitoring program, which sampled juvenile salmon and other fish species for lice loads (Jones and Nemec 2004; Jones and Hargreaves 2009). Plankton sampling for the free-swimming larval stages of sea lice was also carried out in this time period. The plankton and wild fish surveys provided field data

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Table 4.5. Daily egg production, farm inventory of fish, and number of adult female L. salmonis per fish for March 2008 for all the active farm sites in the Broughton Archipelago. Interpolated/extrapolated values are in italics.

Farm Arrow Glacier Humphrey Larsen Midsummer Potts B. Sargeaunt Wicklow Burdwood Cecil Cliffe Bay Cypress Maude Sir Ed. Bay Bennett Total Daily Total Monthly

Adult females/fish

Farm inventory

Daily egg production

0.00 0.08 0.08 0.03 0.05 3.10 0.03 0.93 0.32 0.3 0.1 0.08 0.08 0.25 0.27

1,344,515 614,517 679,551 1,200,929 553,271 35,800 654,949 176,236 564,703 526,869 601,667 36,883 595,970 598,795 153,045

0 2,010,802 2,223,604 1,571,856 1,086,237 4,357,741 857,241 6,458,744 7,021,649 6,206,411 2,362,506 108,619 1,755,102 5,878,071 1,622,552 43,542,127 1,349,805,939

Comments Treated Treated Smolts Treated Brood stock Treated Harvesting Treated

Brood stock Treated Gravid lice only

on planktonic lice concentrations and fish lice loads with which to test and evaluate our model simulations.

March 2008 Farm Production of Sea Lice Eggs We used the egg production model to estimate the daily production of eggs from all the active farms sites in the Broughton Archipelago for March 2008 (Table 4.5). A mean monthly temperature of 7.0◦ C was used on the model. The estimates in Table 4.5 do not take into account the salinity dependent viability coefficient as it was applied later in the particle-tracking simulation. In March 2008, daily production of sea lice eggs from the 14 active farms in the Broughton ranged from 0.1 × 106 to 7.0 × 106 egg d−1 (Table 4.5). Spatially, egg production was generally higher (∼6 × 106 egg d−1 ) in the central Broughton (Fife Sound–Penphrase Passage; Figure 4.1); while near the Tribune Channel–Knight Inlet junction production was generally lower (∼2 × 106 egg d−1 ). We used the daily production estimates from each farm (Table 4.5) to specify the weighting assigned to the simulated particles.

Particle-Release Locations and Schedule Simulated particles were released at the locations of the 14 active salmon farms in the Broughton. At each farm location, a rectangular box (100 m × 100 m × 10 m) represented the net cage structure of the farm, and within this box 20 randomly located

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particles were released every hour for 11 consecutive days. In total, 5,280 particles were released at each of the 14 locations. The release of particles began on March 18 and stopped on March 28, and each particle was tracked for 11 days. Each particle represents a cohort of nauplii and the number of individuals in the cohort is determined by the daily egg production of the individual farm sites. The circulation model’s salinity field is used to determine the egg viability (Table 4.4) and the farm’s daily production of active nauplii. We ran simulations with two swimming behaviors for the copepodids; one with and one without diel vertical migration (passive copepodids). Daily average concentrations or densities of the infective copepodid stage were calculated from March 25 to 30.

Results and Comparisons with Data The results of the simulations with and without diel vertical migration are presented in separate sets of daily maps (Figures 4.12 and 4.13) of copepodid concentrations in the surface layer (0 to 5 m). The highest computed concentrations are around one copepodid in 10 m3 or 0.1 m−3 , but most regions have much lower concentrations. The simulations with diel vertical migration (Figure 4.12) and without (Figure 4.13) in general do not differ from each other. Both show a 5- to 10-km wide band of copepodids at relatively high concentrations hugging the northeast shore of Queen Charlotte Strait. In both simulations concentrations in this band are comparable in magnitude and relatively high at ∼0.1 copepodids m−3 compared to most other areas in the model domain. Inside the study area, the passages surrounding Broughton Island (Fife Sound, Penphrase Passage, Sutlej Channel, and Wells Passage) also show high (10−1 to 10−2 copepodids m−3 ) concentrations in both simulations (Figures 4.12 and 4.13). Concentrations in and around the Tribune Channel–Knight Inlet junction range from nearly zero to ∼10−3 copepodids m−3 . In Knight Inlet east of the junction with Tribune Channel, both simulations produce very low concentrations of copepodids (∼10−5 m−3 ). The model including passive copepodid behavior produced generally higher concentrations throughout Tribune Channel compared with the model including active copepodid behavior. This difference is clearly illustrated by comparing the concentrations in the western and central portions of Tribune Channel on March 25. The simulation with diel vertical migration (Figure 4.12) has estimated almost zero copepodids in the central part of Tribune Channel and estimated 10−3 m−3 at the western end of the channel. In contrast, the simulation with no diel vertical migration (Figure 4.13) estimated concentrations of 10−2 m−3 or higher at the western end of Tribune Channel and concentrations ranging from 10−2 to 10−3 m−3 in the central portions of Tribune Channel. Similar differences in copepodid density were evident in the regions, namely around the Tribune Channel–Knight Inlet junction and in Kingcome Inlet. The temporal changes in the modeled concentrations showed effects of wind in the simulation with diel vertical migration. From March 25 to 28, winds in Knight Inlet were westward but switched to the east late on the 28th, with several strong easterly wind events occurring in the next few days (Figure 4.5). Higher concentrations of copepodids occurred in Knight Inlet near the junction with Tribune Channel and in the passages to the south (Clio and Chatham Channels) on March 29 and 30 than earlier in the simulation period (Figure 4.12). The wind appeared to have reversed the

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Log10 (cop. m -3) 60

Y distance (km)

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-1

March 26

-2 40

-3 20

0

-4 -5 20

80 40 60 X distance (km)

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March 27

March 28

March 29

March 30

Figure 4.12. Maps showing daily average surface concentrations of copepodids from 25 to 30 March, 2008. Copepodids underwent diel vertical migration in this simulation. Location of the farms producing lice are shown by the white circles and the relative strength of farm lice source is represented by the diameter of the white circles. (See also color plate section.)

seaward surface flow and moved water with higher copepodid concentrations eastward in Knight Inlet, and southward into Clio and Chatham Channels. The current meter observations from KIW06-Mid and KIW06-S confirmed the reversal in surface flow starting on March 29, 2008.

Comparison with Plankton Net Tows From March 25 to 29, 2008, 28 plankton net tows were carried out at different locations in Knight Inlet and Tribune Channel and at one location in Fife Sound (Figure 4.14).

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March 25

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-2 40 -3 20 -4 0

-5 20

40 60 X distance (km)

80

100

March 27

March 28

March 29

March 30

Figure 4.13. Maps showing daily average surface concentrations of copepodids from March 25 to 30, 2008. Copepodid behavior was passive in this simulation. Location of the farms producing lice are shown by the white circles and the relative strength of farm lice source is represented by the diameter of the white circles. (See also color plate section.)

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3

6

1

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Figure 4.14. Maps showing location of plankton tows (black diamonds) during the March 25 to 29, 2008, field survey. The number of copepodids caught in the plankton tow is shown by the white number inside the black circle. The black number next to circle indicates number of nauplii in the sample.

A plankton net (0.5 m diameter mouth, 2 m length, and 200 μ mesh size) with flow meter was towed horizontally at a depth of 1 to 2 m. The plankton net was towed very close to shore at a speed of 0.5 to 1 m s−1 against the prevailing current. The plankton net tows covered distances of several hundred meters and filtered volumes of water ranging from 8 to 90 m3 . The plankton samples were preserved and examined under a microscope at the Institute of Ocean Sciences, and the sea lice nauplii and copepodids identified and counted (Galbraith 2005). In 17 of the 28 tows, no lice were found, and in the positive tows copepodid concentrations ranged from 0.02 to 0.21 copepodids m−3 . Total volume of water filtered in the tows was 1124 m3 , and the average copepodid concentration was 0.02 copepodids m−3 . A total of 24 of planktonic larvae of L. salmonis were captured in the tows. Of these, 3 were identified as nauplii and 21 as copepodids. Eleven of the copepodids were located less than 2 km away from a salmon farm and all three nauplii were within 0.1 km of a farm. The remaining 10 copepodids were located more than 3 km away from a salmon farm (Figure 4.14). Of the 28 plankton net tows, six were located adjacent to a farm site. The highest concentration (0.2 copepodids m−3 ) and number of copepodids (6) was found in Fife Sound near the Wicklow Point salmon farm on March 29, 2008. Although the sample size of planktonic larvae was small and more limited in geographical extent, we compared our model results with the field observations of copepodid concentrations. At the location in Fife Sound with the highest observed copepodid concentration, both particle-tracking simulations (diel vertical migration and passive) predicted concentrations of ∼10−2 copepodids m−3 (Figures 4.12 and

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4.13) lower than the observed concentration of 2 × 10−1 copepodids m−3 . At other locations such as Hoeya Head, the simulated concentrations are several orders of magnitude lower than the observed concentrations of 0.1 copepodids m−3 . At many locations where very low concentrations were predicted, no copepodids were found in the plankton samples. Overall, our model predicted concentrations are lower than the observed concentrations.

Wild Fish Survey In 2008, the first survey of the DFO wild fish-monitoring program began at the end of March. The techniques used to collect the wild fish samples and analyses performed on the samples are described by Jones and Hargreaves (2007, 2009). In brief, at locations throughout the Broughton Archipelago beach and purse seines were used to capture wild fish. Subsamples of the catch of juvenile pink and chum salmon and other fish species were examined for sea lice (species, numbers, stage, and gender). Other metrics of the wild fish such as length and weight were also recorded. Almost all the juvenile pink and chum salmon collected in late March and early April 2008 were caught by beach seine in Knight Inlet (between Glendale Cove and the junction with Tribune Channel) and the southern portions of Tribune Channel. Very few juvenile pink and chum were caught in the northern and central regions of the Broughton Archipelago. No sea lice were found on any of the 342 juvenile pink salmon examined (Jones and Hargreaves 2009), and only two nonmotile L. salmonis were found on the 263 juvenile chum salmon examined. The two juvenile chum salmon each with one louse were caught in the central Broughton region near the salmon farm at Cliffe Bay. The comparison between observed infestations on wild fish and predicted copepodid concentrations is hampered by the skewed spatial distribution of the juvenile salmon, in which most fish were caught in Knight Inlet and Tribune Channel, combined with an almost complete absence of lice. However, the coincidence of very low copepodid concentrations predicted by our simulations and the very low infection levels in Knight Inlet and Thompson Sound is noteworthy. The two juvenile chum salmon with lice were netted in the central Broughton where our simulations predicted higher copepodid concentrations relative to those in Knight Inlet.

Discussion and Conclusions We have described, presented, and evaluated results from our coupled physical and biological models of the production and transport of the planktonic larvae of the sea louse L. salmonis in the Broughton Archipelago. To our knowledge, this is the first time biological models of sea lice production and life history have been coupled to a reasonably realistic model of the physical environment to predict copepodid concentrations in physically meaningful units. Our intent was to develop realistic models that could be used to predict the concentrations of the planktonic larval stages of sea lice in order to better understand the sea lice interactions between farmed and wild salmon.

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The present models of the physical environment (circulation, temperature, and salinity) in the Broughton Archipelago and surrounding region are improved from our earlier efforts (Foreman et al. 2006). We forced our physical model (Finite Volume Coastal Ocean Model) with local observations of run-off, winds, and tides, and tested the results against observed currents and temperature and salinity conditions. Although some features of the circulation and hydrography were not reproduced accurately, many important features were reproduced. In the near surface zone that is the habitat of larval sea lice and their hosts, and where wind effects are most important, the model has simulated the wind-driven circulation with reasonable accuracy. The seaward estuarine flow of the surface layer has also been predicted by the model but the vertical structure of the flow was not fully captured in some regions. The model predicted temperature and salinity fields but did not reproduce the events observed in farm monitoring data. However, both the model and observed temperature and salinity fields had a relatively small dynamic range and this inaccuracy did not have a major influence on the biological models. It will be important to accurately model the evolution of the surface temperature and salinity fields later in the season when solar heating increases, the freshet begins and the dynamic ranges become substantially larger. Our implementation of the Finite Volume Coastal Ocean Model used a free slip condition that constrained velocities in coastal triangles to be parallel to the coastline (i.e., the component normal to the coastline was zero). However, the free slip condition may permit particles to move too quickly along the shoreline and may not represent the reduced flows observed very close to shore. A no slip condition, in which velocity both parallel and normal to the coastline is zero, will be tested in future implementations of the Finite Volume Coastal Ocean Model to determine its effects on the results of the particle-tracking simulations. We have developed and presented results of a model for the production of L. salmonis eggs from salmon farms. The model is based on knowledge of the reproductive biology of L. salmonis and the environmental factors affecting its development and fecundity. An important model parameter is the number of eggs carried by a louse, and until now this information was not available for British Columbia farms. We used a setting of 580 eggs per adult female as determined from our analyses of recent samples from a farm in the Broughton collected by Marine Harvest Canada. The required farm specific data on the lice burden carried by the farm fish and the farm fish inventory were also provided by the salmon industry in the Broughton. The resulting calculations indicated high egg production in the fall (2007) and winter (2007–2008), a steep decline from February to April, and then a leveling off at low levels into July 2008. The rapid decline of egg production most likely resulted from the industry’s coordinated area production plan in which farms were either fallowed or treated along the presumed Knight Inlet–Tribune Channel–Fife Sound juvenile salmon migration corridor. For most of the outmigration period (March to June) of juvenile pink and chum salmon and in the summer when juveniles are in the area (Beamish et al. 2006) egg production from the farms was reduced by approximately 70%. Our biological model of the development and mortality of the planktonic larval stages of L. salmonis was in part based on the modeling work of Gillibrand and Willis (2007) and Amundrud and Murray (2009) and the population dynamics of Stien et al. (2005). Egg viability and natural mortality coefficients were based on published literature and on recent unpublished data from laboratory-rearing studies.

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It is recognized that a laboratory setting may not be optimal for rearing sea lice and lead to inaccurate estimates of natural mortality and large variations in the viability of these early life stages. Furthermore, in the natural environment populations of planktonic larvae would be reduced by predation and host attachment; two loss factors not present in laboratory-rearing environments. The swimming behavior of the infective stage of L. salmonis may not be wellunderstood as, contrary to the studies of Heuch et al. (1995), recent studies carried out in the Broughton Archipelago did not show diel vertical migrations (A. Lewis, personal communication). Consequently, we used two modes of swimming behavior (with and without diel vertical migration) in our simulations. The selection of 10 m as the vertical extent of the diel migration was arbitrary as there were no observations from the natural marine environment. This behavioral aspect requires further investigation. The availability of lice count and fish inventory data from salmon farms made possible the inclusion of quantitative estimates of lice production from individual farms in our particle-tracking simulations. This in turn permitted the particle-tracking simulations to compute quantitative estimates of L. salmonis copepodid concentrations in physically meaningful units, i.e., copepodids m−3 , which can be quantitatively compared to plankton sampling observations. One general feature of note in the model results was the low concentration of the predicted copepodids, usually < 10−2 copepodids m−3 . Plankton sampling for the sea lice larvae in the study area over the last several years provided observational evidence that concentrations of copepodids are low (M. Galbraith, personal communication), though not as low as predicted by our model simulations. Our simulations have mapped the spatial and temporal varying copepodid concentrations. Regions of high concentration were noted in the northeast of Queen Charlotte Strait and the passages around Broughton Island. Low concentrations were present in Knight Inlet, Tribune Channel, and western portions of Queen Charlotte Strait. Generally, simulations with passive copepodid behavior showed lower concentrations than those with diel vertical migrations. Some of this spatial variation in concentration is associated with proximity to large sources of sea lice eggs as seen in the central Broughton. Conversely, at the Tribune–Knight junction where farm lice production was minimal, lower concentrations were predicted. Comparisons between predicted and observed concentrations were limited by the small sample size and biased spatial distribution of the March observations. Nevertheless, the comparison suggests some agreement between copepodid catches and predicted concentrations, though the predicted concentrations were lower than the observed concentrations. Further evaluation of our model results with plankton sampling surveys in February and early March 2008 are planned. We provided a preliminary comparison between our simulations and wild fish monitoring data for March 2008. These comparisons are not as direct or as quantitative as with the plankton data. The locations where juvenile salmon acquire lice are not known. Furthermore, little is known about the success rate of copepodid attachment to a juvenile pink or chum salmon. Nevertheless, the coincidence of low predicted copepodid concentrations and the absence of lice on juvenile salmon warrant further study as the transmission of infective pressure to infestation levels is the process of interest. We will continue these comparisons with wild fish monitoring survey data from May and June 2008 when juvenile salmon are more prevalent, and for the 2009 outmigration period. If we can quantify and validate the correspondence between copepodid densities and infestation levels on wild fish, we can begin to implement a

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large-scale or area-wide management strategy for salmon farming in the Broughton Archipelago.

Summary Physical and biological models were used to estimate the production of sea lice (L. salmonis) eggs from salmon farms and predict the concentrations of the infective copepodid stage in the Broughton Archipelago and surrounding regions of British Columbia. To simulate the three-dimensional circulation, temperature, and salinity fields, we implemented the Finite Volume Coastal Ocean Model and forced the model with observed river runoff, local winds, and tides. We validated FVCOM with observations of the circulation and measurements of the temperature and salinity in the near-surface zone. The model of sea lice egg production used the farm-specific lice and environmental monitoring data and the farm’s inventory of fish to estimate of the daily output of eggs from all active farms in the archipelago from September 2007 to July 2008. The egg production results show a clear decline in the egg production from February to April 2008 as a result of farm management actions. A separate biological model for the development, behavior, and transport of the planktonic larval stages of the lice was implemented in the particle-tracking algorithm of FVOCM. Particle-tracking simulations for the 13 March to 3 April 2008 period used the Finite Volume Coastal Ocean Model output and farm egg production rates to map over time the concentrations of copepodids in the surface layer. Model computed copepodid concentrations were compared with concurrent plankton sampling data and lice infestation data on wild juvenile salmon. Predicted copepodid concentrations were lower than observed but spatial associations were observed. Furthermore, juvenile wild salmon carried no lice when sampled in a region where copepodid concentrations were predicted to be very low.

Acknowledgments We thank personnel from Marine Harvest Canada, Mainstream Canada, and Grieg Seafood for sharing their sea lice monitoring data and their environmental monitoring data. In particular, we are most grateful to Marine Harvest Canada for collecting specimens of gravid female lice for us to analyze and use. We also thank Drs. Simon Jones, Brent Hargreaves, and Stewart Johnson for helpful discussions, advice, and for sharing their preliminary wild fish monitoring data with us. Partial financial support for this work was provided British Columbia Pacific Salmon Forum.

References Amundrud, T.L. and Murray, A.G. 2009. Modelling sea lice dispersion under varying environmental forcing in a Scottish sea loch. Journal of Fish Diseases 32: 27–44. Asplin, L., Boxaspen, K., and Sandvik, A.D. 2004. Modelled distribution of sea lice in a Norwegian fjord. ICES CM 2004/P: 11.

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Baker, P. and Pond, S. 1995. The low-frequency residual circulation in Knight Inlet, British Columbia. Journal of Physical Oceanography 25: 747–763. Beamish, R.J., Jones, S., Neville, C-E., Sweeting, R., Karreman, G., Saksida, S., and Gordon, E. 2006. Exceptional marine survival of pink salmon that entered the marine environment in 2003 suggests that farmed Atlantic salmon and Pacific salmon can coexist successfully in a marine ecosystem on the Pacific coast of Canada. ICES Journal of Marine Science 63: 1326–1337. Bennett, A.R. 1992. Inverse Methods in Physical Oceanography. Monographs on Mechanics and Applied Mathematics. Cambridge University Press, Cambridge, 346 p. Bennett, A.R. 2002. Inverse Modeling of the Ocean and Atmosphere. Cambridge University Press, Cambridge, 234 p. Boxaspen, K. 2006. A review of the biology and genetics of sea lice. ICES Journal of Marine Science 63: 1304–1316. Boxaspen, K. and Naess, T. 2000. Development of eggs and the planktonic stages of salmon lice (Lepeophtheirus salmonis) at low temperatures. Contributions to Zoology 69: 51–55. Bricknell, I.R., Dalesman, S., O’Shea, B., Pert, C.C., and Mordue, J. 2006. The effect of environmental salinity on sea lice (Lepeophtheirus salmonis) settlement success. Diseases of Aquatic Organisms 71: 201–212. British Columbia Ministry of Agriculture and Lands (BCMAL). 2008. Fish Health Program/2007, 117 p. Brooks, K.M. 2005. The affects of water temperature, salinity and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada. Reviews in Fisheries Science 13: 177–204. Brooks, K.M. and Jones, S.R.M. 2008. Perspectives on pink salmon and sea lice: scientific evidence fails to support the extinction hypothesis. Reviews in Fisheries Science 16: 403–412. Brooks, K.M. and Stucchi, D.J. 2006. The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of the salmon louse (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada (Brooks, 2005). A response to the rebuttal of Krkoˇsek et al. (2005). Reviews in Fisheries Science 14: 13–23. Chen, C., Beardsley, R.C., and Cowles, G. 2006. An unstructured grid, finite-volume coastal ocean model (FVCOM) system. Oceanography, Special Issue on “Advances in Computational Oceanography” 19: 78–89. Chen, C., Liu, H., and Beardsley, R.C. 2003. An unstructured, finite-volume, three-dimensional, primitive equation ocean model: application to coastal ocean and estuaries. Journal of Atmospheric and Oceanic Technology 20: 159–186. Costelloe, M.J. 2006. Ecology of sea lice parasitic on farmed and wild fish. Trends in Parasitology 22: 475–483. Costelloe, M., Costelloe, J., O’Donohoe, G., Coghlan N.J., Oonk, M., and Van Der Heijden, Y. 1998. Planktonic distribution of sea lice larvae, Lepeophtheirus salmonis, in Killary Harbour, West Coast of Ireland. Journal of the Marine Biological Association of the United Kingdom 78: 853–874. Farmer, D.M. and Freeland, H.J. 1983. The Physical Oceanography of Fjords. Progress in Oceanography 12: 147–220. Foreman, M.G.G., Crawford, W.R., Cherniawsky, J.Y., Henry, R.F., and Tarbotton, M.R. 2000. A high resolution assimilating tidal model for the northeast Pacific Ocean. Journal of Geophysical Research 105(C12): 28629–28651. Foreman, M.G.G., Stucchi, D.J., Zhang, Y., and Baptista, A.M. 2006. Estuarine and tidal currents in the Broughton Archipelago. Atmosphere-Ocean 44: 47–63. Foreman, M.G.G., Czajko, P., Stucchi, D.J. and Guo, M. 2009. A finite volume model simulation for the Broughton Archipelago, Canada. Ocean Modelling 30: 29–47.

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Freeland, H.J. and Farmer, D.M. 1980. Circulation and energetics of a deep, strongly stratified inlet. Canadian Journal of Fisheries and Aquatic Sciences 37: 1398–1410. Galbraith, M.D. 2005. Identification of larval stages of Caligus clemensi and Lepeophtheirus salmonis from the Broughton Archipelago. Canadian Technical Report of Fisheries and Aquatic Sciences 2548: 21 p. Gillibrand, P.A. and Willis, K.J. 2007. Dispersal of sea louse larvae from salmon farms: modelling the influence of environmental conditions and larval behaviour. Aquatic Biology 1: 63–75. Heard, W.R. 1991. Life History of Pink Salmon (Oncorhynchus gorbuscha). In: Pacific Salmon Life Histories ( eds C. Groot and L. Margolis ), pp. 121–230. University of British Columbia Press, Vancouver. Henry, R.F. and Walters, R.A. 1993. A geometrically based, automatic generator for irregular triangular networks. Communication in Numerical Methods in Engineering 9: 555–566. Heuch, P.A. and Mo, T.A. 2001. A model of salmon louse production in Norway: effects of increasing salmon production and public management measures. Diseases of Aquatic Organisms 45: 145–152. Heuch, P.A., Parsons, A., and Boxaspen, K. 1995. Diel vertical migration: a possible hostfinding mechanism in salmon louse (Lepeoptheirus salmonis) copepodids. Canadian Journal of Fisheries and Aquatic Sciences 52: 681–689. Heuch, P.A., Nordhagen, J.R., and Schram, T.A. 2000. Egg production in the salmon louse [Lepeophtheirus salmonis (Krøyer)] in relation to origin and water temperature. Aquaculture Research 31: 805–814. Hull, M.Q., Pike, A.W., Mordue, A.J., and Rae, G.H. 1998. Patterns of pair formation and mating in an ectoparasitic caligid copepod Lepeophtheirus salmonis (Kroyer 1837): implications for its sensory and mating biology. Philosophical Transactions of the Royal Society London, Biological Sciences 353: 753–764. Johnson, S.C. and Albright, L.J. 1991. Development, growth and survival of Lepeophtheirus salmonis (Copepoda: Caligidae) under laboratory conditions. Journal of the Marine Biological Association of the United Kingdom 71: 425–436. Jones, S.R.M. and Hargreaves, N.B. 2007. The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on pink Oncorhynchus gorbuscha and chum O. keta salmon in coastal British Columbia. Journal of Parasitology 93: 1324–1331. Jones, S.R.M. and Hargreaves, N.B. 2009. Infection threshold to estimate Lepeophtheirus salmonis-associated mortality among juvenile pink salmon. Diseases of Aquatic Organisms 84: 131–137. Jones, S.R.M. and Nemec, A. 2004. Pink Salmon Action Plan: sea lice on juvenile salmon and on some non-salmonid species caught in the Broughton Archipelago in 2003. Pacific Scientific Advice Review Committee, PSARC Working Paper H2004–105: 83. Krkoˇsek, M., Lewis, M.A., and Volpe, J.P. 2005. Transmission dynamics of parasitic sea lice from farm to wild salmon. Proceedings of the Royal Society B 272: 689–696. Krkoˇsek, M., Ford, J.S., Morton, A., Lele, S., and Lewis, M.A. 2008. Sea lice and pink salmon declines: A response to Brooks and Jones (2008). Reviews in Fisheries Science 16: 413–420. Krkoˇsek, M., Ford, J.S., Morton, A., Lele, S., Myers, R.A., and Lewis, M.A. 2007. Declining wild salmon populations in relation to parasites from farm salmon. Science 328: 1772–1775. McKibben, M.A. and Hay, D.W. 2004. Distributions of planktonic sea lice larvae Lepeophtheirus salmonis in inter-tidal zone in Loch Shieldaig, Western Scotland in relation to salmon farm production cycles. Aquaculture Research 35: 742–750. Morton, A.B. and Williams, R. 2003. First report of a sea louse, Lepeoptheirus salmonis, infestation on juvenile pink salmon, Onchorynchus gorbuscha, in nearshore habitat. Canadian Field-Naturalist 117: 634–641. Morton, A.B., Routledge, R., Peet, C., and Ladwig, A. 2004. Sea lice (Lepeophtheirus salmonis) infection rates on juvenile pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta)

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salmon in the nearshore marine environment of British Columbia, Canada. Canadian Journal of Fisheries and Aquatic Sciences 61: 147–157. Murray, A.G. and Gillibrand, P.A. 2006. Modelling dispersal of larval salmon lice in Loch Torridon, Scotland. Marine Pollution Bulletin 53: 128–135. Mustafa, A., Conboy, G.A., and Burka, J.F. 2000. Lifespan and reproductive capacity of sea lice, Lepeophtheirus salmonis, under laboratory conditions. Aquaculture Association of Canada Special Publication 4: 113–114. Orr, C. 2007. Estimated sea louse egg production from Marine Harvest Canada farmed Atlantic salmon in the Broughton Archipelago, British Columbia, 2003–2004. North American Journal of Fisheries Management 27: 187–197. Pacific Fisheries Resource Conservation Council. 2002. 2002 Advisory: The protection of Broughton Archipelago pink salmon stocks. Pacific Fisheries Resource Conservation Council, Vancouver, BC, 80 p. Pickard, G.L. and Rogers, K. 1959. Current measurements in Knight Inlet, British Columbia. Journal of the Fisheries Research Board of Canada 16: 635–678. Pike, A.W. and Wadsworth, S.L. 1999. Sealice on salmonids: their biology and control. Advances in Parasitology 44: 233–337. Riddell, B.E., Beamish, R.J., Richards, L.J., and Candy, J.R. 2008. Comment on “Declining wild salmon populations in relation to parasites from farm salmon.” Science 322: 1790. Ritchie, G., Mordue, A.J., Pike, A.W., and Rae, G.H. 1993. The reproductive output of Lepeophtheirus salmonis adult females in relation to seasonal variability of temperature and photoperiod. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye ), pp. 153–165. Ellis Horwood, New York. Ross O. and Sharples, J. 2004. Recipe for 1-D Lagrangian tracking models in space-varying diffusivity. Limnology and Oceanography Methods 2: 289–302. Saksida, S., Constantine, J., Karreman, G.A., and Donald, A. 2007. Evaluation of sea lice abundance levels on farmed Atlantic salmon (Salmo salar L.) located in the Broughton Archipelago of British Columbia from 2003 to 2005. Aquaculture Research 38: 219–231. Stien, A., Bjørn, P.A., Heuch, P.A. and Elston, D. A. 2005. Population dynamics of salmon lice Lepeophtheirus salmonis on Atlantic salmon and sea trout. Marine Ecology Progress Series 290: 263–275. Thomson, R.E. 1981. Oceanography of the British Columbia coast. Canadian Special Publication of Fisheries and Aquatic Sciences 56: 291 p. Tucker, C.S., Sommerville, C. and Wootten, R. 2000. An investigation into the larval energetics and settlement of the sea louse, Lepeophtheirus salmonis, an ectoparasitic copepod of Atlantic salmon, Salmo salar. Fish Pathology 35: 137–143. Tully, O. and Nolan, D.T. 2002. A review of the population biology and host–parasite interactions of the sea louse Lepeophtheirus salmonis (Copepoda: Caligidae). Parasitology 124: S165–S182. Tully, O. and Whelan, K.F. 1993. Production of nauplii of Lepeophtheirus salmonis (Kroyer) (Copepoda: Caligidae) from farmed and wild salmon and its relation to the infestation of wild sea trout (Salmo trutta L.) off the west coast of Ireland in 1991. Fisheries Research 17: 187–200.

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Part II Salmon Louse Management on Farmed Salmon

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Chapter 5

Salmon Louse Management on Farmed Salmon—Norway Gordon Ritchie and Karin K. Boxaspen

The Salmonid Farming Industry The sheltered coastline of Norway, with its multitude of islands, inlets, and fjords offers relatively protected waters and an optimal seawater temperature profile for rearing of Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss L.). This favorable environment has facilitated the major development and expansion of the Norwegian salmon farming industry in the last 50 years. Coastal salmonid rearing was pioneered in the 1950s and for nearly two decades this consisted of small local family-owned companies. In 1971, a modest 98 tons was being produced and since 1985, from being a complementary agricultural operation, the salmon farming industry has exhibited strong growth and the ownership, structure, production technology, innovation, and operating activities have changed dramatically, making salmon farming an important coastal business and employer. All statistics concerning salmon farming up to 1985 were published in the Official Statistics of Norway Salmon and Sea Trout Fisheries and until 1992 they were published in the Official Statistics of Norway Fishing and Rearing of Salmon. Thereafter, salmon farming statistics have been published in the Official Statistics of Norway Fish Farming. The subsequent data is therefore sourced from the Official Statistics of Norway and the Norwegian Directorate of Fisheries.

Production Salmon farming in Norway is currently a modern and internationally competitive industry. The export value of salmon and trout from Norway was 18.4 billion Norwegian Kroner (NOK) and 18.8 billion NOK in 2006 and 2007, respectively, with the main markets being the EU, Japan, and Russia (Anonymous 2008). Production of Atlantic salmon and seawater-reared rainbow trout has seen an expansive and dynamic growth with harvested volumes increasing per annum to over 800,000 tons in 2007 (see Figure 5.1; see Chapter 1 contributed by Asplin et al.). Correspondingly, there has been an increase in the number of smolts transferred (inputs) to seawater for rearing. The growth in production has been matched inversely Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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Figure 5.1. Harvested volume (tons) of Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) from 1971 to 2007, number of fish transferred (input number × 1000) from 1994 to 2007, and average production cost kg−1 (Norwegian Kroner) from 1990 to 2006. Figures for 2007 are preliminary. (Data from Directorate of Fisheries, 2008.)

by a decline in the cost of production in seawater and which currently stands at around 15 NOK kg−1 produced for Atlantic salmon (see Figure 5.1). A dramatic reduction in production cost occurred up to 1997 and with a gradual decrease thereafter. The decrease in production cost has been achieved principally through an increased production efficiency and consolidation in the industry. This consolidation is reflected in the decrease in number of companies rearing salmonids in seawater, which declined by 56% from 1999 to 2007 (see Figure 5.2). Although the number of operating companies decreased, the number of operating licenses for seawater rearing in the same period increased by 16% (from 799 to 929). Since 1994 the number of seawater operating licenses has steadily increased from 722 to 929 in the period 1994–2007. Production efficiency can be quantified in one way by the production (tons of harvested fish) employee−1 (e−1 ) working in the seawater production sector. Despite a 24% reduction in the number of employees from 1994 to 2007, the number has remained relatively stable since 1997 (see Figure 5.3). Based on the number of employees in the seawater production sector and increasing biomass harvested, production (ton harvested fish) e−1 has increased by a dramatic 397% (from 64 to 318 t/e) in the period 1994–2007. Similar trends have also been observed in freshwater (juvenile) production (see Figures 5.4 and 5.5). Despite a dip in the number of juveniles produced in the period 2003–2005, there has been a 2.3-fold increase in production from 1995 to 2007.

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Figure 5.2. Number of companies rearing Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) in seawater from 1999 to 2007 and respective number of seawater operating licenses from 1994 to 2007 (excluding brood stock licenses). Figures for 2007 are preliminary. (Data from Directorate of Fisheries, 2008.)

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Figure 5.3. Number of employees in seawater rearing of Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) and respective production (tons harvested) employee−1 from 1994 to 2007. Figures for 2007 are preliminary. (Data from Directorate of Fisheries, 2008.)

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Figure 5.4. Number of juvenile Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) produced from 1995 to 2007 (× 1000) and respective number of freshwater operating licenses from 1994 to 2007. Figures for 2007 are preliminary. (Data from Directorate of Fisheries, 2008.)

Although the number of freshwater operating licenses has fluctuated over the same period there has been a gradual decrease, with a 27% reduction from 1994 to 2007 (see Figure 5.4). With the exception of a dip during 2004 and 2005, the number of employees working in the freshwater production sector has remained relatively stable in the period 1994–2007. Despite this, a dramatic increase in the number of juveniles produced per employee has occurred (see Figure 5.5).

Regulation and Licensing All aquaculture activity in Norway, including salmon farming, is regulated by the Norwegian Ministry of Fisheries and Coastal Affairs through the Aquaculture Act of 2005 (Anonymous 2005). The Act, which superseded the Fish Farming Act, was entered into force on January 01, 2006. The Act establishes the framework for the industry’s future growth through the responsible management of national interests such as the environment and use of the coastal zone. The salmon farming industry specifically is controlled by a number of laws and Acts, administered by five different Ministries (see Table 5.1). Companies must observe the provision prescribed by the applicable laws and regulations. License applications are handled by the Directorate of Fisheries and several regional authorities and are only granted following a positive assessment of social and environmental considerations. Licenses for land-based operations are evaluated by the Norwegian Water Resources and Energy Directorate.

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Figure 5.5. Number of employees in freshwater rearing of Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) from 1994 to 2007 and respective production (number of juveniles produced × 1000) employee−1 from 1995 to 2007. Figures for 2007 are preliminary. (Data from Directorate of Fisheries, 2008.)

The license itself sets out the conditions and obligations for the holder, who must observe the laws and regulations that apply to the activities encompassed by the license. The license specifies the right to produce a specific species, at a defined biomass, stocking density (25 kg/m3 ), and at a specific location. Following the abolition of the feed quota system in 2005, maximum allowable biomass levels were introduced, limiting biomass per license to 780−900 tons. For each seawater license, there are two to four sites or locations and the majority of salmon farms have between 2300−3120 tons maximum allowable biomass. The biomass per license cannot exceed the maximum allowable biomass stipulated in the license for the locality, pursuant with the Aquaculture Act.

Table 5.1. Ministries and respective Acts regulating salmonid farming in Norway. Ministry

Act/s

Norwegian Ministry of Fisheries and Coastal Affairs Norwegian Ministry of Agriculture and Food Norwegian Ministry of the Environment Norwegian Ministry of Local Government and Regional Development Norwegian Ministry of Petroleum and Energya

The Aquaculture Act, 2005 Act relating to Ports and Harbours, 1984 The Food Law, 2004 Act of Pollution, 1981 Act of Building and Planning, 1985 The Water Resources Act, 2000

a The Norwegian Water Resources and Energy Directorate: for land-based construction for the production of salmonids in freshwater.

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Fish health and disease legislation is regulated by the Fish Disease Act, which came into force in 1997 and was transferred to the Directorate of Fisheries, as part of the Food Law, in 2004. Preventative fish disease work is covered by the Norwegian Food Safety Authority. The Norwegian Food Safety Authority runs an official monitoring program for specific diseases. In addition, the National Veterinary Institute plays an important role in the preventive health program. Diseases are reported to the Norwegian Food Safety Authority and National Veterinary Institute, and official reports are published annually.

Legislation Related to Lice Management The river-bound wild Atlantic salmon returning to the Norwegian coast from the Atlantic Ocean have always been known to carry salmon lice (L. salmonis). An early source from around 1700, cited in Berland and Margolis (1983) , explains the presence of lice as a divine intervention to drive the salmon into freshwater to wash off the burden of the lice, all to man’s benefit. Salmon lice problems were manifested almost immediately from the start of salmon farming in Norway. Development of medicinal products started a few years later and a description of the situation in 1974 can be found in Brandal and Egidius (1977). Here, massive attacks of salmon lice in salmon farms were reported. Fish in some farms had several hundred lice and in one instance as much as 2000 lice per individual was observed. These particular articles documented the effects of treatment with R R ) and dichlorvos (Nuvan ) as delousing agents. The latter was trichlorvon (Neguvon the only available product for use until around 1992, and for the next decade, salmon lice were more or less kept at bay by its use. However, it is clear that the accepted levels of lice and the subsequent trigger level for treatment intervention were connected to the parasites’ effect on production performance. At the lower end of an effect scale, lesions could result in quality downgrading at harvesting and in the most severe cases mortality. Later, it was demonstrated that increased lice intensities, below lethal levels, also resulted in reduced weight gain and subsequent financial loss. An analysis of the Norwegian coast and its suitability for aquaculture (Møller 1990) classified the localization of specific cage systems on whether they were situated in either open coastal areas (A), more sheltered areas (B), or in bays and partially enclosed areas (C). The majority of fish farms at that time were C-classified. Geographical localization of farms was initially based on associations between emerging problems with sediment build-up and consequently eutrophication and oxygen problems. The working hypothesis was that these conditions were also linked to disease outbreaks as well as lice infestations. It was shown that fish farms in more exposed areas had fewer problems with lice (Møller 1990). Many claims have been made that salmon lice from farmed salmonids are responsible for an increased level of lice on wild salmonid hosts. Epizootics of salmon lice on wild fish have been documented in Norway (Grimnes and Jakobsen 1996) and have been associated with significant host pathology (see Chapter 9 contributed by Finstad and Bjørn). Studies have shown that lice infected sea trout (Salmo trutta) return to rivers sooner than uninfected sea trout (Birkeland 1996; Birkeland and Jakobsen 1997). Sea trout returning early to rivers, sometimes within days of running

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to sea, have been recorded (Birkeland 1996; Birkeland and Jakobsen 1997). Although salmon lice are natural parasites of salmonids, the high level of parasitism observed is reported to cause mortality (Grimnes and Jakobsen 1996; Bjørn and Finstad 1997). Bjorn and Finstad (2002) concluded from a study on charr (Salvelinus alpinus) and sea trout (S. trutta) in Norway that fish farming contributed to the elevated sea lice levels found on wild fish. Interaction of pathogens, including sea lice, between wild and farmed salmon is reviewed in the Dipnet report (Raynard et al. 2007). In Norway, it is generally accepted that for Norwegian waters and with the level of salmon production, salmon lice from farms can infect wild salmonids in the same body of water. This assumption cannot be made or be transferred to other countries and areas without rigorous scientific analysis. Thus, today’s legislation and regulations on salmon lice numbers help to protect the migrating wild Atlantic salmon postsmolts.

Early Legislation on Salmon Lice Control Prescription By 1979, Neguvon (Brandal and Egidius 1977, 1979) was authorized for the treatment of salmon lice by the Norwegian Drug Control Authority, provided it was used under a veterinary prescription. At that time all 19 counties within Norway had an appointed county veterinary surgeon and this office would coordinate several district veterinarians. Today, this falls within the Norwegian Food Safety Authority. Traditionally, these veterinarians would be concerned with terrestrial and companion animals but over time they were challenged with treating diseases in the growing salmon farming industry. In the 1980s, it became customary for salmon farming companies to have a contractual agreement with a nongovernmental veterinarian, who gradually became more specialized in fish and fish health-related issues. In addition, specialized fish health practices and networks were established. The overview of the sea lice situation in a region would often come from these networks (Andersen 1993; Jøssund 1994; Romstad 2004).

Animal Welfare Act Prescribing veterinarians would in some instances recommend treatment against salmon lice, but the lack of legislation prevented enforcement of such control measures. The only law that could be used to enforce treatment was the “Law concerning animal welfare” (Anonymous 1974). This law states that no animal should suffer unnecessarily and that the district veterinarian could instruct a producer to treat for lice. There are no records documenting that such instructions were ever applied.

Early Application of Buffer Zones In 1986, the laws controlling fish farming were amended and it was ratified that a salmon farm-free buffer zone could be invoked in a clearly defined area around rivers and tributaries with important wild salmon populations. The regulation Section 5 Part 3 states:

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No legislation for salmon farms can be given in the area if 1) there is danger of the farm dispersing disease to either fish or shellfish 2) any danger of the farm polluting or 3) the placement of the farm will be clearly in violation of the environment or right of passage or other approved uses of the area.

Development of Monitoring Programs From 1992, salmon lice were placed on the C-list of contagious diseases in aquaculture. Consequently, veterinary surgeons were obliged to report salmon lice problems to the veterinary authorities. However, as reported in Rudi and Villabø (2004), there were no clear guidelines for how an individual case should be evaluated or reported, suggesting that at this point the official data forthcoming was of little value. The lesson from Flatanger (see section “Case Studies”) combined with the growing evidence for effects of salmon lice on wild hosts led the Norwegian Research Council to commission a report for a National Action Plan with the goal of facilitating a reduction of salmon lice impacts on both wild and farmed salmonids in Norway. The report aimed to (1) propose a strategy and organization of a national plan for control of salmon lice; (2) provide an overview of existing control measures and research and development activities for combating salmon lice; (3) suggest new measures and outline the research and development needs for the plan; and (4) make suggestions for financing the plan. The first proposal of the working group was published in May 1996 (Kryvi et al. 1996). The main challenge facing the action plan was the lack of legislative anchoring. As described above, no existing law could force a mandatory registration of salmon lice on farms nor force a treatment intervention on individual farms without a veterinarian assessment or breach of the Animal Welfare Act. However, the group-C fish disease status for salmon lice permitted application of the “law on fish diseases,” which stated that the Ministry could apply regulations, and impose measures and injunctions as they saw fit for the prevention, limitation, and eradication of the disease. The first suggestion was thus to order a minimum registration level on all salmon farms with subsequent mandatory reports to the veterinary authorities or fish health services. The other planned measures were that the operational registrations had to be standardized and coordinated every month; and when registrations were done on wild hosts, one should endeavor to conduct this with the same methodology or at least in a comparable fashion. To ensure reliable registrations, all participants were obliged to participate in training programs. Information from registrations would be shared in the local environment and also preferably on a regional basis with the local fish health network and/or the district veterinarians. Recommendations were also made for a synchronized autumn or winter treatment intervention in combination with use of cleaner fish (wrasse).

Norwegian National Action Plan against Salmon Lice The monitoring of salmon lice was thus deemed essential in planning and coordinating treatment regimes in commercial salmonid aquaculture (Heuch and Mo 2001). The National Action Plan report of 1996 was used in the proceeding work to develop a national action plan that was ratified in February 1997 (Eithun et al. 1997). The

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National Animal Health Authority, Directorate of Fisheries, Directorate for Nature Management, Aquaculture Veterinarians Association, and Norwegian Fish Farmers Association participated in this initiative. The short-term goals were to establish regional and local collaborations with participation of all stakeholders for planning and coordination purposes (by end 1997); document levels of salmon lice in all fish farms (by end 1998); document levels of salmon lice on wild hosts (by end 1998); and preventive control measures must also be documented (by end 1998). The long-term goal was to reduce the detrimental effects of salmon lice on both farmed and wild fish. A National Working Group, with an advisory and coordinating role, was formed with representatives from industry, authorities, and research institutes. Besides developing the National Action Plan itself the National Working Group were also mandated to make a yearly report on the progress of the National Action Plan. Furthermore, the County Veterinarian’s office was directed to initiate and facilitate the development of regional collaborative groups for each county with the objectives: to define geographical areas where cooperation was natural; to define areas of priority where organized treatment should be undertaken on the basis of previous problems, e.g., treatment frequency, occurrence of salmon lice, site density or wild fish interests, migratory routes for salmon smolts, and on-growing habitats for sea trout; to appoint local working groups for the areas of priority; to estimate needs for and plan courses in salmon lice registration for producers; to facilitate registrations of salmon lice levels on wild hosts in cooperation with river owners; and to collect the data and reports from all participants. The recommendation for a minimum sampling frequency of salmon lice was that the number of gravid females per fish should be sampled at least once a month on all localities. This was done by anesthetizing 20 randomly chosen fish in the net pen presumed to have the highest number of lice. In the spring of 1998, an amendment to the “Law on fish health” allowed the County Veterinarian to identify geographical zones where special measures against salmon lice could be made and over the year regional amendments were made for all areas. The most important points were as follows: all fish farms must register salmon lice at least once a month at sea temperatures under 9◦ C and every 14 days at temperatures above 9◦ C; levels of gravid females must be reported to the district veterinarian every month and by the 15th of the next month; the level of salmon lice must be minimized by medicinal treatment if necessary, before new smolt go to sea or migration of wild salmon occurs (i.e., spring). The County of Trønderlag had at this time set a treatment target of not more than one gravid female per fish but it was deemed unrealistic to impose this limit in all areas and the target was set at not more than two gravid females per fish. At this time it was possible for the district veterinarian to impose a forced treatment but it was not deemed practical and the use of fines was recommended, if necessary. The results for the first year were reported by Eithun et al. (1999) and for the two consecutive years by Jensen et al. (2002). The results varied slightly from county to county, but overall the goals were reached or lice levels visibly improved. The data indicated that the mean number of lice per fish declined from 1998 to 2002 in the northern areas, for example (Koren 2001). Heuch et al. (2005) summarized some of the data and pointed out that even though the number of lice per fish had declined, the total number of farmed hosts had increased, suggesting the total number of egg-bearing adult female lice and subsequent production of lice larvae may not have decreased.

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Managing Salmon Lice on Farms, 2008 The regulations for managing salmon lice in farms now have legal authority from the Norwegian Food Safety Authority (December 19, 2003, number 124). The latest update of the regulation (FOR 2008–07-09, number 797) states in Section 4 “Counting, registration and reports” that at sea temperatures >4◦ C salmon lice shall be counted and registered every 14 days. The number of adult female lice, mobile lice, number of treatments in the period, sea temperature, and use of cleaner fish (wrasse) shall be reported every month and by the 7th of the next month. Delousing is regulated in the same amendment (Section 5) and states that if by following Section 4 more than 0.5 adult female salmon lice or more than three mobile lice are found per fish in one single net pen, then all net pens shall be treated. In the same paragraph it is also stated that the Norwegian Food Safety Authority can ensure coordinated delousing, and through resolution reduce the trigger limit. During the winter of 2007/08, the Norwegian Food Safety Authority ran a coordinated treatment campaign along the western coast of Norway including all four counties from Stavanger to Stadt ((1) Rogaland, (2) Hordaland, (3) Sogn og Fjordane, and (4) Møre and Romsdal). The winter campaign was continued for the two following winters.

Approaches to Sea Lice Management Integrated Pest Management (IPM) Integrated Pest Management is a multifaceted and systematic approach to pest control. Rather than simply trying to eradicate a pest, IPM makes use of the information, knowledge, and experience gained; accounts for multiple objectives in managing the problem; considers available preventative and curative options; and makes informed decisions aimed at achieving optimum results. Box 5.1 outlines the basic principles and requirements of an IPM program and which have been applied to strategies developed for sea lice control. The general principles of IPM for sea lice are good husbandry and management practices, use of biological controls, and the optimal use of medicines. These in turn serve to optimize present control methods and to contain the threat of resistance development to medicines.

Box 5.1 Basic Principles and Requirements of an Integrated Pest Management Program r Understand the biology and economics of the pest r Monitor pest populations r Establish economic thresholds and take actions when the potential impact is

sufficient to justify action

r When needed, select an appropriate system of cultural, mechanical, biological,

and chemical prevention or control techniques ➢ Cultural practices include modification of habitat and adapting operating procedures so that opportunities for pest damage are reduced

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➢ Augment naturally occurring prophylactics and cures and use biological controls as predators where possible ➢ Medicinal control involves selecting a product with the safest profile and using it in such a way as to prevent or minimize undesirable environmental effects r Regularly evaluate the management program through continuous epidemiological investigation and treatment follow-up by keeping records and building a databank on pest levels

The history of sea lice management in Norway mimics in many ways pest management in terrestrial agriculture and a tremendous amount of knowledge has been gained from the experiences with IPM approaches in this sector and their subsequent application in sea lice intervention strategies. In addition, the same chemical classes that have been or are being used for the medicinal treatment of sea lice have been used over the decades in the terrestrial sector. As the salmon farming industry has expanded, it has become increasingly important to manage sea lice in a way that is seen as being synonymous with environmentally sound and sustainable farming practices. The need to manage sea lice infections through the application of IPM has been well recognized and the principles of IPM have become essential tools in sea lice management. The continued application of these principles will be of even greater importance as it becomes more challenging to replace established treatment chemistries and modes of action with new ones and to protect the long-term viability of treatment options currently at the industry’s disposal. Early approaches toward IPM were aided by an increased understanding of the biology and epidemiology of lice, greater availability to effective medicines, along with improvement in the management and coordination of treatments among sites. Significant progress has been made in the past few years with regard to the use of strategic treatments, better understanding of the epidemiology, and the licensing of several effective control agents. The three main components that constitute IPM in Norway include (1) monitoring of the lice population, (2) husbandry and management approaches, and (3) medicinal cures, when required. Lice levels are continuously monitored on all stocked sites starting 2 to 4 weeks after transfer to seawater, depending on temperature. Monitoring is carried out according to the aforementioned legal requirements and by trained staff who are capable of diagnosing and distinguishing both species and stages of sea lice and reporting lice numbers as legally required. The need for, choice of, and timing of treatment depends on lice population dynamics. Monitoring is necessary, therefore, to ensure interventions are carried out at the correct time, with the correct product. Monitoring also allows the site to build up a picture of the dynamics of the site lice population and make predictions for optimal treatment times. Husbandry and management approaches are used as part of IPM for sea lice control. These represent a series of proactive tools employed by the industry to mitigate sea lice infection (see Box 5.2). The use of cleaner fish (wrasse) as an aid to lice control is well documented and several excellent reviews and studies have been published (Sayer et al. 1994).

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Box 5.2 Husbandry and Management Approaches used as Part of Integrated Pest Management for Sea Lice Control r r r r r r r r

Fallowing between stocks Single-year class separation and an all-in-all-out policy Proper management of fish densities Clean nets for good water circulation Routine removal of moribund fish Regular removal of mortalities Use of cleaner fish (wrasse) Use of health promoting diets and stress reduction

A range of medicines are licensed in Norway for the control of sea lice including both topical (bath or immersion treatment) and oral (in-feed) remedies, details of which are given below. Box 5.3 outlines the main principles, steps, and procedures applied to medicinal treatments for sea lice.

Box 5.3 Main Principles, Steps, and Procedures Applied to Medicinal Treatments r Medicines are prescribed and used according to clinical needs, based on the

safest profile for that application

r Application method, dose, withdrawal period, operator, and environmental

safety will be respected

r For topical treatments, enclosures (tarpaulins or skirts) are used (depending on r r

r r r r r

jurisdiction, pen size, and water currents) and oxygen supplied and monitored throughout the treatment Fish are observed and are not to be left unattended during treatment The therapeutic treatment will be optimized by using the recommended dose and duration, ensuring no concurrent disease during application, careful feeding and appropriate amount of in-feed medication, and avoidance of subtherapeutic doses Target an alternation/rotation of products used Treat whole sites and neighboring sites at the same time Regularly evaluate the treatment effect and program through continuous lice population surveys and treatment follow-up Do not use a product once efficacy to that product begins to decline Always ensure the appropriate withdrawal period for a product is respected

In summary, current strategies toward sea lice control in Norway are based on the principles of IPM, utilizing both management practices and medicines to treat sea lice. Improvements to control strategies are continuous and are updated when new and pertinent information becomes available.

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Medicine Use While husbandry practices and IPM approaches have made a major contribution to the control of sea lice populations in recent years, medicinal treatment is still required to maintain control and even the best managed farms may use medicines from time to time in order not to exceed threshold values and treatment trigger levels (see section on “Managing salmon lice on farms, 2008”). A number of medicines, both topical and oral, are currently available for use. Medicines are prescribed by a qualified veterinary surgeon for use on animals “under his or her care” and according to the respective instructions for use (method of application, dose, duration, withdrawal period, operator, and environmental safety). The choice of medicine and when to perform a treatment depends on a number of operational, biological, and environmental factors including cost per treatment, time of year, water temperature, fish appetite, fish health status, total treatment cost over the production cycle, respective efficacy, and withdrawal time. Timing of treatments also depends on the mode of action, efficacy toward particular stages of sea lice, and properties of the medicine to be used. In addition, medicinal control involves selecting a product with the safest profile for that application, in accordance with the clinical requirements and the need to prevent or minimize undesirable environmental effects. In determining which medicine to use, and when, the benefits and limitations of each product are evaluated before a prescription is issued. Responsibility for defining and ensuring the correct dosage of any medication and safety of the treated fish lies with the prescribing veterinarian. In general, topical medicines are considered time consuming (taking more than 1 day to treat an entire site), labour intensive, and more difficult at exposed sites or during severe weather conditions. Feed is also withheld for up to 48 hours pretreatment. As a consequence of the procedures involved, topical treatments are considered more stressful for the fish; oxygen must be supplemented when necessary, and there is a greater challenge to obtain a homogenous dose within the confines of the treatment unit. In contrast, the application of oral medication has the following characteristics: it is generally less time consuming with little disruption to normal routine, it is more suitable at exposed sites or during severe weather conditions, it allows for simultaneous treatment on a site, and it is less stressful to the fish. However, oral medication relies on accurate biomass calculations and is not suitable when the appetite of the fish is reduced. Further, due to differences in feeding patterns, obtaining a homogenous dose within the entire population can be challenging. Within the last decade, a range of both topical and oral medicines have been used R (active ingredient azamethiphos), for sea lice control in Norway including Salmosan  R R (active ingredient diflubenEktobann (active ingredient teflubenzuron), Lepsidon   R R R (active zuron), Excis and Betamax (active ingredient cypermethrin), Alphamax  R ingredient deltamethrin), and SLICE (active ingredient emamectin benzoate). The total quantities of active ingredient (kg) used per year in the Norwegian salmonid farming industry are shown in Figure 5.6. Since 2001, medicinal control has relied on R R R and Alphamax , and SLICE medicated the use of the topical medicines Betamax feed. Table 5.2 details certain properties of these medicines.

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1600

80

1400

70

1200

60

1000

50

800

40

600

30

400

20

200

10

Cypermethrin, deltamethrin and emamectin (kg active ingredient)

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Azamethiphos, diflubenzuron and teflubenzuron (kg active ingredient)

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0 1997

1998

1999

2000

2001

2002

2003

2004

2005

2006

2007

Year Azamethiphos

Diflubenzuron

Cypermethrin

Deltamethrin

Teflubenzuron Emamectin benzoate

Figure 5.6. Quantity of sea lice medicines (kg active ingredient) historically and presently used in Norwegian salmonid farming from 1997 to 2007. (Data from The Norwegian Institute of Public Health, 2008.)

Methods of Use R SLICE medicated feed was licensed for the treatment of sea lice infections on R has been the dominant farmed salmonids in Norway in 1999. Since 2001, SLICE oral treatment with the total mass used increasing annually from 12 to 73 kg emamectin benzoate from 2001 to 2007 (see Figure 5.6). R premix, which is coated on to feed pellets, consists of 0.2% emamectin SLICE R medicated feed is available benzoate along with several inert premix carriers. SLICE through veterinary prescription and can only be prepared and supplied by designated R medicated feed be delivered at a minifeed mills. It is recommended that SLICE mum of 50% of the total daily ration of the fish to be treated (Anonymous 2007a). R premix is incorpoTo achieve this, and due to variation in fish feeding rates, SLICE R medicated feed. rated into the feed at different inclusion levels to produce SLICE Table 5.3 outlines the four standard daily feeding rates and the respectively adjusted R premix in the feed, together with the resultant conincorporation rates of SLICE centration of emamectin benzoate. The same size of feed pellet as normally fed is used, which may be of any size appropriate to the size of the fish; and in general 4–5 different pellet sizes are used. R In addition to knowing the feeding rate and respective inclusion level of SLICE premix into the feed, the prescribing veterinarian also must know the biomass in each R medicated pen at the start of treatment in order to calculate the quantity of SLICE  R feed to be administered to achieve the recommended dosage. SLICE medicated feed is effective against both Lepeophtheirus salmonis and Caligus elongatus, with all chalimus, preadult, and adult stages being affected (Anonymous 2003). Maximum

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Table 5.2. Properties of medicines currently used to control sea lice in Norway (Anonymous 2000, 2002, 2003, 2007a, 2007b). Medicine Trade name

R Alphamax

R Betamax

R a Slice

Supplier

Pharmaq AS

Novartis/ScanVacc AS

Active ingredient

Deltamethrin

Chemical group Mode of action

Pyrethroid Interference of nerve transmission by blocking sodium channels in nerve cell axon membranes 10 mg deltramethrin mL−1

Cypermethrin (cis 80: trans 20) Pyrethroid Interference of nerve transmission by blocking sodium channels in nerve cell axon membranes 50 mg cypermethrin mL−1

Intervet/Schering— Plough Animal Health Emamectin benzoate

Concentration

Recommended dose

0.002 mg L−1 for 30 min (enclosed treatment); 0.003 mg L−1 for 40 min (skirt treatment)

Indication on sea lice Withdrawal period

Preadult and adult stages 5 degree days (Atlantic salmon); 20 degree days (rainbow trout)

0.015 mg L−1 for 30 min (enclosed treatment); 0.015–0.02 mg L−1 for 40 min (skirt treatment) Chalimus, preadult, and adult stages 3 days

Avermectin Interference with chloride ion movement and transmission of nerve impulses 2 g emamectin benzoate kg−1 premix 50 μg emamectin benzoate kg−1 bodyweight per day, for 7 days

Chalimus, preadult, and adult stages 175 degree days

R R R a In Norway, Slice medicated feed (Slice premix + basal feed) is licensed and not the Slice premix alone.

R Table 5.3. Daily feeding rates, Slice premix inclusion levels and resultant emamectin benzoate concentrations in the feed (Anonymous 2007a).

Daily feeding rate (% bodyweight day−1 )

R Concentration of Slice −1 premix in feed (kg ton )

Concentration of emamectin benzoate in feed (mg kg−1 )

>1.5 1.0–1.5 0.5–1.0 < 0.5

1.67 2.5 5.0 10.0

3.3 5 10 20

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effect is observed 1–2 weeks posttreatment during summer and 3–4 weeks posttreatment in winter, with the duration of protection lasting from 6 to 10 weeks (Anonymous 2007a). Since 1999, the active ingredients cypermethrin and deltamethrin have been the dominant products used for topical treatment of sea lice. From 1999 to 2000, the volume of cypermethrin used increased dramatically; however, from 2000 to 2007, the amount used has gradually decreased from >70 kg to 30 kg active ingredient, respectively (see Figure 5.6). The amount of deltamethrin used remained relatively stable from 1999 to 2005 and has doubled in the period 2005–2007 (see Figure 5.6). R R and Alphamax are provided in Table 5.2. Particular properties of both Betamax  R R −1 consists of 50 mg Alphamax consists of 10 mg deltamethrin mL , while Betamax −1 cypermethrin mL . Both products are indicated for treatment of L. salmonis and C. elongatus infections on Atlantic salmon and rainbow trout (Anonymous 2000, 2002, 2007b). R R and Betamax are performed on a sea Topical treatments with both Alphamax cage unit with a raised net which is either fully enclosed by a tarpaulin or semienclosed with a skirt prior to administration of the medicine. Due to differences in the size of the treatment unit, water current strength, and depth below the unit, topical treatment techniques vary widely. For the sake of this review then the general instructions and recommended practices from the product manufacturers will be described. With use of a tarpaulin the treatment volume is calculated based on the volume of the sea cage and not according to the volume of the tarpaulin. The treatment volume is thus the sea cage surface area multiplied by a maximum of 4-m depth in the treatment unit with the raised net. When the depth of the treatment unit, with raised net, is less than 4 m, the volume is calculated as the area of the sea cage surface multiplied by the actual depth of the raised net. If the depth is greater than 4 m, the calculation is based on the sea cage surface area multiplied with 4-m depth regardless of the actual depth of the raised net and the tarpaulin. Skirt treatments are more commonly used on larger net pens; however, their application is very much dependent on weather conditions and water currents. The net pen is raised to 4 m and the skirt tarpaulin, with a depth of greater than 4 m, is deployed completely around the raised net pen so that the skirts are deployed at a greater depth than the net pen. The volume to be treated is calculated to a maximum of 4-m depth. Better control of the treatment volume and the treatment dosage can be achieved with full tarpaulin enclosures. With a skirt treatment, volume calculations may be less precise. Bjøru et al. (2004) concluded that administered drug is more evenly and quickly distributed using a fully enclosed tarpaulin compared to a skirt. Loss of drug out of the net pen and a more rapid dilution of the drug can occur with use of a skirt, due to exchange of water from beneath the skirt (Bjøru et al. 2004). In general, poor control of the treatment volume, with either fully enclosed tarpaulin or skirt, gives the greatest risk of suboptimal treatment (Anonymous 2002; Bjøru et al. 2004). R is administered at a dose of 0.2 mL m–3 For full tarpaulin treatment, Alphamax seawater in the treatment unit, corresponding to 2 μg deltamethrin L−1 (or 2 ppb) of R is administered at a dosage of 0.3 mL seawater, for a duration of 30 minutes. Betamax  R 3 Betamax per m seawater, corresponding to 15 μg cypermethrin L−1 (or 15 ppb) of R seawater, for a duration of 30 minutes. For semienclosed skirt treatment, Alphamax

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is dosed at 0.3 mL per m3 seawater, corresponding to 3 μg deltamethrin L−1 (or 3 ppb) R is administered at a dosage of of seawater for a duration of 40 minutes. Betamax  R 0.3–0.4 mL Betamax m–3 seawater, corresponding to 15–20 μg cypermethrin L−1 (or 15–20 ppb) of seawater, for a duration of 40 minutes (Table 5.2). Prior to administration, the medicine is brought to room temperature and shaken well. A suitable container is then used to dilute the calculated quantity of medicine into seawater to ensure better dispersion and therefore optimal effect. After a short period of stirring, the diluted solution is spread evenly in the treatment unit. There are many techniques used for dispersing the diluted solution; however, the most common and generally regarded optimal procedure is to pump the solution at low pressure through a perforated hose or tube placed on the surface and across the entire width of the enclosed unit. Dispersion under high pressure is avoided as this can cause foaming or spraying. Safety measures are exercised during treatment. Operators use protective equipment including gloves, safety goggles, and protective clothing when handling medicines to avoid skin contact and inhalation. During treatment, oxygen is supplemented in the unit and monitored throughout to ensure oxygen level is maintained above 7 mg L−1 for the entire treatment period. Oxygenation also aids in mixing the medicine. Fish are monitored for signs of toxicity during treatment, including irregular movements, seizures, loss of balance, and reR duced respiration. At water temperatures below 6◦ C, the safety margin of Alphamax is reduced and extra precautionary measures are exercised to ensure safety to the fish. During topical treatment the fish tend to position themselves nearer the surface and activity levels (restlessness and jumping) increase. Miscalculation of the treatment volume and potential overdosing, low water temperatures, or extended exposure is known to increase the incidence of adverse reactions or signs of intoxication. Any adverse reactions or side effects are recorded and reported by the prescribing veterinary surgeon. Topical medicines are not recommended for use during the presence of infectious disease as clinical signs and mortality may be aggravated (Anonymous 2000, 2002, 2007b). Topical treatments are avoided when large amounts of organic material are present in the seawater or if the cage net is heavily fouled, as this can reduce efficacy of R R and Betamax bind to organic material. In addition, treatment since both Alphamax heavily fouled nets reduce water exchange posttreatment. All equipment that has been in contact with the medicine is cleaned after application and it is recommended that the tarpaulin is disinfected between each use. R R or Betamax , moribund sea lice may Following treatment with either Alphamax remain on treated fish for several days posttreatment (Anonymous 2002, 2007b). In order to optimize and evaluate performance of any sea lice medicine, the following general measures are considered important: always use a medicine according to the suppliers recommendation; always administer at the recommended dose and duration; oral medication should not be used if an intercurrent disease is present onsite which could affect appetite; careful feeding and monitoring of feed consumption should be practiced when using oral medication; ensure medicinal applications do not result in subtherapeutic doses; all fish on a site should be treated simultaneously or at least in as short a time as possible to limit reinfestation; neighboring sites in the same water body are treated at the same time; and continuous lice monitoring posttreatment in order to evaluate treatment effect.

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Synchronized Approaches Strategically timed and coordinated sea lice treatments within appropriate biological areas are performed, where companies are encouraged to develop their treatment strategies in consultation with other companies. Examples of the benefit from planning treatments in such a manner are given below. Strategic and coordinated treatments of sites in zones form an important and integrated approach to lice management. Lice levels are minimized by instigating a series of coordinated, synchronous, strategic treatments during the winter. As noted above, coordinated and strategic treatments are also conducted in certain areas. Winter and spring delousing strategies are based upon seasonal variations in lice numbers and low recruitment of lice during the late winter followed by increased larval settlement observed during the spring (Pike and Wadsworth 1999). Three medicines are currently used for the effective control of sea lice populations. Together with the application of IPM and strategically coordinated treatments, this has led to improved control of sea lice and has reduced the need for frequent repeat treatment.

Case Studies Over the history of salmon farming in Norway, several geographical areas have had challenging periods due to salmon lice that have been solved by applying the approaches mentioned above and by the increased attention from veterinarians and other stakeholders in the specific area. The first geographical area to report problems controlling the overall sea lice situation and to adopt a coordinated regional strategy was the Flatanger/Namdalen area, north of Trondheim in 1991 (see section “Flatanger”). In more recent times, regions within the Hardangerfjord have also implemented a coordinated approach for sea lice management. The main outcome of these developments was a broader cooperation between all producers in the zone, as well as adoption in other geographical areas.

Flatanger In 1991, the Flatanger area (Figure 5.7) experienced salmon mortality and reduced harvesting quality due to heavy sea lice infestations (Andersen 1993). This was also the first area to document a case of treatment failure where resistance to dichlorvos R ) was later shown (Fallang et al. 2004). The topical application of hydrogen (Nuvan peroxide was adopted as a treatment method (Thomassen 1993) and was used up until 1996 (Eithun et al. 1999). Designated crews were used to conduct the treatments because of the specific procedures and equipment needed. Synchronized spring treatments were initiated from March to April in 1992 and the following years with a trigger level of 0.5 gravid females or four mobile lice per fish. The results from this coordinated action took some time before they were manifested. The overall level of gravid females calculated for the whole region were given as 1.56 per fish in 1993 and thereafter showing a steady decline to 0.39 gravid females per fish in 1997 (Eithun et al. op. cit.).

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Figure 5.7. Map of Norway with the two described case study areas circled Flatanger (north) and Hardangerfjord (southern).

The focus and results of these actions led to the realization that coordinated control measures over larger areas and synchronizing treatments on sites gave improved results in the long term. This realization, together with the application of IPM (see section “Integrated Pest Management”), gave rise to the establishment of area-specific fish health networks.

Hardangerfjord The Hardangerfjord is situated in the west coast of southern Norway (Figure 5.7) and with its 150 km total length, one of the longest fjords in the country. Before 1990, there were few reports of sea lice on farms in this area. This was thought to be a consequence of the overall lower salinity, particularly in the upper layers of the water column. This has never been substantiated by any surveys but seems a plausible explanation. Salmon production in this area has grown considerably over the last years and total production in 2007 was estimated to be between 60 and 70,000 tons (www.fiskeridir.no). Populations of wild salmonids in Hardangerfjord, both sea trout and salmon, have had serious problems and several of the populations have been deemed in danger of extinction. Salmon producers and veterinary services perceived the need to work together on a broader basis and an initiative to coordinate efforts against salmon lice was

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established in March 2003 called The Hardanger Fish Health Network (Hardanger Fiskehelsenettverk). At this time the production in the area was an estimated 60,000 tons on a total of 40 localities along the fjord. The number of producers in the network increased and by 2008 nearly all producers were active in the network. The initiative is in their own words to be regarded as a supplement to regular veterinarian services (Olsen et al. 2005). The primary objective of the Hardanger Fish Health Network was that in the Hardangerfjord, where potentially 15–20 million farmed hosts are present at any time, only cooperation between all stakeholders could make this a sustainable operation. The Hardanger Fish Health Network wanted to demonstrate that a model for salmon lice control based on IPM and a surveillance of the salmon lice dispersal dynamics could be successful and applied to comparable systems. The target of the Hardanger Fish Health Network was to reduce the overall lice burden in the system by using cleaner fish (wrasse), good husbandry practices, strict lice monitoring, topical and oral medicines, and by synchronizing treatments at the correct time points. With regard to the timing of synchronized treatment intervention, focus was placed on a combined winter (01 January) and spring (01 May) delousing strategy. By treating at these time points, reductions in lice levels could be optimized. The target for the winter delousing was to reduce the lice burden at a time when the salmon lice had slower growth and then to repeat this exercise in spring when wild Atlantic smolt runs occur, to ensure as few infective lice were present at that time. The first synchronized winter treatment was initiated over the winter of 2004/05 and has been repeated each successive winter. Recommendations for coordinated and synchronized treatment (2004–2008) inR around Christmas cluded that first sea winter salmon should be treated with SLICE and topical treatment of all growing fish between February and April. This will ensure no gravid females in mid-April and thus no free-living salmon lice larvae when both farmed spring smolts and wild postsmolts go to sea. The use of wrasse on all fish, if possible, throughout summer is also recommended. The Hardanger Fish Health Network always emphasized that the treatment of choice will vary, but that the overall principle was sound. In December 2004, the lice load on farmed salmon in the fjord was 0.21 gravid females and 2.93 total lice per fish (Olsen et al. 2005). Separated into production generations the youngest fish had lice intensities of 0.12 gravid females and 1.64 total lice per fish (week 48/49). Adhering to the national trigger level for treatment (0.5 gravid females/5 total lice per fish), few treatments would have been necessary. It was therefore decided to adopt a lower trigger level for treatment of 0.25 gravid females or a total of 2.5 lice per fish. The documentation parameters targeted were as follows: the duration of efficacy R could be compared to untreated groups; if the duration of protection of SLICE extended as a result of the synchronized treatment regime; is this regime cost effective; and will the total quantity of medicine be reduced?

Results from the Synchronized Winter Treatments Fifteen out of 17 farms with 2003 generation salmon were topically treated between week 41(2004) and week 5(2005). A total of 20 out of 25 farms with spring 2004 R (17 farms) or with generation or autumn 2004 generation salmon treated with SLICE

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topical remedies (three farms). Two farms with poor fish appetite (due to intercurrent disease) did not treat and three farms had no lice. This strategic program resulted in salmon being free of lice from 01 May and which consequently had a lower lice level during the summer. It was calculated that the salmon producers following this regime saved approximately 20 million NOK due to improved growth and a lower cost associated with the use of medicine (Olsen 2006). However, the overall success of this program in the future will depend on the efficacy of the medicinal treatments. For the following winter treatment (2005/06), this synchronized approach was adopted for 95% of the biomass in the fjord and in spring 2006 average lice levels ranged from 0 to 0.05 gravid females per fish (Olsen 2006).

Comparison with Sentinel Cage Data Sentinel cages containing farmed Atlantic salmon smolts from a producer (and free of lice) were positioned at previously determined strategic points in Hardangerfjord each spring from 2004 to 2006 (see also Chapter 2 contributed by Murray et al.). Results each year were consistent and showed a very low abundance of lice per fish in cages from the inner part of the fjord and slightly elevated levels in the outer part of the fjord (Finstad et al. 2007). The lowest infections were found in 2005. Abundances ranged from a mean of 0.2 lice per fish up to ten lice per fish per cage. The method ascertained the availability and infection pressure of lice larvae for settlement on hosts. No gravid females were observed in the short exposure time. In the same testing periods, catches of migrating wild Atlantic postsmolts showed an abundance of lice per fish comparable to those recorded in the sentinel cages. All these data are summarized in the report “The Hardanger fjord project 2004–2007” (Finstad et al. 2008). In 2008, the abundance of lice in sentinel cages in the outer areas of the Hardangerfjord showed higher levels (2–3 fold increase) than in preceding years (L. Asplin, personal communication). This could be due to natural variations in physical or environmental parameters such as temperature and salinity.

National Salmon Watercourses and Fjords Stocks of wild Atlantic salmon have been in steady decline since 1970 and the reasons for this are complex and multifactorial. Due to declines in many other geographical areas, Norway is now described as the center of the Atlantic salmon stock, containing most of and several of the largest Atlantic salmon populations (Anonymous 1999). In 1997, a committee was appointed to “review the overall situation of the wild salmon stocks and present proposals for management strategies and action programs. Issues associated with the regulation of fishing, watercourse management, and salmon farming shall be given particular attention.” This was accomplished and presented to the Ministry of Environmental Affairs in 1999 (Anonymous 1999). In Chapter 5 of the committee’s report, several reasons for the decline were proposed such as (for the 1970s and 1980s): overfishing, acid rain, river habitat modification and destruction, and the freshwater parasite Gyrodactylus salaris. However, in later years, salmon farming, which provides hosts for salmon lice in the seawater phase all year round, along with escapees, was also added to the list. Migrating wild Atlantic

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postsmolts are considered particularly vulnerable to salmon lice. In 1997, farmed salmon production outnumbered wild catch by 500-fold. In 2008, the production has more than doubled. The committee believed it was realistic for the Norwegian stock of wild salmon to recover. Several measures and strategies were proposed and covered in the report including: formalized cooperation and increased supervision, knowledge-based management, regulation of the fishery, watercourse management, measures to combat escapees from farms, measures to combat fish diseases, and fish enhancement measures. The main measure was the proposal for establishment of National Salmon Watercourses and National Salmon Fjords. The National Salmon Watercourses and National Salmon Fjords are special protected areas for wild Atlantic salmon and cover the most important migratory watercourses and fjords. The majority of the Committee proposed 50 such National Salmon Watercourses and nine National Salmon Fjords. In 2002, the Norwegian government sanctioned the agreement for the National Salmon Watercourses and National Salmon Fjords (St. prp no. 79) and recommended a total of 37 watercourses and 21 fjords that were ratified by the National parliament in 2003. In the National Salmon Fjords, special conditions for the establishing of fish farms and the management of existing farms within the area apply. The main objective is to protect wild salmonids and, in particular, to protect stocks against the impact of salmon lice. In practical terms, no new licenses can be granted in the National Salmon Fjords and existing farms cannot increase production volume. Several national institutes are charged with the task to review the effectiveness of this approach over a 10-year period. The final list of National Salmon Watercourses and National Salmon Fjords was established in 2006 and a full review is expected in 2016.

Use of Coordinated Sea Lice Areas and Zones The Norwegian Food Safety Authority are working on establishing defined areas that have a coordinated plan for overall handling of salmon lice within the area at all times. Zones are also defined where all farms must adhere to the same production cycle and subsequently fallow the whole area for 3 months before restocking the sites. The area of Sunnhordaland (including Hardangerfjord) was the first to be regulated in this fashion (July 2010). Rogaland (around Stavanger) and the area north of Trondheim (North Trønderlag) are the two next areas proposed to be regulated in this fashion.

Summary Norwegian salmon farming started around 1965 and the first management of salmon lice came about 10 years later with the legislation to use Neguvon as a bath treatment. After this the National Action Plan against salmon lice (1997), governmental protection of some areas as salmon fjords and rivers with specific restrictions on salmon farms (2003), nationally coordinated winter delousing plans for the western coast (started 2007/08), and establishment of designated areas for coordinated lice plans and zones for coordinated fallowing (2010) have followed. There is both national

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and international pressure to protect wild salmon and wild sea trout and the salmon lice issue has to be taken seriously. The Norwegian government by the Ministry of Fisheries and Coastal Affairs have a strategy for an environmentally sustainable aquaculture industry and name disease, including salmon lice, as one of five key issues to be addressed. The other four are (1) organic pollution, (2) escapees, (3) use of area, and (4) use of feed from a marine source.

References Andersen, P. 1993. Bekjempning av lakselus. Norsk Fiskeoppdrett 32–33. Anonymous. 1974. Law on animal welfare LOV-1974–12-20–73. Anonymous. 1999. Til laks ˚at alle kan ingen gjera? Om ˚arsaker til nedgang i de norske villaksbestandene og forslag til strategier og tiltak for ˚a bedre situasjonen. NOU, Oslo, Norway, 297 p. Anonymous. 2000. Betamax vet. (50mg/ml) preparatomtale. ScannVacc AS. Anonymous. 2002. Betamax vet. Praktisk Brukermanual. ScanVacc AS. Anonymous. 2003. Guidance Notes for the use of SLICE in Aquaculture. Technical Report Vol. 1. Schering-Plough Animal Health. Anonymous. 2005. The Aquaculture Act. Norwegian Ministry of Fisheries and Coastal Affairs. Anonymous. 2007a. Praktiske r˚ ad SLICE. Schering-Plough Animal Health. Anonymous. 2007b. Package leaflet, Alphmax 10mg/ml. Pharmaq AS. Anonymous. 2008. Facts about fisheries and aquaculture, 2008. Norwegian Ministry of Fisheries and Coastal Affairs. Berland, B. and Margolis, L. 1983. The early history of “lakselus” and some nomenclatural questions relating to copepod parasites of salmon. Sarsia 68: 281–288. Birkeland, K. 1996. Salmon lice, Lepeophtheirus salmonis Krøyer, infestations and implications for anadromous brown trout, Salmo trutta L. University of Bergen, Bergen, Norway, 20 p. Birkeland, K. and Jakobsen, P.J. 1997. Salmon lice, Lepeophtheirus salmonis, infestation as a causal agent of premature return to rivers and estuaries by sea trout, Salmo trutta, juveniles. Environmental Biology of Fishes 49: 129–137. Bjøru, B., Aunsmo, A., Moen, V., and Markussen, T. 2004. Evaluering av badebehandlingsmetodikk mot lus i oppdrettsanlegg. VESO Trondheim, Rapport 1–2004. Bjørn, P.A. and Finstad, B. 1997. The physiological effects of salmon lice infections on sea trout post smolts. Nordic Journal of Freshwater Research 73: 60–72. Bjørn, P.A. and Finstad, B. 2002. Salmon lice, Lepeophtheirus salmonis (Kroyer), infestation in sympatric populations of Arctic Charr, Salvelinus alpinus (L.), and sea trout, Salmo trutta (L.), in areas near and distant from salmon farms. ICES Journal of Marine Science 59: 131–139. Brandal, P.O. and Egidius, E. 1977. Preliminary report on oral treatment against salmon lice, Lepeophtheirus salmonis, with Neguvon. Aquaculture 10: 177–178. Brandal, P.O. and Egidius, E. 1979. Treatment of salmon lice, (Lepeophtheirus salmonis, Krøyer 1838) with Neguvon – Description of method and equipment. Aquaculture 18: 183–188. Directorate of Fisheries. 2008. Available at http://www.fiskeridir.no/fiskeridirektoratetsstatistikkbank. (Last accessed date July 2010). Eithun, I., Gullaksen, A.S., Baarøy, V., Lyngøy, C., Løvold, T., and Mo, M.A.C. 1997. Nasjonal handlingsplan mot lus p˚a laksefisk – 1997–2001. Statens dyrehelsetilsyn o.a., Oslo, Norway, 19 p. Eithun, I., Gullaksen, A.S., Baarøy, V., Jensen, F., Postmyr, E., and Mo, M. 1999. Nasjonal handlingsplan mot lus p˚a laksefisk. Resultatrapport 1998 Revidererte m˚al for perioden 1999–2001. Statens Dyrehelsetilsyn, Oslo, Norway, 59 p. Fallang, A., Ramsay, J.M., Sevatdal, S., Burka, J.F., Jewess, P., Hammell, K.L., and Horsberg, T.E. 2004. Evidence for occurrence of an organophosphate-resistant type of

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acetylcholinesterase in strains of sea lice (Lepeophtheirus salmonis Kroyer). Pest Management Science 60: 1163–1170. Finstad, B., Boxaspen, K.K., Asplin, L., and Skaala, Ø. 2007. Lakselusinteraksjoner mellom oppdrettsfisk og villfisk – Hardangerfjorden som et modellomr˚ade. In: Kyst og havbruk (eds E. Dahl, P.K. Hansen, T. Haug, and Karlsen), pp. 69–73. Institute of Marine Research, Bergen, Norway. Finstad, B., Økland, F., Boxaspen, K., Asplin, L., Skaala, Ø., Bjørn, P.A., Olsen, R.S., Ritchie, G., Heuch, P.A., and Kvenseth, P. 2008. The Hardanger fjord project. Final report to Norwegian research council. NINA, Trondheim, Norway. Grimnes, A. and Jakobsen, P.J. 1996. The physiological effects of salmon lice infestations on post smolt of Atlantic salmon. Journal of Fish Biology 48: 1179–1194. Heuch, P.A. and Mo, T.A. 2001. A model of salmon louse production in Norway: effects of increasing salmon production and public management measures. Diseases of Aquatic Organisms 45: 145–152. Heuch, P.A., Bjørn, P.A., Finstad, B., Holst, J.C., Asplin, L., and Nilsen, F. 2005. A review of the Norwegian ‘national action plan against salmon lice on salmonids’: the effect on wild salmonids. Aquaculture 246: 79–92. Jensen, P.E, Jensen, F., Gullaksen, A.S., Postmyr, E., Baarøy, V., and Mo, M.A.C. 2002. Nasjonal handlingsplan mot lus p˚a laksefisk. Resultatrapport 2000 og 2001. Statens dyrehelsetilsyn o.a., Oslo, Norway, 67 p. Jøssund, T.B. 1994. Effekt av pyretrum og hydrogenperoksyd ved v˚aravlusning. Akvavet 3: 18–22. Koren, C. 2001. Lus p˚a oppdrettsfisk fra omr˚adet fra Lofoten til Vest-Finnmark 1998–2000. Report to Fiskehelse og Miljøgruppa i Troms. Fiskehelse Nord AS, Tromsø, Norway. Kryvi, H., Bergan, P.I., Løvold, T., Baarøy, V., Eithun, I., Binde, M., Espeland, E., Maroni, K., Lyngøy, C., and Vannebo, H. 1996. Forslag til Nasjonal handlingsplan mot lus p˚a laksefisk. Statens dyrehelsetilsyn o.a., Oslo, Norway, 27 p. Møller, D. 1990. LENKA landsomfattende egnethetsvurdering av den norske kystsonen og vassdragene for akvakultur. NOU (Norwegian Official report series). Ministry of Fisheries, Oslo, Norway, 144 p. The Norwegian Institute of Public Health. 2008. Available at http://www.fhi.no/eway/. (Last accessed date July 2010). Olsen, R.S. 2006. Prosjekt vinteravlusning i Hardangerfjorden 2005/06. Hardanger Fiskehelsenettverk, Eikelandsosen, Norway, 4 p. Olsen, R.S., Malkenes, R.H., and Jensen, F. 2005. Prosjekt vinteravlusning i Hardangerfjorden 2004/05. Prosjektrapport. Hardanger Fiskehelse Nettverk, Eikelandsosen, Norway, 17 p. Pike, A.W. and Wadsworth, S.L. 1999. Sea lice on salmonids: Their biology and control. Advances in Parasitology 44: 234–337. Raynard, R., Wahli, T., Vatsos, I., and Mortensen, S. 2007. Review of disease interactions and pathogen exchange between farmed and wild finfish and shellfish in Europe. Veterinaermedisinsk oppdragssenter AS, Namsos, Norway, 459 p. Romstad, S. 2004. Lakselusbekjempelse i Namsosdistriktet: Avlus p˚a lave niv˚aer. Norsk Fiskeoppdrett 29: 64–66. Rudi, H. and Villabø, M. 1994. Otimal lokalisering, strukturering og drift av matfiskanlegg. Marintek, Trondheim, Norway, 73 p. Sayer, M.D.J., Treasurer, J.W., and Costello, M.J. 1996. Wrasse: Biology and use in aquaculture. Ames Fishing News Books, Blackwell Science Ltd. Oxford, United Kingdom. Thomassen, J.M. 1993. A new method for control of salmon lice. In: Fish Farming Technology (eds H. Reinertsen, T. Dahle, L. Jørgensen, and K. Tvinnereim), pp. 233–236. Balkema, Rotterdam, Netherland.

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Chapter 6

Ireland: The Development of Sea Lice Management Methods David Jackson

Introduction Historically, sea lice on salmon offered for sale were considered as a sign of fresh run fish. The louse was the salmon louse (Lepeophtheirus salmonis) and normally the life stage was the adult female or the adult male. As reported in other chapters (see the introductory chapter contributed by Hayward et al.), sea lice are obligate ectoparasites of fish. The salmon louse L. salmonis is endemic in Irish waters and indeed throughout the North Atlantic where salmonids occur. In general, lice infestation on salmon was only noticed by anglers and those involved in the catching, sale, and handling of salmon for human consumption. Lice levels on wild Atlantic salmon off the Irish coast are significant, with normal prevalences in excess of 90% and intensities of 12–13 lice per fish (Copley et al. 2005). Intensities of 20 lice per fish or more are not that uncommon. As salmon farming developed in Ireland, infestations with salmon lice on the farmed stock quickly became an issue as is described in other chapters of this book. The source of infection was the reservoir of parasites in the migratory stocks of wild salmonids around our coasts. The pursuit of effective control measures to reduce, eliminate, and control lice infestations on farmed salmon off the Irish coast is a complex story involving science, national monitoring programs, cooperative management initiatives, and regulation. There are three distinct regions in Ireland where salmon farming is carried out: (1) the West (Counties Galway and Mayo), (2) the Northwest (County Donegal), and (3) the Southwest (Counties Cork and Kerry). These regions are all located on Ireland’s Western Atlantic coast (Figure 6.1) and comprise peripheral nonurban coastal communities, which in the past have been affected by high levels of emigration and classified as disadvantaged areas. They are also areas of high scenic amenity that support a significant tourist industry. The regions are geographically separate from each other. There is a distance of over 160 km between the northwest and western regions and some 200 km between the west and southwestern regions. In total, there are approximately 50 sites licensed to farm salmonids. Two species are farmed, (1) the Atlantic salmon (Salmo salar L.) and (2) rainbow trout (Oncorhynchus mykiss (Walbaum)). In the early stages of the development of the industry, there was considerable debate as to which species would Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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(A)

(B)

Figure 6.1. Salmon farm sites in (A) the Northwest, (B) Mayo and north Connemara, (C) south Connemara, and (D) the southwest of Ireland.

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(C)

(D)

Figure 6.1. (Continued)

be more suitable to farm. Atlantic salmon won out eventually as their survival at sea in full-strength seawater was better and they fetched a higher price. Today, Atlantic salmon accounts for the vast majority of Irish finfish production with sea-reared rainbow trout stocked at just three sites in 2007 (O’Donohoe et al. 2008). Since initial trials in the early 1970s, the Irish salmon farming industry has grown to become a significant contributor to the economies of the local coastal communities. In fact, in the Gaeltacht (Gaelic speaking) community of south Connemara, County Galway, the aquaculture industry was identified as the single most significant factor contributing to stability and growth (White and Costelloe 1999) in the local community. The stability and viability of these communities now rely on aquaculture. The most important benefits are employment, additional income, increased business to

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local service providers, and reduction in local emigration. Indirect benefits identified include improvements in infrastructure and increased community cohesion. The full-scale commercial farming of salmon started in or around 1978. In 1980, the production of farmed salmon was approximately 350 tons with a value of around €2.6 million. Farmed fish (Atlantic salmon and rainbow trout) production in Ireland grew steadily throughout the 1990s and by 2001 was as high as 24,000 tons but declined to about 12,000 tons with a value in excess of €55 million at point of first sale (wholesale value, not including any value-added processing) in 2006 (Browne et al. 2007). Today, the Irish aquaculture industry provides full-time and part-time employment for about 2000 people and the value of production in 2007 was €131 million. Farming of salmonids in Irish seas in 2007 produced approximately 13,800 tons. Although salmon farming is a major contributor to the sustainability of peripheral coastal communities on Ireland’s west coast, including culturally important Gaeltacht communities, by international standards, the output of the Irish industry is tiny. In 2006, the two main producers of farmed salmon worldwide, Norway and Chile, produced 670,000 tons round weight equivalent (RWE) and 660,000 tons RWE, respectively. Scotland, the other European Union producer of farmed salmon and Ireland’s nearest neighbor, had a production of some 150,000 tons RWE in 2006. The Irish production of farmed salmon is less than one-tenth of the production of the European Union and less than 1% of global production. One of the greatest challenges facing Irish salmon farming is sea lice infestation. Two species of sea lice found on cultured salmonids in Ireland are Caligus elongatus (Nordmann) and L. salmonis (Krøyer). These species of sea lice and sea lice in general are regarded by many as having the most commercially damaging effect on cultured salmon in the world with major economic losses to the fish farming community resulting per annum (Bristow and Berland 1991; Jackson and Costello 1991). They affect salmon in a variety of ways: mainly by reducing fish growth, loss of scales that leaves the fish open to secondary infections (Wootten et al. 1982), and damaging of fish that reduces marketability. The pattern of infestation of C. elongatus on farmed salmonids in Ireland is that of an opportunistic parasite that occurs sporadically (Jackson et al. 2000a). C. elongatus is more common at oceanic sites with consistently high salinity. Higher infestation levels with this species are recorded particularly where shoals of commercially important pelagic teleosts such as herring and mackerel regularly occur. L. salmonis is regarded as the more serious parasite of the two species and has been found to occur most frequently on farmed salmon (Jackson and Minchin 1993a). As described in the introductory chapter contributed by Hayward et al., most of the damage caused by these parasites is thought to be mechanical, carried out during the course of attachment and feeding (Kabata 1974; Brandal et al. 1976; Jones et al. 1990). Inflammation and hyperplasia (enlargement caused by an abnormal increase in the number of cells in an organ or tissue) have been recorded in Atlantic salmon in response to infections with L. salmonis (Jones et al. 1990; Jonsdottir et al. 1992; Nolan et al. 2000). Increases in stress hormones caused by sea lice infestations have been suggested to increase the susceptibility of fish to infectious diseases (MacKinnon 1998). Severe erosion around the head caused by heavy infestations of L. salmonis has been recorded previously (Pike 1989; Berland 1993). This is thought to occur because of the rich supply of mucus secreted by mucous cell-lined ducts in that region (Nolan et al. 1999). As a consequence of sea lice infestation, there is mortality in farmed

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salmon in Ireland (Jackson and Minchin 1993a; Wheatley et al. 1995; O’Donohoe et al. 2008). In addition, sublethal effects including reduced growth rate (Jackson and Minchin 1992), external damage to the fish resulting in downgrading of product at harvest, and reduced FCR levels have major negative economic implications.

The National Monitoring Programme In the 1980s, there was only one licensed sea lice treatment for use on farmed fish R . in Ireland, dichlorvos (Jackson and Costello 1991) marketed as Nuvan 500EC Dichlorvos, an organophosphate, was used as a bath treatment at a concentration of 1 ppm of active ingredient for 30–60 minutes. The half-life of dichlorvos in seawater is from 4–7 days and because of this short half-life and the fact that it is metabolized to harmless breakdown products in living systems, dichlorvos does not bioaccumulate or biomagnify (WHO 1989). There were numerous studies showing its safety to nontarget organisms (McHenery 1990; McHenery et al. 1991; Cusack and Johnson 1990). However, there were many factors limiting the efficacy of this product as a treatment for sea lice infestation. Treatments were labor intensive and could only be carried out at slack water. Treatments had reduced efficacy below a water temperature of 8◦ C, thus making winter treatments difficult. The treatments were quite stressful to the salmon, particularly during periods of high water temperature and were only effective against adult and subadult lice. Any of the juveniles attached by a frontal filament R remained unaffected. There were also signs of emerging resistance to Nuvan 500EC in certain lice populations (Jackson and Costello 1991; Tully and McFadden 2000). In practice, it was not possible to get a complete clearance of sea lice infestation at R treatments. As the active a site even by the application of a series of Nuvan 500EC ingredient is an acetylcholinesterase inhibitor, there were also worker safety issues and workers handling the concentrate were required to wear protective clothing and a respirator. The combined impact of these shortcomings in the only available treatment meant that effective control of lice infestations was difficult. By 1991, there was considerable pressure to develop alternative treatments that would be effective against all stages of lice, easier to apply, and safer to use both in terms of effects on salmon and worker safety. There were occasional problems with C. elongatus; however, the main problems were related to infestations with L. salmonis (Jackson and Minchin 1992). There were a number of different concerns raised about the control of sea lice on farmed salmonids by a range of people representing different interest groups. Firstly, the farmers were having extreme difficulty controlling infestations and were concerned with financial losses and lost stock. Secondly, environmental groups were expressing disquiet at the possible negative impact of dichlorvos in the marine environment (Ross 1989; Jackson and Costello 1991). Finally, conservation interests became concerned about the possible impacts of lice emanating from salmon farms on wild salmonids. In response to these concerns, the Department of Marine and Natural Resources initiated a monitoring program to investigate lice infestation levels on salmonid farms in April–May 1991 (Jackson et al. 1997). Initially, the objective of the monitoring was to obtain an accurate and objective assessment of infestation levels on farms and to investigate the nature of these infestations with a view to developing an appropriate

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management response. The results of these initial investigations were published in 1993 (Jackson and Minchin 1993a) and used to develop a management strategy. Monitoring was established to provide an objective measurement of infestation levels on the farms, to investigate the nature of the infestations, and to facilitate development and refinement of management strategies (Department of the Marine and Natural Resources 2000). On the basis of the results from the early surveys, new management practices were put in place by the Department of the Marine and Natural Resources. The scope of the monitoring program was expanded in subsequent years and by 1993 there was a national monitoring program in place covering all licensed salmon farms in Ireland. Since April 1994, monitoring has been carried out in line with the Monitoring Protocol for Offshore Finfish Farms No. 3—Sea Lice Monitoring and Control (Department of the Marine and Natural Resources 2000). The national sea lice monitoring program involves the inspection and sampling of each year class of fish at all fish farm sites 14 times per annum—twice per month during March, April, and May, and monthly for the remainder of the year except December–January. Only one inspection is carried out during this period. In the early phases, the level of lice per fish that would trigger the need for treatment was set at a level of 2.0 egg-bearing females or ovigerous lice per fish during the spring period from March–May. These trigger levels were effective in reducing lice infestations. However, over the years, as the monitoring and control program has been developed and enhanced and new methods of control have been developed, the trigger levels have been modified to include reduced levels in the spring period and a level of 2.0 ovigerous lice per fish for the remainder of the year. In 2000, the monitoring regime was formally adopted as one of a number of Monitoring Protocols to which all salmon farmers are required to adhere. The inspections are carried out directly by the Marine Institute (MI, a statutory state agency). The program is applied at all marine finfish farms regardless of whether the licensee, through the terms and conditions of its license, is subject to the terms of the Protocol or not. The cooperation of the industry in both facilitating the sampling and in implementing the directions and advice given on the basis of the monitoring results has been a key factor in the successful implementation of sea lice control on Irish farms (Jackson et al. 2002). Lice levels are determined from the sampling process and measured against target levels set out in the protocol or in certain cases in individual licenses. The spring period (March–May) targets are now set at very rigorous levels of 0.3–0.5 egg-bearing (ovigerous) lice per fish. Outside of this time period, a level of 2.0 egg-bearing lice acts as the trigger for treatment. Where measurements at a farm exceed these target levels a “Notice to Treat” is issued to the licensee. Results are reported to farms within 5 working days of the inspection, together with appropriate advice to help manage infestation levels. Monthly reports are compiled for each site of mean numbers of egg-bearing lice and total mobile lice of each species. These reports are circulated to the farms, the Department, and the other stakeholders including the MI, the Central Fisheries Board, the Regional Fisheries Boards, the Irish Salmon Growers’ Association, Save Our Seatrout (a nongovernmental organization representing angling interests), and the Western Gamefishing Association. This ensures that real-time information on the levels on farms is available to all interested parties. These reports are designed to give a clear, unambiguous measure of the infestation level at each site and to act as a basis for management decisions. The sampling strategy and methodology employed in the national monitoring program

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is designed to provide a robust and reliable objective measure of lice numbers on farmed fish while operating within a framework that is cost-effective and capable of being carried out over the range of installations that are in use in offshore farming. The strategy also has to take account of variable weather conditions, fish health issues, environmental effects, and animal welfare considerations. There are four key components to this sampling strategy: (1) the sampling method, (2) the sampling frequency, (3) the sample size, and (4) reporting mechanisms. The full methodology has been described in numerous publications and reports including O’Donohoe et al. (2007). It is essentially a nondestructive sampling method. Fish are removed at random from the cages and anesthetized to reduce stress and risk of injury. All adult and subadult mobile lice are then removed from the fish and retained for examination before the fish are allowed to recover and returned to the cage. Lice that become detached from the fish in the anesthetic are collected and included in the lice count for the sample to ensure that lice numbers are not underreported. As it involves the handling of live animals and as there are animal welfare issues involved, the sampling process is subject to peer review and a licensing process. Strict limits are imposed on the number of fish that may be sampled and changes to these limits must be justified. The sampling frequency, as has already been mentioned, is 14 inspections per year. In addition, there may be follow-up inspections required where instructions to reduce lice levels have been issued or for such other reasons as may be determined by the Department or its agent. The target number of fish sampled is 60 per inspection, comprising two samples of 30 fish. One sample is taken from a standard cage, inspected at each inspection, and one from a cage selected at random. Where there are difficulties in obtaining the full sample size, every effort is made to obtain a minimum of ten fish in each sample. This sample size is statistically robust and also takes into consideration the practicalities and animal welfare issues involved in carrying out the program. The standard cage allows for the monitoring of within-cage trends, the effectiveness of treatment strategies, and provides a good indication on trends in the development of infestation parameters at the site. The sampling of a random cage acts as a spot check on lice levels elsewhere at the site. In addition to the reports to the farm and the circulation of a monthly report on lice levels, each year, the results of the National Survey of Sea lice on Fish Farms is published as a report in the Irish Fisheries Bulletin series. These reports contain all the data, information on trends and treatment strategies, and details of the farm sites. They are available both as hard copy and in PDF format on the MI Web site (www.marine.ie).

Research into Factors Affecting Lice Infestation Preliminary research into the nature of infestations on farms pointed to a cycle of reinfestation within farmed sites. The results of monitoring in 1991 and 1992 showed that lice infestation on two-sea-winter salmon was significantly higher than that on one-sea-winter fish (Jackson and Minchin 1993b). The levels of ovigerous lice on twosea-winter fish were a reservoir for cross-infestation of one-sea-winter fish and smolts on multigeneration sites. The need to reduce both vertical and lateral transmission of lice infestation within farm sites was identified as a key to maintaining effective control

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of sea lice and in particular the salmon louse L. salmonis. Even where lice management strategies and treatment regimes were in place, the progression in infestation level for a given generation of fish was found to be remarkably stable for individual sites (Jackson et al. 2000b) with a trend to increasing levels of infestation with time at sea. In order to address these issues both changes in husbandry practices and treatment regimes were required. To break the cycle of infestation within a farm site, it was necessary to clear both the existing infestation and prevent recruitment of a new generation of parasites. The only R , was not effective against juvenile lice and had available treatment, Nuvan 500EC to be administered as a bath treatment to individual cages at slack water. This meant that treating a whole site quickly in order to clear it of infestation was very difficult and preventing reinfestation was impossible. In the late 1980s, the Fish Disease Group in University College Galway began looking for potential treatments, which could be incorporated into the fish feed, thus allowing strategic treatments of whole sites to be effectively undertaken. Preliminary trials on ivermectin, a drug already widely used to control parasites in cattle and other food animals, were very promising (Palmer et al. 1987). Ivermectin proved to be extremely efficient at controlling lice infestation, allowing lice infestation levels to be reduced by over 90% with suitable treatment regimes (Smith et al. 1993). Environmental studies (Costelloe et al. 1993) carried out on the benthos showed no adverse impacts of ivermectin therapy even in highly sensitive polychaete species. Developments in EU legislation in 1990 allowed for the limited use of veterinary medicines in species and for conditions other than those for which the marketing authorization were granted, generally known as “off-label” use. The off-label use of veterinary medicines under this legislation is often termed “the cascade.” The “cascade” governs the circumstances under which the off-label use of a veterinary medicine is permissible. There are a number of important conditions in these regulations. The animals must be under the care of a veterinary surgeon who may, in the absence of an effective licensed remedy, prescribe an alternative treatment that is authorized for use in other food producing animals. The prescribing vet must specify a withdrawal period to ensure that the food produced does not contain residues, which may be harmful to consumers. If there is no withdrawal period specified for the product, then, in fish, a mandatory withdrawal period of 500-degree days is laid down in the regulations. During the 1990s, the use of ivermectin to control sea lice in farmed salmon, under the cascade principle, was a common practice in Ireland. Because of the long withdrawal period, which in many cases was extended by farmers who operated to a zero residue policy in harvested fish, ivermectin was principally used to control infestation levels in smolts and during the first year at sea. Ivermectin was extremely effective as a sea lice treatment and its use revolutionized lice control on Irish salmon farms by making possible a much more strategic approach. The use of ivermectin to control sea lice infestations on Irish salmon farms continued until the licensing of a number of other preparations that were added to feed for sea lice control rendered its use under the “cascade” no longer permissible. With the development of treatment regimes, the effective control of lice on individual sites became possible. Single generation sites that were fallowed annually for a minimum period of 1 month at the end of each production cycle became standard practice with separate sites used to hold smolts and growers. It became apparent that single generation sites not only assisted in reducing lice infestation, they also showed reduced incidence of other diseases (Jackson et al. 1997).

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There were also site-specific effects with offshore sites that had strong currents (high energy sites) appearing to have a lower transmission rates within the site. At inshore sites, good lice control was also possible at single generation sites where fallowing was practiced. As lice infestation levels fell on farmed salmon, other factors affecting the level of infestation became apparent. At a number of sites, infestation pressure consistent with cross-infection from wild salmonids was observed (Jackson et al. 1997). In a number of instances, early infestation of newly stocked smolts with L. salmonis in sites that have been fallow for several months have been postulated as being as a result of cross-infestation from wild salmonid populations where local populations of salmon or sea trout are known to occur. At sites that were restocked with smolts after a significant fallow period and where there is a known local population of salmonids within the bay, reinfestation occurred surprisingly quickly (Table 6.1). At the site in McSwynes Bay, which does not have a significant population of wild salmonids within the bay, reinfestation occurred much more slowly. The site showing the highest levels Table 6.1. L. salmonis on smolts after a fallow period. The Gurrig, Kilkieran Bay Date

20/12/07

21/1/08

5/2/08

11/2/08

19/2/08

5/3/08

20/3/08

3/4/08

Total Lepeophtheirus

4.28

3.95

7.51

6.71

6.20

2.78

2.93

4.84

Fallow since August 2003. Fish inputted November 2007. Nearest site—Lettercallow, 3 miles, three other sites within 7 miles. Fraochoilean, Ballinakill Bay Date

9/12/03

22/1/04

24/2/04

3/3/04

19/3/04

1/4/04

26/4/04

7/5/04

25/5/04

Total Lepeophtheirus

0.00

0.15

0.06

0.03

0.05

0.03

2.18

2.01

1.35

Fallow since July 2001. Fish inputted November 2002. Nearest site—Inishdeighil, over 9 miles. Salt point, Bertraghboy Bay Date

13/12/02

17/1/03

26/2/03

28/3/03

10/4/03

25/4/03

9/5/03

Total Lepeophtheirus

0.09

0.02

0.00

3.32

1.66

0.35

0.03

Fallow from May 2002. Fish inputted. ∼1 November 2002. Nearest site—Ardmore, 13 miles. McSwyne’s, Donegal Bay Date

26/3/07

10/4/07

24/4/07

9/5/07

23/5/07

22/6/07

24/7/07

9/8/07

26/9/07

Total Lepeophtheirus

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.21

Fallow from March 2003. Fish inputted mid-February 2007. Nearest site—Eany, 11 miles.

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of early infestation is in a bay with both wild salmonids and other salmon farming sites, Kilkieran Bay (Figure 6.1). While there was a good understanding of the dynamics of lice infestation within a site, there were and still remain considerable gaps in our understanding of how the planktonic larvae of L. salmonis spread from site to site. Work by Costelloe et al. (1995) and O’Donohoe et al. (1995) pointed to pulses of settlement rather than an even infestation pressure and investigated factors such as vertical migrations of planktonic lice larvae and the linkage of maximum larval densities with lunar cycles. Research carried out on somatic size and egg string length (Jackson et al. 2000b) also pointed to a spring maximum in infestation pressure. This was consistent with the finding of the National Sea Lice Monitoring Programme and also borne out by the experience of individual farmers. It was becoming clear that to manage lice infestation effectively would require more than the separation of generations and the management of lice on individual sites.

The Development of Bay Management From 1993, a program of bay-wide management was developed and put in place. The initiative was called Single Bay Management (SBM). This management strategy was endorsed by the Department of the Marine and Natural Resources and the Irish Salmon Growers Association as fundamental to the rational management of the salmon farming industry. Bay management is also described in a number of chapters in this book. Single Bay Management arrangements for finfish farms were designed to coordinate husbandry practices in such a way that on individual farms best practice is followed and that stocking, fallowing, and treatment regimes on individual farms were compatible with the arrangements on neighboring farms. The goal was to ensure that practices on individual farms act synergistically to enhance the beneficial effects to the bay as a whole. A major component in this process was the build up of a communication network between the operators. The nonconfrontational environment of SBM meetings between licensed operators proved a valuable forum in the process of conflict resolution and avoidance both within and between the industry and its neighbors. The SBM process proved very effective in enhancing the efficacy of lice control and in reducing the overall incidence of disease in the stocks. Single Bay Management plans are subject to revision for each production cycle. This is necessary to take account of changes in production plans related to new license applications, the need to respond to changing markets emerging and new husbandry requirements, and both internal company restructuring and intercompany agreements. The individual plans were tailored to the needs of each bay but the fundamental principles were common across all plans in the initiative. Each plan set out to formalize the arrangements across all fish farming sites in a bay. In order to achieve this, formal structures for exchange of information and coordination of action between fish farmers were set up. These provided a forum for regular, two-way, exchange of information between fish farmers, fishery owners/Regional Fishery Boards, and other users of the bays. A code of practice covering a range of fish husbandry practices was agreed for each bay. This covered set fallowing periods for each production site in the bay, ensuring that adjacent sites are fallowed synchronously for a period of

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at least 1 month. It also ensured that all stock for aquaculture and fisheries management purposes was disease free and only introduced in accordance with accepted protocols and regulations. The exchange of information among fish farmers regarding disease, lice treatments, and their coordination and other husbandry matters was considered a key to the success of any bay management plan. This information was channeled through facilitators selected by the farmers to be responsible for the organizing of regular meetings and the dissemination of information between meetings. For each bay a regional group was established to develop the Single Bay Management Plan. This group was also the forum for discussion of proposed modifications to the plan. The SBM process allowed for the development of the concept of strategic treatments on a bay-wide basis to target the pulse of infestation identified as occurring in the spring as water temperatures rose. It also allowed such strategic treatments to be timed to occur after all two-sea-winter fish had been harvested out of the area, thus enhancing the impact of the treatment and contributing to a more complete break in the cycle of infestation. The major impact of these practices on lice infestation levels on Irish salmon farms was reported on in Jackson et al. (1997) and detailed case studies of the impacts of SBM processes in Killary Harbour and Kilkieran Bay were presented in Jackson et al. (2002). Significant and sustained improvements in lice control on farmed fish were achieved. The level of complexity involved in developing a workable SBM production schedule is quite significant and in practice the ideals of single generation sites and fallowing before restocking are not always achieved. An example covering the years 2004–2006 illustrates a SBM production schedule similar to those included in the plans developed for each bay (Figure 6.2). The proposed schedule, in this case, covers the stocking and grow-out plans for four sites within a bay and allows for separation of generations and a minimum fallowing period of 1 month, and sometimes considerably in excess of this, at each site before restocking. The proposed plan was consistent with best practice. In fact, the company ended up overlapping production on both of its on-growing sites by stocking them with a new input of autumn smolts (S 1/2) for commercial reasons before the previous generation was complete. Unfortunately, this

SINGLE BAY MANAGEMENT PLAN

SITE SITE 1: Proposed SITE 1: Actual SITE 2 ongrowing: Proposed SITE 2 ongrowing: Actual

These four sites are run by the same company. Top lines represent submitted production plans, bottom line is actual production.

2004 2005 2006 J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D 04 06 05 S1/2 04 06 S 1/2 04 04

03 03

05 SITE 3 harvesting: Proposed SITE 3 harvesting: Actual SITE 4 ongrowing: Proposed SITE 4 ongrowing: Actual = Fallow period

06

05 05 S1/2

03 03

Ovelapping generations due to: -late tranfer of all 04 stock -input of 05 S1/2 and 05 S1s

04

05 05

04 04 S1/2 04 S1/2

- transfer of 05 S1/2 before 04s harvested - input of 06 S1/2 with previous generation

05 S1/2 05 S1/2 06 S1/2

Figure 6.2. Example of a Single Bay Management Plan. S1, smolts in spring of second year; S1/2, smolts in autumn/winter of first year.

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allowed for vertical transmission of sea lice infestation from the older fish to the newly stocked smolts. The methodology for sea lice management has been progressively developed as a result of experience gained in operating the sea lice monitoring program and the bay management program, and based on the results of research carried out by the team at the MI. Currently, it can be summarized in seven principles of best practice (see Box 6.1). These principles are similar to methodologies described in other chapters in this book. Experience has shown that a combination of these principles allows for optimal control of lice infestation; and where one or more of the principles breaks down, difficulties in maintaining control of lice infestation can be experienced.

Box 6.1 The Seven Principles for Sea Lice Management 1. Complete separation of generations. For sites to be considered separate, they must be at least one tidal excursion apart. A tidal excursion is defined as the distance a body of water will travel over a full tidal cycle. 2. Each site to be fallowed annually, or at end of a production cycle, for 1 month (30 days) before restocking. All sites within one tidal excursion need to be fallowed synchronously for a period of at least a month. 3. Annual synchronous “winter” lice treatment for all adjacent sites. Again, “adjacent sites” are less than one tidal excursion apart. This is intended to eliminate overwintering ovigerous females before rising water temperatures accelerate larval development, giving rise to the observed pulse of infestation with juvenile lice in the spring, and thus reduce or eliminate this pulse in infestation pressure. 4. Planned rotation of sea lice treatments over the production cycle. This is to avoid using the same treatment repeatedly on lice, which are potentially survivors of a previous treatment. For this reason it is important that adjacent sites use the same product rotation. 5. Treatment triggers during the spring period should be set at a level of 0.5 eggbearing females per fish. For the rest of the year, the treatment trigger level should be set at 2.0 egg-bearing lice. 6. Experience has shown that all principles need to be set out as part of formal signed Single Bay Management Agreement. 7. Where there is a persistent problem with sea lice control, there is a need for an incremental series of actions up to and including mandatory treatments and other sanctions.

Developments in Treatment Strategies There is a large reservoir of L. salmonis infecting wild salmonids. These wild fish move freely in the same water in which salmon are farmed. For this reason, it is not possible to eradicate L. salmonis. The parasite therefore has to be managed and controlled on farmed salmonids for the foreseeable future. In the absence of an effective vaccine, this control has to be maintained by a combination of husbandry and

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appropriate treatments. Over the years, a variety of treatment types have been used in the struggle to manage lice infestation on Irish farmed salmon. These treatments can be loosely categorized into a number of groups: animal medicines, biological controls, disinfection procedures, immunostimulants, and “alternative” treatments. Treatments specific to other regions are included in other chapters (see Chapter 3 contributed by Chang et al. for New Brunswick Canada, Chapter 5 contributed by Ritchie and Boxaspen for Norway, see Chapter 7 contributed by Revie for Scotland, and see Chapter 8 contributed by Saksida et al. for British Columbia Canada) of this volume. The animal medicines can be further divided on the basis of their method of application. There are two application methods, either the fish are placed in a bath in an enclosed bag or container, or the medicine is applied in feed. Treatments through food have a number of major advantages over bath treatments in terms of their application to sea-reared salmonids. These would include ease of application and the ability to treat in marginal weather conditions and at all stages of the tide. In-feed treatments also avoid the stress to fish associated with enclosing nets in skirts or covers and reducing their volume to facilitate bath treatments. Without a doubt their biggest single advantage in terms of lice management is that they can be used to treat large numbers of fish in a variety of cages and on different sites synchronously. This ability to treat whole populations of fish synchronously makes them invaluable for the carrying out of strategic treatments to break cycles of infestation. Their one major drawback from an efficacy point of view is that where fish are not feeding optimally there is a risk of underdosing and achieving poor clearances. Because of the advantages listed previously, there is a tendency for farmers to rely heavily on in-feed treatments even where feeding rates of the target fish may be suboptimal. This practice carries with it the risk of poor clearances and an enhanced risk of the emergence of lice populations with reduced sensitivity to the treatment. Bath treatments are normally carried out by raising the net enclosure on a cage and surrounding the net either with a complete bag or with a skirt around the cage and a tarpaulin sheet drawn under the raised net to enclose the bottom. The latter method has the advantage that the bottom tarpaulin can be rapidly removed and the net dropped should it be necessary to end the treatment prematurely for whatever reason. Once the cage is enclosed, the treatment is added to the water so as to give an appropriate concentration of active ingredient in the enclosure. Failure to enclose the cage properly can result in losses of active ingredient; and these losses are accelerated where there is a current. Many reports of ineffective treatment or incomplete clearance have been attributed to either incorrect calculations of the enclosed volume resulting in insufficient dosage or losses through ineffective or incomplete enclosure resulting in dosage levels dropping with time. Because it is a labor-intensive operation, it is normally not possible to treat more than a small number of cages on a slack tide. Up to 30% of Ireland’s fish production takes place at offshore or exposed sites where the cages used are generally quite large circular structures, each containing large numbers of fish (some with up to 100 tons biomass). These sites present particular problems when it comes to bath treatments, both in terms of the technical difficulties of safely enclosing such large cages and in terms of available weather windows suitable to carry out treatments. In recent years, Irish farmers have developed a novel solution to these difficulties. Very large live fish carriers or well boats, normally used for transporting live fish to and from growing sites, are used to carry out treatments.

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As well as providing a technical solution to the carrying out of bath treatments on large cages and exposed sites, there are a number of other significant advantages to the use of well boats. These boats are fully equipped with fish pumps, water circulation pumps, and oxygenation equipment, thus obviating the need for separate provision of these. The cubic capacities of the fish holding wells are known and this assists in determining dose rates. This together with the ability to precisely time the period of treatment by reference to how long the well remains sealed allows for great precision in terms of dosage and duration of treatment. With a suitable well boat it is now possible to carry out a treatment of all fish on a production site in a very short period of time. This mitigates the major drawback with bath treatments heretofore, namely the impossibility of synchronously treating all but the smallest of sites. Various species of wrasse have been used as a biological control method in Ireland and elsewhere. Corkwing (Centrolabrus melops) and goldsinny (Centrolabrus rupestris) wrasse have been successfully used to control lice levels on salmon smolts in Ireland (Deady et al. 1995). The use of these species on larger salmon met with mixed results and the practice of using wrasse as a biological method of control has largely ceased. There were major issues with the availability of suitable wrasse and there were also perceived or real concerns over disease risks. Recently, there has been an initiative to seek to establish cultured stocks of wrasse, which could be used for biological lice control on salmon farms. The cultured wrasse would be maintained under controlled conditions and could be certified as free of all significant diseases prior to stocking, and would also provide a ready supply of wrasse without targeting potentially vulnerable wild stocks. This research is still in its initial stages. Hydrogen peroxide (H2 O2 ) is a powerful oxidizing agent and disinfectant with strong bactericidal properties. It has been used as a delousing agent in the past (Thomassen 1993). Recently, the use of hydrogen peroxide as a disinfectant has recommenced in Ireland. The product is used in well boats as part of treatment procedures. It has been found to be very effective in removing sea lice at low temperatures and is often used as a follow-up to clear any remaining infestation after treatments with a veterinary medicine. It is viewed by many farmers as a valuable aid to lice management, allowing for increased product rotation and thus prolonging the effective life of existing licensed veterinary medicines. R R (a blend of aromatic herbs) or Bio-mos Immunostimulants such as Ecoboost have also been used with varying success to enhance the immune response of the salmon to infestation. Farmers tend to feed immunostimulants to the fish on transfer to sea to boost the immune response of smolts. There have been numerous anecdotal reports of significant delays in the onset of infestation associated with the use of various immunostimulants. Farmers regard these products as a valuable aid to reducing the number of treatments required. As part of the SBM initiative, there has been a strong emphasis on the use of strategic and targeted treatments to control lice and to avoid the unnecessary use of repeat treatments. This approach, which is in-line with the best principles of an integrated pest management strategy, has been promoted through local SBM meetings. Wherever possible, there has been a process of product rotation to ensure there is not an overreliance on one product with the consequent risk of resistance developing in the lice populations. As part of an international research project, which was funded by the EU (Denholm et al. 2002; Sevatdal et al. 2006), appropriate field bioassays were developed for a range of veterinary medicines to support this approach. As part of the

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Table 6.2. Veterinary medicines licensed for use in the control of sea lice infestations on farmed salmon in Ireland. Product

Active ingredient

Usage

SLICE EXCIS CALICIDE ECTOBAN ALPHAMAX

Emamectin benzoate (in feed) Cypermethrin (bath) Teflubenzuron (in feed) Teflubenzuron (in feed) Deltamethrin (bath)

Full marketing authorization Full marketing authorization No longer available Available AR16 (special license) Available AR16 (special license)

national sea lice monitoring and control program, the MI has developed the capability to carry out bioassays to assess the sensitivity of lice populations to all but one of the available veterinary medicines used to treat sea lice infestations in Ireland. Sensitivity bioassays have been carried out regularly on lice populations for the relevant medicines since 2005, as required. A total of 26 lice populations have been assessed for sensitivity to four veterinary medicines over the period from 2004 to 2008. While instances of reduced sensitivity have been detected in individual lice populations, persistent resistance has not been observed to any of the currently licensed veterinary products available to treat sea lice infestations. There is no reason for complacency however; and the continued efficacy of the available products will be dependent on careful product rotation and selection, guided by knowledge of the sensitivity of the lice population, the health status of the fish, and the environment in which it is to be administered. The veterinary medicines currently licensed for use to control sea lice on farmed salmon in Ireland are listed in Table 6.2. There are two in-feed treatments and two bath treatments. One of the widely used treated feeds is a second-generation semisynthetic avermectin (McHenery and Johnson 2002). It has been shown to reduce infestation levels by in excess of 95% on farmed Atlantic salmon smolts (Copley et al. 2007). Maximum clearance, an infestation level of zero, was observed 4 weeks posttreatment and total clearance of lice was maintained for a further 4 weeks after which infestation levels commenced to rise. The second additive to feed is a chitin synthesis inhibitor and is only effective on preadult lice, as it works by disrupting the molting process. It has been used effectively in conjunction with bath treatments as part of a planned treatment strategy. Both bath treatments are pyrethroids (cypermethrin and deltamethrin, respectively). They are effective against all stages of lice and have been deployed very effectively to carry out strategic bay-wide treatments when used in conjunction with well boats.

Recent Results and the Emergence of New Issues and Problems Throughout the course of the monitoring program, there has been a relatively consistent relationship between mean numbers of mobile lice and mean incidence of ovigerous females (Figure 6.3). Results on 13 years of monitoring showed that there was a downward trend in sea lice infestation levels (Jackson et al. 2005) from 1990 to 2003, with the lowest infestation levels being recorded in 2001. The results obtained

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192

1995–2007 30 Mean ovigerous L. salmonis

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y = 0.166x + 0.305 R 2 = 0.681

25 20 15 10 5 0 0

20

40

60

80

100

120

140

180

Mean mobile L. salmonis

Figure 6.3. Relationship of ovigerous L. salmonis and total mobile lice.

from inspections of standard and random cages showed that there was no significant difference in lice levels between them over the years, thus giving confidence that the results from the standard cage were representative of infestation levels on the farms. The results of the national monitoring program for 2005 (O’Donohoe et al. 2006) showed an increase in the mean ovigerous and mean mobile lice levels for May compared to the previous year. Both were the highest mean levels recorded in May for 5 years. A number of reasons were advanced for this increase. These included the following: increased water temperatures, poor clearances following treatment in a number of instances, and incomplete or insufficient fallowing at a number of sites. An additional complicating factor was the occurrence of pancreas disease at many sites. Pancreas disease in its chronic form causes reduced appetite and poor feeding response. This in turn affects the uptake of medicated feed and can have an adverse effect on the efficacy of in-feed sea lice treatments. The increasing trend in average national levels of sea lice infestation was not reflected evenly across the country as can be seen from the mean ovigerous L. salmonis levels for 2005 (Figure 6.4). In the Southwest region, lice levels did not reach treatment trigger levels at any time. In the West, there were elevated lice levels for most of the year with levels rising slowly from March through the summer to a peak in October. Lice levels in the Northwest, by contrast, dropped through the spring and were under control for most of the summer before rising steeply from August to a maximum in November. Failure to implement fallowing plans at a number of sites in the West and Northwest was specifically linked to poor lice control in the discussion of the 2005 sea lice monitoring results (O’Donohoe et al. 2006). It is noteworthy that while pancreas disease was prevalent in sites in the West and Northwest, it was not reported from the Southwest where lice control was good. Sea lice infestation levels rose again in 2006. In 2006, fish health issues together with the effects of high water temperatures and the presence of harmful plankton were all cited as reasons for reduced effectiveness of treatments and reduced efficacy in sea lice control (O’Donohoe et al. 2007). Once again, the issues of incomplete fallowing

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16 14

Mean ovigerous L. salmonis

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Treatment-trigger level

12

Southwest West

10

Northwest

8 6 4 2 0 Jan

Figure 6.4.

Feb

Mar

Apr

May

Jun 2005

Jul

Aug

Sep

Oct

Nov

Mean number of ovigerous L. salmonis per month in 2005.

of sites and the stocking of multiple generations on some sites were identified as factors that contributed to poor lice control. Furthermore, two-sea-winter fish, which as early as 1993 had been identified as a significant reservoir of sea lice contributing to cross-infection of younger year classes (Jackson and Minchin 1993b), were again affecting sea lice development in the salmon production sites. Two-sea-winter fish populations were recorded as late as the end of April. By the completion of the 2007 monitoring program, it was evident that sea lice infestation levels were rising steadily since 2004 and corrective action was required (Figure 6.5), which means that >20 mobile L. salmonis per fish were recorded on 29 inspections in 2007 (O’Donohoe et al. 2008). Sea lice are known to cause damage to fish at these levels (Wootten et al. 1982). The maximum level recorded for an individual site was 142.5 mobile L. salmonis in 2007, compared to a maximum of 85.93 in 2006. The May mean annual trend of infestations with L. salmonis on one-sea-winter fish showed that there was

Treatment-trigger level

Ovigerous sea lice levels nationally (May)

Mean ovigerous sea lice (SE)

3.0

Mean ovigerous L. salmonis

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an increase in both the mean ovigerous levels and mean mobile levels nationally. The mean ovigerous level was the highest since 1992 and the mobile levels were the highest since inspections began. Complicating factors that adversely affected the control of sea lice infestations in 2007 included disease, plankton blooms, and ineffective treatments. Pancreas disease was present on many sites in 2007, which caused difficulties when treating fish for sea lice. The reduced appetite renders in-feed treatments unusable and the poor health status of the fish complicates the administration of bath treatments. Plankton blooms damage fish epithelia and fish gills. This weakens the fish and renders bath treatments more difficult to carry out without incurring mortalities. A variety of treatments were used throughout the country in 2007 with varying results. There were cases where treatment effort did not achieve full clearance of the sea lice and multiple treatments were required. Combinations of two treatments proved effective at some sites. Achieving near-zero sea lice proved very difficult on occasions and this led to population recovery being more rapid and the need for more treatments. Other factors were also identified as contributing to more rapid development of infestations. Increases in water temperature have long been known to accelerate the life cycle of the sea louse and also an increase in reproductive output (Hogans and Trudeau 1989). In the last few years, mean monthly sea temperatures in Ireland have been steadily climbing, with the average sea temperature in 2006 being 1.38◦ C higher than the 30-year mean (worked from source data from Met ´ Eireann—www.met.ie). The monthly mean sea lice figures for 2007 (Figure 6.6) show all three regions as exceeding the treatment trigger levels throughout the spring period (from March to

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Figure 6.6. Mean number of ovigerous L. salmonis by region per month in 2007.

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May inclusive). Outside the spring period, the situation is more variable but toward the latter half of 2007 both the West and Northwest regions exhibited levels generally in excess of treatment triggers. It was noticeable in the results presented on the 2007 monitoring program (O’Donohoe et al. 2008) that higher sea lice infestation levels often occurred prior to harvest. Factors contributing to this increase included fish to fish transfer of lice from harvest fish as they are removed from the system, but also included the fact that some or all cages on site were being left untreated in expectation of harvest. Where harvest was delayed for any reason, such as market trends or weather events, sea lice levels rose very quickly in these cages. Not treating the entire site at the same time can result in a residual sea lice population, which reinfests the other cages and makes clearing sea lice populations hugely problematic. Staggering the treatment of cages on a site can have the same effect and has led to the reinfestation of previously treated cages, from those yet untreated.

The Development of a Strategy for Improved Pest Control on Irish Salmon Farms The persistent difficulty of achieving sea lice control targets at certain sites and in certain bays resulted in a series of meetings and seminars to discuss the problem and to attempt to identify solutions. It was evident from late 2005 that over a number of seasons there had been a growing problem with lice control at a number of diverse locations. The possible causes and contributory factors were examined and evaluated in the search for solutions. While on-farm management issues could not be ruled out in all cases, they did not explain the breadth and scale of the difficulties experienced in achieving control of lice infestations experienced on many sites, which in the past had very good records of lice control. In general, there was very good cooperation from farms in carrying out lice control measures. In particular, all farms cooperated with the initiatives to carry out strategic winter treatments during December–January on all stocks due to be overwintered. All relevant stocks were treated and treatments were timed to occur after harvesting had been completed locally. There had been an issue with inclusion rates for in-feed treatments in some cases leading to underdosing. The effects of pancreas disease, which was present on many sites, also complicated the application of in-feed treatments. Together, these factors reduced the efficacy of in-feed lice treatments. There was growing evidence that some populations of lice were exhibiting reduced sensitivity to lice treatments. Fish health professionals and veterinary surgeons had expressed concerns about additional treatments required to reduce lice levels to comply with trigger levels. The need to carry out extra treatments was exacerbated in those areas where there was mixing of generations on the same or adjacent sites or strategic lice management was not the norm or both. It was recognized by industry and by the authorities that the difficulties in sea lice control were most acute in areas where the full implementation of Single Bay Management principles, in particular the separation of generations by the use of single generation sites and synchronous fallowing of adjacent sites, was either not being carried out effectively or was not possible to achieve. A working group comprising state agencies and government departments was established to review the

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systems and processes in place for the control of sea lice. In 2007, the responsibility for management and licensing of marine finfish aquaculture in Ireland passed to the Department of Agriculture Fisheries and Food. A review of the work carried out by the interagency working group was followed by the development of a new control strategy for sea lice being prepared and published by the department in May 2008 (Department of Agriculture Fisheries and Food 2008). In seeking to address the current problems in sea lice infestation control, the new strategy identified the need for a number of approaches by way of response options. In the short term, the necessity of tackling the problem of severe infestations at certain sites, some of which may be experiencing reduced sensitivity to currently available medicines, was identified as a key issue. The methodology is laid out in the strategy for how this is to be tackled on a bay-by-bay rather than a site-by-site or company basis to ensure that the extent of the management response is appropriate to the biological area of impact of the infective stages of the pest. In the short to medium term, the strategy foresees the necessity to review management practices to optimize lice control and to integrate this with overall health management, again on a bay-bybay basis. Strategies for bay management are also included in other chapters of this volume. Three strategies are outlined that need to be addressed to ensure effective sea lice management on Irish salmon farms. Each of the strategies is seen as presenting its own particular challenges; however, as a suite of responses they are regarded as the best way forward in the current circumstances. The strategies outlined are included in Box 6.2 below.

Box 6.2 Strategies for Bay Management A. Availability of a suite of novel lice treatments and methods (including well boats): To address the issue of sites where remedial action is urgently required to tackle high infestation levels, the availability of a suite of novel lice treatment methods, including the use of well boats to administer bath treatments of both existing licensed treatments and combination treatments is envisaged. In particular, well boats are seen as a key to effective use of bath treatments on exposed sites or those with large cages. B. Full implementation of both site and bay management: Fallowing between generations for a minimum period of 1 month and up to 8 weeks is seen as a vital exercise to break the cycle of infestation. Similarly, the exclusive use of single generation sites is necessary to eliminate the vertical transmission of lice infestations from year class to year class. While it has not been a feature of the Irish industry to date, the utilization of “all in all out” bay-by-bay stocking strategies may be recommended in specific cases, at least on an interim basis to break persistent cycles of reinfestation. It is recognized that in order to make these strategies work, a flexible and/or novel approach on currently licensed sites, including the species to be cultured at those sites, will be required. C. The development of an enhanced role for Single Bay Management: This is envisaged to include integration of sea lice and health management protocols. This includes a bay management approach that is defined by specific targets and goals, goal led, and both flexible and enforceable.

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In conclusion, the solution most likely to have the best medium- and long-term results is a combination of all three response options shown in Box 6.2. A flexible, inclusive approach can only be achieved by continuing to adapt management practices at site and bay levels to emerging trends in sea lice control. In an effort to optimize management practices with regard to sea lice control at fish farms, there have been a number of ad hoc initiatives, including the setting up of a small working group comprising Irish Salmon Growers Association and the MI. This group met regularly over the course of 2007 and 2008 to improve coordination of efforts to achieve optimum benefit from the fish farmers control efforts. The enhancement and formalization of this approach through the formation of a management cell approach involving farmers, state agencies, and the Department of Agriculture Fisheries and Food at a local regional level is planned. It is aimed to use the formalized management cell to underpin a focused SBM approach to addressing the ongoing management of sea lice control. In response to an emerging consensus that additional space is necessary to facilitate fallowing and separation of generations, the Department set out a process to address the challenges to be faced in making this additional space available. These challenges have been identified as including the limited availability of space for new sites, the difficulties of access to existing licensed areas for fallowing purposes, environmental and other licensing constraints, and potential objections from a variety of interested parties. In order to implement the strategy, the Department of Agriculture Fisheries and Food have set out a list of recommendations and an action plan. The main recommendations are outlined in Box 6.3 below.

Box 6.3 Recommended Strategies to Facilitate Bay Management 1. The setting up of a joint Department of Agriculture Fisheries and Food/industry working group to identify “break out” site options in areas that have persistent sea lice problems. These options would include the possibility of using redundant sites, to optimize fallowing and separation of generations. In accordance with the Steering a New Course report (Strategy for a Restructured, Sustainable and Profitable Irish Seafood Industry 2007–2013, Cawley et al. 2006), the Department of Agriculture Fisheries and Food should “support and facilitate the acquisition of fallowing sites for the salmon farming sector to assist with more effective sea lice and disease control. Provision of these sites should not necessarily involve an increase in the permitted output of the industry, but should facilitate improved spatial and temporal stock management and reduced incidence of sea louse infestation and other diseases. This initiative, which will make a very valuable contribution to the national effort to control sea lice numbers, should involve the applicants and the agents of the Department of Agriculture Fisheries and Food entering into detailed consultation on the location of proposed fallowing sites and agreeing to binding stock rotation and fish health management protocols prior to the submission of applications for an aquaculture licence.” It is very important that where break out space is made available, it should be used by the industry for fallowing and separation of generations, and not merely to enable an increase in output.

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2. Effective and appropriate use of chemical intervention to be reviewed to take ongoing account of changing environmental conditions, developing farming practices, sensitivity of lice to treatments, and fish health issues. In particular, the development of efficient protocols and mechanisms for the sourcing and use of well boats (also known as very large live fish carriers) for controlled bath treatments and for the optimization of product rotation for strategic treatments should be pursued by the relevant state agencies. 3. That the increased availability of well boat capacity coming on stream in the industry is utilized to best advantage for the carrying out of controlled bath treatments for sea lice control. 4. The optimization of product rotation for strategic treatments should be given further consideration as a matter of urgency to protect the efficacy of the available licensed treatments. 5. That the state agencies are to engage in intensive consultation with the fish farming industry, both with individual fish farmers and representative organizations, to ensure ongoing optimization of management practices, and to report back to the Minister on progress. 6. That a working group be established immediately to report in 3 months on the potential of alternative treatment approaches and to set out the steps necessary to introduce these approaches. 7. To set up a national implementation group with appropriate representation from the relevant divisions of the Department of Agriculture Fisheries and Food, the state agencies and the industry to oversee the implementation of the strategy. The group is to provide the Minister, within 6 months of its establishment, with a full update of the actual situation on the ground. The groups will also be responsible for assessing progress made to reduce sea lice levels and the further steps required, if any, to redress the situation. 8. The Department sets out a new role for Single Bay Management as a focus for management cells to manage sea lice control at a local and regional level reporting to the national implementation group. The Department recommended that efforts should be intensified to revitalize the SBM approach and make it central to national policy for sea lice management. In this regard, it was proposed that a new feature of the strategy to enhance the control of sea lice infestations on Irish salmon farms should be the creation of an integrated mandatory “real time” management regime, which will vigorously deal with failures to control sea lice infestations on a case-by-case basis. One of the perceived shortcomings of the current arrangements was that they are not sufficiently proactive in dealing with situations where, despite attempts to treat, the sea lice infestation was not brought adequately under control. The rationale behind this new initiative is to bring all of the relevant state expertise to bear on problem situations in real time, actively engaging the affected farmer and ensuring that a high priority is given to dealing with the infestation by all concerned. The regime is designed to bring progressively tougher actions to bear on areas of high infestation to ensure the highest possible level of compliance. The structure and modus operandi of this new more vigorous regime are set out in Box 6.4 below, exactly as published in the official Department of Agriculture Fisheries and Food strategy document.

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Box 6.4 Modus Operandi for Bay Management r Following established best practice for environmental management, a bay man-

r

r

r

r

r

r

r

agement cell approach will be taken to the problem of controlling sea lice infestations on individual farms, where despite attempts to treat, the level of infestation has not been brought under control. Each bay where salmon farming takes place will have a contingency management cell formed and available for immediate action. The cell shall consist of appropriate representation from the Marine Institute Sea Lice Monitoring Programme, Bord Iascaigh Mhara (Irish Sea-fisheries Board), an industry representative from the Single Bay Management Group for the bay and a veterinary surgeon of record. The cell will be convened by the Marine Institute Sea Lice Monitoring Programme representative when a “notice to treat” has been issued to a farmer in the bay, followed by an inspection that determines that either the “notice to treat” was not acted upon, or that the attempted treatment did not prove successful. The cell will take into account inter alia such factors as the time of the year relative to the so-called critical period and the spatial location of the affected farm in determining the relative urgency of its responses and the speed at which it ratchets up its responses. The cell will attempt to convene within 72 hours of the meeting being called by the MI and it will meet with the farmer concerned, and review all pertinent data and facts. The MI representative shall act as the chair of the cell. The cell will then issue a recommendation for further action. The farmer concerned will be obliged to follow the further action recommendation of the sea lice management cell, insofar as humanly possible. The further action recommendation from the cell shall be time specified and will be set down in writing and copied to the Coastal Zone Management Division of the Department of Agriculture Fisheries and Food at the conclusion of the cell meeting or as soon as possible thereafter. Once the recommended course of action has been pursued, a further inspection will take place as soon as possible, and the results will be disseminated to the cell members. Depending on the relative success achieved, the cell may decide that no further action is required or that a further meeting and that a further action recommendation is needed. The subsequent further action recommendation of the cell shall also be mandatory and shall also be copied to the Coastal Zone Management Division of the Department of Agriculture Fisheries and Food. Courses of action open to the cell for recommendation to the affected fish farmer shall include selection of treatment medicine and the selection of treatment methodology. If after a number of attempts satisfactory control has not been achieved, the cell may move to recommend accelerated harvesting, followed by extended fallowing postharvesting. In exceptional circumstances, the cell may also recommend mandatory restocking arrangements and/or an indefinite prohibition on restocking.

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Ovigerous sea lice levels nationally (May)

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Figure 6.7. (A) Annual trend in the mean number of ovigerous L. salmonis on one-sea-winter salmon in May, and (B) mean total number of mobile L. salmonis on one-sea-winter salmon in May.

This new strategy for improved pest control is currently being implemented in Ireland and the initial results are promising. The May mean L. salmonis annual trend graphs (Figure 6.7) of one-sea-winter fish up to 2009 show that a reduction in infestation levels was seen from 2007 to 2008; and this was maintained in 2009, reflecting improvements in control of infestation across a broad range of fish farm sites. Ovigerous sea lice levels in 2009 were similar to 2008 and mobile sea lice levels continued a decreasing trend.

Conclusions Results from a variety of sources demonstrated the efficacy of fallowing and single generation sites as aids to fish health. Wheatley et al. (1995) showed significantly reduced mortality in smolts stocked into sites that had been fallowed and similar benefits were associated with single generation sites. The results of the National Sea Lice Monitoring Programme would support these views and the fact that these practices

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need to be combined with effective product rotation in terms of sea lice treatments and the deployment of strategic treatments in a planned and coordinated way.

References Berland, B. 1993. Salmon lice on wild salmon (Salmo salar L.) in western Norway. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 179–187. Ellis Horwood, West Sussex, UK. Brandal, P.O., Egidius, E., and Romslo, I. 1976. Host blood: a major food component for the parasitic copepod Lepeophtheirus salmonis Kroyer, 1838 (Crustacea: Caligidae). Norwegian Journal of Zoology 24: 341–343. Bristow, G.A. and Berland, B. 1991. A report on some metazoan parasites of wild salmon (Salmo salar L.) from the west coast of Norway with comments on their interactions with farmed salmon. Aquaculture 98: 311–318. Browne, R., Deegan, B., O’Carroll, T., Norman, M., and O’Cinneide, M. 2007. Status of Irish Aquaculture 2006. Marine Institute Report, Ireland (ISBN 1–902895–28–2). Cawley, N., Murrin, J., and O’Bric, R. 2006. Steering a New Course (Strategy for a Restructured, sustainable and Profitable Irish Seafood Industry, 2007–2013), Department of Communications, Marine and Natural Resources, Ireland. Copley, L., O’Donohoe, P., Kennedy, S., Tierney, D., Naughton, O., Kane, F., Jackson, D., and McGrath, D. 2007. Lice infestation pressures on farmed Atlantic salmon smolts (Salmo salar R (0.2% emamectin benzoate) treatment. Linnaeus) in the west of Ireland following a SLICE Fish Veterinary Journal 9: 10–21. Copley, L., Tierney, T.D., Kane, F., Naughton, O., Kennedy, S., O’Donohoe, P., Jackson, D., and McGrath, D. 2005. Sea lice, Lepeophtheirus salmonis and Caligus elongatus, levels on salmon returning to the west coast of Ireland, 2003. Journal of the Marine Biological Association of the United Kingdom 85: 87–92. Costelloe, M., Costelloe, J., O’Connor, B., and Smith, P. 1993. Densities of polychaetes in sediments under a salmon farm using ivermectin. Bulletin of the European Association of Fish Pathologists 18(1): 22–24. Costelloe, J., Costelloe, M., and Roche, N. 1995. Variation in sealice infestation on Atlantic salmon smolts in Killary Harbour, West Coast of Ireland. Aquaculture International 3: 379–393. Cusack, R. and Johnson, G. 1990. A study of dichlorvos (Nuvan; 2,2 dichloroethenyl dimethyl phosphate), a therapeutic agent for the treatment of salmonids infected with sea lice (Lepeophtheirus salmonis). Aquaculture 90: 101–112. Deady, S., Varian, S.J.A., and Fives, J.M. 1995. The use of cleaner-fish to control sea lice on two Irish salmon (Salmo salar) farms with particular reference to wrasse behaviour in salmon cages. Aquaculture 131: 73–90. Denholm, I., Devine, G.J., Horsberg, T.E., Sevatdal, S., Fallang, A., Nolan, D. and Powell, R. 2002. Analysis and management of resistance to chemotherapeutants in salmon lice, Lepeophtheirus salmonis (Copepoda: Caligidae). Pest Management Science 58: 528–536. Department of Agriculture Fisheries and Food. 2008. A Strategy for Improved Pest Control on Irish Salmon Farms. May 2008, Ireland, 51 p. Department of Marine and Natural Resources. 2000. Monitoring Protocol No. 3 Offshore Finfish Farms—Sea Lice Monitoring and Control. May 2000, Department of Marine Natural Resources, Dublin, Ireland, 7 p. Hogans, W.E. and Trudeau, D.J. 1989. Preliminary studies on the biology of sea lice, Caligus elongatus, Caligus curtus and Lepeophtheirus salmonis (Copepoda: Caligidae) parasitic on cage-cultured salmonids in the Lower Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Sciences 1715: 14 p.

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Jackson, D. and Costello, M. 1991. Dichlorvos and alternative sea lice treatments. In: Aquaculture and the Environment (eds N. De Pauw and J. Joyce), pp. 215–221. European Aquaculture Society Special Publication 16, Ghent, Belgium. Jackson, D. and Minchin, D. 1992. Aspects of the reproductive output of two caligid copepod species parasitic on cultivated salmon. Invertebrate Reproduction and Development 22: 87–90. Jackson, D. and Minchin, D. 1993a. Variation in sea lice infestation on farmed salmonids in Ireland. ICES CM/1993/F: 30. Jackson, D. and Minchin, D. 1993b. Lice infestations of farmed salmon in Ireland. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 188–201. Ellis Horwood, West Sussex, UK. Jackson, D., Deady, S., Leahy, Y., and Hassett, D. 1997. Variations in parasitic caligid infestations on farmed salmonids and implications for their management. ICES Journal of Marine Science 54: 1104–1112. Jackson, D., Deady, S., Hassett, D. and Leahy, Y. 2000a. Caligus elongatus as parasites of farmed salmonids in Ireland. Contributions to Zoology 69: 65–70. Jackson, D., Hassett, D., Deady, S., and Leahy, Y. 2000b. Lepeophtheirus salmonis (Copepoda: Caligidae) on farmed salmon in Ireland. Contributions to Zoology 69: 71–77. Jackson, D., Hassett, D., and Copley, L. 2002. Integrated lice management on Irish salmon farms. Fish Veterinary Journal 6: 28–38. Jackson, D., Copley, L., Kane, F., Naughton, O., Kennedy, S., and O’Donohoe, P. 2005. Thirteen years of monitoring sea lice in farmed salmonids. In: Long-term Monitoring: Why, What, Where, When & How? (ed J. Solb´e), pp. 92–105. Sherkin Island Marine Station, Ireland. Jones, M.W., Sommerville, C., and Bron, J. 1990. The histopathology associated with the juvenile stages of Lepeophtheirus salmonis on the Atlantic salmon, Salmo salar L. Journal of Fish Diseases 15: 303–310. Jonsdottir, H., Bron, J.E., Wootten, R., and Turnbull, J.F. 1992. The histopathology associated with the pre-adult and adult stages of Lepeophtheirus salmonis on the Atlantic salmon, Salmo salar L. Journal of Fish Diseases 15: 521–527. Kabata, Z. 1974. Mouth and mode of feeding of Caligidae (Copepoda), parasites of fishes, as determined by light and scanning electron microscopy. Journal of the Fisheries Research Board of Canada 31(10): 1583–1588. MacKinnon, B.M. 1998. Host factors important in sea lice infections. ICES Journal of Marine Science 55: 188–192. McHenery, J.G. 1990. Effects of dichlorvos treatment at fish farms upon lobster larvae and mussels maintained in cages. Scottish Fisheries Working Paper No. 10/90, 14 p. R : good news for salmon, bad news for sea lice. Fish McHenery, J. and Johnson, J.D. 2002. Slice Veterinary Journal 5: 76–81. McHenery, J.G., Turrell, W.R., and Munro, A. 1991. Control of the use of the insecticide dichlorvos in Atlantic salmon farming. In: Problems of Chemotherapy in Aquaculture: From Theory to Reality. OIE, Paris, 409 p. Nolan, D.T., Reilly, P., and Wendelaar Bonga, S.E. 1999. Infection with low numbers of the sea louse Lepeophtheirus salmonis (Kroyer) induces stress related effects in post-smolt Atlantic salmon Salmo salar L.) Canadian Journal of Fisheries and Aquatic Sciences 56: 947–959. Nolan, D.T., Ruane, N.M., van Der Heijden, Y., Quabis, E.S., Costelloe, J. and Wendelaar Bonga, S.E. 2000. Juvenile Lepeophtheirus salmonis (Kroyer) affect the skin and gills of rainbow trout Oncorhynchus mykiss (Walbaum) and the host response to a handling procedure. Aquaculture Research 31: 823–833. O’Donohoe, G., Costelloe, M., and Costelloe, J. 1995. Development of a management strategy for the reduction/elimination of sea lice larvae, Lepeophtheirus salmonis, parasites of salmon and trout. Marine Resource Series No. 6. Marine Institute, Ireland, 51 p. O’Donohoe, P., Kennedy, S., Kane, F., Naughton, O., Nixon, P., Power, A., and Jackson, D. 2006. National survey of sea lice (Lepeophtheirus salmonis Kroyer and Caligus elongatus

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Nordmann) on fish farms in Ireland-2005. Irish Fisheries Bulletin No 24. Marine Institute, Ireland, 32 p. O’Donohoe, P., Kennedy, S., Kane, F., Naughton, O., Nixon, P., Power, A., and Jackson, D. 2007. National survey of sea lice (Lepeophtheirus salmonis Kroyer and Caligus elongatus Nordmann) on fish farms in Ireland-2006. Irish Fisheries Bulletin No 28. Marine Institute, Ireland, 35 p. O’Donohoe, P., Kane, F., Kelly, S., Nixon, P., Power, A., Naughton, O. and Jackson, D. 2008. National survey of sea lice (Lepeophtheirus salmonis Kroyer and Caligus elongatus Nordmann) on fish farms in Ireland-2007. Irish Fisheries Bulletin No 31. Marine Institute, Ireland, 35 p. Palmer, R., Rodger, H., Drinan, E., Dwyer, C., and Smith, P.R. 1987. Preliminary trials on the efficacy of ivermectin against parasitic copepods of Atlantic salmon. Bulletin of the European Association of Fish Pathologists 7(2): 47–54. Pike, A. 1989. Sea lice—major pathogens of farmed Atlantic salmon. Parasitology Today 5: 291–297. Ross, A. 1989. Nuvan use in salmon farming: the antithesis of the precautionary principle. Marine Pollution Bulletin 20: 372–374. Sevatdal, S., Copley, L., Wallace, C., Jackson, D., and Horsberg, T.E. 2006. Monitoring of the sensitivity of sea lice (Lepeophtheirus salmonis) to pyrethroids in Norway, Ireland and Scotland using bioassays and probit modelling. Aquaculture 244: 19–27. Smith, P.R., Moloney, M., McElligott, A., Clarke, S., Palmer, R., O’Kelly, J., and O’Brien, F. 1993. The efficiency of oral ivermectin in the control of sea lice infestations of farmed Atlantic salmon. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 296–307. Ellis Horwood, West Sussex, UK. Thomassen, J.M. 1993. Hydrogen peroxide as a delousing agent for Atlantic salmon. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 290–296. Ellis Horwood, West Sussex, UK. Tully, O. and McFadden, Y. 2000. Variation insensitivity of sea lice [Lepeophtheirus salmonis (Kroyer)] to dichlorvos on Irish salmon farms in 1991–92. Aquaculture Research 11: 849–854. Wheatley, S.B., McLoughlin, M.F., Menzies, F.D., and Goodall, E.A. 1995. Site management factors influencing mortality rates in Atlantic salmon (Salmo salar) during marine production. Aquaculture 136: 195–207. White, F. and Costelloe, J. 1999. Socio-economic evaluation of the impact of the aquaculture industry in counties Donegal, Galway, Kerry and Cork. Marine Resource Series No 7, Marine Institute, Ireland, 93 p. WHO 1989. Environmental Health Criteria 79: Dichlorvos. World Health Organization, Geneva, 157 p. Wootten, R., Smith, J., and Needham, E.A. 1982. Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids and their treatment. Proceedings of the Royal Society Edinburgh 81B: 185–197.

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Chapter 7

Salmon Louse Management on Farmed Salmon in Scotland Crawford W. Revie

Historical Perspective This chapter outlines the progression in the understanding of Lepeophtheirus salmonis population dynamics on Scottish salmon farms, starting from relatively simple field observation studies to more extensive quantitative epidemiological approaches to population modeling techniques that can assist not only in explaining host–parasite interactions but also in predicting likely future trends in sea lice dynamics on salmon farms. While this chapter has been written by a single author, the knowledge contained in it would not have evolved as it has had I not been privileged to work closely with a number of colleagues in the area. First, I must note my colleague and friend George Gettinby with whom most of my scientific output in the area of sea lice research has been shared. Both George and I were initially inspired by the work and enthusiasm of Gordon Rae who convinced us that this was an area both of interest and value. In the early stages of my research, a number of colleagues at Marine Harvest Scotland Ltd. were supportive and influential, including Jim Treasurer, Simon Wadsworth, Andrew Grant, and Graeme Dear. This involvement has continued over the past decade from fish health professionals at Marine Harvest Scotland Ltd. and other companies operating in Scotland. In particular, I am grateful for the support of Chris Wallace, Dave Cockerill, Gordon Ritchie, Tom Turnbull, John Rae, Hugh Richards, and John McHenery. In the latter stages of the research activity at the University of Strathclyde, George and I were joined by a research fellow, Fiona Lees, who made significant practical and theoretical contributions to our work. In addition Chris Robbins, Eddie McKenzie, Mark Baillie, and a number of summer students all contributed to our growing understanding, particularly with regard to the use of various time series, intraclass correlation, and population modeling approaches.

The Early Years: Identifying the Problem (1975–1989) Gordon Rae was an employee of the Unilever Company, one of the first to introduce large-scale salmon aquaculture to Scotland in the early 1970s. As early as 1975 he began to recognize that sea lice infestations may pose a health problem for some of Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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the farms for which he was acting as health manager. Therefore, Gordon began to systematically collect data on sea lice levels from a number of farms on the west coast of Scotland. By 1979, he had collected a large number of records documenting sea lice levels at different sites over the full production cycle. He wrote a short article in Fish Farmer (Rae 1979), which focused on the potential use of dichlorvos as a bath treatment on Scottish farms. This was the first publication to deal specifically with sea lice on Scottish salmon farms. To my knowledge, the only other papers published prior to 1980 on sea lice within a farmed setting also related to potential treatments, specifically the use of trichlorphon (NEGUVON) on Norwegian farms (Brandal and Egidius 1977; Brandal 1979; Brandal and Egidius 1979). Because the early data collected by Gordon Rae was in the form of paper-based logbooks, it was never transformed into a format that could be published. I had the opportunity to create a database containing these early data sets, material from which constituted a chapter of my PhD thesis (Revie 2006). It is informative to look at some of these early infestation patterns on Scottish salmon farms to see how the emerging problem was perceived and managed. However, before focusing on these quantitative summaries it is important to note that Gordon Rae’s early work reflected his more general observations and questions relating to the infestation of farmed salmon with sea lice. Most of Gordon’s notes were written before there were any published papers describing the behavior of these parasites, particularly not in a farmed context. For example, on November 26, 1976, an entry appeared relating to gravid lice and egg strings (Figure 7.1). This was an early observation of the fact that females produce multiple batches of eggs, something that Rae confirmed in another entry 1 week later

Figure 7.1. A page from Gordon Rae’s logbook from November 26, 1976, commenting on gravid females and egg strings found on fish at the Ephesus farm site.

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Figure 7.2. A further note from Rae’s Ephesus log from November 30, 1976, on egg strings and the relative fecundity of the two lice species present on this farm.

(Figure 7.2). In that note Gordon also commented on the apparently relative higher fecundity levels of L. salmonis compared to Caligus elongatus, as well as noting that these levels of egg output seemed surprisingly low for ectoparasites. Gordon Rae’s logbooks contained many such observations that were later formally confirmed or expanded upon by scientists working in laboratories in Scotland and elsewhere. Moving on to the more quantitative material, the first thing that becomes apparent is the attention to detail and comprehensiveness of the data Gordon Rae collected. The exhibit in Figure 7.3 shows the scanned image of a typical page from one of his field logbooks. For any given fish up to 30 elements of data might be recorded, with up to 15 stage and gender elements for each of the two lice species. In total, around 1400 fish sample records of this format existed, most of which came from two sites in the Loch Ailort area between 1976 and 1979. Gordon did make some attempt at the time to summarize key trends in a quantitative or graphical manner. The scanned graph shown in Figure 7.4 is one example of the type of time-based summary that occasionally appeared in his logbooks. However, there are limitations on what can be achieved using manual mark-up with squared paper. For a number of the sites, the underlying patterns and relationships between lice stages and species were left unexplored. For example, looking at the data summarized in Figure 7.4, are the patterns of infestation for L. salmonis and C. elongatus

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Figure 7.3. A page from one of Gordon Rae’s lab books. This record relates to a sample taken at the Loch Ailort site on January 15, 1978.

similar; or within each species are the relative levels of attached and mobile stages comparable? Some of these questions have been addressed in my thesis (Revie 2006). There is no space to discuss this fully here, but two graphs illustrate both the value of the detailed approach Rae adopted as well as some general patterns that would be seen in Scottish aquaculture for decades to come. The first “digital” exhibit based on Rae’s data set (Figure 7.5) illustrates the breakdown of L. salmonis by attached and mobile stages for the same site (Ephesus) as was originally graphed by Gordon (Figure 7.4). The updated graph illustrates a number of elements. In the first place, it is possible to get some idea of the variability in the data. It can be seen that the standard error estimates are fairly tightly distributed about the mean weekly values. Secondly, it can be seen that the number of mobiles tended to be significantly higher than the associated chalimus loads. The mobile levels appear to “trail” the rise in chalimus levels. In general, the level of infestation appears to

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Figure 7.4. A hand-drawn graph taken from Rae’s notes illustrating total lice counts of both species per fish in 1-year class growing at the Ephesus site in 1976/1977.

rise as the fish mature. The data on treatments is also of interest. The bath treatments appear to have been applied as “pairs” of treatments. This pattern of usage was also observed much later on Scottish salmon farms when the synthetic pyrethroid cypermethrin was used as the primary treatment option (1998–2001). This usage was reported from treatment records (Revie et al. 2002a) and was also predicted to be optimally efficient based on a mathematical model for treatment interventions using that topical medication (Revie et al. 2005c; Robbins et al. 2010). It is also clear that the application of dichlorvos was relatively effective in reducing lice loads at this point in the Scottish industry’s development. There was a dearth of published information about sea lice infestations on Scottish fish farms in the 1980s. A paper outlining some data from Scottish farms was presented at the 17th Scientific Meeting of the Scottish Marine Biological Association held in Stirling in 1980. The authors noted that, while L. salmonis were present on farms throughout the year, C. elongatus were “not present till June” (Wootten et al. 1982). It seems that the data reported came from one, or at most two, sites and it is thus not possible to determine whether they represented “typical” patterns. Indeed, as Needham worked with Rae, it is likely that these data were a subset of the data summarized previously in this section. An updated overview of the situation in Scotland was submitted to the ICES Mariculture Committee a few years later (Wootten 1985) but little additional data were contained in that report. The first review of the growing literature focusing on sea lice infestations of both wild and farmed salmon was published toward the end of the 1980s (Pike 1989). This review confirmed that there was little published material relating to sea lice infestation patterns on Scottish

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60 Treatment intervention 50 L. salmonis chalimus per fish

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Figure 7.5. Mean abundance (+/−SE) per fish of L. salmonis chalimus (A) and mobiles (B) for a year-class at Ephesus from November 1976 to April 1978.

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salmon farms at that time. To Pike’s credit, he appears to have been one of the first researchers to mention the importance of considering “integrated control” management techniques, including the use of cleaner fish (Pike 1989). Integrated Pest Management (IPM) continues to provide a range of challenges. It was also around this time that a wider range of sea lice research programs was initiated. A number of these programs would be reported at the First International Sea Lice Conference held in Paris in the autumn of 1992. The majority of the talks given at that conference appeared in a book that was published in the following year (Boxshall and DeFaye 1993). In many ways, this conference and the associated research represented the maturing of knowledge in a number of subject areas related to the host–parasite dynamics of salmon and sea lice, not just in Scotland but across the globe, as summarized in the next section and in other chapters (for example, see Chapter 5 contributed by Ritchie and Boxaspen, Chapter 6 contributed by Jackson, Chapter 7 contributed by Revie and Chapter 8 contributed by Saksida et al.) in this volume.

A Maturing Understanding: Management and Collaboration (1990–1999) A number of the papers presented at the Paris conference (Boxshall and DeFaye 1993) came from researchers working in Scotland and provided an introduction to some key themes that would form the focus of Scottish research over the ensuing decade. Three of these papers dealt with the basic biology of lice. The first (Pike et al. 1993) considered the biology of C. elongatus, and in particular the species’ stage development times as they related to temperature. This formalized earlier work carried out on Scottish farms (Wootten et al. 1982) and complemented the findings for this species coming from research in Canada (Hogans and Trudeau 1989; see Chapter 3 contributed by Chang et al.). It also mirrored detailed studies of temperature-dependent stage development for the L. salmonis species that were being undertaken around the same time (Tully 1989; Johnson and Albright 1991). In addition to this laboratory-based research, the group from the University of Aberdeen contributed another paper on basic biology, this time based on research carried out in field situations (Ritchie et al. 1993). The authors examined the size of female lice, length of egg strings, and number of eggs per string on two Scottish salmon farms over an 18-month period. They found distinct seasonal variation and postulated that both temperature and photoperiod had a significant effect on reproductive output. Subsequent fundamental research on the reproductive system of L. salmonis (Ritchie et al. 1996a), together with observations of mating behavior (Ritchie et al. 1996b), were central to a more complete understanding of pair formation and mating biology (Hull et al. 1998). These findings would also ultimately inform the more recent work of the Aberdeen group on the place and importance of pheromones in attracting or repelling sexually active lice, and the potential for strategies to use semiochemicals as part of a lice control strategy (Ingvarsd´ ottir et al. 2002). A third Scottish paper from the Paris conference also looked at lice biology, focusing on the behavior of L. salmonis larvae (Bron et al. 1993c). Knowledge of how copepodid larvae locate and attach to the salmon host was seen as key to understanding the interaction between host and parasite at this initial point of contact. These behavioral

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characteristics of larvae, the mechanics of their dispersion within the water column, and host attachment would form a theme for research over the succeeding decade. Some of the most important work in this area was carried out in Norway by Heuch and colleagues (Heuch 1995; Heuch et al. 1995; Heuch and Karlsen 1997), while Tucker and colleagues studied larval energetics and settlement patterns in detail in a laboratory setting within Scotland (Tucker et al. 2000). These studies helped to inform the growing research program that applied knowledge of the behavior of planktonic copepods to studies of farm and wild fish interactions in the Loch Torridon area (see also Chapter 2 contributed by Murray et al.). Two of the other Scottish-based papers given at the 1992 conference focused on farm management issues. One dealt with site fallowing (Grant and Treasurer 1993) and the other with the use of wrasse as cleaner fish (Treasurer 1993a). Once again the theme of management aspects of lice control then formed an important ongoing topic of research. Toward the end of the 1990s it tended to be conflated with treatment issues as part of the search for IPM strategies. The importance and benefits of breaking “the cycle of caligid infestation” (Grant and Treasurer 1993) through fallowing was claimed for both major lice species seen in Scotland. However, the data used by these authors related to a single site over a limited time period. In an alternative paper that appeared at around the same time (Bron et al. 1993a), it was stated that fallowing appeared to have no effect on the emergence of C. elongatus; something that was in direct contrast to its beneficial effects in reducing infection levels of L. salmonis in the first year of salmon production. However, the assertion was also made in this paper (Bron et al. 1993a) that longer fallowing periods produced higher levels of subsequent L. salmonis reduction, a point that would not be substantiated in a risk factor study using a much more substantial set of data points (Revie et al. 2003a). Despite the lack of complete knowledge at this time, the importance of site fallowing was accepted by many of the key aquaculture leaders. Over the next 5 years, the entire Scottish industry, with few exceptions, moved to a single-year class, all-in-all-out with at least 6 weeks fallowing model of operation (Rae 2002). The use of cleaner fish as biological controls (Treasurer 1993a) was promoted more widely in an article targeted at commercial salmon farmers within the Scottish industry (Treasurer 1993b) and later through a full book of edited articles on the subject (Sayer et al. 1996). Unfortunately, the use of wrasse on Scottish salmon farms was effectively ended as a result of a series of infectious salmon anemia (ISA) outbreaks around 2000, where they were implicated as potential carriers of the virus (Treasurer 2005). Despite the fact that it has been demonstrated that wrasse are not likely to be carriers of the ISA virus (Kvenseth 1998), their use, which was also in decline in Norway by the end of the 1990s (Heuch et al. 2003), has in general not been adopted as a control measure on Scottish farms over the past decade. The final two papers from Scottish researchers in the Boxshall and DeFaye (1993) collection both dealt with lice treatments. One looked at the well-established treatment compound dichlorvos (Bron et al. 1993b), while the other reported initial findings based on the use of two synthetic pyrethroids (Roth et al. 1993). Of all the sea lice-related topics investigated over the subsequent decade, the issue of treatment interventions would undoubtedly form the basis of one of the best researched, particularly when the issues of “strategic” treatment and IPM are included within this broad categorization. IPM programs are included in a number of chapters in this volume. Studies into treatment intervention options already existed in Scotland, relating to the

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use of dichlorvos within the industry (Ross and Horsman 1988), as well as to its potential effects of lobster and herring larvae (McHenery et al. 1991). Early summaries of the treatment situation were provided by Roth and colleagues (1993) as well as by Branson (1996). These were followed by a large number of studies in Scotland looking at the potential and limitations of compounds such as azamethiphos (Roth et al. 1996), hydrogen peroxide (Kiemer and Black 1997; Treasurer and Grant 1997; McAndrew et al. 1998; Treasurer et al. 2000), ivermectin (Black et al. 1997; Davies et al. 1997; Davies and Rodger 2000), and emamectin benzoate (Stone et al. 1999, 2000, 2002; Treasurer et al. 2002, 2003). This list is not exhaustive; a more complete summary of the situation with respect to treatment was provided by Roth (2000) and, from a more practical veterinary management perspective, by Grant (2002). The possibility of timing multiple treatments in some “strategic” manner was first investigated by a group of scientists working with Marine Harvest Scotland Ltd. who adopted a “three winter treatments” approach on fish in the 1996 year class (Wadsworth et al. 1998; Treasurer 1998). This research was a core part of Wadsworth’s doctoral work (Wadsworth 1998) and influenced a proposed national treatment strategy for Scotland (Rae 1999). The success or otherwise of this approach was one of the issues explored as part of the risk factors analysis I carried out (Revie et al. 2003a). The potential of mathematical models to explore various treatment intervention strategies in a more formal and structured manner has also been the subject of ongoing research (Robbins et al. 2010). The set of Scottish papers presented at the first conference in 1992 led to the categories of the major research directions taken in the succeeding decade as follows: basic biology and behavior, including sexual reproduction and mating biology; larval dispersion and host attachment; lice management issues, including fallowing and the use of biological controls; and treatment interventions and the “strategic” timing of these. There are a few additional topics that were not covered during this first conference but saw research activity in Scotland during the 1990s. They included the following: the incidence of infestation on wild fish populations (reports on this area were included from Norway and Ireland at the Paris meeting but none relating to Scotland); the use of genetic techniques for identifying lice populations (research too novel to have been covered at the 1992 meeting); and more formal quantitative approaches to describing and modeling the dynamics of sea lice. As far as infestations of wild fish are concerned, work as early as 1989 noted unusually high levels of C. elongatus on herring (MacKenzie and Morrison 1989). A study of sea lice infections on saithe (Bruno and Stone 1990) in laboratory and farmed settings noted both L. salmonis and C. elongatus as parasitic and potential sources of lice for fish farms. This finding has been questioned by many since (Jim Treasurer, personal communication, March 10, 2006) with many believing that L. salmonis is exclusively a natural parasite of salmonid species (see the introductory chapter contributed by Hayward et al.). In 1991–1993, the levels of lice infection on wild sea trout were observed in a study of eight river areas (Sharp et al. 1994). Large variations in lice populations and structures were found. L. salmonis were observed at all sites, most with prevalences of over 75%, while C. elongatus were only seen at one site. The authors noted that the mean abundance levels were very similar to those “reported by Boxshall (1974) of 9.8 and 4.0” on sea lice in the North Sea for C. elongatus and L. salmonis, respectively. It was found that for C. elongatus (unfortunately limited to one sample site and

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13 fish) the adult female lice accounted for over 90% of all lice. In all cases the pattern of lice infection was overdispersed, with variance to mean ratios of as high as 13.4. The authors stated that this overdispersion implied an uneven distribution of lice larvae within the sea lochs, a pattern that matched what was proposed by a theoretical model of particle transport almost a decade later (Murray 2002; and see Chapter 2 contributed by Murray et al.). In a study of wild sea trout (Salmo trutta) caught off the east coast of England in 1992–1993 (Tingley et al. 1997), the mean level of L. salmonis was around five lice per fish (at a prevalence level of around 95%), while C. elongatus were found on just over half the fish, at a mean intensity of around 1.5 lice per fish. The authors noted that the pattern of infection for both lice species was “highly seasonal.” Indeed, they noted that day of the year was the best predictor of abundance. However, the data set was rather small. No seasonal values were reported, simply annual means, and the analysis was both nonstandard and simplistic, so it is difficult to know what important lessons can be taken from this study. The authors did state that mean abundance levels were lower than numbers typically seen on wild trout caught off the west coast of Scotland and they also stated that there appeared to be “a long-term, dynamic stability in the populations of both species of lice.” A study of wild trout looked specifically at the Scottish situation with data from 20 sites and a total of 622 sea trout (MacKenzie et al. 1998). This study sampled fish largely between late April and July 1994, with 17 of the locations being in areas with salmon farming activity. For L. salmonis, they found lice on about one-third of fish sampled, with a mean of 24 lice per fish. However, this number of lice included many copepodid and chalimus stages. For the two sites on the east coast, they found prevalence levels to be around twice as high, but with lower mean abundances of around four lice per fish. For the remaining site in the extreme southwest, only 3 of the 82 fish examined had any lice and only a few chalimus stages were observed on these fish. The authors noted that “Although areas of intense salmon farming and heavy infestations on sea trout are positively associated, these results provide no direct evidence of the role and significance of salmon farms in the transmission of sea lice to wild sea trout.” As far as C. elongatus are concerned, this study showed significantly lower levels on sea trout than was the case for L. salmonis with an overall prevalence of just 3%. Indeed, on only 3 of the 20 sites sampled were C. elongatus found, with a mean abundance level of 0.25 lice per fish at these sites. The authors made the interesting and useful general observation that “the observed differences in the infection patterns at different sites serve to illustrate the difficulties in interpretation of data from field situations where a wide range of physical and biological factors may be affecting the level of lice on an individual fish” (MacKenzie et al. 1998). The most extensive work on returning wild salmon in Scotland has been carried out by Todd and colleagues from the Scottish Fisheries Research Service. In a study looking at two sites in Scotland, they reported data on L. salmonis and claimed it to be “unusual amongst parasitic species in demonstrating extremely high levels of prevalence, essentially at 100%” (Todd et al. 2000). They pointed out that, in a review conducted on 211 parasitic species (Shaw and Dobson 1995), only 15 showed prevalences of greater than 90% and just two of these, both endoparasitic arthropods, were stated as being at 100%. The work by Todd looked at fish caught near the mouth of the River Tay in 1995/1996, as well as wild salmon returning to Scotland at effectively the first point of landfall in Strathy Point, with samples being taken

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from this site in 1998/1999. Here, I shall consider only the data from Strathy Point, which in addition to indicating a prevalence of 100%, showed an abundance of mobile L. salmonis of around 20 lice per fish. The authors stated that in the River Tay C. elongatus were “extremely rare” (probably due to the brackish waters there) but that they were highly prevalent and abundant at Strathy Point. Unfortunately, they stated that time did not allow for enumeration of that species; though they ended the paper by stating “we believe it is essential to obtain more data in Scotland on wild salmon infestations, not only for L. salmonis but also for C. elongatus” (Todd et al. 2000). For the wild salmon sampled at Strathy Point, they also noted that 90% of all lice were in the adult stage and that around 70% were female. They also noted greater abundance on two-sea-winter fish (30 lice per fish) than was the case on one-sea-winter fish (17 lice). They noted that the female predominance on wild fish appeared to be characteristic, as do the very high levels of prevalence. This appears to contrast strongly with evidence from the farmed situation (Bron et al. 1993b). However, it is important not to overinterpret the finding from this single site study and a fuller discussion on gender ratios from a broader range of sites can be found in the author’s PhD thesis (Revie 2006). The data collection at Strathy Point was continued and has now resulted in a rich data set with L. salmonis infection patterns from 1998 to 2005 together with data for C. elongatus from 1999 to 2005 (Todd et al. 2006). These data support the earlier work, and once again show prevalence data for L. salmonis to be 100% in all years under review. In addition, they show similarly high prevalence levels for C. elongatus, with all years over 90% and in 4 years being 100%. The levels of abundance were significantly higher for L. salmonis (17–31, min.–max.) than for C. elongatus (3–15, min.–max.), except for 1 year where C. elongatus was unusually high at 23.8 lice per fish. They showed that there was a slight positive correlation between the two species for individual fish within a given year. However, with an R2 of less than 0.02, this is clearly of limited interest, even if the large sample size means it is statistically significant. Of more significance may be the fact that there was clearly no negative correlation, which would be expected if there were some form of competitive pressure between the two species on wild fish. Arguably, the most significant result from this research was that it showed no association between levels of lice infestation and host condition factor: “poor condition fish were no more likely to carry infestations than were high condition fish.” Returning to sea trout, there are two other pieces of work from the Scottish context that deserve mention, though both restrict themselves to discussing L. salmonis. The first is a summary paper (Butler 2002), which is based on a more extensive report surveying sea lice infections along the west coast of Scotland between 1998 and 2000 (Butler et al. 2001). In these studies, the authors stated that no C. elongatus were observed; this may be due to the effect of freshwater within the river traps where the samples were taken. Unfortunately, the size of samples available were rather small and one site, Dundonnell, with very high mean levels of lice abundance dominated the sampling, particularly in 2000. Given that the work was carried out by Fisheries Trust biologists, there was a natural interest in associations between trout decline and lice levels of farms. This can lead to an overstatement of the situation that it is difficult to justify from the data, such as “epizootics occurred every year and coincided with the presence of ovigerous lice on local farms” (Butler 2002). There does appear to be consistent evidence that lice levels were higher on sea trout in river areas where

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salmon farms were in their second year of production (and would therefore tend to have higher levels of lice on fish). The other recent study involving wild sea trout and farmed salmon was carried out in a single bay in the northwest of Scotland between 1998 and 2001 (Marshall 2003; see Chapter 2 contributed by Murray et al.). This bay was fallowed for a whole year at a time (1998 and 2001) and data were collected for these years as well as over the intervening two-year production period on a salmon farm within the bay. There was some evidence of a weak correlation between lice levels on the farm and lice on wild trout; however, this was more likely to be due to a common underlying seasonality in both sets of data. As the author concluded “it would appear from this study that the abundance of lice on wild fish is not directly related to that on the neighbouring farm.” Given the high levels of natural variation within sites over years, it is not surprising that this conclusion should be reached. It is also the reason why a number of sea lice review workshops over the past decade have not “been able to conclude that there is a cause-effect relationship between salmon lice on farms and variations in wild salmonid populations” (McVicar 2004). A second area where increasing research effort has been targeted recently is in the use of a range of genetic techniques and this area has also seen activity in Scotland. An early paper (Todd et al. 1997) looked at Polymerase Chain Reaction (PCR) and random amplified polymorphic DNA analysis techniques to distinguish populations of sea lice from one another (see the introductory chapter contributed by Hayward et al.). These authors stated at the time that “RAPD analysis showed striking patterns of genetic differentiation.” Around this time similar work was being carried out in Norway (Isdal et al. 1997) and in Canada (MacKinnon 1998; Mustafa and MacKinnon 1999). These approaches were further developed to look at PCR analysis for microsatellite typing with Shinn and colleagues (2000), focusing on differences between L. salmonis lice taken from wild and farmed fish. In a more extensive study, L. salmonis samples from Ireland and Norway, as well as Scotland, were assessed in a similar manner and it was found that PCR analysis “could detect genetic variation both within and between L. salmonis groups” (Nolan et al. 2000). The approach of this group was part of a broader set of techniques used within the European Union project, SEARCH, which looked at the emergence and management of chemical resistance in sea lice (Denholm et al. 2002). An earlier, more general article explored the possible mechanisms leading to the selection of resistant sea lice (Treasurer et al. 2000) within the context of practices on Scottish salmon farms. The potential of breeding to produce genetically resistant host stocks was outlined (Jones 2001; Jones et al. 2002) and a number of experimental trials in this area have been carried out by Glover and colleagues (Glover et al. 2001, 2003, 2004). The potential of DNA variation to distinguish between lice populations was also inferred by Tully and Nolan (2002), and further explored by Andy Shinn’s research team at the University of Stirling (Dixon et al. 2004). However, the latest paper by Todd and colleagues (2004) on this issue does not support the earlier optimism of their group and others in using PCR techniques to type populations. In this more extensive study the researchers looked at L. salmonis from both the North Atlantic and North Pacific, and concluded that genetically the former comprised a single population. In summarizing their work they stated “Contrary to our previous studies on random amplified polymorphic DNA variation. . . the present data provide no evidence to suggest

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that there is substructuring or differentiation of L. salmonis populations infesting wild and farmed salmonids. Overall, gene flow and migration (cross-infection) between parasite populations on the two host components [i.e., wild and farmed] is at a high level” (Todd et al. 2004). However, work continues in the area with researchers looking at both L. salmonis (Kolstad et al. 2005; Tjensvoll et al. 2005) and C. elongatus (Øines and Heuch 2005; Øines et al. 2006). Despite these advances in the knowledge of how to manage salmon lice on Scottish fish farms, it remained the case that much of the research carried out in the 1990s looked at data collected from no more than a single site over a couple of production cycles, or a number of sites over a limited time period (typically, just 1 year). Due to natural year-to-year and site-to-site variation, it is very difficult to discern clear trends from such studies. In addition, in a farmed setting the fish hosts must, for economic and fish welfare reasons, be treated to control the parasite and so there can be no farm-based studies that illustrate completely “natural” underlying patterns of sea lice epidemiology. At the end of the decade, Pike was to join with his doctoral student Simon Wadsworth and write what remains one of the best overall reviews of core knowledge regarding sea lice (Pike and Wadsworth 1999). The fact that this paper ran to 100 pages, compared to the seven of Pike’s review 10 years previously (Pike 1989) is an illustration of how far the research had moved in the intervening period. Nevertheless, in this later and extensive review the authors make the following observation: “published information on prevalence and intensity of infection with sea lice is surprisingly sparse for cage-cultured salmon, considering the frequency with which the parasites occur” (Pike and Wadsworth 1999). This was about to change.

The “Modern” Era: Quantitative Epidemiology and Models (2000–Present) While the range of research activities carried out during the 1990s definitely led to a maturing of our understanding of sea lice dynamics on Scottish salmon farms and their control, it was recognized that some of this was based on some flimsy evidence. In particular, the published reports on sea lice infestation patterns on farms were often based on just one site over a number of years or two to three sites in a single year. This was not really an adequately representative sample to properly describe a complex set of host–parasite interactions, which exhibited the expected range of variation and ecological “noise.” In recognition of this and in an attempt to uncover key trends and patterns in sea lice data collected over a number of years, Marine Harvest Scotland Ltd. approached our epi-informatics group at the University of Strathclyde for assistance. Marine Harvest Scotland Ltd. were one of the largest salmon producers in Scotland, operating over 50 sites along the west coast and in the Western Isles. Thus, their data presented an unprecedented opportunity to gain a more complete picture of sea lice dynamics across Scottish salmon farms. Our group had experience in analyzing host–parasite interactions in the terrestrial context (Gu et al. 1999; McKendrick et al. 2000), as well as a growing reputation for marshaling large epidemiological data sets using novel informatics approaches (Revie et al. 1994; McKendrick et al. 1995; Seidel et al. 2003). We thus began a project in 2000 to try to bring some quantitative rigor to

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the understanding of sea lice epidemiology on Scottish salmon farms, little imagining that a decade later the work would have resulted in close to 20 peer-reviewed papers and had impact on the understanding and control of sea lice, not only in Scotland but also in most of the major salmon producing regions. Trying to summarize a decade of work and this amount of scientific output in this chapter is difficult. However, the initial part of this section will attempt to do so, making reference to other studies that relate to our growing quantitative understanding of sea lice dynamics on salmon farms. Other research over the past 10 years, which has often been complementary to these quantitative epidemiology themes, is summarized at the end of the chapter. Other chapters in this volume also describe some of the results of these studies. Our initial work led to the publication of the first large-scale summary of the sea lice situation across Scottish farms. It was based on samples from over 88,000 fish and covered the period from 1996 to 2000 (Revie et al. 2002a). This publication confirmed and quantified previous anecdotal observations that the levels of L. salmonis infestation in the second year of production were significantly higher than those seen in the first year, with levels of mobile lice being anything from three to ten times higher in the latter year of the production cycle. Interestingly, this contrasted with the abundance of mobile C. elongatus, which were seen to be consistently higher in the first year of production. Despite being considered to be of lesser importance to the aquaculture industry in Scotland, this observation led to a more detailed consideration of this nonspecific parasite (Revie et al. 2002b). Unlike L. salmonis, this species was found to be regular enough in its pattern of seasonal infestation to be amenable to modeling using time series methods (McKenzie et al. 2004). The data presented in these early papers were used to create a graph indicating the typical pattern of infestation of mobile lice, of both species, over the course of a typical production cycle on a Scottish salmon farm (Figure 7.6). The fact that these species demonstrated such

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Figure 7.6. Typical pattern of infestation by the two main lice species found of Scottish farms. Mean weekly mobile abundance levels recorded from over 100 production cycles between 1996 and 2000.

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different dynamics, and that one species tended to be higher when the other was lower, led to consideration of the potential that some form of competitive pressure existed between them (Revie et al. 2002b, 2005a; Revie 2006). The results seemed to indicate such a relationship but the nature of the data made it difficult to be conclusive. Recent findings discussed later raise further questions. A key observation from these initial papers was that sea lice treatments had a major impact on the levels of infestation. This may appear obvious, but there were those who doubted whether, given the levels of noise and seasonal/spatial variation in lice numbers as well as doubts around data quality, it would be possible to pick up the potentially “subtle” effects (in terms of signal-to-noise ratio) of treatment interventions. The graph shown here (Figure 7.7) is a simplified version of a more involved diagram from our initial descriptive epidemiology paper (Revie et al. 2002a) and illustrates that the impacts of treatments can be seen clearly. In particular, the impact in the second year of production of the “strategic” treatment intervention program in place at that time in Scotland (coordinated treatments around weeks 10, 16, and 22) can be plainly seen. The presence of treatment interventions has a number of important implications for any research in this area. In the first place, it must be accepted that any prediction of lice dynamics based on a model of “natural” growth/death rates will be of limited value. A variety of laboratory-based studies had been carried out to predict various growth rates/patterns, (summarized in Stien et al. 2005), but these were always carried out in the absence of treatments, a situation that hardly ever holds in the field. In addition, any epidemiological study looking at risk factors affecting lice levels needs to take account of treatment interventions as a confounding variable. Having carried out research to summarize the descriptive epidemiological trends of sea lice on Scottish farms, a natural next step for our group was the investigation

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of factors affecting these levels and/or trends. An initial paper (Revie et al. 2002c) considered some potential factors, including stocking type (photoperiod manipulated versus “normal” smolts), geographical region within Scotland, and level of coastal exposure; but none of these factors appeared to be associated with significant differences in lice levels in a relatively simplistic analysis. Similarly, and somewhat against initial expectations, it was found that there was no evidence that differences in water temperature across sites led to variation in mean annual abundance levels of L. salmonis infestation. Indeed, in this initial review of a limited set of factors, only treatment was clearly associated with variation in mean lice levels. In a more formal and extensive risk factor analysis (Revie et al. 2003a), a much wider range of variables was considered. A total of 21 potential factors relating to both farm management and environmental variables were identified by experts, of which adequate data were found to exist for 15 factors that were incorporated into the subsequent linear regression analysis. Once again, both the type and level of treatment administered at a salmon farm were found to be important factors in determining mobile L. salmonis levels. In addition, the current speed at a site, overall loch flushing time and, for parts of the production cycle, cage volume were also found to be explanatory factors. In particular, these factors, together with mean lice levels from the preceding 6-month period, could be used to adequately predict the likely mobile L. salmonis infestation in the first half of the second year of production (adjusted R2 of 72%). However, a number of factors that had previously been postulated as being likely risk factors were not found to be so in this fairly extensive data set; these included the following: stocking density, site biomass, water temperature, and the presence of neighboring farms. While risk factors for C. elongatus were not discussed in the above-mentioned paper, a similar linear regression exercise was carried out for this additional species (Table 7.1; Revie et al. 2003b, 2006). The results from analyzing large sea lice data sets were shared with a number of colleagues looking at data from Norwegian farms. By encouraging these researchers to adopt similar approaches, it was possible to carry out some meaningful comparisons between the two countries, both in terms of sea lice infestations seen and treatments used on salmon farms (Heuch et al. 2003). Due to the fact that many of the Norwegian sites had mixed year classes of fish and, therefore, that size varied in a different way Table 7.1. Summary of risk factors associated with (or not) abundance levels of the two main species of sea lice found on Scottish salmon farms. (Factors shown in [] demonstrated some association or were likely to have been seriously impacted by confounding.) See Revie (2006) for details.

Significant association

No significant association

L. salmonis

C. elongates

Treatment level (+) Treatment type Current speed (−) [Water temperature (+)] Biomass Stocking density Increased fallowing [Strategic treatment]

Biomass (−) Cage volume (−) Current speed (−) Treatment level Increased treatment [Strategic treatment]

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over the course of any year to that seen in Scotland, a novel measure of lice per m2 of surface area (skin) was developed to make comparative analysis possible. The data implied that levels of both chalimus and mobile L. salmonis were significantly higher in Scotland than was seen on the Norwegian farms in the period under study (1997–1999). These higher lice levels were reflected in a more extensive use of veterinary medicine on the Scottish farms. It was not possible to ascertain the key factors responsible for these differences, though variation in environmental conditions, such as the more dramatic fluctuations in water temperature, deeper water bodies, and larger nets in Norway, were all postulated as possibilities. However, it should also be noted that Norwegian legislation meant that a broader range of treatments were available to the farms in Norway. Also, the sample represented only around 5% of total Norwegian production (while the Scottish data was closer to representing 30% of all production over the period under comparison). The value of this approach was nevertheless demonstrated outside of the Scottish context and a similar approach has recently been used by Norwegian researchers when providing an epidemiological summary of the sea lice situation on farms within the Hardangerfjord (Heuch et al. 2009). A key question when analyzing data resulting from any form of field observation is whether the sampling method adopted is adequate and relatively free from bias. Early consideration to this issue was given by Treasurer and Pope (2000), though their discussion was based on the assumption of simple random sampling. In many sampling contexts relating to individuals nested within groups (or clusters), it has become clear that the assumptions of simple random sampling do not hold. The statistical term for such nonrandom phenomena is intraclass correlation, and knowing its magnitude allows for an assessment of the likely consequence of ignoring clustering within a given sampling protocol. Empirical data relating to lice sampled on Scottish farms was analyzed to gain estimates of intraclass correlation values associated with abundance measures for chalimus and mobile stages of L. salmonis (Revie et al. 2005b). The results indicated that significant clustering was present in most farm settings, especially for the mobile stages of lice with intraclass correlation values as high as 0.35, which implies significantly more fish must be sampled to achieve the accuracy that was presumed based on simple random sampling. The finding also has important implications for the relative benefit of sampling a small number of fish from many cages, as compared to sampling many fish from just a few cages, as was the practice in a number of countries at that time (notably Norway and Ireland). Despite the empirical basis of this work, it appeared that the message was not being picked up by policy makers who develop protocols for such sampling activities. Thus, in a follow-up paper, the practical implications of various sampling regimes were illustrated through the use of Monte Carlo simulation methods (Revie et al. 2007). In addition, a much broader range of intraclass correlation estimates were provided, based on lice data sampled from both Scottish and Norwegian farms. Once again it was demonstrated that the “few fish from many cages” approach led to significant improvements in precision of the L. salmonis abundance estimates in cage-based salmon production systems. A summary of the situation worldwide with respect to sampling protocols is given in a recent review (Revie et al. 2009), and illustrates that the full implications of these findings have yet to impact sampling practices in a number of regions. The Norwegian authorities altered their protocol at the end of 2009 to an approach that is more in line with the scientific evidence gained from these studies on Scottish and

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other salmon farms. This move should lead to other countries, which tend to follow Norway’s lead, making improvements in their sampling protocols. These changes together with an overall reduction in levels being set as treatment triggers (e.g., down to 0.5 adult females per fish in Norway during the wild migration period) has led to some research as to whether prevalence, rather than abundance, may be a better metric for estimating sea lice infestation on salmon farms (Baillie et al. 2009). The author is currently working with colleagues to write a short “history” of what has often been a confusing area so that future sampling protocols will be the most effective possible (Revie et al. 2010). Returning to the specific situation on Scottish farms, while historical analyses using epi-informatics techniques in the early part of the decade had demonstrated the utility of these methods in summarizing L. salmonis infestation patterns, a number of key changes had taken place in salmon production as the decade progressed. A process pioneered by Gordon Rae (2002) to encourage stakeholders with an interest in both wild and farmed salmon to work together and to share data had taken root. As a result, by the middle of the decade, 15 Area Management Agreements (AMAs) had been established along the Scottish coast. A key role of these AMAs, as indicated in a number of chapters in this volume, is to foster strategic approaches to the management of fish farming activities at the local level, while ensuring that the interests of wild salmon populations are taken into account. Such strategies included lice control programs using coordinated fallowing and treatments, which it is hoped will lead to the most effective use of ectoparasitic medicines (Scottish Executive 2005). Arguably, even more importantly, the range of medicine that was available for sea lice interventions had altered, and for the first time in-feed medication was available. In the light of these and other changes, it was therefore important to update our understanding of the sea lice situation on Scottish farms. The potential impact of medications in feed on the Scottish situation had been explored to a limited extent in the literature. Stone and colleagues carried out much of the initial research around the effectiveness of emamectin benzoate, the active ingredient of SLICETM (Schering-Plough Animal Health), which gained marketing authorization in the United Kingdom in 2000 (Stone et al. 1999). This included a field trial of the product in a Scottish production setting (Stone et al. 2000). However, this study involved only two farm sites and investigated feeding the product to fish at one of two time points. Following registration of the product, Treasurer and colleagues reported on the use of SLICETM on two Scottish farms (Treasurer et al. 2002), while a similar Norwegian study incorporated a total of four farms (Ramstad et al. 2002). Prior to the work described below, the only other extensive surveys of emamectin use and efficacy in farmed settings had been carried out in the Bay of Fundy and in British Columbia; though both studies involved less than 20 treatments (Gustafson et al. 2006; Saksida et al. 2007). Against this background, the group at Strathclyde set out to update our understanding of sea lice dynamics on Scottish salmon farms. This work extended the lice data collection to over 50 salmon farms in Scotland and summarized the situation over an 11-year period from 1996 to 2006 (Lees et al. 2008a). Levels of sea lice infection on Scottish farms were clearly seen to have decreased in the latter years, with on average a threefold reduction seen in mobile L. salmonis in the period 2002–2006, as compared to the levels previously reported from 1996 to 2000 (Revie et al. 2002a), a pattern particularly obvious from the spring of the second year of production. A

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Table 7.2. Mean annual abundance of lice on Scottish farms shown for the first or second year of production, between the periods 1996−2000 and 2002−2006. First year of production cycle

Second year of production cycle

Reduction Reduction 1996−2000 2002−2006 [95% CI] 1996−2000 2002−2006 [95% CI] L. salmonis Mean mobiles C. elongatus Mean mobiles Number of sites Number of site-years

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43 70

Source: Data from Table 1 of Lees et al. 2008a.

summary of the mean annual levels of lice abundance collected across 262 site-years of production activity clearly shows that the situation changed significantly pre- and post-2001 (Table 7.2). It can be seen that in both the first and second years of production all stages of lice showed significant mean reductions, when mean abundance levels from 2002 to 2006 were compared to those from 1996 to 2000. As an aside, it is interesting to note that this reduction was also seen for C. elongatus, an observation that may cast doubt on the thesis that there is some competitive pressure between the species (i.e., given the significant decreases in L. salmonis over the period one might have expected the other species to increase in abundance if such competition existed). Instead, it is interesting to note that the ratio of each species’ infestation levels in both years of production remained remarkably consistent over the whole period under consideration. In addition, the previously observed pattern of higher C. elongatus numbers in the first year of production on Scottish salmon farms was maintained, with levels being around three times higher than those observed in the second year of production between 2002 and 2006. When consideration was given to regional patterns, it could be seen that the reductions after 2001 were observed throughout the Scottish industry (Lees et al. 2008a). Arguably, the most telling difference between the overall trends since 2001 and those in the prior 5 years was the improved control of mobile lice numbers during the second year of production. This can be seen very clearly in the graph shown in Figure 7.8, where the strategic spring treatments (around weeks 64, 69, and 74) drove the overall mobile numbers to a level low enough such that the exponential growth previously seen during the second years was avoided. Similarly, the “fire-fighting” mode seen in those earlier years, with large increases in lice numbers followed by rapid but shortlasting reductions, was absent from this later period. Without doubt, a key to this successful turnaround was access to more efficacious therapeutic agents. In addition to describing changes in sea lice patterns, this review paper by Lees et al. (2008a; see also Chapter 2 contributed by Murray et al.) summarized the use of chemical treatments against sea lice on Scottish farms over the period. In total, the distribution of 1149 treatment episodes, associated with 184 and 181 site-years of production in the first and second years, respectively, were analyzed. A graphical

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30 25 1996–2000 2002–2006

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Figure 7.8. Mean weekly abundance of L. salmonis mobiles on Atlantic salmon in Scottish salmon farms over two-year production cycles between 1996 and 2000 and 2002 and 2006. (Data from Figure 2b of Lees et al. 2008a.)

summary of this distribution in Figure 7.9 shows the growing use of both ExcisTM from around 1999 and then SLICETM from 2001 is evident. The older treatments, particularly dichlorvos and hydrogen peroxide, which had seen widespread use up until 1998 were largely unused after 2000. Indeed, during the first year of salmon production in Scotland, one drug (SLICETM ) became dominant, accounting for over 90% of use in 2005. While levels of SLICETM use in the second year of production only reached around 50%, due to the relatively higher cost of using an in-feed treatment on larger fish, the predominance of one active compound raises concerns as to potential lice tolerance to this chemical. In addition, from 2004 onwards the alternative treatment was limited to ExcisTM , with the other bath treatment, azamethiphos, falling into disuse. Around the time that this work was being carried out (early 2007), anecdotal reports of sea lice treatment failures associated with the use of SLICETM began to circulate in the Scottish industry. This was of particular concern, as this drug was widely considered to be the most effective option—a fact apparently borne out in reduced sea lice levels since 2001. Similar trends were being discussed in Chile and would be formally reported (Bravo et al. 2008). However, the louse species is different in Chile and there was excessive use of a number of generic emamectin benzoate products, which meant that the implications for the North Atlantic situation were unclear. The group at Strathclyde undertook an in-depth study, which reviewed the application and effectiveness of 185 SLICETM treatments used on Scottish salmon farms from 2002 to 2006 (Lees at al. 2008b). Due to data quality issues relating to adequately estimating pre- and posttreatment lice levels, only 108 interventions could be fully assessed; these were, however, associated with around 85% of the 54 farm sites from which these data had been collected. Further analysis indicated that this set was highly representative of the Scottish industry as a whole, and represented more than a fivefold increase on

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Figure 7.9. Proportion of treatments, by compound, given on Scottish salmon farms between 1996 and 2006. (Data from Figure 5 of Lees et al. 2008a that summarized 1149 treatment events from over 350 site years of data.)

the extent of data used in any other in-feed treatment efficacy analysis carried out to date (Gustafson et al. 2006; Saksida et al. 2007). A graph illustrating posttreatment knockdown in percentage sea lice levels is shown in Figure 7.10, from which it can be seen that there has been a steady reduction in effectiveness over time, most clearly evident in 2006. A more formal analysis, using general linear modeling, indicated that the issue may be more complex, with regional and seasonal factors also playing a part in the reduction in efficacy. In a follow-on paper, Lees et al. (2008c) used a range of statistical modeling techniques to examine in more detail the differences between ineffective and effective SLICETM interventions. In the initial study, ineffective treatments had been shown to result in lice numbers around ten times higher than those observed following effective treatments. A logistic regression model confirmed that there was a definite problem

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with SLICETM treatments carried out in 2006, as well as with those administered in winter—both these groups being around 11 times more likely to fail than was the case of the referent groups (2003 and spring, respectively). The analysis also showed that treatments carried out within the south region were significantly less effective than those administered elsewhere in Scotland. However, given the fact that overall lice numbers were still at a near historic low and that the mainstream media tends to latch onto any reference to drug “resistance,” the authors were cautious in their claim that clear evidence was emerging of tolerance to SLICETM in sea lice populations on Scottish farms. Recent trends in Scotland, as well as in Norway and eastern Canada, have shown that these patterns were indeed early indicators of a much wider and substantive resistance problem. While little has been published on these recent developments, reports from the field indicate that there is widespread tolerance to SLICETM across a range of lice populations (Robbins et al. 2010; and personal communications: C. Wallace, Scotland; G. Ritchie, Norway; L. Hammell, Canada). One of the key problems in quantifying such tolerance issues is the fact that gaining clear interpretations from the bioassay techniques currently available is difficult (Westcott et al. 2008). Indeed, to my knowledge, there is not one peer-reviewed article that reports on trends in bioassay tests for any lice treatment compound carried out on lice taken from Scottish farms. A number of papers investigating the potential use of mathematical models to simulate the dynamics of sea lice populations on salmon have been produced by authors with links to the situation in Scotland (Tucker et al. 2002; Revie et al. 2005c; Stien et al. 2005; Murray and Gillibrand 2006). However, little work has been carried out on applying these models to sea lice on salmon farms or to simulate, e.g., the effect of treatment strategies. The farm-focused approach adopted by the SLiDESim (Sea Lice Difference Equation Simulation) model is unique in attempting to use

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mathematical simulation techniques to predict monthly sea lice burdens in the first and second years of production on Scottish farms (Revie et al. 2005c) and explore how these infestation levels are influenced by the number, frequency, and efficacy of cypermethrin treatments (Robbins et al. 2010). One other area of research that has seen a fair bit of development over the past decade in Scotland (and around the globe) relates to the application of a range of genetic techniques, which may lead to a clearer understanding of inter alia issues of emerging resistance.

References Baillie, M., Lees, F., Gettinby, G., and Revie, C.W. 2009. The use of prevalence as a measure of lice burden: a case study of Lepeophtheirus salmonis on Scottish Atlantic salmon (Salmo salar L.) farms. Journal of Fish Diseases 32: 15–25. Black, K.D., Fleming, S., Nickell, T.D., and Pereira, P.M.F. 1997. The effects of ivermectin, used to control sea lice on caged farmed salmonids, on infaunal polychaetes. ICES Journal of Marine Science 54: 276–279. Boxshall, G.A. 1974. Infections with parasitic copepods in North Sea marine fishes. Journal of the Marine Biological Association of the United Kingdom 54: 355–372. Boxshall, D.E. and Defaye, D. (eds.) 1993. Pathogens of Wild and Farmed Fish: Sea Lice. Ellis Horwood, Chichester. Brandal, P.O. 1979. Delousing of salmon with trichlorphon. [Norwegian.] Norsk Veterinaertidsskrift 91: 665–672. Brandal, P.O. and Egidius, E. 1977. Preliminary report on oral treatment against sea lice, Lepeophtheirus salmonis with Neguvon. Aquaculture 10: 177–178. Brandal, P.O. and Egidius, E. 1979. Treatment of salmon lice (Lepeophtheirus salmonis Krøyer, 1838) with Neguvon – description of method and equipment. Aquaculture 18: 183–188. Branson, E. 1996. Sea lice – clinical signs and treatment. Veterinary Annual 36: 445–457. Bravo, S., Sevatdal, S., and Horsberg, T.E. 2008. Sensitivity assessment of Caligus rogercresseyi to emamectin benzoate in Chile. Aquaculture 282: 7–12. Bron, J.E., Sommerville, C., Wootten, R., and Rae, G.H. 1993a. Fallowing of marine Atlantic salmon, Salmo salar L., farms as a method for the control of sea lice, Lepeophtheirus salmonis (Krøyer, 1837). Journal of Fish Diseases 16: 487–493. Bron, J.E., Sommerville, C., Wootten, R., and Rae, G.H. 1993b. Influence of treatment with dichlorvos on the epidemiology of Lepeophtheirus salmonis (Krøyer, 1837) and Caligus elongatus Nordmann, 1832 on Scottish salmon farms. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. DeFaye), pp. 263–274. Ellis Horwood, Chichester. Bron, J.E., Sommerville, C., and Rae, G.H. 1993c. Aspects of the behaviour of copepodid larvae of the salmon louse Lepeophtheirus salmonis (Krøyer, 1837). In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. DeFaye), pp. 125–142. Ellis Horwood, Chichester. Bruno, D.W. and Stone, J. 1990. The role of saithe Pollachius virens L. as a host for the sea lice of Lepeophtheirus salmonis and Caligus elongatus. Aquaculture 89: 201–207. Butler, J.R.A. 2002. Wild salmonids and sea louse infestations on the west coast of Scotland: sources of infection and implications for the management of marine salmon farms. Pest Management Science 58: 595–608. Butler, J.R.A., Marshall, S., Watt, J., Kettlewhite, A., Bull, C.R., Bilsby, M., Ribbens, J., Sinclair, C.A., Stoddart, R.C., and Crompton, D.W.T. 2001. Patterns of sea lice infestations on Scottish west coast sea trout: survey results, 1997–2000. 1–22. Association of West Coast Fisheries Trusts.

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Davies, I. and Rodger, G. 2000. A review of the use of ivermectin as a treatment for sea lice [Lepeophtheirus salmonis (Krøyer) and Caligus elongatus Nordmann] infestation in farmed Atlantic salmon (Salmo salar L.). Aquaculture Research 31: 869–883. Davies, I.M., McHenery, J.G., and Rae, G.H. 1997. Environmental risk from dissolved ivermectin to marine organisms. Aquaculture 158: 263–275. Denholm, I., Devine, G.J., Horsberg, T.E., Sevatdal, S., Fallang, A., Nolan, D.V., and Powell R. 2002. Analysis and management of resistance to chemotherapeutants in salmon lice, Lepeophtheirus salmonis (Copepoda: Caligidae). Pest Management Science 58: 528–536. Dixon, B., Shinn, A. and Sommerville, C. 2004. Genetic characterisation of populations of the ectoparasitic caligid, Lepeophtheirus salmonis (Krøyer, 1837) using randomly amplified polymorphic DNA. Aquaculture Research 35: 730–741. Glover, K.A., Nilsen, F., Skaala, O., Taggart, J.B., and Teale, A.J. 2001. Differences in susceptibility to sea lice (Lepeophtheirus salmonis) infection between a sea run and a freshwater resident population of brown trout (Salmo trutta). Journal of Fish Biology 59: 1512– 1519. Glover, K.A., Hamre, L.A., Skaala, Ø. and Nilsen, F. 2004. A comparison of sea louse (Lepeophtheirus salmonis) infection levels in farmed and wild Atlantic salmon (Salmo salar L.) stocks. Aquaculture 232: 41–52. Glover, K.A., Skaala, O., Nilsen, F., Olsen, R., Teale, A.J. and Taggart, J.B. 2003. Differing susceptibility of anadromous brown trout (Salmo trutta L.) populations to salmon louse (Lepeophtheirus salmonis (Krøyer, 1837)) infection. ICES Journal of Marine Science 60: 1139–1148. Grant, A.N. 2002. Medicines for sea lice. Pest Management Science 58: 521–527. Grant, A.N. and Treasurer, J.W. 1993. The effects of fallowing on caligad infestations on farmed Atlantic salmon (Salmo salar L.) in Scotland. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall G.A. and D. DeFaye), pp. 255–260. Ellis Horwood, Chichester. Gu, Y., Gettinby, G., McKendrick, I.J., Murray, M., Peregrine, A., and Revie, C. 1999. Development of a Decision Support System for Trypanocidal Drug Control of Bovine Trypanosomosis in Africa. Veterinary Parasitology 87: 9–23. Gustafson, L., Ellis, S., Robinson, T., Marenghi, F., and Endris, R. 2006. Efficacy of emamectin benzoate against sea lice infestations of Atlantic salmon, Salmo salar L.: evaluation in the absence of an untreated contemporary control. Journal of Fish Diseases 29: 621–627. Heuch, P.A. 1995. Experimental evidence for aggregation of salmon louse copepodids (Lepeophtheirus salmonis) in step salinity gradients. Journal of the Marine Biological Association of the United Kingdom 75: 927–939. Heuch, P.A. and Karlsen, H.E. 1997. Detection of infrasonic water oscillations by copepodids of Lepeophtheirus salmonis (Copepoda: Caligidae). Journal of Plankton Research 19: 735–747. Heuch, P.A., Parsons, A., and Boxaspen, K. 1995. Diel migration: a possible host-finding mechanism in salmon louse (Lepeophtheirus salmonis) copepodids? Canadian Journal of Fisheries and Aquatic Sciences 52: 681–689. Heuch, P.A., Revie, C.W. and Gettinby, G. 2003. A comparison of epidemiological patterns of salmon lice (Lepeophtheirus salmonis) infections in Norway and Scotland. Journal of Fish Diseases 26: 539–551. Heuch, P.A., Stigum, O., Malkenes, R., Revie, C.W., Gettinby, G., Baillie, M., Lees, F., and Finstad, B. 2009. The spatial and temporal variations in Lepeophtheirus salmonis infection on salmon farms in the Hardanger fjord 2004–2006. Journal of Fish Diseases 32: 89–100. Hogans, W.E. and Trudeau, D.J. 1989. Caligus elongatus (Copepoda: Caligoida) from Atlantic salmon (Salmo salar) cultured in marine waters of the lower Bay of Fundy. Canadian Journal of Zoology 67: 1080–1082. Hull, M.Q., Pike, A.W., Mordue, A.J., and Rae, G.H. 1998. Patterns of pair formation and mating in an ectoparasitic caligid copepod Lepeophtheirus salmonis (Krøyer 1837): implications for its sensory and mating biology. Philosophical Transactions of the Royal Society of London Series B–Biological Sciences 353: 753–764.

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Ingvarsd´ ottir, A., Birkett, M.A., Duce, I., Genna, R.L., Mordue, W., Pickett, J.A., Wadhams, L.J., and Mordue (Luntz), A.J. 2002. Semiochemical strategies for sea louse control: host location cues. Pest Management Science 58: 537–545. Isdal, E., Nylund, A., and Naevdal, G. 1997. Genetic differences among salmon lice (Lepeophtheirus salmonis) from six Norwegian coastal sites: evidence from allozymes. Bulletin of the European Association of Fish Pathologists 17: 17–22. Johnson, S.C. and Albright, L.J. 1991. Development, growth, and survival of Lepeophtheirus salmonis (Copepoda: Caligidae) under laboratory conditions. Journal of the Marine Biological Association of the United Kingdom 71: 425–436. Jones, S.R.M. 2001. The occurrence and mechanisms of innate immunity against parasites in fish. Developmental & Comparative Immunology 25: 841–852. Jones, C.S., Lockyer, A.E., Verspoor, E., Secombes, C.J., and Noble, L.R. 2002. Towards selective breeding of Atlantic salmon for sea louse resistance: approaches to identify trait markers. Pest Management Science 58: 559–568. Kiemer, M.C.B. and Black, K.D. 1997. The effects of hydrogen peroxide on the gill tissues of Atlantic salmon, Salmo salar L. Aquaculture 153: 181–189. Kolstad, K., Heuch, P.A., Gjerde, B., Gjedrem, T. and Salte, R. 2005. Genetic variation in resistance of Atlantic salmon (Salmo salar) to the salmon louse Lepeophtheirus salmonis. Aquaculture 247: 145–151. Kvenseth, A.M. 1998. Wrasse – do they transfer diseases to salmon? Caligus Newsletter, Issue 5: 2–4. Lees, F., Gettinby, G., and Revie, C.W. 2008a. Changes in epidemiological patterns of sea lice infestation on farmed Atlantic salmon (Salmo salar L.) in Scotland between 1996 and 2006. Journal of Fish Diseases 31: 251–262. Lees, F., Baillie, M., Gettinby, G., and Revie, C.W. 2008b. The efficacy of emamectin benzoate against infestations of Lepeophtheirus salmonis on farmed Atlantic salmon (Salmo salar L.) in Scotland between 2002 and 2006. PLoS One 3(2): e1549.F. Lees, F., Baillie, M., Gettinby, G., and Revie, C.W. 2008c. Factors associated with changing efficacy of emamectin benzoate against infestations of Lepeophtheirus salmonis on Scottish salmon farms. Journal of Fish Diseases 31: 947–951. Mackenzie, K. and Morrison, J.A. 1989. An unusually heavy infestation of herring (Clupea harengus L.) with the parasitic copepod Caligus elongatus Nordmann, 1832. Bulletin of the European Association of Fish Pathologists 9: 12–13. MacKenzie, K., Longshaw, M., Begg, G.S., and McVicar, A.H. 1998. Sea lice (Copepoda: Caligidae) on wild sea trout (Salmo trutta L.) in Scotland. ICES Journal of Marine Science 55: 151–162. Mackinnon, B.M. 1998. Host factors important in sea lice infections. ICES Journal of Marine Science 55: 188–192. Marshall, S. 2003. The incidence of sea lice infestations on wild sea trout compared to farmed salmon. Bulletin of the European Association of Fish Pathologists 23: 72–79. McAndrew, K.J., Sommerville, C., Wootten, R. and Bron, J.E. 1998. The effects of hydrogen peroxide treatment on different life-cycle stages of the salmon louse Lepeophtheirus salmonis (Krøyer, 1837). Journal of Fish Diseases 21: 221–228. McHenery, J.G., Saward, D., and Seaton, D.D. 1991. Lethal and sub-lethal effects of the salmon delousing agent dichlorvos on the larvae of the lobster (Homarus gammarus L.) and herring (Clupea harengus L.). Aquaculture 98: 331–347. McKendrick, I.J., Gettinby, G., Gu, Y., Peregrine, A., and Revie, C. 1995. Hybrid information systems for agriculture: the case of cattle trypanosomiasis in Africa. Outlook on Agriculture 23: 261–267. McKendrick, I.J., Gettinby, G., Gu, Y., Reid, S.W.J., and Revie, C.W. 2000. Using a Bayesian belief network to aid differential diagnosis of tropical bovine diseases. Preventative Veterinary Medicine 47: 141–156.

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Todd, C.D., Whyte, B.D.M., MacLean, J.C., and Walker, A.M. 2006. Ectoparasitic sea lice (Lepeophtheirus salmonis Krøyer, Caligus elongatus Nordmann) infestations of wild adult one sea-winter Atlantic salmon Salmo salar L. returning to Scotland, 1998–2005. Marine Ecology Progress Series 328: 183–193. Treasurer, J.W. 1993a. Management of sea lice (Caligidae) with wrasse (Labridae) on Atlantic salmon (Salmo salar L.) farms. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. DeFaye), pp. 335–345. Ellis Horwood, Chichester. Treasurer, J.W. 1993b. More facts on the role of wrasse in louse control. Fish Farmer 16: 37–38. Treasurer, J.W. 1998. Sea lice management methods in Scotland. Caligus Newsletter, 5: 8–12. Treasurer, J.W. 2005. Cleaner fish: a natural approach to the control of sea lice on farmed fish. Veterinary Bulletin 75: 17N–29N. Treasurer, J.W. and Grant, A. 1997. Optimal timing for lice treatments. Fish Farmer Nov/Dec: 20–21. Treasurer, J.W. and Pope, J.A. 2000. Selection of host sample number and design of a monitoring programme for ectoparasitic sea lice (Copepoda: Caligidae) on farmed Atlantic salmon, Salmo salar. Aquaculture 187: 247–260. Treasurer, J.W., Wadsworth, S., and Grant, A. 2000. Resistance of sea lice, Lepeophtheirus salmonis (Krøyer), to hydrogen peroxide on farmed Atlantic salmon, Salmo salar L. Aquaculture Research 31: 855–860. Treasurer, J.W., Wallace, C., and Dear, G. 2002. Control of sea lice on farmed Atlantic salmon S. salar L. with the oral treatment emamectin benzoate (SLICE). Bulletin of the European Association of Fish Pathologists 22: 375–380. Treasurer, J., Wallace, C., and Dear, G. 2003. Success of oral treatment set to boost Scotland’s National Sea Lice Treatment Strategy. Fish Farmer 26: 38–39. Tucker, C.S., Sommerville, C., and Wootten, R. 2000. An investigation into the larval energetics and settlement of the sea louse, Lepeophtheirus salmonis, an ectoparasitic copepod of Atlantic salmon, Salmo salar. Gyobyo Kenkyu = Fish Pathology 35: 137–143. Tucker, C.S., Norman, R., Shinn, A.P., Bron, J.E., Sommerville, C., and Wootten, R. 2002. A single cohort time delay model of the life-cycle of the salmon louse Lepeophtheirus salmonis on Atlantic salmon Salmo salar. Gyobyo Kenkyu = Fish Pathology 37: 107–118. Tully, O. 1989. The succession of generations and growth of the caligoid copepods Caligus elongatus and Leopeoptheirus salmonis parasitising farmed Atlantic salmon smolts (Salmo salar L.). Journal of the Marine Biological Association United Kingdom 69: 279– 287. Tully, O. and Nolan, D.T. 2002. A review of the population biology and host-parasite interactions of the sea louse Lepeophtheirus salmonis (Copepoda Caligidae). Parasitology 124: s165–s182. Wadsworth, S.L. 1998. The control of Lepeophtheirus salmonis (Krøyer 1837) (Copepoda: Caligidae) on Atlantic salmon Salmo salar L. production sites. PhD Thesis. University of Aberdeen, Scotland, UK. Wadsworth, S., Grant, A., and Treasurer, J. 1998. A strategic approach to lice control. Fish Farmer 21: 8–9. Westcott, J.D., Stryhn, H., Burka, J.F., and Hammell, K.L. 2008. Optimization and field use of a bioassay to monitor sea lice Lepeophtheirus salmonis sensitivity to emamectin benzoate. Diseases of Aquatic Organisms 79: 119–131. Wootten, R. 1985. Experience of sea lice infestations in Scottish salmon farms. ICES Mariculture Committee M1985/F:7/Ref. M. Wootten, R., Smith, J.W., and Needham, E.A. 1982. Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids and their treatment. Proceedings of the Royal Society of Edinburgh 81B: 185–197.

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Chapter 8

Sea Lice Management on Salmon Farms in British Columbia, Canada Sonja M. Saksida, Diane Morrison, Mark Sheppard, and Ian Keith

Introduction In Canada, salmon farming occurs in British Columbia and in a number of the provinces that border the Atlantic Ocean on Canada’s east coast—primarily New Brunswick, Nova Scotia, Prince Edward Island, and Newfoundland. The salmon farming industry in British Columbia is significantly bigger than the east coast industry and on its own is considered the fourth largest salmon farming area in the world. A relative newcomer amongst the province’s agriculture-based industries, the salmon farming sector has grown rapidly to become a vital part of the local economy in many coastal communities. In the span of 20 years, the salmon farming industry has become the province’s largest agricultural exporter and an enormous contributor to coastal economies. Farmed Atlantic salmon (Salmo salar) is the province’s single-most significant commodity with the largest harvest and highest landed value of any species—wild or cultured. In 2008, the farm gate value of Atlantic salmon was estimated to be $394.1 million dollars (British Columbia Ministry of Environment 2009). The first salmon farm in British Columbia began operation in 1971. The salmon aquaculture industry developed quickly from 12 operating farms in 1984 to 137 tenures in 2009 (Figure 8.1). In general, only 70–90 of these tenures operate at any one time, thus allowing others to fallow. Since the mid-1990s, very few new farm tenures have been made available; and in 2008, a moratorium was placed on salmon farm expansion into the province’s north coast. Through rationalization and consolidation, the number of companies has declined from 70 in 1989 to 14 in 2002 and by 2008 only four major salmon producers remained: three rearing Atlantic salmon and one rearing chinook salmon (Oncorhynchus tschawytscha) (Figure 8.1). In addition to these four companies, a few smaller producers who raise mainly Pacific salmon species continue to operate. In the early days of fish farming, mostly Pacific salmon species—chinook and coho (Oncorhynchus kisutch) salmon—were raised. Over time, there was a gradual switch to Atlantic salmon that were better suited to being reared in a cultured environment and,

Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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History of salmon farming in British Columbia (B.C. Ministry of Environment Oceans and Marine Fisheries)

140 120 100 80 60 40 20 0 1984 1989 1992 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009

Companies

RndWt Production (’000 tons)

SW salmon tenures

Figure 8.1. The production, number of tenures, and companies farming salmon since the early 1980s to 2009.

therefore, achieved better growth, feed conversion, and higher survival than Pacific salmon species raised in the same environment. As a result, a steady increase in Atlantic salmon production occurred during the 1990s and into the early 2000s. Part of this production growth resulted from egg importations (mainly McConnell and Mowi stocks originally obtained from Europe) during the late 1980s and mid-1990s. Farmed salmon production in 1995 was approximately 27,000 metric tons (mt), 68% of which was Atlantic salmon. By 2008, production tripled to 81,400 mt, of which 94% were Atlantic salmon (Figure 8.1). British Columbia’s salmon farms are situated primarily around Vancouver Island, the largest island off the west coast of North America (over 31,000 km2 ). Between Vancouver Island and the British Columbia mainland there are four major farming clusters and on the western coast of Vancouver Island there are three major farming clusters (see Figure 8.2). Salmon are also farmed in a region located on the midcoast of the mainland around the First Nation community of Klemtu. For the specific purposes of surveillance and reporting of health issues, the provincial coastline is divided into a series of fish health zones (see Figure 8.2). In general, zonal boundaries follow major drainages or watersheds. Currently, British Columbia salmon farms are contained within seven zones. British Columbia is home to significant runs of five species of Pacific salmon, some of which utilize large river systems to travel deep into the interior of the province (Groot and Margolis 1991). These salmon are critical to the ecological, cultural, and economic fiber of the region (Gende et al. 2002). This makes British Columbia one of the few regions in the world that farms salmon in waters with an abundance of wild salmon. And not surprisingly, when these animals appear to be threatened—people notice. Recent studies suggest that sea lice from farmed Atlantic salmon are infesting and killing wild juvenile salmon in coastal British Columbia (Morton et al. 2004, 2008; Krkoˇsek et al. 2005, 2006a, 2006b, 2007).

P1: SFK/UKS BLBS084-08

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July 6, 2011

14:32

Trim: 244mm×172mm

Sea Lice Management on Salmon Farms in British Columbia, Canada

237

Klemtu 3–5

Port Hardy area 3–4

Broughton Archipelago

British Columbia Campbell River area 3–2

3–3 Quatsino Sound

Sunshine Coast

2–2 2–4

3–1 Nootka Sound

Clayquot Sound

2–3 2–1

Figure 8.2. Map of southwestern British Columbia illustrating the location of salmon farms and the fish health monitoring zones.

Sea Lice Species Infesting Salmon in British Columbia Although there are 12 species of sea lice in British Columbia (Kabata 1972), the two species of sea lice most commonly reported on wild (Beamish et al. 2005) and farmed salmonids (Saksida et al. 2007a) in coastal British Columbia are Lepeophtheirus salmonis and Caligus clemensi. On occasion, other marine ectoparasitic copepods, including L. cuneifer (Kabata 1974), have been observed on farmed salmon in British Columbia (Johnson and Albright 1991a). The introductory chapter contributed by

P1: SFK/UKS BLBS084-08

P2: SFK BLBS084-Beamish

238

July 6, 2011

14:32

Trim: 244mm×172mm

Salmon Lice

Hayward et al. has summarized the biology of L. salmonis. C. clemensi, like Caligus elongatus that is found in the Atlantic Ocean, has a broad host range including both nonsalmonid teleost and elasmobranch hosts (Johnson et al. 2004). In a recent study, Beamish et al. (2009) presented data to support a proposal that Pacific herring (Clupea pallasii) are an important source of C. clemensi for juvenile salmon in coastal British Columbia. Furthermore, the evidence of infection in the spawning area and the abundance and migratory nature of Pacific herring led them to propose that C. clemensi could be transported from the spawning area by these same adult Pacific herring. While the authors studied only one area and even though they did not link C. clemensi on the salmon to the spawning Pacific herring, the finding may be an important contribution to an understanding of the factors that regulate C. clemensi abundance in coastal British Columbia.

Health Effects of L. salmonis in British Columbia An important distinction exists between sea lice infections of farmed Atlantic salmon in the North Atlantic and those which occur in the North Pacific, especially with regards to the degree of health concerns that result from L. salmonis infestations. Serious health issues associated with L. salmonis infections on farmed salmon are frequently reported by salmon farming regions located in Europe and eastern North America, but not in Japan and on Canada’s west coast (British Columbia) (Johnson et al. 2004). In British Columbia, heavy infestations and damage as a result of infections with L. salmonis are rare and aquaculture veterinarians do not consider sea lice to be a serious health concern (Saksida et al. 2007a). In the past, these differences in pathology and epidemiology were difficult to explain as the lice in British Columbia were believed to be the same species found in the North Atlantic. However, a growing body of scientific evidence suggests this may not be the case. Several studies (see the introductory chapter contributed by Hayward et al.) suggest that the Pacific variety of L. salmonis is not only genetically different from that occurring in the Atlantic Ocean, but may also exhibit differences that potentially lower infectivity in Atlantic salmon.

Sea Lice on Salmon Farms in British Columbia Sea lice infestations are not considered a significant health issue on farmed salmon in British Columbia since pathogenic lesions as described in the literature (Finstad et al. 2000) and observed in Europe are rarely seen in British Columbia. As a consequence, prior to 2003, enumeration of sea lice only occurred if there were health and/or welfare concerns at the farm. Consequently, treatments were rare and few records were kept. In 2002, an unexpectedly low return of pink salmon (Oncorhynchus gorbuscha) led to reports in scientific journals (Morton and Williams 2003) and in the popular press suggesting that sea lice from Atlantic salmon farms were having negative impacts on juvenile wild pink salmon and, as a result, were affecting wild salmon returns. Farms located in the Broughton Archipelago were singled out: between 2000 and 2006, farms in this area constituted 35–39% of the total farmed Atlantic salmon production in British Columbia. In response, in 2003, the provincial government instituted stringent

P1: SFK/UKS BLBS084-08

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July 6, 2011

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Sea Lice Management on Salmon Farms in British Columbia, Canada

239

sea lice monitoring systems and control measures on salmon farms (described in Saksida et al. 2007a). In March of that year, routine sea lice monitoring began on Atlantic salmon farms in the Broughton Archipelago. Originally, this monitoring was part of the Broughton Archipelago Sea Lice Action Plan (Saksida et al. 2007a). In October 2003, the monitoring program was expanded to include all British Columbia salmon farms as part of a provincial management plan known as the Sea Lice Management Strategy. The Sea Lice Management Strategy stipulated that during the period of juvenile pink salmon migration out of the nearshore (March–July), L. salmonis are to be below three motile lice per fish (including all preadult and adult male and female L. salmonis stages). During this period (March–July), if sea lice levels exceed this threshold, the fish must either be treated with medicant or be harvested. Management options during the rest of the year remain at the discretion of the farmer and the attending veterinarian. This threshold was not based on scientific evidence but instead was determined by government and industry as a level that would allow precautionary management while more scientific data were gathered to better inform the issue. This precautionary level was an acknowledgment of the lack of serious disease occurring on British Columbia farmed salmon compared to other jurisdictions that had L. salmonis; and the large populations of wild salmon in British Columbia that are known to carry sea lice and thus greatly influence the sea lice abundance on the farmed salmon, particularly in the autumn months. By comparison, in Europe, where serious problems with sea lice infestations had been reported on farmed salmon since the 1970s (Brandal and Egidius 1979; Wootten et al. 1982), the maximum thresholds in Norway had been set at two adult female L. salmonis during spring and summer until 2000 when the levels were decreased to 0.5 adult female L. salmonis (or six motile L. salmonis) (Heuch et al. 2005; see also Chapter 5 contributed by Ritchie and Boxaspen). The threshold level in British Columbia was therefore lower than that prescribed in Norway during the same time. Since October 2003, farms growing Atlantic salmon in British Columbia have been required to report sea lice data. This included compulsory reporting of the abundance of chalimus and motile stages (preadult and adult stages) of C. clemensi and L. salmonis on a monthly basis. Monitoring and reporting of sea lice data on a farm began as soon as 1 month had passed since the entry of the third pen of smolts; reporting ended when less than three pens remain during harvest. The mandatory reporting may be interrupted in the event of sea lice treatment, fish health events, or environmental problems, such as low dissolved oxygen. The protocol for monitoring sea lice on salmon farms required that 20 fish from each of three pens be assessed. Sampled pens include one index pen, i.e., the first pen populated in the system, and two randomly selected pens per sample period. Farms growing Pacific salmon were required to monitor and report sea lice information less frequently: 30 fish per farm on a quarterly basis. For assessment, fish were most often sedated in totes and examined for sea lice. The totes were examined for detached lice as well. Motile stages of L. salmonis and C. clemensi were identified and counted. Attached stages (copepodid and chalimus stages) were counted also, but species determination was not required. The farms reported counts to a central database owned by the British Columbia Salmon Farmers Association, and monthly reports summarizing sea lice abundance for motile L. salmonis, adult female L. salmonis, and motile C. clemensi by zone were provided to the British Columbia Ministry of Agriculture and Lands (Table 8.1). These monthly sea

240

Zone 2.3 Oct-03 Nov-03 Dec-03 Zone 2.4 Oct-03 Nov-03 Dec-03

0.1 0.0

0.8 0.1 0.7

1.7 0.9 1.3

se

0.3 0.1 ∗

All motile stages

0.6 0.3 0.6

0.1 0.0 ∗

Adult female only

L. salmonis

0.4 0.0 0.4

0.1 0.0

se

0.0 0.0 0.0

0.0 0.0 ∗

All motile stages

0.0 0.0 0.0

0.0 0.0

se

C. clemensi

3 2 3

2 2 0

Number of farms

0.5 2.3 1.7

3.9 2.6 2.2

All motile stages

0.0 0.9 0.7

0.0 0.0 0.0

se

0.4 1.1 0.8

0.1 2.0 2.1

Adult female only

L. salmonis

0.0 0.4 0.4

0.0 0.0 0.0

se

0.0 0.0 0.1

0.0 0.0 0.0

All motile stages

0.0 0.0 0.4

0.0 0.0 0.0

se

C. clemensi

1 3 3

1 1 1

Number of farms

14:32

Year 2

July 6, 2011

Year 1

BLBS084-Beamish

A: 2003

BLBS084-08

Table 8.1. (a–g). Monthly mean abundance and standard error (se), by zone, month, and year from 2003 to 2009, for motile L. salmonis (all male and female preadult and adult stages), female L. salmonis (adult female only), and motile C. clemensi (all male and female preadult and adult stages), on Atlantic salmon in seawater less than 1 year (Year 1) and greater than 1 year in seawater (Year 2).

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.0

0.0

0.9 0.8 0.6

0.0 0.0 0.0

2.0 ∗ 0.1

2.1 1.9 1.3

1.6 0.9 1.8 ∗ ∗ ∗

0.0 0.0 0.0 ∗ ∗ ∗

0.8 0.0 1.3

0.5 1.0 0.5

0.1 ∗ 0.0

0.0 0.0 ∗

0.0 0.0 0.0

0.3 0.7 0.3

0.0

0.0

0.0 0.0

0 0 0

1 1 1

7 7 5

1 0 1

2 2 0

∗ ∗ ∗

1.0 ∗ 2.1

8.9 5.2 5.9

4.2 ∗ 12.8

1.6 ∗ 0.8

0.0

0.6

3.1 3.2 2.5

0.0

4.2

0.2

0.0

∗ ∗ ∗

0.1 ∗ 0.4

2.8 2.4 2.8

1.6 ∗ 4.9

1.2 ∗ 0.4

0.4

0.1

1.1 1.6 1.3

0.0

1.6

0.1

0.0

∗ ∗ ∗

0.0 ∗ 0.0

3.5 2.1 4.1

0.1 ∗ 0.9

0.0 ∗ 0.0

0.0

0.0

2.2 1.3 2.3

0.0

0.1

0.0

0.0

(Continued )

0 0 0

2 0 2

5 5 7

2 0 1

1 0 2

14:32

0.6 0.6 1.5

0.3 0.3 0.3

0.0

0.0

0.1 0.3

July 6, 2011

0.5 0.6 0.5

0.9 ∗ 0.0

0.1 0.6 ∗

BLBS084-Beamish

∗ ∗ ∗

0.1 0.6

0.2 1.1 ∗

BLBS084-08

Zone 3.1 Oct-03 Nov-03 Dec-03 Zone 3.2 Oct-03 Nov-03 Dec-03 Zone 3.3 Oct-03 Nov-03 Dec-03 Zone 3.4 Oct-03 Nov-03 Dec-03 Zone 3.5 Oct-03 Nov-03 Dec-03

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

241

242

0.6 1.6 3.9 0.1 0.0 0.1 0.1

0.9 1.3 0.1 0.2 0.2 0.3 0.4

1.5 1.6 0.2 0.4 0.5 0.3 0.5

0.4 0.0 0.0 0.0

0.6 0.1 0.2 0.1 ∗ 1.5 2.0 4.1 0.2 0.1 0.3 0.3 0.3 0.4 0.0 0.0 0.2 0.1 0.1

0.4 0.0 0.1 0.1 ∗ 1.0 0.4 1.6 0.0 0.0 0.1 0.2 0.2 0.4 0.0 0.0 0.1 0.1 0.0

0.6 0.3 1.5 0.0 0.0 0.0 0.1

0.3 0.0 0.0 0.1

se

0.0 0.1 0.0 0.0 0.0 0.0 0.1

0.0 0.0 0.1 0.1 ∗ 1.9 0.2 1.7 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.1

1.7 0.1 1.7 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0

se

4 4 3 3 3 2 3

2 1 1 2 0 4 5 3 4 5 4 3

Number of farms

3.7 4.8 8.8 2.6 0.4 0.3 0.4

1.0 2.8 2.6 0.1 0.1 0.8 ∗ ∗ ∗ 0.9 0.0 0.0

All motile stages

0.7 1.2 3.7 1.2 0.2 0.1 0.2

0.0 0.0 0.0

0.0 1.4 1.4 0.0 0.1 0.3

se

1.7 1.7 3.5 1.3 0.2 0.1 0.2

0.7 1.1 1.5 0.1 0.1 0.5 ∗ ∗ ∗ 0.6 0.0 0.0

Adult female only

L. salmonis

0.3 0.6 1.5 0.6 0.1 0.1 0.1

0.0 0.0 0.0

0.0 0.3 0.6 0.0 0.1 0.2

se

0.0 0.0 0.1 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.1 1.7 ∗ ∗ ∗ 0.0 0.0 0.0

All motile stages

0.0 0.0 0.1 0.0 0.0 0.0 0.0

0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.0 1.0

se

C. clemensi

4 4 5 5 5 4 3

1 2 2 1 2 3 0 0 0 1 1 1

Number of farms

14:32

Zone 2.3 Jan-04 Feb-04 Mar-04 Apr-04 May-04 Jun-04 Jul-04 Aug-04 Sep-04 Oct-04 Nov-04 Dec-04 Zone 2.4 Jan-04 Feb-04 Mar-04 Apr-04 May-04 Jun-04 Jul-04

se

All motile stages

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

B: 2004

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.1 0.1 0.2 1.1 0.1 0.2 0.1

0.0 0.0

0.0 0.0 0.8 0.6 0.3 0.3 0.5 0.4 0.1 0.0 0.1 0.1

0.0 0.0

0.1 0.0 0.9 1.2 0.5 0.7 0.8 1.1 0.4 0.1 0.2 0.4

0.0

0.0

2.9 0.5 0.0

0.0 0.0 0.3 0.2 0.2 0.2 0.2 0.4 0.1 0.0 0.1 0.1

0.0 0.0 0.3 0.1 0.1 0.1 0.2 0.2 0.0 0.0 0.1 0.1

0.0 1.0 0.4 0.4 0.3 0.2 0.1 0.2 0.0 0.0 0.1 0.2

0.0 0.0

0.0 ∗ ∗ 0.0 0.1 0.0 0.0 0.0 0.1 0.0

0.0 0.0 0.0 ∗ 0.0

0.0 0.0 0.4 0.0 0.2 0.1 0.1 0.2 0.0 0.0 0.1 0.1

0.0 0.0

0.0 0.1 0.0 0.0 0.0 0.1 0.0

0.0

0.0

0.0 0.0 0.0

1 1 2 2 3 4 4 4 2 4 4 4

1 2

1 0 0 2 2 2 2 3 2 3

3 2 1 0 1

0.0 0.1

0.0 0.0 0.6 0.0 0.6 0.0 0.0 0.0 0.0 0.0 0.0

∗ 4.1 0.1 1.0 2.0 2.1 0.6 1.3 1.5 1.1 1.8 0.3

0.0 0.2 0.0 0.1 0.2 0.1 0.0 0.0 0.0

0.1 0.5 0.8

0.6

0.0 0.1

1.1 0.9 0.3 1.2 0.6 1.4 1.8 0.3 0.1 ∗

3.8 ∗ 0.3 1.4 2.0

∗ 2.2 0.0 0.0 0.4 0.4 0.5 0.7 0.5 0.5 0.6 0.0

0.0 0.1

0.7 0.4 0.2 0.7 0.4 1.0 1.2 0.1 0.0 ∗

1.8 ∗ 0.1 0.4 0.9

0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.1

0.0 0.1 0.0 0.0 0.2 0.1 0.0 0.0 0.0

0.0 0.2 0.4

0.7

∗ 0.2 1.0 0.1 0.0 0.5 0.0 0.3 0.1 0.1 0.0 0.0

0.0 0.1

0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 ∗

0.0 ∗ 0.1 0.0 0.0

0.0 0.0 0.1 0.0 0.4 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0

0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0

0.1 0.0 0.0

0.0

243

(Continued )

0 1 1 1 1 1 1 1 1 1 1 1

2 2

1 2 1 2 2 2 1 1 1 0

2 0 2 5 5

14:32

0.0 0.0

0.0 0.0 0.1 0.5 0.0 0.1 0.1

0.0

0.0

0.7 0.4 0.0

July 6, 2011

0.0 0.0

0.0 ∗ ∗ 0.0 0.0 0.1 0.5 0.0 0.1 0.1

1.3 0.4 2.0 ∗ 0.0

BLBS084-Beamish

0.3 ∗ ∗ 0.2 0.1 0.3 1.1 0.1 0.3 0.2

5.2 0.6 4.2 ∗ 0.0

BLBS084-08

Aug-04 Sep-04 Oct-04 Nov-04 Dec-04 Zone 3.1 Jan-04 Feb-04 Mar-04 Apr-04 May-04 Jun-04 Jul-04 Aug-04 Sep-04 Oct-04 Zone 3.1 Nov-04 Dec-04 Zone 3.2 Jan-04 Feb-04 Mar-04 Apr-04 May-04 Jun-04 Jul-04 Aug-04 Sep-04 Oct-04 Nov-04 Dec-04

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

244

Zone 3.3 Jan-04 Feb-04 Mar-04 Apr-04 May-04 Jun-04 Jul-04 Aug-04 Sep-04 Oct-04 Nov-04 Dec-04

1.0 0.9 1.0 1.6 2.5 2.4 1.7 2.4 2.3 1.6 2.3 2.6

0.6 0.5 0.4 0.5 0.7 0.6 1.1 2.0 1.3 1.2 2.1 2.3

se 0.3 0.3 0.3 0.1 0.4 0.7 0.3 0.8 0.6 0.6 0.7 0.8

0.2 0.2 0.2 0.0 0.2 0.3 0.2 0.7 0.3 0.5 0.6 0.7

se 1.8 0.2 0.3 0.3 1.1 0.2 0.2 0.1 0.1 0.1 0.3 0.3

All motile stages 1.8 0.1 0.1 0.1 0.6 0.1 0.1 0.1 0.1 0.1 0.2 0.1

se 6 5 5 2 4 4 4 3 4 4 3 3

Number of farms 8.8 3.4 2.0 4.4 7.0 4.5 2.0 1.9 2.1 2.5 3.6 4.6

All motile stages 4.6 0.1 0.6 1.2 2.8 1.9 0.6 0.6 0.9 1.5 2.1 1.8

se

4.6 1.7 1.0 1.1 4.0 2.0 0.9 1.1 1.2 1.6 1.9 2.3

Adult female only

L. salmonis

2.5 0.7 0.3 0.3 1.8 0.9 0.3 0.4 0.6 0.9 0.9 0.9

se

4.2 0.9 0.4 0.3 0.7 0.7 0.1 0.1 0.3 0.8 0.4 1.3

All motile stages

3.5 0.5 0.2 0.1 0.3 0.3 0.1 0.1 0.2 0.5 0.3 0.7

se

C. clemensi

8 7 10 12 11 11 11 10 7 6 9 9

Number of farms

14:32

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

B: 2004

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.1 1.8 0.9 0.3 0.1 0.1 0.3 0.1 0.3 1.5

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

∗ ∗ 3.7 8.0 15.7 1.9 0.3 0.1 0.8 0.6 1.0 1.9

∗ ∗ ∗ ∗ 0.1 0.0 0.6 0.1 0.1 0.3 0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.4

0 0 0 0 1 1 1 1 1 1 1 2

∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗

3.3 ∗ ∗ ∗ ∗ 2.6 0.6 1.4 2.6 4.0 11.0 9.9 2.2 0.2 0.8 0.4 1.3 3.9 0.0

0.0

∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗

1.2 ∗ ∗ ∗ ∗ 1.2 0.2 0.5 0.7 2.7 7.0 5.9 0.9 0.1 0.4 0.1 1.1 3.4 0.0

0.0

∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗ ∗

0.0 ∗ ∗ ∗ ∗ 0.0 0.0 0.1 0.0 0.4 0.2 1.5 0.0 0.0 0.1 0.0 0.4 0.0 0.0

0.0

0 0 0 0 0 0 0 0 0 0 0 0

1 0 0 0 0 2 2 2 2 2 2 1

14:32

∗ ∗ ∗ ∗ 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.4

0.4 0.1 0.1 0.0 0.0 0.1 0.1 0.3 0.1 0.1

0 0 2 2 2 4 4 4 3 3 4 3

July 6, 2011

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.3 0.5 0.3 0.0 0.0 0.0 0.0 0.0 0.1 0.3

∗ ∗ 0.5 0.2 0.2 0.0 0.0 0.1 0.2 0.3 0.2 0.1

BLBS084-Beamish

∗ ∗ ∗ ∗ 0.0 0.0 0.1 0.0 0.0 0.1 0.4 0.0

∗ ∗ 1.3 1.4 7.6 0.1 0.0 0.0 0.1 0.1 0.2 0.3

BLBS084-08

Zone 3.4 Jan-04 Feb-04 Mar-04 Apr-04 May-04 Jun-04 Jul-04 Aug-04 Sep-04 Oct-04 Nov-04 Dec-04 Zone 3.5 Jan-04 Feb-04 Mar-04 Apr-04 May-04 Jun-04 Jul-04 Aug-04 Sep-04 Oct-04 Nov-04 Dec-04

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

245

246

0.4 0.7 0.9 0.2 0.5 0.2 0.3 0.2 0.5 0.4 1.6 0.3

0.1 0.1 0.1 0.1 0.0 0.1

0.9 1.7 1.7 0.8 1.1 0.5 0.6 0.5 0.9 1.1 3.5 0.4

0.1 0.1 0.1 0.1 0.1 0.1

0.0 0.0 0.0 0.0 0.0 0.0

0.3 0.9 0.6 0.2 0.4 0.1 0.2 0.2 0.4 0.6 1.3 0.1 0.0 0.0 0.0 0.0 0.0 0.0

0.2 0.4 0.5 0.1 0.2 0.1 0.1 0.1 0.3 0.2 0.7 0.1

se

0.0 0.0 0.0 0.0 0.0 0.0

0.1 0.2 0.0 0.2 0.2 0.4 0.2 0.1 0.1 0.1 0.2 0.1 0.0 0.0 0.0 0.0 0.0 0.0

0.1 0.2 0.0 0.1 0.1 0.2 0.1 0.0 0.1 0.1 0.1 0.1

se

3 3 3 3 3 2

3 3 3 6 7 4 3 5 3 4 5 3

Number of farms

2.2 3.5 0.7 0.6 0.5 0.7

0.3 3.8 2.3 1.1 0.0 0.1 0.1 0.5 1.4 ∗ 1.3 4.2

All motile stages

1.1 1.8 0.3 0.2 0.2 0.0

0.0 3.4

0.0 3.6 1.2 0.3 0.0 0.1 0.1 0.3 0.0

se

0.9 1.4 0.3 0.3 0.3 0.5

0.2 2.1 1.3 0.5 0.0 0.1 0.1 0.3 0.9 ∗ 0.9 1.0

Adult female only

L. salmonis

0.4 0.6 0.2 0.1 0.1 0.1

0.0 0.8

0.0 2.0 0.6 0.1 0.0 0.1 0.0 0.2 0.0

se

0.2 0.1 0.0 0.0 0.0 0.0

0.0 0.0 0.4 0.0 0.0 0.0 0.0 0.0 0.0 ∗ 0.0 0.1

All motile stages

0.1 0.1 0.0 0.0 0.0 0.0

0.0 0.1

0.0 0.0 0.4 0.0 0.0 0.0 0.0 0.0 0.0

se

C. clemensi

5 5 4 4 4 2

1 3 4 4 2 2 2 2 1 0 1 2

Number of farms

14:32

Zone 2.3 Jan-05 Feb-05 Mar-05 Apr-05 May-05 Jun-05 Jul-05 Aug-05 Sep-05 Oct-05 Nov-05 Dec-05 Zone 2.4 Jan-05 Feb-05 Mar-05 Apr-05 May-05 Jun-05

se

All motile stages

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

C: 2005

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0

0.7 0.2 0.1 0.2 0.5 0.9 0.1 0.1 0.3 0.4 0.6 0.8

0.0 0.0 0.1 0.1 0.1 0.2 ∗ 0.1 ∗ ∗ 0.1 0.0

1.0 0.2 0.8 0.9 1.6 1.7 0.3 0.2 0.5 1.0 1.2 1.1

0.4 0.0 0.1 0.1 0.1 0.4 0.1 0.0 0.0 0.2 0.3 0.4

0.0 0.0 0.2 0.0 1.1 2.1 2.0 0.3 0.0 0.1 0.2 0.1 0.1 0.2

0.0 0.0 0.0 0.1 0.0 0.0 ∗ 0.0 ∗ ∗ 0.0 0.0

0.2 0.0 0.8 0.0 ∗ ∗

0.1 0.0 1.1 1.4 1.2 0.3 0.0 0.0 0.1 0.1 0.1 0.1

0.0 0.0

0.0

0.0 0.0 0.0 0.0 0.0 0.0

0.2 0.0 0.0 0.0

6 3 3 4 4 4 5 5 4 4 5 3

1 0 0 1 1

2 2 1 1 1 1

2 1 1 1 0 0

0.4 1.2 2.7 4.9 1.1 0.3 0.1 1.4 0.7 1.8 6.5 2.4

2.2 0.1 0.1 0.1 0.2 0.1 0.1 ∗ 0.1 0.1 0.1 0.2

0.4 1.3 2.5 2.7 4.7 5.6

0.0 0.5 0.5 1.4 0.7 0.1 0.1 0.0 0.2 0.7 3.6 0.0

0.0 0.0 0.0 0.0

2.4 0.0 0.0 0.0 0.0 0.0 0.1

0.2 0.4 0.6 0.8 1.7 2.6

0.1 0.5 0.9 1.8 0.6 0.1 0.1 0.0 0.3 0.7 2.8 1.1

1.7 0.1 0.0 0.1 0.1 0.1 0.0 ∗ 0.1 0.0 0.1 0.1

0.2 0.7 1.5 1.6 2.3 2.4

0.0 0.3 0.3 0.4 0.5 0.1 0.1 0.0 0.1 0.2 1.6 0.0

0.0 0.0 0.0 0.0

1.6 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.2 0.5 0.5 0.6 1.1

0.0 0.4 0.2 0.1 0.1 0.2 0.0 0.0 0.2 0.1 0.1 1.0

0.0 0.1 0.0 0.0 0.0 0.0 0.0 ∗ 0.0 0.0 0.1 0.0

0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.2 0.1 0.0 0.1 0.1 0.0 0.0 0.2 0.1 0.1 0.0

0.0 0.0 0.0 0.0

0.0 0.1 0.0 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.0

247

(Continued )

1 5 5 4 6 6 5 4 2 4 4 4

3 2 3 3 4 2 2 0 1 1 1 1

2 3 3 3 3 4

14:32

0.0

0.0 0.0 0.0 0.0 0.0 0.0

0.1 0.0 0.0 0.0

July 6, 2011

0.5 0.0 0.2 0.2 0.4 0.5 0.1 0.1 0.1 0.6 0.5 0.4

0.0 0.0 0.0 0.0 0.1 0.1 ∗ 0.0 ∗ ∗ 0.0 0.0

0.2 0.5 1.4 0.3 ∗ ∗

BLBS084-Beamish

0.0

0.1 0.0 0.0 0.0

0.7 1.2 0.3 1.0 ∗ ∗

BLBS084-08

Jul-05 Aug-05 Sep-05 Oct-05 Nov-05 Dec-05 Zone 3.1 Jan-05 Feb-05 Mar-05 Apr-05 May-05 Jun-05 Jul-05 Aug-05 Sep-05 Oct-05 Nov-05 Dec-05 Zone 3.2 Jan-05 Feb-05 Mar-05 Apr-05 May-05 Jun-05 Jul-05 Aug-05 Sep-05 Oct-05 Nov-05 Dec-05

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

248

Zone 3.3 Jan-05 Feb-05 Mar-05 Apr-05 May-05 Jun-05 Jul-05 Aug-05 Sep-05 Oct-05 Nov-05 Dec-05

0.8 1.2 1.1 1.6 1.4 1.3 0.6 1.4 0.9 1.7 2.6 1.5

0.2 0.4 0.3 0.5 0.5 0.4 0.1 0.7 0.3 0.4 0.9 0.6

se 0.2 0.3 0.3 0.5 0.6 0.5 0.2 0.2 0.4 0.8 1.0 0.7

0.1 0.1 0.1 0.2 0.3 0.2 0.1 0.1 0.2 0.3 0.5 0.3

se 0.4 0.4 0.6 0.6 0.2 0.3 0.1 0.1 0.0 0.6 0.4 0.1

All motile stages 0.2 0.2 0.2 0.3 0.1 0.1 0.1 0.0 0.0 0.4 0.2 0.1

se 7 7 6 8 8 9 10 8 10 4 8 7

Number of farms 8.8 3.9 1.4 0.4 1.1 1.5 2.4 1.6 6.0 6.9 5.1 9.4

All motile stages 2.6 1.1 0.7 0.2 0.9 0.8 1.0 1.0 2.7 2.0 1.5 3.0

se

4.8 2.2 1.0 0.2 0.4 0.7 1.1 1.0 3.3 3.8 3.1 6.1

Adult female only

L. salmonis

1.6 0.7 0.6 0.1 0.3 0.4 0.4 0.6 1.7 1.3 0.8 2.2

se

1.6 0.5 0.0 0.1 0.5 0.1 0.1 0.0 0.1 0.3 0.8 1.3

All motile stages

0.7 0.3 0.0 0.0 0.4 0.0 0.1 0.0 0.0 0.2 0.6 1.1

se

C. clemensi

9 7 5 4 6 5 5 5 5 5 6 6

Number of farms

14:32

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

C: 2005

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.0 0.0 0.1 0.0 0.1 0.0 0.0 0.2 1.1 1.5 2.0 ∗

0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 1.0 0.4

0.4 0.1 0.4 0.2 0.2 0.0 0.0 0.0

0.4 0.4 0.1 0.6 0.6 2.1 1.4 0.3 0.1 0.3 0.0 ∗

0.4 0.2 0.0 0.0 0.1 1.7 0.4 1.0 ∗ 2.2 0.3 0.2 0.2 0.4 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.3 0.1

0.3 0.2 0.0 0.0 0.1 0.0 0.0 0.0

2 2 2(3) 2(4) 1(2) 1(2) 1 1 1 1 1

4 2 3 4 2 1 1 1 0 1 2 3 0.0 0.2 0.0 0.2 0.6 0.0 0.3 0.7 1.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.8

∗ ∗ ∗ ∗ 0.1 0.3 0.7 0.6 4.6 6.9 8.8 4.1

0.0

9.9 ∗ ∗ 1.0 0.3 0.7 0.9 2.0 1.6 0.5 1.1 2.1 ∗ ∗ ∗ ∗ 0.0 0.1 0.4 0.3 2.1 4.4 5.6 2.3

6.1 ∗ ∗ 0.3 0.0 0.0 0.0 0.4 0.6 0.1 0.5 1.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.5

0.0 0.0 0.0 0.0 0.2 0.1 0.0 0.5 0.6

0.0

∗ ∗ ∗ ∗ 0.3 0.3 1.0 0.2 0.2 0.0 0.1 0.2

0.3 ∗ ∗ 0.0 0.0 0.1 0.0 0.1 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.2

0.0 0.0 0.1 0.0 0.1 0.0 0.0 0.0 0.0

0.0

(Continued )

0 0 0 0 1(2) 1(2) 1 1 1 1 1 2

1 0 0 1 3 3 4 4 2 3 5 3

14:32

0.1 0.1 0.4 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

1.3 0.5 0.6 0.2 0.2 0.1 0.1 0.1 ∗ 3.5 1.0 0.5

July 6, 2011

0.0 1.3 0.7

1.3 0.4 1.1 0.7 0.7 0.0 0.0 0.0

BLBS084-Beamish

0.1 0.1 0.4 0.1 0.2 0.2 0.5 1.0 1.8 2.4 3.2 ∗

3.7 1.8 1.8 1.0 0.8 0.5 0.8 0.4 ∗ 6.4 2.0 1.0

BLBS084-08

Zone 3.4 Jan-05 Feb-05 Mar-05 Apr-05 May-05 Jun-05 Jul-05 Aug-05 Sep-05 Oct-05 Nov-05 Dec-05 Zone 3.5 Jan-05 Feb-05 Mar-05 Apr-05 May-05 Jun-05 Jul-05 Aug-05 Sep-05 Oct-05 Nov-05 Dec-05

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

249

250

0.5 0.8 0.1 0.7 0.7 0.9 0.4 0.6 0.2 0.1 0.2 0.1

0.2 0.3 0.1 0.2 0.1 0.1 0.3

0.2 0.3 0.1 0.2 0.1 0.2 0.7

0.0 0.1 0.0 0.0 0.0 0.1 0.3

0.3 0.4 0.1 0.1 0.5 0.3 0.3 0.4 0.2 0.1 0.2 0.3 0.0 0.1 0.0 0.0 0.0 0.1 0.1

0.2 0.4 0.0 0.1 0.3 0.2 0.1 0.2 0.1 0.0 0.1 0.1 0.0 0.0 0.0 0.0 0.1 0.1 0.3

0.1 0.1 0.1 0.0 0.3 0.2 0.5 0.6 0.2 0.0 0.4 0.1 0.0 0.0 0.0 0.0 0.1 0.0 0.2

0.1 0.1 0.0 0.0 0.1 0.2 0.2 0.3 0.1 0.0 0.1 0.0

se

2 2 3 3 3 3 4

4 4 2 3 4 4 4 4 5 4 6 3

Number of farms

3.5 1.6 0.7 1.0 1.3 1.2 0.6

1.2 0.4 1.1 3.7 4.0 2.1 6.7 ∗ 0.6 0.2 0.0 0.1

All motile stages

1.7 1.0 0.2 0.3 0.4 0.4 0.3

0.0 0.2 0.0 0.1

0.3 0.2 0.4 0.6 0.0 1.1 0.0

se

1.8 1.0 0.5 0.5 0.5 0.7 0.3

0.7 0.2 0.4 1.3 1.7 1.0 3.4 ∗ 0.5 0.2 0.0 0.1

Adult female only

L. salmonis

0.9 0.9 0.1 0.2 0.2 0.2 0.1

0.0 0.2 0.0 0.1

0.1 0.1 0.2 0.2 0.0 0.5 0.0

se

0.0 0.0 0.4 0.4 0.1 0.1 0.0

0.0 0.0 0.1 0.0 0.0 0.0 0.7 ∗ 0.0 0.0 0.0 0.0

All motile stages

0.0 0.0 0.3 0.4 0.1 0.1 0.0

0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0

se

C. clemensi

5 3 4 3 4 4 2

2 3 4 4 1 3 1 0 1 2 1 2

Number of farms

14:32

0.9 1.0 0.3 1.3 2.3 1.2 1.2 1.5 0.5 0.3 0.6 0.7

se

All motile stages

C. clemensi

Year 2 July 6, 2011

Zone 2.3 Jan-06 Feb-06 Mar-06 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Zone 2.4 Jan-06 Feb-06 Mar-06 Apr-06 May-06 Jun-06 Jul-06

se

Adult female only

L. salmonis

Year 1

D: 2006

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.9 0.5 0.5 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.5 0.2 0.5 0.1 0.1 0.3 0.6 0.6 0.8

1.6 2.1 3.3 2.6 0.3

0.1 0.0 0.1 0.1 0.1 0.1 0.1 ∗ ∗ ∗ ∗ ∗

1.7 3.4 4.9 0.7 0.6 1.2 0.5 0.6 0.5 1.1 1.9 1.6

0.0 0.0 0.0 0.0 0.0 0.8 0.4 3.5 2.3 1.6 1.5 1.3

0.0 0.0 0.0 0.0 0.1 0.6 0.2 1.6 0.9 0.8 0.4 0.7

0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.2 0.3 0.2 0.0 0.0

1 1 1 3 4 5 4 5 4 4 4 6

1 1 1 1 1 1 1 0 0 0 0 0

2 4 4 1 2

3.3 4.0 1.9 1.9 1.1 0.4 0.4 0.3 0.5 2.9 2.8 4.0

0.3 0.5 0.2 0.5 0.2 0.2 0.2 ∗ ∗ ∗ ∗ ∗

0.8 1.7 1.1 3.9 2.3

0.8 1.7 1.1 1.5 0.9 0.3 0.1 0.1 0.1 1.1 1.2 1.8

0.1 0.2 0.0 0.3 0.0 0.0 0.0

0.0 0.0 0.0 1.4 1.2

1.6 2.4 0.7 0.6 0.5 0.2 0.1 0.2 0.2 1.1 1.3 2.4

0.1 0.1 0.1 0.3 0.1 0.1 0.2 ∗ ∗ ∗ ∗ ∗

0.5 1.2 0.5 1.7 1.1

0.5 1.1 0.5 0.3 0.4 0.2 0.0 0.1 0.0 0.4 0.6 1.0

0.0 0.1 0.0 0.2 0.0 0.0 0.0

0.1 0.0 0.0 0.8 0.6

0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.2 0.7 0.7 0.0 0.3

0.0 0.0 0.0 0.0 0.0 0.0 0.0 ∗ ∗ ∗ ∗ ∗

0.0 0.0 0.0 0.1 0.0

0.1 0.1 0.0 0.1 0.0 0.0 0.0 0.2 0.6 0.3 0.0 0.3

0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.0

(Continued )

5 5 5 4 6 4 5 5 4 4 4 4

2 3 1 2 1 1 1 0 0 0 0 0

2 1 1 4 4

14:32

0.0 0.0 0.0 0.0 0.0 0.2 0.0 0.0 0.1 0.3 0.3 0.5

0.0 0.1 0.0 0.0 0.0 0.0 0.0 ∗ ∗ ∗ ∗ ∗

0.9 0.3 0.4 0.0 0.0

July 6, 2011

0.8 1.1 2.2 0.0 0.0 0.3 0.1 0.2 0.2 0.4 0.4 0.7

0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.4 0.3 0.2 0.0 0.0

BLBS084-Beamish

0.0 0.0 0.1 0.0 0.0 0.0 0.0 ∗ ∗ ∗ ∗ ∗

0.6 0.7 1.3 1.4 0.0

BLBS084-08

Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Zone 3.1 Jan-06 Feb-06 Mar-06 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Zone 3.2 Jan-06 Feb-06 Mar-06 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

251

252

Zone 3.3 Jan-06 Feb-06 Mar-06 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06

2.8 2.6 2.7 1.0 0.6 0.2 0.2 0.9 1.5 3.6 2.5 1.5

1.7 0.8 1.0 0.4 0.2 0.1 0.1 0.8 0.8 1.3 0.9 0.4

se 0.9 0.8 0.9 0.2 0.1 0.0 0.0 0.3 0.3 1.5 0.9 0.4

0.4 0.3 0.4 0.1 0.0 0.0 0.0 0.3 0.1 0.6 0.4 0.3

se 0.7 0.2 0.2 0.2 0.0 0.0 0.1 0.3 0.7 1.6 0.5 0.2

All motile stages 0.4 0.1 0.1 0.1 0.0 0.0 0.0 0.2 0.4 0.8 0.3 0.0

se 8 8 8 5 4 3 5 5 6 7 7 5

Number of farms 5.0 4.4 0.8 1.1 0.9 1.2 1.1 1.4 1.0 2.6 2.7 4.4

All motile stages 1.8 2.5 0.2 0.7 0.4 0.7 0.5 0.7 1.0 1.3 1.7 1.9

se

2.3 2.4 0.4 0.4 0.3 0.7 0.7 0.7 0.5 1.1 1.7 2.5

Adult female only

L. salmonis

0.7 1.4 0.1 0.3 0.1 0.4 0.4 0.4 0.5 0.8 1.0 1.1

se

0.2 0.2 0.0 0.0 0.2 0.1 0.2 0.2 0.3 0.2 0.3 0.3

All motile stages

0.1 0.1 0.0 0.0 0.2 0.1 0.2 0.2 0.3 0.2 0.2 0.2

se

C. clemensi

7 6 7 9 9 7 7 6 5 5 6 10

Number of farms

14:32

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

D: 2006

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.1 0.2 0.4 0.4 0.5 0.1 0.2 0.2 0.7 0.1 0.1 0.4

0.0 0.1 0.0 0.0 0.0 0.1 0.6 0.6 0.2 0.0

0.3 0.3 0.6 0.6 0.7 0.6 0.7 1.4 2.9 0.4 0.2 0.4

∗ ∗ 0.2 0.1 0.1 0.0 0.1 1.5 2.8 2.8 0.6 0.1 0.0 0.0 0.0 0.1 0.0 0.0 0.5 0.1 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.1 0.1 0.0 0.0 0.0

1 2 2 2 2 2 2 2 2 2

3 4 3 4 5 6 6 7 7 5 5 3 4.1 1.2 0.3 0.1 0.0 0.3 0.4 2.5 10.6 21.0 6.4 0.3

2.7 3.5 0.7 0.4 4.2 1.5 0.1 0.2 0.8 0.4 0.2 0.3 1.3 1.0 0.2 0.0 0.0 0.0 0.1 0.3 1.1 5.5 3.2 0.1

0.0 0.0 0.7 0.2 0.8 0.3 0.0 0.1 0.0 0.0 0.2 0.3 2.2 0.8 0.1 0.1 0.0 0.1 0.2 1.0 3.3 12.3 4.3 0.2

1.2 1.8 0.4 0.0 1.9 0.8 0.1 0.1 0.3 0.2 0.0 0.1 1.1 0.7 0.1 0.0 0.0 0.0 0.1 0.2 0.3 3.0 1.5 0.1

0.0 0.0 0.4 0.0 0.5 0.2 0.0 0.1 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.2 3.2 0.7 0.2 0.0

0.0 0.0 0.0 0.5 0.8 0.0 0.0 0.1 1.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.3 0.5 0.1 0.0

0.0 0.0 0.0 0.1 0.4 0.0 0.0 0.1 0.0 0.0 0.0 0.0

(Continued )

2 2 2 1 1 1 2 2 2 2 2 2

1 1 3 2 2 2 2 2 1 1 2 2

14:32

∗ ∗ 0.0 0.1 0.1 0.1 0.0 0.0 0.8 0.3 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.1 0.1 0.0 0.0 0.0

July 6, 2011

0.0 0.0 0.0 0.0 0.0 0.1 0.3 0.2 0.1 0.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.1 0.0 0.0 0.1

BLBS084-Beamish

∗ ∗ 0.1 0.0 0.1 0.0 0.0 0.2 0.5 0.8 0.2 0.1

0.0 0.0 0.2 0.0 0.0 0.0 0.0 0.2 0.4 0.0 0.0 0.1

BLBS084-08

Zone 3.4 Jan-06 Feb-06 Mar-06 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06 Zone 3.5 Jan-06 Feb-06 Mar-06 Apr-06 May-06 Jun-06 Jul-06 Aug-06 Sep-06 Oct-06 Nov-06 Dec-06

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

253

254

0.3 0.5 0.5 0.3 0.4 0.2 0.3 0.2 0.3 0.5 0.9 2.2

0.2 0.6 0.4 0.2 0.1 0.2

0.6 1.3 1.1 1.2 1.6 1.0 0.8 0.6 0.7 1.9 2.0 3.6

0.6 1.3 0.7 0.2 0.2 0.4

0.0 0.1 0.1 0.0 0.0 0.0

0.2 0.5 0.4 0.6 0.4 0.4 0.3 0.2 0.4 1.1 1.1 1.8 0.0 0.0 0.1 0.0 0.0 0.0

0.1 0.2 0.2 0.1 0.1 0.1 0.2 0.1 0.2 0.3 0.5 1.1

se

0.0 0.1 0.0 0.0 0.0 0.0

0.1 0.4 0.1 0.2 0.4 0.2 0.2 0.1 0.0 0.0 0.7 0.2 0.0 0.1 0.0 0.0 0.0 0.0

0.1 0.2 0.1 0.2 0.3 0.1 0.2 0.1 0.0 0.0 0.1 0.1

se

4 4 5 5 5 3

4 5 5 4 5 5 4 5 5 5 4 4

Number of farms

0.4 0.2 0.3 0.3 0.5 0.9

0.0 1.1 1.0 1.5 0.1 0.1 0.2 0.2 0.1 0.5 6.8 13.5

All motile stages

0.2 0.1 0.2 0.1 0.2 0.3

0.0 0.5 0.0 0.5 0.0 0.0 0.2 0.0 0.0 0.0 2.9 0.0

se

0.2 0.0 0.1 0.1 0.2 0.4

0.1 0.3 0.3 0.6 0.0 0.1 0.1 0.1 0.1 0.3 3.7 7.1

Adult female only

L. salmonis

0.1 0.0 0.0 0.0 0.1 0.1

0.0 0.1 0.0 0.2 0.0 0.0 0.0 0.0 0.0 0.1 1.7 0.0

se

0.0 0.1 0.5 0.1 0.1 0.1

0.1 0.2 0.1 0.1 0.0 0.0 0.1 0.8 0.0 0.0 0.0 0.0

All motile stages

0.0 0.1 0.4 0.1 0.1 0.1

0.1 0.2 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

se

C. clemensi

5 4 5 4 3 5

2 3 1 5 3 3 3 1 2 2 2 1

Number of farms

14:32

Zone 2.3 Jan-07 Feb-07 Mar-07 Apr-07 May-07 Jun-07 Jul-07 Aug-07 Sep-07 Oct-07 Nov-07 Dec-07 Zone 2.4 Jan-07 Feb-07 Mar-07 Apr-07 May-07 Jun-07

se

All motile stages

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

E: 2007

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.2 0.4 1.0 1.9 3.4 1.2

0.7 0.2 0.3 0.5 0.6 0.2 0.1 0.0 0.0 0.0 0.1 0.4

0.6 0.0 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.2 0.3 0.0

0.5 1.1 4.3 3.8 4.0 2.4

1.3 0.3 0.5 0.7 0.9 0.4 0.1 0.1 0.1 0.2 0.7 1.4

1.7 1.3 0.3 0.3 0.4 0.2 0.2 0.2 0.5 0.4 0.4 0.3

0.5 0.1 0.1 0.3 0.1 0.2 0.2 0.0 0.2 0.1 0.2 0.1

0.3 0.0 0.1 0.1 0.1 0.1 0.2 0.0 0.1 0.1 0.1 0.1

0.6 0.2 0.4 0.7 0.8 0.2 0.0 0.0 0.1 0.0 0.1 0.0

0.2 1.1 0.2 0.1 0.0 0.0

6 6 7 9 7 9 11 9 10 8 5 3

6 5 4 5 7 7 8 8 8 7 6 6

6 5 2 4 2 2

1.9 1.1 1.1 1.1 0.9 0.2 0.4 0.3 0.9 1.0 1.1 1.9

3.0 1.8 0.4 1.2 0.8 1.5 1.2 0.4 0.4 0.5 2.7 3.6

0.4 0.6 0.4 2.4 4.7 2.3

0.9 0.3 0.5 0.6 0.5 0.0 0.1 0.1 0.4 0.3 0.3 0.5

1.4 0.9 0.2 0.6 0.3 0.7 0.8 0.4 0.4 0.2 1.1 1.3

0.4 0.5 0.0 1.2 2.1 0.9

0.9 0.6 0.7 0.4 0.3 0.0 0.1 0.1 0.4 0.5 0.5 0.8

1.9 1.1 0.1 0.3 0.4 0.6 0.9 0.2 0.3 0.4 0.8 2.0

0.2 0.3 0.3 1.1 2.2 1.0

0.4 0.2 0.4 0.3 0.2 0.0 0.1 0.1 0.2 0.2 0.2 0.3

1.0 0.6 0.0 0.1 0.2 0.3 0.6 0.2 0.2 0.2 0.3 0.9

0.2 0.2 0.0 0.5 1.1 0.4

0.2 0.1 0.1 0.2 0.2 0.5 0.8 0.1 0.1 0.1 0.3 0.3

0.0 0.7 0.1 0.4 0.5 1.1 0.7 0.2 0.1 1.0 0.2 0.2

0.0 0.0 0.0 0.0 0.0 0.0

0.2 0.0 0.1 0.2 0.2 0.3 0.4 0.1 0.0 0.1 0.1 0.1

0.0 0.4 0.1 0.4 0.5 0.8 0.4 0.2 0.1 0.1 0.1 0.1

0.0 0.0 0.0 0.0 0.0 0.0

255

(Continued )

8 8 8 6 6 5 5 6 7 9 11 13

5 5 5 5 5 3 3 3 3 4 5 6

2 3 1 4 6 7

14:32

0.2 0.0 0.1 0.0 0.0 0.0 0.0 0.1 0.1 0.1 0.1 0.0

1.7 0.3 0.7 0.9 1.0 0.5 0.1 0.1 0.1 0.1 0.1 0.1

0.3 1.7 0.8 0.1 0.0 0.0

July 6, 2011

0.3 0.5 0.2 0.1 0.1 0.1 0.1 0.1 0.2 0.2 0.1 0.1

0.5 0.1 0.0 0.2 0.3 0.1 0.0 0.0 0.0 0.2 0.1 0.1

0.1 0.1 0.6 0.8 1.0 0.3

BLBS084-Beamish

0.7 0.1 0.0 0.2 0.3 0.2 0.1 0.0 0.0 0.1 0.1 0.4

0.1 0.4 2.4 1.5 1.3 0.3

BLBS084-08

Jul-07 Aug-07 Sep-07 Oct-07 Nov-07 Dec-07 Zone 3.2 Jan-07 Feb-07 Mar-07 Apr-07 May-07 Jun-07 Jul-07 Aug-07 Sep-07 Oct-07 Nov-07 Dec-07 Zone 3.3 Jan-07 Feb-07 Mar-07 Apr-07 May-07 Jun-07 Jul-07 Aug-07 Sep-07 Oct-07 Nov-07 Dec-07

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

256

Zone 3.4 Jan-07 Feb-07 Mar-07 Apr-07 May-07 Jun-07 Jul-07 Aug-07 Sep-07 Oct-07 Nov-07 Dec-07

0.9 0.3 0.3 0.5 0.6 0.8 0.8 ∗ ∗ ∗ ∗ ∗

0.6 0.2 0.2 0.0 0.3 0.0 0.0

se 0.3 0.0 0.0 0.1 0.0 0.3 0.3 ∗ ∗ ∗ ∗ ∗

0.2 0.0 0.0 0.0 0.0 0.0 0.0

se 0.2 0.0 0.0 0.0 0.0 0.6 0.9 ∗ ∗ ∗ ∗ ∗

All motile stages 0.2 0.0 0.0 0.0 0.0 0.0 0.0

se 5 3 3 1 2 1 1 0 0 0 0 0

Number of farms 0.4 0.5 1.3 1.0 1.2 1.1 1.0 0.8 1.6 3.3 3.6 3.2

All motile stages 0.2 0.3 0.5 0.3 0.3 0.4 0.3 0.1 0.5 1.2 1.4 1.2

se

0.1 0.1 0.2 0.2 0.3 0.1 0.4 0.3 0.5 1.5 1.9 1.6

Adult female only

L. salmonis

0.0 0.1 0.2 0.1 0.1 0.0 0.1 0.0 0.1 0.6 0.7 0.6

se

0.0 0.0 0.0 0.0 0.1 0.1 0.6 0.2 0.6 0.2 0.3 0.1

All motile stages

0.0 0.0 0.0 0.0 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.1

se

C. clemensi

2 3 4 6 6 6 6 7 4 5 4 5

Number of farms

14:32

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

E: 2007

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.2 0.3 ∗ ∗ ∗ 0.0 0.1 0.1 1.2 4.4 2.8 2.2

0.0 0.0 ∗ ∗ ∗ 0.0 0.0 0.0 0.2 2.5 1.3 0.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0

0.0 0.1 ∗ ∗ ∗ 0.1 0.0 0.0 0.1 0.1 0.5 0.2 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0

1 1 0 0 0 1 1 1 1 1 1 1

0.5 0.3 0.1 0.2 0.2 0.7 0.5 2.4 6.3 25.1 29.7 15.2

0.3 0.1 0.0 0.1 0.0 0.1 0.4 0.9 0.7 0.5 10.4 5.2

0.4 0.2 0.0 0.0 0.0 0.2 0.2 1.1 2.0 16.7 17.9 10.2

0.3 0.1 0.0 0.0 0.0 0.1 0.1 0.5 0.5 0.6 8.5 3.7

0.0 0.0 0.2 0.3 0.5 0.1 0.2 0.2 0.4 0.3 0.0 0.2

0.0 0.0 0.1 0.2 0.5 0.1 0.1 0.1 0.4 0.3 0.0 0.0

July 6, 2011 14:32

(Continued )

3 2 3 2 2 2 2 2 2 2 2 2

BLBS084-Beamish

0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.0

BLBS084-08

Zone 3.5 Jan-07 Feb-07 Mar-07 Apr-07 May-07 Jun-07 Jul-07 Aug-07 Sep-07 Oct-07 Nov-07 Dec-07

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

257

258

3.9 1.1 0.2 0.2 0.0 0.6 0.3 0.1 0.2 0.2 0.3 0.5

0.8 1.3 0.8 0.3 0.1

4.5 1.2 0.4 0.4 0.3 0.6 0.3 0.4 0.6 0.9 1.0 0.9

3.1 2.0 0.8 0.3 0.3

0.8 1.1 0.5 0.2 0.1

2.2 0.6 0.2 0.1 0.0 0.1 0.1 0.1 0.2 0.2 0.4 0.5 0.6 1.0 0.5 0.2 0.1

1.9 0.6 0.2 0.0 0.0 0.1 0.1 0.0 0.1 0.1 0.1 0.3

se

0.0 0.0 0.0 0.0 0.0

0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 4.0 0.2 1.7 1.1 0.0 0.0 0.0 0.0 0.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3.9 0.1 1.3 0.9

se

2 2 2 2 2

3 2 2 3 1 2 2 3 5 4 5 5

Number of farms

0.9 1.3 0.5 0.5 0.5

2.3 0.7 0.8 1.5 1.3 2.4 0.2 0.3 ∗ 0.0 1.5 0.3

All motile stages

0.2 0.8 0.1 0.2 0.2

0.0 0.0 0.0

2.1 0.3 0.6 1.4 0.7 1.9 0.1 0.0

se

0.4 0.5 0.2 0.1 0.2

1.1 0.3 0.3 0.6 0.6 0.7 0.1 0.2 ∗ 0.0 0.9 0.2

Adult female only

L. salmonis

0.1 0.2 0.1 0.1 0.1

0.0 0.0 0.0

1.0 0.1 0.2 0.6 0.4 0.6 0.0 0.0

se

0.0 0.2 0.0 0.0 0.0

0.0 0.0 0.1 0.3 0.1 0.2 0.0 0.0 ∗ 0.0 0.2 0.0

All motile stages

0.0 0.2 0.0 0.0 0.0

0.0 0.0 0.0

0.0 0.0 0.1 0.3 0.1 0.1 0.0 0.0

se

C. clemensi

7 6 7 6 6

3 3 2 2 4 3 3 1 0 1 1 1

Number of farms

14:32

Zone 2.3 Jan-08 Feb-08 Mar-08 Apr-08 May-08 Jun-08 Jul-08 Aug-08 Sep-08 Oct-08 Nov-08 Dec-08 Zone 2.4 Jan-08 Feb-08 Mar-08 Apr-08 May-08

se

All motile stages

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

F: 2008

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.1 0.0 0.1 0.0 3.4 2.2 2.7

0.7 0.4 0.6 0.4 0.2 0.8 0.3 0.6 0.3 0.1 0.0 0.1

0.1 0.3 0.2 0.2 0.0

0.1 0.0 0.2 0.4 4.8 3.0 3.2

1.6 1.2 1.4 0.9 0.8 1.3 0.5 1.3 0.7 0.3 0.4 0.6

0.3 0.5 0.3 0.2 0.3

0.2 0.3 0.2 0.3 0.0

0.1 0.2 0.2 0.2 0.0

0.0 0.1 0.1 0.0 0.1 0.0 0.3 1.8 0.2 0.1 0.0 0.5

0.0 0.0 0.0 0.0 0.2 0.1 1.0

5 3 4 2 1

6 5 8 5 4 4 2 4 5 3 1 2

3 1 2 1 3 2 2

2.0 1.5 1.1 0.5 0.6

2.4 0.8 2.2 3.3 1.7 0.3 0.4 0.4 0.9 0.7 1.3 2.9

0.8 1.1 2.0 4.3 0.9 1.7 2.7

0.8 0.9 0.5 0.2 0.3

0.6 0.6 0.8 1.4 0.7 0.1 0.1 0.1 0.2 0.1 0.3 0.5

0.5 0.5 1.1 3.3 0.3 0.5 1.6

0.9 0.6 0.5 0.2 0.3

1.3 0.4 1.0 0.9 0.8 0.2 0.2 0.2 0.3 0.3 0.6 1.3

0.3 0.4 0.8 1.2 0.7 0.8 1.6

0.3 0.3 0.3 0.1 0.2

0.4 0.3 0.4 0.4 0.3 0.0 0.1 0.1 0.1 0.1 0.2 0.3

0.2 0.2 0.4 0.6 0.2 0.6 1.0

0.3 0.1 0.1 0.2 0.2

0.1 0.0 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.2 0.3 0.8

0.0 0.0 0.1 0.0 0.0 0.0 0.1

0.1 0.0 0.1 0.1 0.1

0.1 0.0 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.1 0.1 0.4

0.0 0.0 0.1 0.0 0.0 0.0 0.1

(Continued )

11 9 10 12 12

7 5 6 9 10 8 8 7 7 8 11 11

5 7 6 3 2 3 4

14:32

0.1 0.1 0.1 0.1 0.0

0.2 0.3 0.2 0.2 0.2 0.0 0.3 2.0 0.0 0.2 0.0 0.8

0.0 0.0 0.0 0.0 0.2 0.1 1.0

July 6, 2011

0.1 0.2 0.1 0.1 0.0

0.5 0.2 0.2 0.1 0.1 0.3 0.0 0.1 0.1 0.0 0.0 0.1

0.0 0.0 0.1 0.0 0.6 0.9 1.2

BLBS084-Beamish

0.8 0.5 0.4 0.1 0.2 0.4 0.1 0.2 0.2 0.1 0.1 0.2

0.0 0.0 0.1 0.2 1.2 1.3 1.4

BLBS084-08

Jun-08 Jul-08 Aug-08 Sep-08 Oct-08 Nov-08 Dec-08 Zone 3.2 Jan-08 Feb-08 Mar-08 Apr-08 May-08 Jun-08 Jul-08 Aug-08 Sep-08 Oct-08 Nov-08 Dec-08 Zone 3.3 Jan-08 Feb-08 Mar-08 Apr-08 May-08

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

259

260

Jun-08 Jul-08 Aug-08 Sep-08 Oct-08 Nov-08 Dec-08 Zone 3.4 Jan-08 Feb-08 Mar-08 Apr-08

∗ ∗ ∗ ∗

0.2 0.1 0.5 0.7 1.1 1.1 0.3

0.1 0.0 0.4 0.4 0.4 0.4 0.1

se

∗ ∗ ∗ ∗

0.0 0.1 0.1 0.2 0.3 0.4 0.1

0.1 0.0 0.1 0.1 0.2 0.2 0.0

se

∗ ∗ ∗ ∗

0.2 0.0 0.1 0.1 0.2 0.3 0.3

All motile stages 0.1 0.0 0.1 0.1 0.1 0.2 0.3

se

0 0 0 0

3 2 2 5 6 7 3

Number of farms

3.8 3.4 2.7 1.9

0.4 0.4 0.3 0.3 0.6 1.6 1.8

All motile stages

1.2 0.8 1.0 0.9

0.3 0.2 0.1 0.2 0.2 0.6 0.7

se

2.5 1.8 1.8 1.1

0.2 0.1 0.1 0.2 0.2 0.6 0.8

Adult female only

L. salmonis

0.7 0.4 0.8 0.7

0.2 0.1 0.1 0.1 0.1 0.3 0.3

se

0.2 0.2 0.1 0.0

0.2 0.1 0.3 0.2 0.1 0.2 0.3

All motile stages

0.1 0.1 0.1 0.0

0.1 0.0 0.3 0.1 0.0 0.1 0.2

se

C. clemensi

4 3 4 4

11 11 9 10 9 8 9

Number of farms

14:32

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

F: 2008

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.3 0.1 0.1 0.1 0.2 0.0 0.2 0.5

0.3 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.4 0.2 0.2 0.6 1.0 0.9 1.0 1.4

0.7 0.2 0.2 0.1 0.1 0.0 0.0 0.0 0.2 0.3 ∗ ∗

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.3 0.0 0.0 0.0 0.0 0.0 0.1 ∗ ∗

0.0 0.1 0.2 0.4 1.1 0.7 0.3 1.4 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.1 0.1 0.2 1.0 0.4 0.2 0.6 2 1 2 1 1 1 1 1 1 1 0 0

3 3 3 3 3 3 4 3 1.6 0.7 0.8 0.9 0.1 0.0 0.1 0.2 0.3 0.3 0.0 0.0

1.3 0.8 0.4 0.3 0.8 0.9 0.7 0.3 0.1 0.6 0.0 0.6 0.0 0.0 0.0 0.1 0.1 0.2 0.0 0.0

0.9 0.5 0.0 0.0 0.0 0.0 0.0 0.0 1.0 0.4 0.5 0.5 0.0 0.0 0.0 0.0 0.1 0.1 0.0 0.0

1.0 0.3 0.1 0.1 0.2 0.3 0.3 0.1 0.1 0.4 0.0 0.4 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0

0.7 0.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.1 0.2 0.2 0.8 0.2 0.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0

0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0

July 6, 2011 14:32

(Continued )

2 2 1 3 2 2 1 2 2 2 2 1

3 2 1 1 1 1 1 1

BLBS084-Beamish

0.1 0.1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.1 ∗ ∗

0.1 0.1 0.1 0.1 0.3 0.4 0.4 0.5

BLBS084-08

May-08 Jun-08 Jul-08 Aug-08 Sep-08 Oct-08 Nov-08 Dec-08 Zone 3.5 Jan-08 Feb-08 Mar-08 Apr-08 May-08 Jun-08 Jul-08 Aug-08 Sep-08 Oct-08 Nov-08 Dec-08

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

261

262

0.4 0.4 0.3 0.2 0.3 0.1 0.1 0.2 0.2 0.3 0.2 0.3

0.4 0.6 0.9 0.9 0.3

0.8 0.6 1.0 0.4 0.5 0.3 0.3 0.5 0.4 0.1 0.4 0.8

1.5 0.8 1.1 1.0 0.3

0.6 0.4 0.4 0.4 0.1

0.3 0.2 0.2 0.1 0.2 0.1 0.1 0.2 0.2 0.3 0.2 0.3 0.3 0.3 0.4 0.4 0.1

0.2 0.1 0.1 0.1 0.2 0.0 0.1 0.1 0.1 0.2 0.1 0.1

se

0.2 0.0 0.0 0.0 0.0

0.5 0.2 0.3 0.2 0.2 0.3 0.3 0.1 0.1 0.1 0.1 0.3 0.1 0.0 0.0 0.0 0.0

0.2 0.0 0.2 0.2 0.1 0.3 0.2 0.1 0.0 0.0 0.0 0.2

se

3 3 3 3 4

7 3 4 5 5 6 7 7 5 7 6 5

Number of farms

3.1 4.7 1.3 0.6 1.0

0.3 0.7 0.6 0.7 0.6 0.8 0.4 0.0 0.1 0.2 0.3 0.2

All motile stages

1.8 2.6 0.6 0.2 0.9

0.0 0.5 0.1 0.2 0.2 0.7 0.3 0.0 0.1 0.0 0.2 0.1

se

1.2 1.4 0.4 0.2 0.2

0.1 0.2 0.2 0.2 0.2 0.5 0.2 0.0 0.1 0.2 0.1 0.1

Adult female only

L. salmonis

0.9 0.6 0.2 0.1 0.1

0.0 0.1 0.1 0.1 0.1 0.4 0.2 0.0 0.0 0.0 0.1 0.0

se

0.1 0.0 0.0 0.2 0.0

0.2 1.7 0.2 0.3 0.1 0.0 0.2 0.0 0.0 0.1 0.0 0.1

All motile stages

0.1 0.0 0.0 0.2 0.0

0.0 0.9 0.1 0.2 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0

se

C. clemensi

2 2 3 5 2

1 4 3 3 5 2 4 2 3 3 3 4

Number of farms

14:32

Zone 2.3 Jan-09 Feb-09 Mar-09 Apr-09 May-09 Jun-09 Jul-09 Aug-09 Sep-09 Oct-09 Nov-09 Dec-09 Zone 2.4 Jan-09 Feb-09 Mar-09 Apr-09 May-09

se

All motile stages

C. clemensi

Year 2

July 6, 2011

Adult female only

L. salmonis

Year 1

G: 2009

BLBS084-Beamish

All motile stages

(Continued)

BLBS084-08

Table 8.1.

P1: SFK/UKS P2: SFK Trim: 244mm×172mm

0.1 0.2 2.8 3.3 5.3 0.5 0.5

0.1 0.9 0.2 0.4 0.3 0.4 0.3 0.4 0.5 0.5 0.6 0.6

0.1 0.1 0.1 0.1 0.1

0.2 0.5 3.3 4.7 7.2 3.0 2.8

0.6 1.5 0.7 0.6 0.5 0.6 1.1 1.3 1.1 1.2 1.4 1.4

0.3 0.2 0.2 0.2 0.1

0.3 0.5 0.3 0.1 0.2

0.3 0.3 0.2 0.1 0.2

1.7 0.2 1.1 0.1 1.6 0.4 2.7 0.9 0.3 0.1 0.0 0.3

0.0 0.0 0.0 0.0 0.0 0.1 0.1

3 3 4 3 4

2 2 2 2 2 4 5 5 6 5 5 7

5 5 3 6 6 5 6

1.0 1.0 1.1 0.1 0.2

3.3 2.3 1.4 0.4 0.5 0.6 1.0 0.8 2.6 ∗ 1.1 2.0

0.6 0.7 3.6 11.7 5.8 11.5 6.2

0.3 0.3 0.7 0.0 0.1

0.0 0.0

0.4 0.6 0.8 0.2 0.2 0.2 0.5 0.3 0.1

0.2 0.5 3.1 6.6 4.2 6.1 2.0

0.6 0.5 0.6 0.0 0.1

1.5 1.0 0.6 0.1 0.2 0.3 0.5 0.5 1.1 ∗ 0.3 1.0

0.3 0.5 1.4 6.7 2.3 5.3 2.7

0.2 0.2 0.4 0.0 0.1

0.0 0.0

0.2 0.3 0.3 0.1 0.1 0.1 0.2 0.1 0.5

0.1 0.2 1.2 3.9 1.5 2.8 0.9

0.3 0.1 0.0 0.0 0.1

1.9 1.2 0.4 0.3 0.3 0.2 0.9 0.2 0.5 ∗ 1.2 0.5

0.0 0.9 0.0 0.3 0.1 0.0 0.1

0.1 0.1 0.0 0.0 0.0

0.0 0.0

1.1 0.6 0.3 0.3 0.2 0.2 0.4 0.1 0.1

0.0 0.4 0.0 0.1 0.1 0.0 0.0

(Continued )

13 12 11 11 9

11 11 9 9 8 6 4 4 2 0 1 1

4 4 2 4 3 3 5

14:32

0.0 0.0 0.0 0.0 0.0

4.4 1.9 2.5 0.2 1.8 0.6 3.5 1.8 0.5 0.2 0.1 0.5

0.0 0.0 0.0 0.0 0.0 0.1 0.1

July 6, 2011

0.0 0.0 0.0 0.1 0.0

0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.3 0.2 0.2 0.2

0.0 0.0 1.0 1.6 2.2 0.3 0.3

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0.2 0.2 0.1 0.2 0.1 0.1 0.2 0.2 0.5 0.4 0.5 0.6

0.0 0.0 1.1 2.1 3.0 1.2 0.9

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Jun-09 Jul-09 Aug-09 Sep-09 Oct-09 Nov-09 Dec-09 Zone 2.5 Jan-09 Feb-09 Mar-09 Apr-09 May-09 Jun-09 Jul-09 Aug-09 Sep-09 Oct-09 Nov-09 Dec-09 Zone 3.3 Jan-09 Feb-09 Mar-09 Apr-09 May-09

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263

264

0.6 0.3 0.1

1.3 0.7 0.3 ∗ 0.2 0.1 0.2 0.5 1.0 3.6 1.9 0.3

0.1 0.0 0.1 0.2 0.6 2.2 0.9 0.1

0.0 0.1 0.0 0.2 0.6 0.1 0.2

0.1 0.1 0.1 0.5 1.5 0.1 0.3 0.3 0.2 0.1 ∗ 0.0 0.0 0.0 0.1 0.4 1.3 0.8 0.2

0.0 0.0 0.0 0.1 0.5 0.0 0.0

0.0 0.0 0.0 0.1 0.3 0.8 0.3 0.1

0.1 0.1 0.1

0.0 0.0 0.0 0.0 0.2 0.0 0.0

se

0.4 0.2 0.3 ∗ 0.1 0.5 1.0 0.8 0.7 0.5 0.4 0.9

0.2 0.0 0.1 0.3 0.6 0.1 0.0

0.1 0.3 0.1 0.4 0.4 0.2 0.4 0.9

0.1 0.1 0.1

0.2 0.0 0.1 0.2 0.4 0.0 0.0

se

2 3 2 0 2 3 3 3 3 3 3 2

6 7 7 7 5 3 4

Number of farms

1.1 2.0 2.5 1.2 0.9 0.8 0.6 0.4 0.3 4.5 5.7 4.3

0.1 0.1 0.3 0.7 2.5 3.1 3.8

All motile stages

0.1 1.2 1.7 0.5 0.3 0.4 0.3 0.2 0.3 1.0 1.5 1.2

0.0 0.1 0.1 0.5 0.9 0.9 2.1

se

0.6 1.0 1.3 0.5 0.3 0.3 0.3 0.2 0.1 3.1 3.7 2.7

0.0 0.1 0.1 0.6 1.3 1.7 1.6

Adult female only

L. salmonis

0.1 0.4 1.1 0.3 0.2 0.2 0.1 0.1 0.1 0.9 0.9 0.9

0.0 0.0 0.0 0.3 0.5 0.6 0.8

se

0.5 0.9 0.6 0.1 0.0 0.3 0.1 0.5 0.1 0.1 0.1 0.2

0.1 0.3 0.1 0.1 0.1 0.8 0.7

All motile stages

0.5 0.0 0.2 0.0 0.0 0.2 0.1 0.2 0.1 0.0 0.1 0.0

0.1 0.2 0.0 0.1 0.0 0.3 0.4

se

C. clemensi

2 2 2 4 3 3 3 3 2 3 3 3

8 8 8 5 8 11 9

Number of farms

14:32

Jun-09 Jul-09 Aug-09 Sep-09 Oct-09 Nov-09 Dec-09 Zone 3.4 Jan-09 Feb-09 Mar-09 Apr-09 May-09 Jun-09 Jul-09 Aug-09 Sep-09 Oct-09 Nov-09 Dec-09

se

All motile stages

C. clemensi

Year 2

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Adult female only

L. salmonis

Year 1

G: 2009

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All motile stages

(Continued)

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Table 8.1.

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0.6 0.7 0.2 0.4 0.0 0.0 0.1 0.5 0.2 2.3 3.7 7.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.6 0.0

0.3 0.2 0.1 0.1 0.0 0.0 0.0 0.1 0.4 0.4 1.0 3.0

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.5 0.0

0.0 0.3 0.8 1.0 0.0 0.0 0.0 0.1 0.1 0.0 1.0 0.2

0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.5 0.0

2 1 1 2 1 1 1 1 1 1 2 1

0.2 0.2 0.2 0.3 1.0 0.9 2.3 3.0 3.5 ∗ 0.6 1.9

0.1 0.0 0.0 0.1 0.5 0.5 1.2 1.9 2.3 ∗ 0.2 0.4

0.1 0.0 0.2 1.7 0.1 0.1 0.0 0.0 0.0 ∗ 0.1 0.2 0.0 0.1

0.1 0.0 0.2 0.9 0.1 0.1 0.0 0.0 0.0

2 2 2 2 3 3 2 1 2 0 1 3

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0.0 0.3

0.1 0.0 0.0 0.1 0.2 0.3 0.2 0.0 2.3

BLBS084-Beamish

0.0 1.6

0.2 0.2 0.1 0.3 0.4 0.4 0.4 0.0 3.4

BLBS084-08

Zone 3.5 Jan-09 Feb-09 Mar-09 Apr-09 May-09 Jun-09 Jul-09 Aug-09 Sep-09 Oct-09 Nov-09 Dec-09

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lice abundance data summaries were made available to the public through the government Web site.

Government Auditing of Industry Sea Lice Monitoring in British Columbia In January 2004, the British Columbia Ministry of Agriculture and Lands initiated random sea lice audits on Atlantic salmon farms to assess the capacity of the farm staff to properly identify and enumerate sea lice, particularly motile L. salmonis, and the validity of the data reported by the salmon farm industry. Audited farms were selected at random by zone. Thus, zones with more farms had more audits. The audits were conducted on a quarterly basis with 50% of the salmon farms audited between April to July (quarter 2) and 25% of farms audited in each of the other quarters. For the majority of zones, more than one farm (ranging from one to nine) was audited during each sampling period or quarter. Farm personnel followed the protocol just described. For the actual audit, the 20 fish per pen were split such that Ministry technicians (auditors) evaluated lice on ten of the fish and the farm personnel evaluated the other ten. This was done for all three pens. The counts obtained by the auditor from the 30 assessed fish were statistically compared to the assessment made by the farm personnel. This enabled the auditor to determine the proficiency of farm personnel at sea lice identification. Audits conducted between 2004 and 2009 found that in 93% of the assessments (approximately 250 of 271) there was no statistical difference (at 5% error) in the assessment for motile L. salmonis and adult female L. salmonis between the farm personnel and the government auditors (BC-MAL 2003–2005, 2006, 2007, 2008, 2009), indicating that lice were properly identified and enumerated by farm personnel. More importantly, the audit program has been used to verify the accuracy of the sea lice data that industry provided to the provincial government on a monthly basis. While government audits were conducted quarterly, industry collected and submitted data on a monthly basis. Given the dynamic nature of lice abundance in zones—with some farms seeing increasing levels while others having decreasing levels in the same quarter—verification of accuracy was based on whether the mean abundance values obtained from audited farms during the quarter fall within the 95% confidence interval of all data collected from all farms in that zone and during that quarter. Saksida et al. (2006) reported that, for the 2004–2005 period, the audit data was not significantly different than the industry reported data most (about 75%) of the time. In 2004 and 2005, in instances where significant difference between the audit findings and the L. salmonis abundance levels reported by the salmon farms were observed, these differences were equally split (six and six, respectively) between the two parties—auditor and farmer. A similar comparison for data collected in 2009 showed a parallel trend with data collected during a quarter not being significantly different than the industry reported information (average 72% of the time). This provided confidence that the data reported by the industry was an accurate assessment of lice levels on the farms (BC-MAL 2006, 2007, 2008, 2009). In addition to the aggregated sea lice data provided by the salmon farming industry as a whole, individual farm sea lice counts are made available by two of the largest salmon producing companies in the region, (1) Marine Harvest Canada and

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(2) Mainstream Canada, through their respective company Web sites. Together, these companies make up approximately 80% of Atlantic salmon production in British Columbia. This level of data sharing is unique and provides the public with access to information not available in other farming regions. The following sections discuss the epidemiology of sea lice on salmon farms in British Columbia.

Epidemiology of Sea Lice on Farmed Salmon in British Columbia Sea Lice on Farmed Pacific Salmon As discussed previously, the sea lice assessment of and reporting on farmed Pacific salmon (chinook and coho salmon) are less stringent than requirements for farmed Atlantic salmon. Saksida et al. (2006) examined the sea lice data collected from farmed Pacific salmon in 2004, and found regional differences with salmon farmed east of Vancouver Island having higher mean abundance of motile L. salmonis than those farmed on the west coast of the Island. However, even during the autumn when higher lice levels would be expected, the mean level of motile L. salmonis was 3.7 for the farms located east of Vancouver Island. During the spring, when lice on the salmon farms need to be maintained below three motile L. salmonis, the mean abundance reported on farms with Pacific salmon was 0.7. Even without treatment, these lice levels were maintained at equal to or below those observed on the farmed Atlantic salmon. Reduced infection levels on Pacific salmon may occur because of an elevated innate immunity (see the introductory chapter contributed by Hayward et al.). C. clemensi levels on farmed chinook and coho salmon in British Columbia were even lower than those reported for L. salmonis with mean levels ranging between zero and 0.03 (Saksida, personal communication). As a consequence of the low levels of sea lice on farmed Pacific salmon in British Columbia, and due to the handling stress experienced by Pacific salmon, by the end of 2004 the provincial government stopped the required quarterly monitoring and reporting of sea lice abundance for these species. Continued monitoring was limited to opportunistic counts during routine handling events, and details of this monitoring were subject to audit.

C. clemensi on Atlantic Salmon in British Columbia C. clemensi infects a wide variety of fish species that are residents of British Columbia’s coastal waters (Parker and Margolis 1964; Beamish et al. 2005). Parker and Margolis (1964) suggested that this ecto-parasite is “specific to environment rather than host”—most likely a reflection of its wide host specificity. C. clemensi tends to be the less common sea louse species occurring on farmed Atlantic salmon. Even so, in 2003, C. clemensi made up 42% of the motile sea lice observed (Saksida et al. 2007a), and Beamish et al. (2006) reported a similar proportion (40.6% between February and July) from their study in the Broughton Archipelago. Unlike L. salmonis levels, which tend to be higher on farmed populations with longer ocean residency times, Saksida et al. (2007a, 2007b) reported that motile C.

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clemensi abundance levels did not appear to have a predilection to any year class. Additionally, these authors reported that C. clemensi levels showed annual variation though there did not appear to be consistent seasonal variation in the Broughton Archipelago. However, a more recent analysis utilizing Saksida et al. (2006, 2007a) methodology with a more extensive data set (2004–2009), which was taken from random British Columbia Agriculture and Lands sea lice audits data from all zones, indicates a higher abundance C. clemensi in younger salmon populations when combined data were assessed (I. Keith, personal communication). Conversely, when the data were assessed by year, C. clemensi abundance levels on younger farmed salmon populations were significantly higher than those seen in older farmed salmon populations in only 3 of the 6 years examined (2004, 2005, and 2008) (I. Keith, personal communication, 2010). These new findings are similar to reports of C. elongatus infestation in Scotland in which higher abundance was seen in younger salmon populations (Revie et al. 2002a; McKenzie et al. 2004). Evidence indicates that significant seasonal differences in mean abundance of C. clemensi were, from highest to lowest, respectively: autumn, winter, summer, and spring (see Chapter 3 contributed by Chang et al.). In addition, significant differences in abundance of C. clemensi exist: highest abundance is observed in the Campbell River and Port Hardy regions and lowest abundance in the Sunshine Coast region (I. Keith, personal communication). This new evidence of year-class combined with seasonal and regional pattern differences could be a reflection of the greater statistical power achieved through examination of a more extensive data set. However, it may also be a consequence of the higher frequency for sea lice treatments that occur in older populations as compared to younger salmon populations and treatment timing necessary to meet L. salmonis thresholds for the period (Saksida et al. 2007a).

L. salmonis on Atlantic Salmon in British Columbia L. salmonis levels on farmed Atlantic salmon tend to fluctuate both temporally and spatially. Levels generally rise as time spent in seawater increases. This trend has been reported in both wild and cultured salmon and is likely attributable to increased exposure time (Nagasawa 1985; Bron et al. 1991; Tully and Nolan 2002; Revie et al. 2002b; Heuch et al. 2003; Trudel et al. 2007). Saksida et al. (2006) reported that levels of L. salmonis on Atlantic salmon more than 1 year in seawater were 2.5 times higher than on salmon less than 1 year in seawater. The rate of increase of motile L. salmonis on farmed salmon in British Columbia was estimated at 2% per month (Saksida et al. 2007b).

Variation in Sea Lice Abundances between Seasons With few exceptions, L. salmonis levels increase in the autumn on farmed Atlantic salmon in British Columbia (Saksida et al. 2006, 2007a, 2007b). The lowest levels are most often reported in the summer. Beamish et al. (2006) reported that, in one region, prevalence of sea lice infected Atlantic salmon ranged from 85% in February to 46% in August and the intensity of all lice stages on fish was highest in February (21 lice per fish) and lowest in July (3.3 lice per fish). Orr (2007) looked at numbers of gravid

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female lice to estimate egg production from selected farms located in the Broughton Archipelago. He estimated that maximum egg production occurred during November and December 2003 and that by January–February egg production was down by 50%. By March–April, egg production was down to 6% of the maximum estimated levels. The increase in lice abundance on farmed salmon in the autumn may be associated with the return of adult Pacific salmon to their natal rivers (Saksida et al. 2006, 2007a; Beamish et al. 2005). The British Columbia coast has much larger wild salmon populations than other salmon farming regions. Beamish et al. (2005; see also Chapter 10 contributed by Jones and Beamish) reported 100% prevalence with abundance ranging between 10 and 20 mobile L. salmonis on all five species of adult Pacific salmon returning to spawn along the coast of British Columbia. These authors suggested that in some years there could be between 10 and 40 million Pacific salmon in the Queen Charlotte Strait (the body or water adjacent to zones 3.3 and 3.4) (see Figure 8.2). Direct transfer of motile stages has been reported to occur in situations where host densities are high such as within salmon farms in Europe (Ritchie 1997; Tully and Nolan 2002) and from wild to farmed salmonids in Japan (Ho and Nagasawa 2001). For the period between March and July, when L. salmonis threshold levels were in effect, the majority of farms were in compliance with the maximum threshold of three motile L. salmonis, as seen in the aggregated data provided in Table 8.1. All zones were in compliance in 2007–2009. Of the years when there were zones not in compliance, three zones reported levels greater than three lice in at least one and in some cases up to 3 months of the 4-month period in 2004. Compliance was higher for farms with younger salmon than for those with older farmed salmon populations. For populations in seawater less than a year, compliance ranged from 85% (2004 and 2006) to 100% (2005, 2007–2009) of the zones compared to between 66% (2004 and 2006) and 100% (2007–2009) for salmon populations in seawater for more than 1 year (see Table 8.1). Saksida et al. (2007a, 2007b) summarized sea lice levels in the Broughton Archipelago between 2003 and 2005 and found mean motile lice levels were four times higher in 2004 than in either 2003 or 2005.

Variation in Sea Lice Abundances between Farming Regions There is considerable variation in L. salmonis abundance between farming regions or zones and in some cases within zones. For example, Saksida et al. (2006) reported that the abundance of L. salmonis ranged from 0.47 to 3.29 for 2004. Similar variations can be seen in the monthly values shown in Table 8.1. Furthermore, Saksida et al. (2007a) noted large standard deviation (SD) associated with the mean abundance within zones. For example, in October 2004, a SD of 6 was associated with a motile L. salmonis mean of 2.5 for farms in the Broughton Archipelago. Saksida et al. (2007b) described significant interzone variation for farms operating in this region. Variation in lice abundance between the different farming regions has been suggested to be partly related both to the species of wild salmon found in a zone and to their respective abundances or exposure risks (Saksida et al. 2006; Jones et al. 2006). The role that alternate host species may play in the natural infestation patterns of sea lice on wild and farmed salmon has not been determined as yet.

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Observed regional differences may be linked to environmental factors, including differences in temperature and salinity, or to local hydrography (Jones et al. 2006). For example, regions with the highest salinity reported the highest sea lice abundance levels (Saksida et al. 2006, 2007a). Laboratory studies confirm associations between environmental factors and lice abundance and in British Columbia there are differences in environment factors between salmon farming regions or zones. Changes in salinity and temperature are reported to affect L. salmonis survival and growth rates. Johnson and Albright (1991b) reported that at salinities of 20 and 25 mg/L, the majority of active nauplii died at the copepodid molt stage. Active copepodids were only obtained at 30 mg/L. Salinity varies considerably among the different coastal regions in British Columbia. For instance, both the west coast regions of Vancouver Island as well as the Broughton Archipelago show intraannual variation in surface (0–1 m) salinity. While farms on the west coast of Vancouver Island report lowest levels of salinity in the winter and highest in the summer with a mean difference of 4 mg/L (23–27 mg/L), farms situated in the Broughton Archipelago report highest salinity levels in the winter and lowest in the summer with mean differences of almost 6 mg/L reported (range 23–29 mg/L) (Saksida et al. 2006). On the west coast of Vancouver Island, variation in salinity is associated with precipitation, which is especially high during the fall and winter, while in the Broughton Archipelago, the variation is associated with snowmelt in the summer (Foreman et al. 2006; Saksida et al. 2006, 2007a, 2007b; Beamish et al. 2006). Saksida et al. (2007b) used a generalized linear model to assess factors in a 3-year data set that were associated with L. salmonis abundance in the Broughton Archipelago. Although several factors such as salmon age, farm location, and time of year were found to be significantly associated with abundance—salinity was not. There is less intraannual variation in the other farming regions even though there are differences in the average salinity values between regions. For instance, the Sunshine Coast farms report annual salinity of about 23 mg/L, while the other regions report about 30 mg/L (Saksida et al. 2006). The Sunshine Coast (zone 3.1), which is the southernmost farming region, reported the lowest sea lice level on a consistent basis with mean monthly motile levels frequently below one L. salmonis per fish without the use of therapeutants. Consequently, the requirement for monthly reporting within zone 3.1 was discontinued in 2006 (see Table 8.1). Even so, the government continued to include these farms in the audit program (Saksida et al. 2006). The farms in zone 3.1 voluntarily started reporting into the database in 2010. There are few differences in the water temperature profiles among the various regions. Sea temperatures (at 5 m) are higher in the summer than the winter months for each region. In the Broughton Archipelago, water temperatures at salmon farms range from 6 to 13.2◦ C (Saksida et al. 2007a). Water temperatures in the other regions do not decrease much below those reported in the Broughton Archipelago (Saksida et al. 2006); however, some regions experience higher summer water temperatures. Temperature does not have a significant effect on the abundance of sea lice on farmed salmon in the Broughton Archipelago (Saksida et al. 2007b) or in the other salmon farming areas of British Columbia (Saksida et al. 2006). This may be because the reported temperatures are within the tolerance levels of L. salmonis (Johnson and Albright 1991b). It is interesting that, during the summer when water temperatures are the warmest and the development of L. salmonis is expected to be greatest, the abundance levels of lice in all zones is lower than in the winter (Saksida et al. 2006).

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Hydrographic Effects on Abundance Other environmental factors such as current speed and flushing time are significant contributors to sea lice levels in Scotland according to Revie et al. (2003) . As previously mentioned (see Chapter 4 contributed by Stucchi et al.), a study conducted by Foreman et al. (2006) indicates that the primary transport mechanisms in the Broughton Archipelago are estuarine flows resulting from considerable river and glacier melt runoff. These influences are particularly strong in the inlets of the region especially during the summer months when river flow is highest. Wind-driven circulation likely plays a significant role in sea lice dispersion (Asplin et al. 1999; Murray and Gillibrand 2006). The significance of these factors around the salmon farms in British Columbia is still not understood.

Treatments for Sea Lice in British Columbia Treatment for sea lice prior to the establishment of threshold levels in 2003 was rare (Figure 8.3). Prior to 2000, the only therapeutant used with any frequency for the treatment of sea lice on farmed salmon in British Columbia was ivermectin (available by veterinary prescription). The product was administered via medicated feed (4-day treatment at 0.05 mg/kg/fish/day). Ivermectin has been reported to be quite toxic to Atlantic salmon (Johnson et al. 1993; Palmer et al. 1996) and, in an attempt to minimize toxicity, veterinarians often instructed that the medicated feed be provided every other day or every third day until the full 4-day treatment regime was completed or until signs of potential toxicity were noted. The other tool used in the management of sea lice was to move the salmon through a fish pump (i.e., SILKSTREAMTM , ETI, Washington, USA) in order to dislodge the motile lice from the fish. The discharge water would sometimes be filtered to collect the detached lice. This method was very labor intensive and resulted in stress and physical injury to the fish. 0.4

Grams/mt of salmon produced

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lvermectin

Emamectin benzoate

0.3

0.2

0.1

0.0 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009

Figure 8.3. The quantity of products used by the aquaculture industry for sea lice treatment between 1996 and 2009.

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R In 1999, emamectin benzoate (SLICE , Intervet-Schering Plough Animal Health) became available to veterinarians under a special permit, called an emergency drug release or EDR, obtained from federal government regulatory authorities (Health Canada). Shortly after this, it became the only therapeutant used for sea lice treatment R , Nutreco), in British Columbia. Another in-feed product, teflubenzuron (Calicide did achieve registration in Canada for use in salmon; however, the product has not been used in British Columbia due to difficulties with availability and to the product’s limited effectiveness on adult lice. The option of bath treatments has yet to be implemented in British Columbia. R is an approved therapeutant in most major salmon aquaculture countries SLICE R is including Norway, Scotland, Ireland, and Chile. The treatment regime for SLICE the same as that used in other regions (7-day treatment at 0.05 μg emamectin benzoate per kg of fish/day). In Canada, the withdrawal period—the amount of time following treatment that the fish must be held before they can be harvested—has been amended several times since the drug has been available under the Emergency Drug Release permit. Initially, it was set at 25 days when used at water temperatures above 5◦ C with a maximum residue limit set at 100 parts per billion (ppb). In 2005, Health Canada R residues after completing a reassessment amended its policy on permitted SLICE of available data and modified the maximum residue limit down to 42 ppb, while increasing the withdrawal level to 68 days when the product was used at temperatures above 5◦ C. In 2008, Health Canada revised the Emergency Drug Release conditions R such that the harvest of fish prior to the 68-day withdrawal period was for SLICE permitted if the farm demonstrated that the populations to be harvested were equal to or less than the maximum residue limit of 42 ppb based on the results of three tissues taken from ten fish in each harvest pen. This amendment was introduced to accommodate salmon farmers on the east coast of Canada who had experienced R finally gained full registration problems with Infectious Salmon Anemia. SLICE approval in July 2009 with a recommended withdrawal period of zero days. Figure 8.3 shows the total amount of emamectin benzoate used in the treatment of R usage after sea lice to the end of 2009. This figure illustrates an increase in SLICE the introduction of the threshold limits with quantities in 2005 over 2.5 times greater than levels that existed when the BC Sea Lice Management Strategy was implemented in October 2003. However, use does not appear to have climbed any further with the amount used in both 2007 and 2009 being lower than in 2004/2005. Saksida et al. (2006) examined sea lice treatment data collected from all farms during the first 2 years of the regular monitoring program (2004, 2005) and reported R treatments for Atlantic salmon ranged from zero to that the total number of SLICE three per production cycle (i.e., smolt entry to harvest). In another report, the average number of treatments per production cycle was estimated to be 1.6 in the Broughton Archipelago with the average farmed salmon residing in the ocean almost 9 months before receiving its first treatment (Saksida et al. 2007a). Additional data reported in Saksida et al. (2010) suggest that frequency of treatment has not changed over the 5 years since the establishment of the maximum threshold levels. This same data set shows that each year there are farms that do not require treatment for sea lice. This level of treatment frequency is lower than levels reported in other national and international salmon farming jurisdictions (Johnson et al. 2004). Sea lice levels have been reported to remain lower than pretreatment levels for R treatment on salmon farms in British Columbia 3 to 5 months following a SLICE

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(Saksida et al. 2007a, 2010). This is apparently a substantially longer efficacy period than in Europe and Eastern North America where reported duration of efficacy ranged from 43 days to 14 weeks (Armstrong et al. 2000; Stone et al. 2000a, 2000b; Treasurer et al. 2002). The other explanation for the long efficacy period may be infection pressures during the summer as discussed previously. However, the length of the “lice-free” period in British Columbia and the generation time for lice reproduction at ambient water temperatures in British Columbia indicate that reinfestation from within a farm following a site-wide treatment is unlikely. R treatments are reported to occur in populations of Atlantic Almost 75% of SLICE salmon during their second year in seawater and between October and March (Saksida et al. 2007a, 2010). This differs from the reported situation in Norway and Scotland where the majority of treatments occur in the summer and fall months (Heuch et al. 2003). The difference is likely the result of trying to reduce the mean motile L. salmonis abundance levels to below three for the start of the spring wild juvenile Pacific salmon migration out of the nearshore in March and adherence to required withdrawal periods as set out under the special permit (Emergency Drug Release). However, there is very little evidence to suggest that any of the treatments were provided in response to health concerns in the farmed salmon. As such, the treatment of animals in the absence of a diagnosed medical condition results in an ethical conundrum for the aquaculture veterinarians—more than once, the question has been raised “if the health of the animal is not dependent upon medicinal treatment, is treatment of the animal ethical?” An immediate concern for the salmon farming industry in British Columbia continues to be the inherent limitation of having only one sea lice treatment product available for use. In other agricultural industries, integrated pest management (IPM), including a rotation of treatments, is used to prevent or delay development of resistance in a pathogen. Concerns regarding emamectin benzoate treatment failures, reduced sensitivity, and/or potential resistance have been voiced and confirmed in Scotland, Ireland, Chile, eastern Canada, and Norway (Lees et al. 2008a, 2008b; O’Donohoe et al. 2008; Bravo et al. 2008; T. Horsberg, personal communication). For example, Lees et al. (2008a, 2008b) analyzed abundance data from Atlantic salmon farms in Scotland between 2002 and 2006 and found that following some treatments, efficacy reduced over time. Conversely, Saksida et al. (2010) conducted a similar analysis with data collected from farms in British Columbia from 2003 when mandatory monitoring and lice thresholds were implemented to 2008 and found that there was no change in the efficacy of the emamectin benzoate’s apparent duration of effect. The latter study found that 1 month (26–34 days) posttreatment lice levels had fallen to below 20% of pretreatment levels and remained at or below 10% of pretreatment levels for at least 1 month, the time period assessed. By comparison, Lees et al. (2008a) defined an “effective” treatment in Scotland, as a treatment where the abundance of motile L. salmonis fell to less than 40% of their pretreatment level at some point in the 13 weeks posttreatment. Based on this definition, all of the treatments evaluated in British Columbia clearly fulfilled the criterion of being effective, with levels by 13 weeks posttreatment remaining at or below 10% of pretreatment levels. Review of 2009 data showed the same pattern (D. Morrison, personal communication). This suggests that, unlike most other salmon farming regions, a decline in efficacy R ) is not evident on salmon farms in British Columbia. of emamectin benzoate (SLICE

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While this may be good news for the British Columbia salmon farming industry, it does not lessen the need for additional sea lice treatment options. It is vital for the salmon farming industry in British Columbia to monitor closely the continued efficacy R . Furthermore, other methods for sea lice control of its sole treatment option, SLICE must be approved and adopted for use so that salmon farmers in British Columbia can employ the IPM methods used in other salmon farming jurisdictions.

Summary Sea lice on salmon farms—their levels and their impacts on wild populations—have been heavily debated in British Columbia. Initially, much of the debate (as well as research) about sea lice on farmed salmon centered around farms operating in the Broughton Archipelago, but this focus has expanded to other farming regions over the last few years. This controversy has resulted in substantive and critical changes to how sea lice on British Columbia farmed salmon are monitored and managed. Upon establishment of a British Columbia Sea Lice Management Strategy, data have been collected to show that sea lice abundance does vary among the different farming regions or zones in the province. This data appeared to support the claim that patterns of infestation and pathogenicity of L. salmonis on farmed Atlantic salmon in British Columbia are quite different to what has been commonly reported in Europe and the east coast of North America. In British Columbia, levels of sea lice appear to be lower and require fewer treatments to maintain these low levels. Emamectin benzoate R ) continues to be efficacious even while resistance against the compound is (SLICE being demonstrated in other farming regions in the world. Sea lice in British Columbia do not appear to pose a significant health risk to farmed salmon. The availability of sea lice data provided through provincial government Web sites as well as private fish farm companies has made British Columbia one of the most transparent salmon farming jurisdictions. While there are some concerns regarding the designation of the subzones, the British Columbia Sea Lice Management Strategy has proven itself to be quite flexible with ongoing, responsive modifications occurring as new data are collected and reviewed. A good example of this flexibility is the discontinuance of regular monitoring for farmed Pacific salmon and for all salmon species farmed on the Sunshine Coast. However, a concern regarding the flexibility of the treatment thresholds is whether the government will see fit to modify the treatment thresholds (up or down or perhaps by subzone) as the results of ongoing and future scientific work being conducted on the effects of sea lice (if any) on juvenile salmon health becomes available. As McVicar (2004) noted, a more thorough understanding of factors influencing sea lice levels on cultured salmon in British Columbia, including local hydrography, would be prudent to ensure that management practices reflect the true level of risk to both farmed and wild populations.

Acknowledgments Thank you to Joanne Constantine and Grace Karreman for their vision and dedication to bringing the sea lice audit program and the sea lice database into fruition. Acknowledgment is due to a number of people for their help in the collection of data

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and the preparation of this chapter: Howie Manchester, Christopher Diamond, Maria Coombs who conducted the sea lice audits on behalf of the British Columbia Ministry of Agriculture and Foods; Brad Boyce for his assistance in collecting farm data; Sean Cheesman who prepared the map for the manuscript; Howie Manchester and Carmen Matthews for double checking audit data and Paula Galloway for her editorial assistance. We would also like to thank Tor Horsberg for providing information of R in Norway. the efficacy issues with SLICE

References Armstrong, R., MacPhee, D., Katz, T., and Endris, R. 2000 A field efficacy evaluation of emamectin benzoate for the control of sea lice on Atlantic salmon. Canadian Veterinary Journal 41: 607–612. Asplin, L., Salvanes, A.G.V., and Kristoffersen, J.B. 1999 Nonlocal wind-driven fjord—coast advection and its potential effect on plankton and fish recruitment. Fisheries Oceanography 8: 255–263. Beamish, R.J., Neville, C.M., Sweeting, R.M., and Ambers, N. 2005. Sea lice on adult Pacific salmon in the coastal waters of central British Columbia, Canada. Fisheries Research 76: 198–208. Beamish, R.J., Jones, S., Neville, C.M., Sweeting, R., Karreman, G., Saksida, S., and Gordon, E. 2006. Exceptional marine survival of pink salmon that entered the marine environment in 2003 suggest that farmed Atlantic salmon and Pacific salmon can coexist successfully in a marine ecosystem on the Pacific coast of Canada. ICES Journal of Marine Sciences 63: 1326–1337. Beamish, R.J., Wade, J., Pennell, W., Gordon, E., Jones, S., Neville, C., Lange, K., and Sweeting, R. 2009. A large, natural infection of sea lice on juvenile Pacific salmon in the Gulf Islands area of British Columbia, Canada. Aquaculture 297: 31–37. Brandal, P. and Egidius, E. 1979. Treatment of salmon lice (Lepeophtheirus salmonis Krøyer, 1838) with Neguvon-description of method and equipment. Aquaculture 18: 183– 188. Bravo, S., Sevatdal, S. and Horsberg, T.E. 2008. Sensitivity assessment of Caligus rogercresseyi to emamectin benzoate in Chile. Aquaculture 282: 7–12. British Columbia Ministry of Agriculture and Lands (BC-MAL). 2003–2005, 2006, 2007, 2008, 2009. Fish Health Program Annual Report 2003–2005, 2006, 2007, 2008, 2009. Available at: http://www.agf.gov.bc.ca/ahc/fish_health/index.htm (accessed June 6, 2011). British Columbia Ministry of Environment. 2008. British Columbia Seafood Industry: Year in review 2009. Oceans and Marine Fisheries Branch, Victoria. Available at: http://www.env.gov.bc.ca/omfd/reports/YIR-2009.pdf (accessed June 6, 2011). Bron, J.E., Sommerville, C., Jones, M., and Rae, G.R. 1991. The settlement and attachment of early stages of the salmon louse, Lepeophtheirus salmonis (Copepoda: Caligidae) on the salmon host Salmo salar. Journal of Zoology 224: 201–212. Finstad, B., Bjorn, P.A., Grimnes, A., and Hvidsten, N. 2000. Laboratory and field investigations of salmon lice [Lepeophtheirus salmonis (Krøyer)] infestation on Atlantic salmon (Salmo salar L.) post-smolts. Aquaculture Research 31: 795–803. Foreman, M.G.G., Stucchi, D.J., Zhang, Y., and Baptista, A.M. 2006. Estuarine and tidal currents in the Broughton Archipelago. Atmosphere-Ocean 44: 47–63. Gende, S.C., Richards, R.T., Willson, M.F., and Wipfli, M.S. 2002. Pacific salmon in the aquatic and terrestrial ecosystems. BioScience 52: 917–928. Groot, C. and Margolis, L. 1991. Preface. In: Pacific Salmon Life Histories (eds C. Groot and L. Margolis), pp. ix–xi. UBC Press, Vancouver, BC.

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Heuch, P.A., Revie, C.W., and Gettinby, G. 2003. A comparison of epidemiological patterns of salmon lice, Lepeophtheirus salmonis, infections on farmed Atlantic salmon, Salmo salar L., in Norway and Scotland. Journal of Fish Diseases 26: 539–551. Heuch, P.A., Bjorn, P.A., Finstad, B., Holst, J.C., Asplin, L., and Nilsen, F. 2005. A review of the Norwegian ‘National Action Plan Against Salmon Lice on Salmonids’: The effect on wild salmonids. Aquaculture 246: 79–92. Ho, J.S. and Nagasawa, K. 2001. Why infestation by Lepeophtheirus salmonis (Copepoda: Caligidae) is not a problem in the coho salmon farming industry in Japan. Journal of Crustacean Biology 21: 954–960. Johnson, S.C. and Albright, L.J. 1991a. Lepeophtheirus cuneifer Kabata, 1974 (Copepoda: Caligidae) from seawater-reared rainbow trout, Oncorhynchus mykiss, and Atlantic salmon, Salmo salar, in the Strait of Georgia, British Columbia. Canadian Journal of Zoology 69: 1414– 1416. Johnson, S.C. and Albright, L.J. 1991b. Development, growth, and survival of Lepeophtheirus salmonis (Copepoda: Caligiae) under laboratory conditions. Journal of the Marine Biological Association of the United Kingdom 71: 425–436. Johnson, S.C., Kent, M.L., Whitaker, D.J., and Margolis, L. 1993. Toxicity and pathological effects of orally administered ivermectin in Atlantic, chinook and coho salmon and steelhead trout. Diseases of Aquatic Organisms 17: 107–112. Johnson, S.C., Treasurer, J.W., Bravo, S., Nagasawa, K., and Kabata, Z. 2004. A review of the impact of parasitic copepods on marine aquaculture. Zoological Studies 43: 229–243. Jones, S.R.M., Prosperi-Porta, G., Kim, E., Callow, P., and Hargreaves, N.B. 2006a. The occurrence of Lepeophtheirus salmonis and Caligus clemensi (Copepoda: Caligidae) on three-spine stickleback Gasterosteus aculeatus in coastal British Columbia. Journal of Parasitology 92: 473–480. Jones, S.R.M., Kim, E., and Dawe, S. 2006b. Experimental infections with Lepeophtheirus salmonis (Krøyer) on threespine sticklebacks, Gasterosteus aculeatus L., and juvenile Pacific salmon, Oncorhynchus spp. Journal of Fish Diseases 29: 489–495. Kabata, Z. 1972. Development stages of Caligus clemensi (Copepoda: Caligidae). Journal of Fisheries Research Board of Canada 29: 1571–1593. Kabata, Z. 1974. Lepeophtheirus cuneifer sp. Nov. (Copepoda: Caligidae), a parasite of fishes from the Pacific coast of North America. Journal of Fisheries Research Board of Canada 31: 43–47. Kent, M.L., Traxler, G.S., Kieser, D.,Richard, J., Dawe, S.C., Shaw, R.W., Prosperi-Porta, G., Ketcheson, J., and Evelyn, T.P.T. 1998. Survey of salmonid pathogens in ocean-caught fishes in British Columbia, Canada. Journal of Aquatic Animal Health 10: 211–219. Krkoˇsek, M., Lewis, M.A., and Volpe, J.P. 2005. Transmission dynamics of parasitic sea lice from farm to wild salmon. Proceedings of the Royal Society B 272: 689–697. Krkoˇsek, M., Lewis, M.A., Morton, A., Frazer, L.N., and Volpe, J.P. 2006a. Epizootics of wild fish induced by farm fish. Proceedings of the National Academy of Science 103: 15506–15510. Krkoˇsek, M., Lewis, M.A., Volpe, J.P., and Morton, A. 2006b. Fish farms and sea lice infestations of wild juvenile salmon in the Broughton Archipelago—a rebuttal to Brooks (2005). Reviews in Fisheries Science 14: 1–11. Krkoˇsek, M., Ford, J.S., Morton, A., Lele, S., Myers, R.A., and Lewis, M.A. 2007. Declining wild salmon population in relation to parasites from farmed salmon. Science 318: 1772– 1775. Lees, F., Baillie, M., Gettinby, G., and Revie, C. 2008a. The efficacy of emamectin benzoate against infestations of Lepeophtheirus salmonis on farmed Atlantic Salmon (Salmo salar L.) in Scotland, 2002–2006. PloS ONE 3: e1549. Lees, F., Baillie, M., Gettinby, G., and Revie, C.W. 2008b. Factors associated with changing efficacy of emamectin benzoate against infestations of Lepeophtheirus salmonis on Scottish salmon farms. Journal of Fish Diseases 31: 947–951.

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McKenzie, E.G., Gettinby, G., McCart, K., and Revie, C.W. 2004. Time series models of sea lice Caligus elongatus (Nordmann) abundance on Atlantic salmon Salmo salar L. in Loch Sunart, Scotland. Aquaculture Research 35: 764–772. McVicar, A.H. 2004. Management actions in relation to the controversy about salmon lice infections in fish farms as a hazard to wild salmonid populations. Aquaculture Research 35: 751–758. Morton, A.B. and Williams, R. 2003. First report of a sea louse, Lepeophtheirus salmonis, infestation on juvenile pink salmon, Oncorhynchus gorbuscha, in nearshore habitat. Canadian Field Naturalist 117: 634–641. Morton, A., Routledge, R., and Krkoˇsek, M. 2008. Sea louse infestation in wild juvenile salmon and Pacific herring associated with fish farms off the east-central coast of Vancouver Island, British Columbia. North American Journal of Fisheries Management 28: 523–532. Morton, A., Routledge, R., Peet, C., and Ladwig, A. 2004. Sea lice (Lepeophtheirus salmonis) infection rates on juvenile pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon in the nearshore marine environment of British Columbia, Canada. Canadian Journal of Fisheries and Aquatic Sciences 61: 147–157. Murray, A.G. and Gillibrand, P.A. 2006. Modelling salmon lice dispersal in Loch Tirridon, Scotland. Marine Pollution Bulletin 53: 128–135. Nagasawa, K. 1985. Comparison of the infestation levels of Lepeophtheirus salmonis (Copepoda) on chum salmon captured by two methods. Japanese Journal of Ichthyology 32: 368–370. Nagasawa, K. 2001. Annual changes in the population size of the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae) on high-seas Pacific salmon (Oncorhynchus spp.), and relationship to host abundance. Hydrobiologia 453/454: 411–416. Nagasawa, K., Ishida, Y., Ogura, M., Tadokora, K., and Hiramatsu, K. 1993. The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on six species of Pacific salmon in offshore waters of the North Pacific Ocean and Bering Sea. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 166–178. Ellis Horwood, Chichester, UK. O’Donohoe, P., Kane, F., Kelly, S., Nixon, P., Power, A., Naughton, O., and Jackson, D. 2008. National Survey of Sea Lice (Lepeophtheirus salmonis Krøyer and Caligus elongatus Nordmann) on Fish Farms on Ireland—2007. Available at: http://www.marine.ie/home/ publicationsdata/ publications/Irish+Fisheries+Bulletin.htm (accessed April 20, 2011). Orr, C. 2007. Estimated sea louse egg production from Marine Harvest Canada farmed Atlantic salmon in the Broughton Archipelago, British Columbia, 2003–2004. North American Journal of Fisheries Management 27: 187–197. Palmer, R., Coyne, R., Davey, S., and Smith, P. 1996. Case notes on adverse reactions associated with ivermectin therapy of Atlantic salmon. Bulletin of the European Association of Fish Pathologists 17: 62–67. Parker, R. and Margolis, L. 1964. A new species of parasitic copepod, Caligus clemensi sp.nov. (Caligoida: Caligidae), from pelagic fishes on the coastal water of British Columbia. Journal of Fisheries Research Board of Canada 21: 873–889. Pert, C.C., Urquhart, K., and Bricknell, I.R. 2006. The sea bass (Dicentrarchus labrax L.): a peripatetic host of Lepeophtheirus salmonis (Copepoda: Caligidae)? Bulletin of the European Association of Fish Pathologists 26: 162–165. Pert, C.C., Mordue, A.J., Fryer, R.J., O’Shea, B., and Bicknell, I.R. 2009. The settlement and survival of the salmon louse, Lepeophtheirus salmonis (Krøyer, 1837), on atypical hosts. Aquaculture 288: 321–324. Pike, A.W. and Wadsworth, S.L. 1999. Sea lice on salmonids: their biology and control. Advances in Parasitology 44: 233–337. Revie, C.W., Gettinby, K., Treasurer, J.W., and Rae, G.H. 2002a. The epidemiology of the sea lice, Caligus elongatus Nordmann, in marine aquaculture of Atlantic salmon, Salmo salar L., in Scotland. Journal of Fish Diseases 25: 391–399.

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Revie, C.W., Gettinby, G., Treasurer, J.W., and Wallace, C. 2003. Identifying epidemiological factors affecting sea lice (Lepeophtheirus salmonis) abundance on Scottish salmon farms using general linear models. Diseases of Aquatic Organisms 57: 85–95. Revie, C.W., Gettinby, G., Treasurer, J.W., Rae, G.H., and Clark, N. 2002b. Temporal, environmental and management factors influencing the epidemiological patterns of sea lice (Lepeophtheirus salmonis) infestations on farmed Atlantic salmon (Salmo salar) in Scotland. Pest Management Science 58: 576–584. Ritchie, G. 1997. The host transfer ability of Lepeophtheirus salmonis (Copepoda: Caligidae) from farmed Atlantic salmon, Salmo salar L. Journal of Fish Diseases 20: 153–157. Saksida, S., Constantine, J., Karreman, G.A., and Donald, A. 2007a. Evaluation of sea lice abundance levels on farmed Atlantic salmon (Salmo salar L.) located in the Broughton Archipelago of British Columbia from 2003 to 2005. Aquaculture Research 38: 219–231. Saksida, S., Karreman, G.A., Constantine, J., and Donald, A. 2007b. Differences in Lepeophtheirus salmonis abundance levels on Atlantic salmon farms in the Broughton Archipelago, British Columbia, Canada. Journal of Fish Diseases 30: 357–366. Saksida, S.M., Morrison, D., and Revie, C.W. 2010. The efficacy of emamectin benzoate against infestations of sea lice (Lepeophtheirus salmonis) on farmed Atlantic salmon (Salmo salar L.) in British Columbia. Journal of Fish Diseases 33: 913–917. Saksida, S., Constantine, J., Karreman, G.A., Neville, C., Sweeting, R., and Beamish, R. 2006. Evaluation of sea lice Lepeophtheirus salmonis, abundance levels on farmed salmon in British Columbia, Canada. Paper read at 11th International Symposium on Veterinary Epidemiology and Economics, Cairns, Australia. Stone, J., Sutherland, I.H., Sommerville, C., Richards, R.H., and Endris, R.G. 2000a. The duration of efficacy following oral treatment with emamectin benzoate against infestions of sea lice, Lepeophtheirus salmonis (Krøyer), in Atlantic salmon Salmo salar L. Journal of Fish Diseases 23: 185–192. Stone, J., Sutherland, I.H., Sommerville, C., Richards, R.H., and Varma, K.J. 2000b. Commercial trials using emamectin benzoate to control sea lice Lepeophtheirus salmonis infestations in Atlantic salmon Salmo salar. Diseases of Aquatic Organisms 41: 141–149. Treasurer, J.W., Wallace, C., and Dear, G. 2002. Control of sea lice on farmed Atlantic salmon S. salar L. with the oral treatment Emamectin benzoate (SLICE). Bulletin of the European Association of Fish Pathologists 22: 375–380. Trudel, M., Jones, S.R.M., Thiess, M.E., Morris, J.F.T., Welch, D.W., Sweeting, R.M., Moss, J.H., Wing, B.L., Farley Jr., E.V., Murphy, J.M., Baldwin, R.E., and Jacobson, K.C. 2007. Infestations of motile salmon lice on Pacific salmon along the west coast of North America. American Fisheries Society Symposium 57: 1–25. Tully, O. and Nolan, D. 2002. A review of the population biology and host-parasite interactions of the sea louse Lepeophtheirus salmonis (Copepoda: Calgidae). Parasitology 124: S165–S182. Wootten, R, Smith, J.W., and Needham, E.A. 1982. Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids, and their treatment. Proceedings of the Royal Society of Edinburgh Section B 81: 185–197.

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Part III Salmon Lice on Wild Salmonids in Coastal Zones: Present Status and Implications

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Present Status and Implications of Salmon Lice on Wild Salmonids in Norwegian Coastal Zones Bengt Finstad and P˚ al Arne Bjørn

Introduction In the early 1990s, sea trout (Salmo trutta) in fish farming areas along the coast of Norway were recorded returning to rivers and estuaries shortly after they had descended to sea (“premature return”). These sea trout were heavily infected with salmon lice (Lepeophtheirus salmonis), and the infection was associated with significant skin pathology and severe emaciation (Jakobsen et al. 1992; Finstad et al. 1992; Sivertsen et al. 1993; Finstad 1993; Birkeland and Jakobsen 1994, 1997; Finstad et al. 1994a; Birkeland 1996). The epidermis is a physiological interface and it was obvious that salmon lice infection led to osmoregulatory dysfunction in heavily infected and wounded fish (Bjørn and Finstad 1997). Simultaneously, there seemed to be a collapse in the seawater survival among sea trout stocks in areas with intensive salmon farming activity. Preliminary investigations in Norway in the early 1990s indicated that lice infections also occurred on Atlantic salmon (Salmo salar) postsmolts migrating through the long and intensively farmed fjords of western and middle Norway (Finstad et al. 1994b; Holst et al. 2003). Furthermore, the Arctic charr (Salvelinus alpinus) in northern Norway probably became heavily infected in areas with salmon farms (Finstad 1993). It was therefore hypothesized that salmon lice epidemics may be partly responsible for the decline of certain populations of wild anadromous salmonids all along the Norwegian coast. Also in the early 1990s, knowledge of the physiological effects of salmon lice infection on salmonids was limited (Wootten et al. 1982) to only a few field studies on wild salmonids (Boxshall 1974; Johannessen 1975; Jakobsen et al. 1992; Tully et al. 1993; Finstad et al. 1994a, 1994b; Sharp et al. 1994). Physiological and ecological consequences of the observed infections, and the possible causal relationship between fish farming and salmon lice infection on wild salmonids had not been clarified. A further clarification of the phenomenon of premature return and more information on the physiological effects of salmon lice infection was therefore needed. In addition, thorough studies of the infection level, population structure, and the potential ecological effects of lice in wild salmonids were required. Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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Initial research on the physiological and the ecological effects of salmon lice infection on anadromous salmonids focused on testing the effects of controlled laboratory infections on sea trout, Atlantic salmon, and Arctic charr postsmolts. The development, survival rate, distribution, and pathogenicity of salmon lice on artificially infected postsmolts were also described (Grimnes and Jakobsen 1996; Bjørn and Finstad 1997, 1998; Finstad et al. 2000; Wagner et al. 2003, 2004; Wells et al. 2006, 2007). The second phase of research focused on trying to show a causal connection between the salmon lice epidemics in wild salmonids and the rapidly growing salmon farming industry. Of interest was the fraction of wild salmonid populations that were infected with salmon lice levels and had negative physiological or even lethal effects. This was done by performing extensive field studies capturing a representative subpopulation of sea trout, Atlantic salmon, and Arctic charr both in intensively farmed areas and in control areas, and studying the infection levels on these fish (Finstad et al. 1994a; Birkeland and Jakobsen 1997; Schram et al. 1998; Bjørn et al. 2001a; Bjørn and Finstad 2002; Holst et al. 2003; Rikardsen 2004; Heuch et al. 2005; Revie et al. 2009; Bjørn et al. 2008, 2009, 2010). The third phase of research focused on effects of annual salmon lice epidemics on populations of wild salmonids, especially sea trout and Atlantic salmon postsmolts, in intensively farmed coastal areas. This was done by releasing Carlin-tagged salmon and sea trout smolts in the vicinity of their native river after they were protected with medicated food or a bath treatment. This treatment protects the fish for several weeks, and provided it does not interfere with the fish in other ways, these experiments give estimates of population effects of lice (Finstad and Jonsson 2001; Hazon et al. 2006; Hvidsten et al. 2007; Skilbrei and Wennevik 2006, Skilbrei et al. 2008). Finally, the research focused on whole fjord studies, including integrated pest management (IPM), and with the long-term objective to facilitate a sustainable coexistence of fish farming and wild salmonids in the intensively farmed fjords of Norway. The establishment of the Norwegian National Salmon Fjords in recent years protected fjord areas without salmon farming (Anon. 2006).

Physiology and Pathology of Lice Infections in Atlantic Salmon, Sea Trout, and Arctic Charr Laboratory studies identified the effect of salmon lice (Figure 9.1) on the physiology of Atlantic salmon, sea trout, and Arctic charr (e.g., Grimnes and Jakobsen 1996; Grimnes et al. 1996; Bjørn and Finstad 1997, 1998; Nolan et al. 1999; Finstad et al. 2000; Bjørn et al. 2001a; Wagner et al. 2003, 2004; Wells et al. 2006, 2007; Finstad et al. 2007a). Major primary, secondary, and tertiary physiological effects (Wendelaar Bonga 1997; Iwama et al. 2006), including high levels of plasma cortisol (Bjørn and Finstad 1997; Finstad et al. 2000) and glucose (Wells et al. 2006), reduced osmoregulatory ability (Grimnes and Jakobsen 1996; Bjørn and Finstad 1997; Nolan et al. 1999), and reduced nonspecific immunity occur when the lice develop from the sessile chalimus 4 stage to the mobile first preadult stage. Sublethal tertiary effects, such as reduced growth, reduced reproduction, reduced swimming performance, and impaired immune defense have also been reported (Bjørn and Finstad, 1997; Nolan et al., 1999, 2000; Finstad et al. 2000; Bjørn et al. 2001a; Wagner et al. 2003, 2004; Tveiten et al. 2010). Also, the host may show differing genetic susceptibility to salmon

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Figure 9.1. Adult female salmon lice on an adult Atlantic salmon. (Photo: Bengt Finstad, NINA.) (See also color plate section.)

lice (Glover et al. 2001, 2003, 2004). A number of reviews examined the effects of lice on wild salmonids (Pike and Wadsworth 1999; Tully and Nolan 2002; Johnson et al. 2004; Heuch et al. 2005; Boxaspen 2007; Costello 2006; Boxaspen et al. 2007; Wagner et al. 2008; Revie et al. 2009; Finstad et al. 2011).

Osmotic and Ionic Regulation in Salmonid Fish The body fluids of a freshwater fish (about 320 milliosmols (mOsm)) have a higher concentration of salts than the aqueous medium of its environment. Water will thus tend, by osmosis, to enter the body, while salts will tend to exit. In consequence, the fish would gradually become hydrated. The fish compensates this by excreting diluted urine and by an active uptake of salts (Na+ and Cl− ) through the gills (Evans 1979; Marshall and Grosell 2006). In seawater (about 1000 mOsm) where the fish faces salmon lice attacks, the body fluids of the fish are less concentrated than its surroundings. Water will thus tend to leave the fish, by osmosis, while salts will enter. The fish would gradually become dehydrated. To compensate for this, the fish drink seawater and excrete excess salts actively through the gills (Na+ and Cl− ) and the kidneys (Mg2+ , Ca2+ , and SO4 2− ) (Evans 1979; Marshall and Grosell 2006). Salmon lice attacks create an osmotic and ionic imbalance in fish due to the fact that the parasite feeds on the mucus, skin (Kabata 1974; Bjørn and Finstad 1998), and blood (Brandal et al. 1976) of the host. This feeding activity causes mechanical damage, such as skin and fin erosion (Wootten et al. 1982; Jones et al. 1990; Bjørn and Finstad 1998), osmotic stress due to “leakage” in the skin, and in extreme cases, results in death (Grimnes and Jakobsen 1996; Grimnes et al. 1996; Bjørn and Finstad 1997).

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Further, increased cortisol is caused by infection with young and older salmon lice stages (e.g., increased stress; Bjørn and Finstad 1997; Finstad et al. 2000), which further exaggerates the osmotic and ionic imbalance in fish.

Atlantic Salmon Grimnes and Jakobsen (1996) showed that before adult lice appear, infection intensity above 30 salmon lice larvae per fish caused death of Atlantic salmon postsmolts with an initial weight of 40 g. The physiological responses were shown as an increase in plasma chloride levels and a decrease in total protein, albumin, and hematocrit in infected fish. Finstad et al. (2000) confirmed the work of Grimnes and Jakobsen (1996) and showed that osmoregulatory problems for fish infested by salmon lice first occurred after the preadult stages of the lice appeared. It was shown that over 30 chalimus larvae could kill a 40-g salmon postsmolt once the larvae developed into the preadult stages. A relative intensity of approximately 0.75 (lice/g) indicated that 11.3 chalimus larvae may have a detrimental effect on a wild smolt of 15 g. The consequences for wild smolts were also shown by Holst et al. (2003) who examined more than 3000 postsmolts for lice. No fish carrying more than ten adult lice were found. Further support for this threshold comes from an experimental study of naturally infected salmon smolts collected during a monitoring cruise. Half of the fish were deloused as a control, and the health of the two fish groups were monitored. Only fish carrying 11 lice or less survived (Holst et al. 2003). Wagner et al. (2003, 2004) investigated sublethal levels of salmon lice (0.02–0.13 lice/g) on adult Atlantic salmon and found that the swimming performance of salmon was significantly reduced in fish with higher salmon lice numbers. Interestingly, these findings showed that the level of salmon lice infection was much lower than has previously been reported to be detrimental to Atlantic salmon and further raises the concern for the health and fitness of wild Atlantic salmon infected by sublethal levels of salmon lice. Early chalimus larvae did not seem to have any physiological impact (in terms of increased chloride levels) on the host. However, the higher cortisol levels measured in infested fish compared to uninfested fish (Finstad et al. 2000) were already found at the first sample postinfection (at chalimus stages) showing that infested Atlantic salmon also suffered from primary alteration prior to osmotic stress (secondary alteration). Increased cortisol levels are known to cause immunosuppression, which results in increased susceptibility for infectious diseases (Ellis 1981; Pickering and Pottinger 1989; Wedemeyer 1996). Implantation of corticosteroids in fish is shown to increase their susceptibility to a variety of parasitic diseases. In a laboratory study, coho salmon (Oncorhynchus kisutch) were shown to be more susceptible to salmon lice infections when artificially stressed by cortisol implants relative to coho salmon without cortisol implants (Johnson and Albright 1992a). Atlantic salmon seem to have a low effective immunity against both sea lice, Caligus elongatus, (MacKinnon 1993, 1998) and salmon lice, L. salmonis (Grayson et al. 1991; Johnson and Albright 1992b). Thus, stress caused by salmon lice infestations may further increase the host susceptibility for reinfection by salmon lice as well as secondary infections. Prior residence of Atlantic salmon in freshwater of suboptimal quality may further increase the susceptibility to salmon louse infections. This is seen in a study by Finstad et al. (2007a) where Atlantic salmon smolts were exposed to water containing varying

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Figure 9.2. Smolt exposed to acid aluminum containing water is more sensitive to salmon lice attacks. (Photo: Bengt Finstad, NINA.)

degrees of acid aluminium (Figure 9.2). Mortality was low in noninfected control groups, and significantly elevated in the lice infected groups. Plasma chloride levels were within the normal range in the noninfected groups, while fish in the infected high acid and moderate acid groups had elevated plasma chloride levels.

Sea Trout Bjørn and Finstad (1997) observed a sudden increase in fish mortality when they artificially infected hatchery-reared postsmolts of sea trout (mean weight 91 g). Chalimus stages of the lice caused minor osmoregulatory disturbances in the fish but even early chalimus stages caused high levels of plasma cortisol and a significantly reduced lymphocyte–leukocyte ratio. The infected fish contracted severe osmoregulatory problems and anemia after the first preadult stage of the lice had appeared. This was shown by increased plasma chloride levels and decreased hematocrit levels. Mortality was observed in the group with highest infection. From this study it was predicted that infection intensities above 90 salmon lice copepodids or 50 preadult or adult lice may result in mortality of small sea trout postsmolts (60 g). In subsequent studies, Wells et al. (2006) concluded that 13 mobile lice (Figure 9.3) per fish was the critical intensity that elicited sublethal stress responses in postsmolt sea trout (weight range 19–70 g). Based on the previous findings, a conservative and precautionary approach to protect wild fish would be to adopt a critical level of less than ten mobile lice per fish for sea trout in their first year. The abundance of salmon lice and the physiological effects of infection were examined in two stocks of sympatric sea trout and anadromous Arctic charr in northern Norway at locations with and without fish farming activity (Bjørn et al. 2001a). The results showed that the lice infection was significantly higher at the farm locality. Blood samples taken from sea trout at sea at the farm locality showed a positive correlation between intensity of parasite infection and an increase in the plasma cortisol, chloride, and blood glucose concentrations.

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Figure 9.3. Sea trout infected with mobile salmon lice. (Photo: Bengt Finstad, NINA.) (See also color plate section.)

Up to 47% of the fish caught in freshwater and 32% of those captured at sea carried lice at intensities above the level that has been shown to induce mortality in laboratory experiments. Almost half of all fish from the farm locality had lice intensities that would probably cause osmoregulatory imbalance. At the location without farms, the infection intensities were low, and few fish carried more than ten lice. The latter are probably within the normal range of natural infection and such intensities are not expected to affect the stock negatively. Negative correlations were found between the number of preadult and adult salmon lice and host plasma chloride levels on prematurely returned sea trout (Bjørn et al. 2001a) in freshwater. In a later study by Wells et al. (2007) on wild sea trout from northern Norway, it was shown that the physiological imbalance caused by lice in seawater returned to control levels in freshwater while significant lice effects persisted for fish maintained in seawater.

Arctic Charr and Atlantic Salmon A few studies on the impact of salmon lice on Arctic charr have been performed. Arctic charr from laboratory experiments (Grimnes et al. 1996) were found to suffer from stress and mechanical skin damage, which resulted in severe osmoregulatory problems, reduced growth, and mortality. As with Atlantic salmon and sea trout, the Arctic charr had increased cortisol levels 7 days postinfection. Mechanical damages and increased cortisol levels were found first after the preadult stages occurred. A field study by Bjørn et al. (2001a) revealed a positive correlation between the relative density of lice (lice/fish weight) and plasma chloride, glucose, and cortisol showing that the lice affected stress responses and physiological disturbances to the charr. Salmon lice have also been shown to impair the reproductive performance of Arctic charr. Reduced plasma levels of testosterone and estradiol-17β were measured in female Arctic charr with high salmon lice infection compared to medium and low infection leading to reduced number of spawning females, delayed ovulation, and reduced total fecundity among spawners (Tveiten et al. 2010). Such effects are likely to be caused by stress (Pankhurst and Van Der Kraak 1997).

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Effects of Salmon Lice on Wild Sea Trout, Arctic Charr, and Atlantic Salmon in Coastal Zones and Fjords of Norway Elliott (1994) states that “the role of predators, including man, on wild fish populations has been given much attention in models, but surprisingly little is known about the quantitative effects of parasites and diseases.” When the net harm that a parasite causes the host is severe, parasitic diseases can be major contributors to host mortality rates (Threlfall 1968; Croften 1971; Johnsen and Jensen 1992; Heggberget et al. 1993; Jaenike et al. 1995), and even act to regulate host population size (Anderson and May 1978, 1979, 1981; Dobson and Hudson 1992; Tompkins and Begon 1999; Tompkins et al. 2000). However, detecting the effects of parasitism in wild host populations is inherently very difficult (Anderson and Gordon 1982; Pacala and Dobson 1988), and registration and quantification of effects in wild fish have been hampered by difficulties of capturing infected fish (Lester 1984). Until recently, monitoring the effects of salmon lice on wild populations of sea trout, Arctic charr, and Atlantic salmon has been limited by the difficulties in capturing wild postsmolts at sea. The marine migratory behavior of Atlantic salmon, Arctic charr, and sea trout diverge in several important aspects, although knowledge of the detail is still limited. Most of the information gathered to date suggests that postsmolts of Atlantic salmon move relatively quickly through estuaries and fjords close to the surface (e.g., Moore et al. 2000; Thorstad et al. 2004; Finstad et al. 2005; Davidsen et al. 2008; Plantalech Manel-la et al. 2009), although this also may vary between populations and years (Rikardsen et al. 2004). In contrast, sea trout and Arctic charr usually feed in littoral areas close to their native river throughout summer and autumn (Berg and Jonsson 1990; Lyse et al. 1998; Rikardsen et al. 2000). Sea trout and Arctic charr therefore seem to belong to a “near shore, surface-orientated guild of fishes,” as previously suggested by Grønvik and Klemetsen (1987), although these fish may also occasionally feed pelagically in open waters within fjords and coastal areas (Rikardsen and Amundsen 2005). Investigations on the effects of sea lice on wild salmonid stocks in Norway have been limited to studies of prematurely returned postsmolts of sea trout in estuaries and freshwater (e.g., Birkeland 1996). This may give biased abundance estimates of lice in the total seagoing population, as it has been presumed that the most heavily infected fish return to freshwater (Birkeland and Jakobsen 1997; Bjørn et al. 2001b). The significance of the observed epizootics on wild salmonids have thus not been established, and clearly emphasizes the need for better sampling methods and more accurate estimates of the infection level on the hosts at sea as well as on those which prematurely return to freshwater. Methodology for capturing sea trout and Arctic charr (Mo and Heuch 1998; Schram et al. 1998; Bjørn et al. 2001a, 2001b) as well as Atlantic salmon postsmolts (Holst and McDonald 2000) in the sea was, however, successfully developed during the late-1990s (Anon. 2010). In addition, two characteristics of salmon lice biology facilitate estimates of their effects: (1) recent infections can be recognized (as individuals at the chalimus stage), and (2) the chalimus stage is unlikely to be very pathogenic to the host (e.g., Bjørn and Finstad 1997; Wells et al. 2007). Thus, this enabled scientists for the first time to address mortality due to sea lice infection in wild populations of salmonids, as the infection could be recorded over time and compared with the infection dose-response from the laboratory studies above.

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Sea Trout and Arctic Charr A large-scale sampling program and research program for wild sea trout and Arctic charr on their feeding grounds in fjords and coastal areas and for those fish that prematurely return to estuaries and freshwater was initiated in Norway in the mid-1990s. In 1997, a working group including representatives from the salmon farming industry, fish health personnel, and the Animal Health Authority presented a “National Action Plan against Salmon Lice on Salmonids.” The long-term goal of the plan was to reduce harmful effects of lice on farmed and wild fish to a minimum. It was also agreed that the infection levels recorded on wild salmonids were the most important indicators of success of the plan (Heuch et al. 2005). Gathering reliable annual salmon lice infection data from sea trout both from intensively farmed and control areas all along the Norwegian coastline, and connecting this with the measures taken in the fish farms, was a key requisite in the plan. Therefore, the Norwegian Directorate for Nature Management increased the wild sea trout sampling programme in the early 1990s with additional funding from the Norwegian Research Council and the salmon farming industry. Central to these initiatives was a thorough monitoring of sea trout. A number of locations were selected all along the coastline and a time series sampling protocol using modified gill nets and electrofishing was developed (see Anon. 2010 for details). Usually, a series of 12 gill nets were used at each locality, and a targeted number of 15–30 sea trout and Arctic charr (e.g., Bjørn and Finstad 2002) were fished at each locality and time. If possible, electrofishing was simultaneously conducted in the lower part of the river (Bjørn et al. 2001b). Salmon lice infections on immature sea trout and Arctic charr are acknowledged to indicate local sources of infection because these hosts usually use nearshore coastal waters for feeding journeys and seldom migrate far from their native rivers (Berg and Jonsson 1990; Lyse et al. 1998; Rikardsen et al. 2000). A protocol involving sampling both in intensively farmed as well as in control areas was therefore assumed capable of answering questions about the relationship between fish farming and epidemics on wild salmonids. Sampling sea trout and Arctic charr every second or third week from just after they had entered seawater in the spring until they again descended rivers in autumn, enabled scientists to follow the development, and estimate the possible consequences, of the infection. Furthermore, annual sampling at the same localities was designed to measure the success of the measurement taken by the plan and the fish farming industry. We now have almost 10 years of data from some of the localities, and much of the Norwegian coastline is covered (Figure 9.4). However, the results from the long-term field monitoring on wild sea trout and Arctic charr are somewhat depressing. The results from the Vik watershed in Northern Norway emphasize the possible effects of salmon lice as a potential cause of direct parasite induced mortality (Bjørn et al. 2008). Furthermore, the data set also shows how copepodids from farmed salmon infect local wild sea trout and Arctic charr. The study from 1997 shows that the salmon lice infection on wild sea trout and Arctic charr differed significantly between the area close to, and the area distant from salmon farming activity (Bjørn et al. 2001a). At the exposed locality (Vik), the mean infection intensity in wild hosts both at feeding grounds at sea as well as those prematurely returned to freshwater was high compared to historical levels (Boxshall 1974) and areas without fish farming activity (Tingley et al. 1997; Schram et al. 1998). Premature return to freshwater resulted in delousing and reestablishment of homeostasis among the

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Figure 9.4. Test fishing for sea trout in Vik in Vester˚alen (northern Norway). (Photo: Rune Nilsen, IMR.)

heaviest infected fish. In addition, the observation of significant numbers of fish with infections known to be eventually lethal in experiments (e.g., Bjørn and Finstad 1997), and the apparent lack of lice development with time, pointed toward an excessive mortality of the heaviest infected fish. Infection intensities at this level (100–200 lice larvae per fish in June–July) cause both stress and physiological imbalance. It was estimated that 30–50% of the smallest sea trout in the area would die or be greatly disadvantaged by their infections (Bjørn et al. 2001a). Furthermore, new doseresponse results (e.g., Wagner et al. 2003; Wells et al. 2007) indicate that the effect of the 1997 epidemics among wild sea trout in the Vik system may even be worse than estimated, and, if maintained, may render the stocks at the risk of eradication. The long-time monitoring series in Vik has been maintained annually since the extremely high infection level (medians between 30 and 80 lice for the combined material from 1997) was observed both on sea trout at sea and in freshwater in 1997 (Figure 9.5). In the following years (1998, 1999, and 2000), infection levels were somewhat reduced, however, not significantly. Median infection intensities in sea trout at sea varied between 25 and 50 lice, and were dominated by larval lice (Grimnes et al. 1999, 2000; Bjørn et al. 2001b). Sea trout with even higher intensities of infection were annually captured after having returned prematurely to freshwater. In 2001 a somewhat different situation appeared; no fish were observed returning prematurely to freshwater and most of those at sea carried less than ten lice, which gradually developed into preadult and adult lice during summer and autumn (Bjørn et al. 2002). Thereafter (2002–2008), lice infection again increased and median infection intensities seems to have stabilized around 20 to 30 lice/fish in seawater (Figure 9.5). The longtime monitoring series in Vik therefore indicate that although infection intensities have been reduced from the extremely high levels in 1997, chronically high levels have still been found annually (except in 2001) during the last 10 years of investigations.

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Figure 9.5. Box-and-whiskers plot showing median abundance of salmon lice on sea trout in Vik in Vester˚alen (northern Norway). Dotted bars represent fish taken in seawater and open bars represent fish taken in freshwater (premature returns). Horizontal lines indicate medians. The lower and upper hinges give the 25th and 75th percentile. Outliers are presented, and the whiskers give the largest and smallest observed values that are not outliers. (Data from Bjørn et al. 2009.)

With the exception of 2001, salmon lice epidemics are therefore still expected to negatively influence the wild sea trout population in Vik, and imply that the main aim of the National Action Plan against Salmon Lice on Salmonids has not been achieved (Heuch et al. 2005; Wells et. al. 2007). As the monitoring series of Vik was developed, other monitoring series were developed for the intensively farmed Altafjord system in the very northernmost part of Norway, at Hitra in middle Norway, and at Romsdal and Hardangerfjord in the more western part of Norway. Although infection intensities varied between localities, strikingly few differences have been seen over the years. For example, in Hitra (Figure 9.6), which was the heart of the salmon farming industry in Norway in the 1970s and still is one of the most intensively farmed areas in Norway, no significant reduction in infection intensities has been seen between 1998 and 2009 (Bjørn et al. 2010). However, there is a tendency for reduced median infection intensity in the sea trout that prematurely returned to freshwater, compared to the very high infection levels found in the first years of investigations. The same general picture is also found in the Altafjord and the Romsdalsfjord systems, although levels in Alta also are

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Figure 9.6. Box-and-whiskers plot showing median abundance of salmon lice on sea trout in Hitra (Sør Trøndelag). Dotted bars represent fish taken in seawater and open bars represent fish taken in freshwater (premature returns). Horizontal lines indicate medians. The lower and upper hinges give the 25th and 75th percentile. Outliers are presented, and the whiskers give the largest and smallest observed values that are not outliers. (Data from Bjørn et al. 2010.)

lower. There is a general tendency toward lower infection intensities in the systems in northern Norway, probably because of a combination of lower fish farming activity and lower seawater temperatures, especially in winter (Bjørn et al. 2008), compared to the fjords of western Norway. The intensively farmed fjords of western Norway have been given special focus in recent years, including IPM to facilitate a profitable salmon farming industry and sustainable wild sea trout stocks (the Hardangerfjord project 2004–2009). The Hardangerfjord system is 150 km long and has the highest density of fish farms in Norway, producing annually around 70,000 tons of salmon. This system is an ideal study area because it is mainly affected by inner fjord dynamics, has important wild salmon, and sea trout stocks affected by salmon lice since the early 1990s (Finstad et al. 2007b, 2007c), and nearly all salmon farms are cooperating through a fish health network. Infection level in wild sea trout is the most important success criterion. A long-term data series from Hardangerfjord started in 2004, and due to severely depressed sea trout stocks, a reduced sample size of fish was collected by a number of methods (gill-nets, otter board, trawling (Ocean Fish Lift)), both from inner, middle, and outer parts of the fjord (see Anon. 2010 for a description of sampling methods). Although

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strategies for lice treatment in fish farms have greatly improved through synchronized delousing in almost all farms in the fjord, infection levels continue to be high on wild salmonids (Finstad et al. 2007b, 2007c). In 2004–2006, high prevalence and median intensities between 4 and 16 lice were observed on sea trout. No significant improvements were observed before (2004) and after (2005–2007), the period of synchronized delousing. In 2008 and 2009, improved methods for capturing sea trout at sea (outlined in Bjørn et al. 2008, 2009, 2010) were implemented and high infection levels (mean intensity from 50 to 80 lice per sea trout) were observed in the outer and also middle parts of the fjord. These levels are also in agreement with the concurrently high infection levels seen in trawl-captured sea trout in outer parts of the fjord in 2004–2009 (Finstad et al. 2007b; Bjørn et al. 2008, 2009, 2010). Overall, this indicates that infection levels in the outer part of the Hardangerfjord system are still high. Moreover, a synchronized delousing of almost all salmon farms in the area has not been able to reduce infection levels on local sea trout to a sustainable level. Management in Norway is now discussing measures for the fjord, including restricting the salmonid production at lower levels until the industry operates within a “carrying capacity” for lice that is sustainable within the fjord. Overall, the long-term sea trout and Arctic charr monitoring program in Norway implies that infection levels still are too high in areas of intensively fish farming activities all along the Norwegian coastline and fjords. For example, in the Hardangerfjord, more than 70,000 tons of Atlantic salmon are produced annually. Most likely, the mean intensity of salmon lice infection should be lower than 10–13 lice per sea trout, Arctic charr, and Atlantic salmon postsmolt (Finstad et al. 2000; Wells et al. 2007), or about 0.1 lice per gram fish weight (Wagner et al. 2003, 2004) for no negative effect on individual fish to be detected (Heuch et al. 2005). Currently, the total biomass of farmed salmon in intensively farmed areas along the Norwegian coast and fjords (e.g., the Hardangerfjord) may be so high that even low lice levels on each farmed fish may not be sufficient to reduce the overall infection pressure, especially on sea trout, to a sustainable level. Therefore, it seems necessary both to reduce the lice level on each farmed fish as well as optimize delousing strategies if the aim is to achieve less than ten lice per wild sea trout, and thus no negative effects.

Atlantic Salmon Atlantic salmon postsmolts have been monitored using a specially designed trawl, the Ocean Fish Lift, which catches live smolts with minimal scale loss, thus preserving their natural ectoparasitic infections (Holst and McDonald 2000). This gear gives reliable estimates of lice infection levels, and also allows estimates of mortality due to lice using the methods detailed previously. Large numbers of uninfected and healthy smolts have been caught in several areas by using the Ocean Fish Lift (Holst et al. 2003; Finstad et al. 2000; Hvidsten et al. 2007; Bjørn et al. 2008, 2009, 2010). Results show large variations in salmon louse prevalence between years and between fjords. The mean intensity ranges from zero to more than 100 lice per fish, giving mortality estimates from zero to over 90% of fish (Holst et al. 2003; Heuch et al. 2005; Bjørn et al. 2008, 2009, 2010). Some examples of these surveys are given as follows. In the Trondheimsfjord, we have monitored lice load on postsmolts of Atlantic salmon

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since 1992 (Finstad et al. 1994a, 1994b, 2000; Hvidsten et al. 2007). Trondheimsfjord is completely without fish farms and is assumed to give reliable data about infection pressure in such areas. However, the near coastline outside the Trondheimsfjord system (e.g., Hitra) has intensive farming activity. Advection of coastal waters in some years is assumed to be able to increase infection pressure in the outer parts of the fjord system. By gradient trawling along smolt migratory routes, infection intensities and consequences of salmon lice on migrating postsmolts can be estimated. The results from the long-term field study on wild Atlantic salmon postsmolts showed that smolts leaving coastal waters became infected with salmon lice (Finstad et al. 2000, Hvidsten et al. 2007; Bjørn et al. 2008, 2009, 2010). The migrating smolts were only infected with the chalimus stages, indicating that the fish had recently left the river. In some years (1992, 1998, and 2003) there was a moderate infection pressure from pelagic copepodids in the fjord (Finstad et al. 2000; Hvidsten et al. 2007). For example, in 1992, a postsmolt was found carrying 285 chalimus (Finstad et al. 1994a, 1994b), and 8% had more than 10 sea lice (Finstad et al. 2000). In 1998, 53% of the fish were infected and 11% had more than ten lice (Finstad et al. 2000; Hvidsten et al. 2007). In the other years, infections were low (Hvidsten et al. 2007; Bjørn et al. 2007a, 2008, 2009, 2010), and not assumed to influence migrating smolts negatively. These observations contrast those made in western Norway (Holst et al. 2003). In 1998, the Institute of Marine Research in cooperation with the University of Bergen initiated a fjord survey program in the intensively salmon farmed fjords of western Norway (Holst et al. 2005). Special focus was given to the Sognefjord system. Sognefjord is a long and narrow fjord just north of Bergen with intensive farming activity in the middle and outer parts. The fjord was trawled annually between 1998 and 2004. Mean infection intensities were observed to vary from one to 104 between these years. Based on a conservative mortality limit at 15 lice per fish, parasiteinduced mortality estimates varying from 0 to 95% have been presented (Holst et al. 2003, 2005), and imply that salmon lice epidemics may be a major factor regulating stock size in Sognefjord. In later years (2002, 2003, and 2004) the situation improved and mean infection intensities were reduced to below 2.3, probably due to improved conditions in the farms during winter and spring (Holst et al. 2005). A larger scale fjord trawl program was initiated in 2000–2004 that covered larger parts of the Norwegian coastline (Rikardsen et al. 2004). In addition to Sognefjord in western Norway and Trondheimsfjord in middle Norway, special focus were given to the two fjords in northern Norway, the intensively farmed Altafjord system, and the protected Malangsfjord system without farms (Holst et al. 2005; Bjørn et al. 2007b). The Altafjord system was trawled annually between 2000 and 2004 and Malangen was trawled in 2000, 2001, and 2002 (Rikardsen et al. 2004; Holst et al. 2005; Bjørn et al. 2007b). Results from Atlantic salmon postsmolts in Altafjord showed no salmon lice in 2000, 2001, and 2003 and a mean infection intensity of 0.1 in 2002 and 2004. No lice were seen in any year in Malangen (Holst et al. 2005; Bjørn et al. 2007b). However, sea trout and Arctic charr were moderately infected later in summer in both systems. This indicates that a “mismatch” seemingly exists between the time of salmon migration and the rise in infection pressure even in the intensively farmed Altafjord in northern Norway (Bjørn et al. 2007b). However, trawling for Atlantic salmon postsmolts is expensive. Since 2004 only two fjords have been annually monitored, (1) the Hardangerfjord in western Norway and

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Figure 9.7. Map of the trawling zones (A through E) for the Ocean Fish Lift in the Hardangerfjord in May 2006. (Data from Bjørn et al. 2007a.)

(2) the Trondheimsfjord in middle Norway (Bjørn et al. 2010). For the Hardangerfjord, the smolts have been captured by Ocean Fish Lift along their migratory routes in the outer part of the fjord (Figure 9.7). Results from the period 2004–2006 in the Hardangerfjord indicate low infection levels: prevalence varied between 15 to 48 and mean intensity between 0.6 and 1.9. No significant difference before (2004) and after (2005 and 2006) the synchronized delousing was found. However, infection levels have increased during 2007 and 2008. In 2007, 58% of the few smolts captured were infected and mean intensity was 8.9 lice (Bjørn et al. 2008). In 2008, both prevalence and mean intensity were higher (Bjørn et al. 2009). These results are also in accordance with the results from sea trout for 2007 and 2008, and imply that despite the measures taken, the lice situation in the Hardangerfjord system has not improved. For 2009, trawl data showed that the infection pressure on Atlantic salmon postsmolts occurred in the last part of our trawl survey (Bjørn et al. 2010). Overall, our long-term monitoring series on Atlantic salmon postsmolts has shown that lice infections were severe in some fjords of western Norway in the late 1990s and early 2000. The situation then improved (Sognefjord and Hardangerfjord 2002–2006) in western Norway, but seemingly has turned worse again in the last 2 years in Hardangerfjord. This implies that although good measures have been taken in the farming industry, farm production in some of the western fjords of Norway is simply too high to secure sustainable salmon production. In northern Norway (e.g., the Altafjord system), salmon lice seem to not be a threat to migrating salmon smolts, and suggests that in the conditions found in some fjords extensive salmon farming can coexist with wild salmon stocks (Bjørn et al. 2007b). However,

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a future scenario as increased sea water temperatures (climate change) may also increase the salmon lice pressure in these regions.

Population Levels—Can Salmon Lice Regulate Populations of Wild Salmonids in Norway? Only lice infections above a threshold intensity, when affecting a significant portion of the population (prevalence) will have population level impacts. Atlantic salmon and sea trout differ in their behavior during the sea phase. Understanding of the early marine phase of the Atlantic salmon and the environmental factors that may influence their behavior and distribution at sea is limited (Moore et al. 2000), and even less is known about the sea trout. This lack of information is particularly critical because the heaviest mortality of salmonids in the sea apparently takes place during the first months after the smolts leave freshwater (Hansen et al. 2003; Rikardsen et al. 2004). Smolts have been reported to move deeper in the water column during the day than during the night (Thorpe and Morgan 1978; Davidsen et al. 2008) and this behavior may also influence the exposure to salmon lice. Atlantic salmon migrate to the open ocean (Hansen et al. 2003; Finstad et al. 2005; Thorstad et al. 2007) and may be infected by salmon lice for a short period on their way out through the fjord system (Finstad et al. 2000; Hvidsten et al. 2007), but this period is dependent on the length of the fjord system. Sea trout remain in the inner fjord systems (Jonsson 1985; Knutsen et al. 2001; Finstad et al. 2005; Thorstad et al. 2007) and may be susceptible to reinfections of salmon lice during this time. Typically found in coastal areas is an overlying brackish water (less than 16 ppt) layer from the spring freshet. Several studies have reported that salmon lice tend to avoid water with salinities less than approximately 20 ppt (Heuch 1995; Bricknell et al. 2006). As a result, the brackish water layer may be viewed as an area of refuge from lice infestation for migrating Atlantic salmon postsmolts throughout the fjord system. However, as mentioned above, sea trout remain in the fjord system throughout the whole period and may be reinfested by salmon lice. The following discussion regarding population effects on fish are based mainly on Norwegian results but in Ireland and Scotland significantly higher infestations of sea lice occurred on wild fish in bays that contained lice infested farmed salmon, which may be regarded as a significant influence on the population dynamics in these bays in both countries (Tully et al. 1999; Gargan et al. 2003; Butler and Watt 2003). To investigate the effect of salmon lice on postsmolt survival, individually tagged salmon and sea trout smolts have been protected against lice by an in-feed medication R ) or bath treatment (Substance EX, Pharmaq), and released in the vicinity of (Slice R and Substance EX protect the fish for several weeks, their native river. Both Slice and assuming they do not interfere with the fish in other ways, the experiments provide estimates of the effect of lice at the population level. Tagging experiments were performed on Substance EX-treated and nontreated sea trout in the River Bondhus (Hordaland County) in 1996 (Finstad and Birkeland 1997). Fish were tagged with Carlin tags with two different colors to observe them visually through the water. One month after release, large shoals of sea trout (> 250 fish) were observed in the estuary and about one-tenth of these were treated fish. After approximately 3 months, 22 untreated and 13 treated trout were recaptured. Untreated fish were collected in

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the lower part of the river and were heavily infested with salmon lice while the treated fish were captured in the estuary and had very few lice attached. These results have shown that infections of salmon lice on sea trout postsmolts may change the behavior of the fish (premature returns), which is observed in several rivers in Norway. For the Substance EX treatment of sea trout smolts from the Hardangerfjord (Finstad et al. 2007b) the return rate, which is reflecting sea survival, was very low for both treated and untreated groups. However, the recapture rate of the EX-treated smolt group from the 2004 smolt cohort was significantly higher than that of the untreated control group after the two first sea migrations. Mean weight and condition factor were also higher in the treated group than in control group, although not statistically significant. As the chemical treatment by Substance EX is not expected to give a full protection against salmon lice, and survival of the treated group was twice that of the untreated control group, the observed difference in survival between the two groups represents an underestimate of the mortality caused by salmon lice. Data from Agdenes (Sør-Trøndelag County, middle Norway) and Daleelva (Hordaland County, southwest Norway) on Atlantic salmon show that in years with high salmon louse infection pressure, the returns of Substance EX-treated fish have been higher than returns of unprotected control groups (Finstad and Jonsson 2001; Hvidsten et al. 2007). In some years, we also see that Substance EX-treated fish had a better growth than unprotected fish (Hazon et al. 2006). However, these investigations have long been hampered by low tag recapture rates, primarily because they were undertaken in commercially exploited systems. In the present project we were able, for the first time, to include experiments on the only two Norwegian watercourses with permanent fish traps (Imsa and Talvik) and which offered complete control and census of the populations, and an evaluation of the effectiveness of a laboratory-based treatment protocol under field conditions. For the Imsa and Talvik releases (Figure 9.8), the results of the present experiment show that although the Substance EX-treated Atlantic salmon smolts in most instances were significantly longer and heavier on return than untreated smolts, there was no significant increase in condition. In addition, for the Imsa releases, there were sufficient returns to the fish trap to allow sex-specific differences in subgroups of control and treated fish to be examined. Returning summer 1 SW males tend to be longer and heavier than females, but no difference in WR is expected between the sexes and within years. Information on sex could only be collected from fish that returned to the trap, because this information was not collected from fish caught by rod and line or in the commercial fishery. At Imsa, treated male fish were significantly longer and heavier than their respective controls, but showed no significant difference in WR . Treated female fish were not significantly longer or heavier than control female fish; however, treated female fish actually returned at a significantly lower condition. Increases in size and condition may have an influence on the spawning success of the fish and therefore affect future generations. However, further recaptures and results are needed to draw the final conclusions here. These studies are also supported by Skilbrei and Wennevik (2006) showing that R recapture rates were in several releasing experiments with smolts treated with Slice highest in the treated groups. This higher recapture in treated fish suggests from these releases that salmon lice load became high enough to result in greater mortality among the untreated smolts. Studies in Ireland (Hazon et al. 2006) revealed a significant R treated groups compared to nontreated groups, difference in the return rate of Slice and therefore indicating a protection from salmon lice infestation to these fish in

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(A)

(B)

Figure 9.8. (A) River Imsa fish trap. (B) River Halselva (Talvik) fish trap. (Photo: Bengt Finstad, NINA.)

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aquaculture bays. Treatment of Atlantic salmon smolts with these drugs may be an effective enhancement procedure protecting salmon smolts against salmon lice infections during their migration through the fjord system in areas where populations are at very low abundances.

Summary Since the early 1990s, significant information on the physiological effect of salmon lice on salmonids has been obtained. Information relating to threshold levels for lice induced mortality effects and levels leading to suboptimal conditions for Atlantic salmon, sea trout, and Arctic charr have been used for estimating the threshold levels in wild captured salmonids in our field-monitoring programs. The present monitoring on wild salmonids shows that the salmon lice infection pressure still is relatively high all along the Norwegian coast. Establishing the Norwegian National Salmon Fjords (protected fjord areas without salmon farming) has been a management practice to protect wild salmonids from salmon lice. Some of our national salmon fjords, especially the larger ones, seem to have a positive effect, but a longer time series is needed before conclusions can be drawn. However, migrating salmonids meet a rather high infection pressure in outer fjords and coastal areas. The total biomass of farmed salmon may therefore be so high that even low lice levels on each farmed fish may not be sufficient to reduce the overall infection pressure to a manageable level. In addition to the national salmon fjords, it seems to be necessary to both reduce the lice level on each farmed fish as well as optimize delousing strategies if the aim of less than ten lice per wild fish, and thus no negative effects on wild salmonid populations, is to be achieved.

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lice between farmed- and wild fish—the Hardangerfjord system as a modelling area). In: Kyst og havbruk. Fisken og havet (eds. E. Dahl, P.K. Hansen, T. Haug, and Ø. Karlsen), pp. 69–73. særn. 2–2007, Institute for Marine Research, Bergen. Finstad, B., Økland, F., Thorstad, E.B., Bjørn, P.A., and McKinley, R.S. 2005. Migration of hatchery-reared Atlantic salmon and wild anadromous brown trout post-smolts in a Norwegian fjord system. Journal of Fish Biology 66: 86–96. Finstad, B., Kroglund, F., Strand, R., Stefansson, S.O., Bjørn, P.A., Rosseland, B.O., Nilsen, T.O., and Salbu, B. 2007a. Salmon lice or suboptimal water quality—reasons for reduced postsmolt survival? Aquaculture 273: 374–383. Finstad, B., Økland, F., Uglem, I., Boxaspen, K.K., Skaala, Ø., Skilbrei, O., Asplin, L., Bjørn, P.A., Butterworth, K., McKinley, R.S., Stigum Olsen, R., Malkenes, R., Ritchie, G., Heuch, P.A., and Kvenseth, P.G. 2007c. The Hardangerfjord salmon lice project—2004–2007. Final Report to the Norwegian Research Council, 33 p. Finstad, B., Bjørn, P.A., Todd, C.D., Whoriskey, F., Gargan, P.G., Forde, G., and Revie, C. 2011. The effect of sea lice on Atlantic salmon and other salmonid species (Chapter 10). In: Atlantic Salmon Ecology (eds Ø. Aas, S. Einum, A. Klemetsen, and J. Skurdal), pp. 253–276. Blackwell Publishing Ltd., Oxford. Gargan, P.G., Tully, O., and Poole, W.R. 2003. The relationship between sea lice infestation, sea lice production and sea trout survival in Ireland, 1992–2001. In: Salmon at the Edge (ed. D. Mills), pp. 119–135. Blackwell Science, Oxford. Glover, K.A., Hamre, L.A., Skaala, O., and Nilsen, F. 2004. A comparison of sea louse (Lepeophtheirus salmonis) infection levels in farmed and wild Atlantic salmon (Salmo salar L.) stocks. Aquaculture 232: 41–52. Glover, K.A., Nilsen, F., Skaala, Ø., Taggart, J.B., and Teale, A.J. 2001. Differences in susceptibility to sea lice infection between sea run and freshwater resident population of brown trout. Journal of Fish Biology 59: 1512–1519. Glover, K.A., Skaala, Ø., Nilsen, F., Olsen, R., Taggart, J.B., and Teale, A.J. 2003. Differing susceptibility of anadromous brown trout Salmo trutta L. populations to salmon lice infections. ICES Journal of Marine Science 60: 1139–1148. Grayson, T.H., Jenkins, P.G., Wrathmell, A.B., and Harris, J.E. 1991. Serum responses to the salmon louse, Lepeophtheirus salmonis (Krøyer, 1838), in naturally infected salmonids and immunised rainbow trout, Oncorhynchus mykiss (Walbaum), and rabbits. Fish and Shellfish Immunology 1: 141–155. Grimnes, A. and Jakobsen, P. 1996. The physiological effects of salmon lice infection on postsmolt of Atlantic salmon (Salmo salar). Journal of Fish Biology 48: 1179–1194. Grimnes, A., Finstad, B., and Bjørn, P.A. 1996. Økologiske og fysiologiske konsekvenser av lus p˚a laksefisk i fjordsystem (Ecological and physiological consequences of salmon lice on salmonids in Norwegian fjord systems). NINA Oppdragsmelding 381: 37 p., Trondheim. Grimnes, A., Finstad, B., and Bjørn, P.A. 1999. Registreringer av lakselus p˚a laks, sjøørret og sjørøye i 1998 (Registrations of salmon lice on Atlantic salmon, sea trout and Arctic charr in 1999). NINA Oppdragsmelding 579: 33 p., Trondheim. Grimnes, A., Finstad, B., and Bjørn, P.A. 2000. Registreringer av lakselus p˚a laks, sjøørret og sjørøye i 1999 (Registrations of salmon lice on Atlantic salmon, sea trout and Arctic charr in 1999). NINA Oppdragsmelding 634: 34 p., Trondheim. Grønvik, S. and Klemetsen, A. 1987. Marine food and diet overlap of co-occurring Arctic charr Salvelinus alpinus (L.), brown trout Salmo trutta L. and Atlantic salmon S. salar L. off Senja, N. Norway. Polar Biology 7: 73–177. Hansen, L.P., Holm, M., Holst, J.V., and Jakobsen, J.A. 2003. The ecology of post-smolts of Atlantic salmon. In: Salmon at the Edge (ed D. Mills), pp. 25–39. Blackwell Science, Oxford. Hazon, N., Todd, C., Whelan, B., Gargan, P., Finstad, B., Bjørn. P.A., Wendelaar Bonga, S.E., and Kristoffersen, R. 2006. Sustainable management of interactions between aquaculture

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Index Abundances C. clemensi levels of, 268, 319 collapse in pink salmon population, 325 data on L. salmonis, 108 hydrographic effects on, 271 of L. salmonis in southwestern New Brunswick, 86–99, 88f–93f, 94f, 96f–99f, 100t, 101–2, 101f–102f of L. salmonis on pink salmon, 315 of L. salmonis on wild salmon, 108 models of L. salmonis, 31–49 of planktonic larval stages of L. salmonis, 31–49 of planktonic salmon lice, 38–47, 40f–43f, 44t, 45f, 47f risk factors with abundance of L. salmonis, 220–21, 220t of sea louse on wild salmon, 108 variation between farming regions of L. salmonis, 269–70 variation between seasons of L. salmonis’, 268–69 Accuracy, of data, 266 AMGs. See Area Management Groups Animals. See also Fish; National Animal Health Authority companion, 159 food, 184 welfare, 149, 159, 183 Application, of medicines, 189 Approaches IPM and husbandry, 163–64 L. salmonis management, 162–72, 166f, 167f, 171f of management in IPM, 164 synchronized, 170 Aquaculture Bay Management Areas (ABMAs), 105, 105f Arctic charr capturing, 287 in Norwegian fjords, 288–92 physiology/pathology of L. salmonis infections in, 282–84, 286

Area Management Agreements (AMAs), 58, 222 Area Management Groups (AMGs), 58 case study of Loch Torridon, 59–67, 62f, 66f Atlantic ocean L. salmonis in, xii, 8–9 salmon farms in, xii Atlantic salmon C. clemensi on, 267–68 as farmed in Bay of Fundy, 83, 84f, 85–86 as farmed in British Columbia, 235 as farmed in Ireland, 177, 179 inflammation in, 180–81 L. salmonis in Norway as always carried by, 158 L. salmonis on, 1, 268–70 migration routes of adult, 107–8 monitoring, 292–94 physiology/pathology of L. salmonis infections in, 282–85, 283f protecting, 159 temperature for farmed, 31–32 Auditing by government of L. salmonis industry monitoring, 266–67 random, 166 Azamethiphos, 86 Bath, treatments for L. salmonis, 57, 86, 168, 189–90 Bay of Fundy. See also New Brunswick Atlantic salmon farmed in, 83, 84f, 85–86 salmon in rivers near, 106 Bays. See also Aquaculture Bay Management Areas; Bay of Fundy; Passamaquoddy Bay management, 186–87, 187f modus operandi for management of, 199–200, 200f strategy for management of, 196–97

Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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Behavior copepodids patterns of, 138, 140 of L. salmonis, 5–6, 138, 140, 211–12 of L. salmonis larvae, 5–6, 211–12 of planktonic louse, 135–38, 136f Benefits, salmon farms’ economic, xi, 179–80 Bias, 221 Biology of C. elongatus, 211 pink salmon’s population, 309–13, 311f–312f, 312t sea lice basic, 2–6, 211 Blooms, plankton, 194 Boats. See Well boats Breeding, selective, 14 British Columbia, Canada. See also Broughton Archipelago, British Columbia C. clemensi on Atlantic salmon in, 267–68 control measures for curbing L. salmonis in, xii debates on L. salmonis in, 274 epidemiology of L. salmonis on farmed salmon in, 267 government auditing of industry L. salmonis monitoring in, 266–67 health effects of L. salmonis in, 238 immediate concerns for salmon farming industry in, 272–73 L. salmonis management on salmon farms in, 235–75 L. salmonis on Atlantic salmon in, 268–70 “lice free” periods in, 273 medicated feed in, 271 routine monitoring for L. salmonis in, 239 salmon producers in, 235–36 sea lice species infesting salmon in, 237–38 size of salmon farming industry in, 235 treatments for L. salmonis in, 271–74, 271f Vancouver Island, 236 Broughton Archipelago, British Columbia, 308f C. clemensi in, 268 location of, 117, 118f map of, 124f modeling sea lice production and concentrations in, 117–47 particle tracking in, 128–30, 129f physical oceanography of, 117, 119 pink salmon in, 310

salinity of, 127 salmon farming in, 117, 118f, 238–39 temperature of, 127, 128f Cages. See also Sentinel cages of floating nets, 83 Caligidae. See Sea lice Caligus clemensi (C. clemensi), 237–38 abundance levels of, 268, 319 on Atlantic salmon in British Columbia, 267–68 host specificity of, 267 on juvenile Pacific salmon, 323 Caligus elongatus (C. elongatus), 61 biology of, 211 fish species infected with, 86 immune response of, 13 infestations of, 180, 207, 213 occurrence of, 15, 89, 93 treatment of, 168 Canada. See also Bay of Fundy; British Columbia, Canada; Broughton Archipelago, British Columbia; New Brunswick L. salmonis as observed in Atlantic, 83–84 parasites of, 16 Capture of fish, 143, 287 recapture and, 295–96 tow, 143 Case studies of Loch Torridon AMGs, 59–67, 62f, 66f on medicinal treatment of L. salmonis, 170–73 Catches, restrictions on size of, xi Centrolabrus melops, 190 Centrolabrus rupestris, 190 Challenges, IPM, 211 Change climate, 52 in salinity, 270 temperature, 270 Channels, spawning, xii Chemicals, for treating L. salmonis, 57, 86, 103, 223–24 Chile, L. salmonis in, 224–25 Circulation estuarine-type, 321 in sea lochs, 52–53 water, 95, 97, 99–102, 321 wind driven, 120–21, 271 Cleanliness, 212

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Climate change, 52 fluctuations in, xii Coast advection of Norwegian waters on, 293 economies of Irish communities on, 179–80 exposure of L. salmonis, 220 L. salmonis in, 281–325 models and, 37, 119, 145 Norwegian, 31–32, 32f, 153, 281–98 salmon in rivers on, 34 sampling larvae lice on, 61 of Scotland, 50–53, 75 sea trout on, 281 Community cohesion, 180 First Nation, 136 fish farming, 180 growth, 179 Concerns, salmon farming immediate, 272–73 Conditions factor and L. salmonis, 12 observation of environmental, 35–36, 109–10 Control biological, 189 chemicals for L. salmonis, 57, 86, 103, 223–24 complicating factors affecting L. salmonis, 194 measures for L. salmonis, xii, 57–59, 102–6, 104f–105f strategy in Ireland for improved pest, 195–99, 199f topical/bath treatments for, 57, 86, 168, 189–90 wrasse used as method of biological, 190 Copepodids behavioral patterns ascribed to, 138, 140 energy supply of L. salmonis, 5 as free swimming, 4 migration of, 5 water accelerations and, 5 Copepods. See Copepodids; Sea lice Costs, production, 154 Currents, 122–23, 126f and L. salmonis transmission, 185 tidal, 120 variability in fjords of, 41–42, 42f Cypermethrin, 168

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Damages, from L. salmonis, xi–xii, 18, 180–81 Dark Harbour, Grand Manan Island, 83 Data, 274 audits used for verifying accuracy of, 266 collection on L. salmonis, 108, 205–6, 239 Rae’s collection of L. salmonis, 206–11 on sea louse abundance, 108 on sentinel cages, 173 sharing, 267 Debates around wild pink salmon, 108 in British Columbia on L. salmonis, 274 on effect of marine farming, 55 Deltamethrin, 106, 168 Detection, of L. salmonis, 9 Development L. salmonis stages of, 2–4 of L. salmonis management methods in Ireland, 177–201 of Norwegian monitoring programs, 160, 289–91 of planktonic louse, 135–38, 136f, 145–46 rapid infestation, 194 of SBM, 186, 196 of treatment strategies, 188–91, 191t water temperature and L. salmonis, 3–4, 135–36, 211 Dichlorvos, 86, 181, 206, 224 Diseases, 194 pancreas, 192 parasitic, 287–88 in salmon farming industry, 159 spread of, xi Distribution interannual variation on L. salmonis, 314–16 L. salmonis’ geographical, 7 of L. salmonis’ planktonic larval stages in Norway, 31–49 methods determining planktonic louse, 34–39, 36f, 38f of planktonic salmon lice, 39–47, 40f–43f, 44t, 45f, 47f spatial and temporal patterns in L. salmonis’, 314 Dynamics of fjords, 34–35 of L. salmonis, 19, 222–23 of L. salmonis on Scottish salmon farms, 222–23 population, 19

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Economics benefits of salmon farms, xi, 179–80 of L. salmonis infestations on salmon farms, xi–xii, 18, 181 Eggs farm production of sea lice, 131–35, 133f–134f, 139–40 multiple batches of, 206–7, 206f production of L. salmonis, 34, 119, 130–31, 145, 147 Rae on, 206–7, 206f stage of L. salmonis, 4 viability of L. salmonis, 132–33 Emamectin benzoate, 86, 105–6, 272–73 Emergency Drug Release, 106 Emigration, 180 Environment abundance of L. salmonis and factors of, 270 L. salmonis effected by factors of, 119 negative impacts on marine, 181 observing conditions of, 35–36, 109–10 Epibionts, on L. salmonis, 6–7 Epidemiology of L. salmonis, 217, 267 quantitative, 217–27, 218f–219f, 220t, 223t, 224f–226f Erosions, skin, 1, 10 Evaluation, of medicines, 169 Export value, 153 Fallowing, 200 Farmed salmon Atlantic, 31–32, 83, 84f, 85–86, 177, 179 epidemiology of L. salmonis on, 267 as hosts to L. salmonis, xiii interactions between wild and, 17–18, 53, 54f, 55–56, 106–9 in Ireland, 177, 179–80, 189 L. salmonis abundance in southwestern New Brunswick on, 86–99, 88f–93f, 94f, 96f–99f, 100t, 101–2, 101f–102f L. salmonis management on farmed salmon in Norway, 153–75 mortality from L. salmonis, 180–81 as overwinter hosts, 320 Pacific, 267 Farmers. See also Salmon farms financial losses from L. salmonis of, 181 hunter gatherers as becoming, xi Farming. See Marine fish farming; Open net pen farming

Farms. See Marine fish farming; Salmon farms Feed ivermectin treated, 86 medicated, 166, 168, 189, 222, 271 underdosing and medicated, 195 Feeding L. salmonis’ stages of, 6 parasites’ activities of, 10 First International Sea Lice Conference, 211–12 First Nation, 236 Fish. See also Marine fish farming; Salmon; Sticklebacks C. elongatus infected, 86 capturing, 143, 287 as clean, 212 interactions between wild and farmed, 17–18, 53, 54f, 55–56, 106–9 L. salmonis occurrence on nonsalmonid, 15–16 laws on health of, 161 osmotic and ionic regulation in salmonid, 283–84 pump, 271 surveys of wild, 144 Fish Farmer, 206 Fish Health Management Plan, 134 Fjords brackish layer in, 32–33, 41 current variability, 41–42, 42f dynamics of, 34–35 hydrography’s variability, 40–41, 40f lengths of, 31, 295 models, 37–38, 38f, 42–43, 43f, 44t in Norway, 174–75, 287–94 oceanography of, 31 spread of salmon lice in, 44–47, 45f–47f trawl program, 293–94, 294f Flatanger, L. salmonis treatment in, 170–71 Food, 184 Generation, time for L. salmonis, 4 Growth. See also Irish Salmon Growers Association community, 179 of L. salmonis, 37–38 models of L. salmonis, 38–39, 44–47, 45f–47f of salmon farming in Norway, 153–54 Gyrodactylus salaris, 173

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Habitats L. salmonis on juvenile salmon in nearshore, 313–19 modification and destruction of rivers’, 173 Hardangerfjord, 33f, 221 brackish water in, 41 L. salmonis treatment in, 171–72 numerical fjord model, 37–38, 38f Harvest. See also Marine Harvest Scotland Ltd. L. salmonis levels before, 195 Health. See also Fish Health Management Plan effects of L. salmonis, 238 laws on fish, 161 Herring, xii Pacific, 238 Hormones, stress, 180 Hosts attachment, 212 farmed salmon as L. salmonis, xiii farmed salmon as overwinter, 320 L. salmonis as transferring, 3 L. salmonis on atypical, 56 mortality of L. salmonis, 1 nonsalmonid, 15–16 overwintering L. salmonis, 319–22, 321f–322f parasites and, 9–19 populations, 60–61 selection of, 9–10 specificity of C. clemensi, 267 Hunter gatherers, as becoming farmers, xi Husbandry approaches in IPM, 163–64 practices in SBM, 186 problems and controversies brought with, xi Hydrogen peroxide, 224 as delousing agent, 190 Hydrography, 271 of fjords, 40–41, 40f Hyperplasia, 180–81 Identification, of L. salmonis, 9 Immunostimulants, 189 for enhancing immune response of salmon, 190 Impacts of L. salmonis on Pacific salmon, 323–25 negative marine environment, 181

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of SBM, 187–88 of treatments for L. salmonis, 219 Industry auditing L. salmonis, 266–67 disease in salmon farming, 159 immediate concerns for salmon farming, 272–73 Norwegian salmonid farming, 153–56, 154f–156f, 282 size of salmon farming, 235 Infection clinical signs of sea lice, 10–11 factors for level of L. salmonis, 185–86 L. salmonis related, 12–15, 19, 281–84, 283f, 286, 316–18 levels, 289 pressure maps, 72–73 Infectious salmon anemia (ISA), 103 Infestations of Atlantic salmon with L. salmonis, 1 breaking cycle of farms’ L. salmonis, 184 of C. elongatus, 180, 207, 213 economic significance of salmon farms’ L. salmonis, xi–xii, 18, 181 factors effecting L. salmonis, 183–86, 185t in Ireland of L. salmonis, 93 of L. salmonis on salmon in British Columbia, 237–38 rapid development factors for, 194 in Scotland of L. salmonis, 218–19, 218f skin erosion and, 1–10 treatments’ impact on L. salmonis, 219 Inflammation, in Atlantic salmon, 180–81 Infrastructure, 180 Integrated Pest Management (IPM), 212, 272, 282 approaches toward, 163 challenges provided by, 211 husbandry approaches used in, 163–64 main components of, 163 management approaches used in, 164 principles and requirements of basic, 162–63 program, 162–64 Interactions between Pacific salmon and L. salmonis, 309 between pink salmon and L. salmonis, 307 between wild and farmed fish, 17–18, 53, 54f, 55–56, 106–9 IPM. See Integrated Pest Management

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Ireland Atlantic salmon as farmed in, 177, 179 economies of coastal communities in, 179–80 improved pest control plans on salmon farms in, 195–99, 199f initial infestation of L. salmonis in, 93 L. salmonis larvae concentration in seawater of, 6 L. salmonis levels on wild salmon in, 177–78 L. salmonis management methods in, 177–201 for L. salmonis on farmed salmon in, 189 licensing of marine finfish aquaculture in, 196 national monitoring programme in, 181–86, 185t, 200 production of farmed salmon in, 180 rainbow trout farmed in, 177, 179 salmon farming regions in, 177, 178f–179f SBM in, 186–88 Irish Salmon Growers Association, 197 ISA. See Infectious salmon anemia Ivermectin, 86, 184, 272 Japan, coho salmon farming in, 15 Larvae behavior and dispersal of L. salmonis, 5–6, 211–12 L. salmonis stage of planktonic, 31–49 lice sampling, 61–67, 62f Laws, on fish health, 161 Layout, of sentinel cages, 36f Legislation, L. salmonis management and, 158–62 Lengths, of fjords, 31, 295 Lepeophtheirus cuneifer, 320 abundance trends of, 88 ovigerous, 319 relationships with other sea lice, 9 Lepeoptheirus salmonis (L. salmonis), xiii, 2f. See also Larvae; Planktonic louse abundance on farmed salmon in southwestern New Brunswick, 86–99, 88f–93f, 94f, 96f–99f, 100t, 101–2, 101f–102f abundance on wild salmon of, 108 animal welfare act for enforcing treatment of, 159

approaches to management of, 162–73, 166f, 167t, 171f Atlantic and Pacific lineages of, xii, 8–9 in Atlantic Canada as observed, 83–84 Atlantic salmon as infested by, 1 on Atlantic salmon in Norway, 34 on atypical hosts, 56 behavior of, 5–6, 138, 140, 211–12 biology, 2–6, 11 chalimus stage of, 9 in Chile, 224–25 coastal exposure of, 220 condition factor and, 12 control in Scottish aquaculture of, 57–59 control measures for, xii, 57–59, 102–6, 104f–105f daily migration of, 5 damage caused by, xi–xii, 18, 180–81 data collection on, 108, 205–6, 239 densities of, 101–2 detection of, 9 developmental stages of, 2–4 dynamics on Scottish salmon farms, 222–23 economic loss and, xi–xii, 18, 181 economic significance of salmon farms’ infestations of, 18 egg production, 34, 119, 130–31, 145, 147 egg stage of, 4 energy supply of copepodids of, 5 environmental factors effecting, 119 epibionts on, 6–7 epidemiology of, 217 epizootiology of, 18–19, 158 factors affecting infestation of, 183–86, 185t feeding stages of, 6 female fecundity of, 4, 208 first severe outbreaks of, 15 generation time for, 4 genetic population structure of, 7–8 geographical distribution of, 7 government auditing of monitoring of, 266–67 gravid, 322, 322f growth of, 37–38 health effects of, 238 host mortality from infestations of, 1 identification of, 9 immune response of salmon infected with, 12–13 immunomodulatory compounds secreted by, 13

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impacts on juvenile Pacific salmon of, 323–24 impacts on populations of Pacific salmon, 324–25 infection occurrence on farmed salmonid fish of, 15 infections related to presence of, 12–14, 19 infestations of, 1, 18, 93, 183–86, 185t, 218–19, 218f, 237–38 interannual variation on distribution of, 314–16 Ireland’s seawater concentrations of larvae of, 6 Irish development of management methods for, 177–201 legislation related to management of, 158–62 levels, 177–78, 185–86, 195 life cycle of, 2–3, 3f literature on, 1 management on farmed salmon in Norway, 153–75 management on farmed salmon in Scotland, 205–27 management on salmon farms in British Columbia, 235–75 management principles for, 188 mating of, 211 maximum thresholds of, 239 medicinal treatments for, 164–73 mobile stages of, 16, 220 modeling dispersal in Loch Torridon of, 68–74, 73f–74f modeling distribution and abundance of planktonic larval stages of, 31–49 modeling production of, 117–47 monitoring, 160–61, 287–88 morphology of, 7 mortality in farmed salmon from, 180–81 motile, 240t–265t, 320 naupliar stages of, 6–7 in Norwegian coastal zones current status, 281–98 Norwegian national action plan against, 160–61 nutrition of, 6–7 observation of, 36, 83–84 occurrence of infection on wild salmonid fish of, 14–15 occurrence on nonsalmonid fish, 15–16 osmoregulatory problems for fish infected with, 284

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overwintering hosts of, 319–22, 321f–322f on Pacific salmon, xii, 8–9, 267 pathophysiology, 11–12 physiological effects of infection of, 281–82 population level studies on, 307 prescription for treatment of, 159 reporting data on, 239 resistance of, 216–17 resistance to, 323–24 risk factors associated with abundance of, 220–21, 220t risk of introduction to Southern Hemisphere of, 16 salinity effects on, 4–5, 74, 95 in salmon farms, xi on salmonids in northeast Pacific ocean, 307–25 SBM’s impact on, 187–88 in Scotland, 53, 54f, 55–59, 218–19, 218f on sea trout, 215–16 sea trout infected with, 281 sexual maturity of, 313 skin erosions from infestations of, 1, 10 in Southern Hemisphere, 15 spatial and temporal patterns in distribution on, 314 spatial variation on juvenile salmon of, 318–19 spread of, 39, 44–47, 45f–47f, 102–3 stocking type of, 220 swimming stage of, 146 temporal variation and infection of, 316–18 transferring hosts, 3 transmission of, 313–14 treatment of, 57, 86, 159, 164–73, 166f, 186–88, 191–95, 192f–194f, 271–74, 271f variability of spread of, 39, 47, 48f, 49 water circulation and transmission of, 95, 97, 99–102 wild salmon as effected by, xii on wild salmonids in coastal zones, 281–325 wild salmonids population regulation by, 294–96, 297f wrasse used for control of, 190 Levels C. clemensi, 268, 319 factors for L. salmonis, 185–86 infection, 289 of L. salmonis before harvest, 195 of L. salmonis on wild salmon in Ireland, 177–78

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Levels (Continued ) plasma chloride, 286 of salinity, 74, 95, 97f Lice. See Lepeoptheirus salmonis Licensing, 156–58, 157f, 157t of Irish aquaculture, 196 Life cycle, of L. salmonis, 2–3, 3f Locations Broughton Archipelago, 117, 118f of particle release, 139–40 of pink salmon, 310 of salmon farms, xii Lochs. See Sea lochs Loch Shieldaig, 60, 73–74 Loch Torridon AMG case study, 59–67, 62f, 66f modeling sea lice dispersal in, 68–74, 73f–74f observations summary on lice in, 67 populations in, 60–61 Lords Cove, Deer Island, 83 Management. See also Area Management Groups; Fish Health Management Plan; Integrated Pest Management; Sea Louse Management Zones approaches to L. salmonis, 162–73, 166f, 167t, 171f of bays, 186–88, 187f IPM and approaches of, 164 Irish methods of L. salmonis, 177–201 for L. salmonis control in New Brunswick, 102–6, 104f–105f of L. salmonis on farmed salmon in Norway, 153–75 of L. salmonis on salmon farms in British Columbia, 235–75 of L. salmonis on Scottish farmed salmon, 205–27 legislation and L. salmonis, 158–62 modus operandi for bay, 199–200, 200f optimizing practices of, 197 principles for L. salmonis, 188 strategies for bay, 195–98 Maps of Broughten Archipelago, 124f infection pressure, 72–73 Marine fish farming. See also Open net pen farming; Salmon farms debate around, 55 first attempts of, xi

in hunting gathering economy, xi of salmon, xi yield of, xi Marine Harvest Scotland Ltd., 217–18 Marine Institute Sea Lice Monitoring Programme, 199 Mating, of L. salmonis, 211 Maturity L. salmonis’ sexual, 313 of planktonic louse, 139 Measures L. salmonis control, xii, 57–59, 102–6, 104f–105f safety, 169 of salinity, 35 of temperature, 35 Medicines. See also Treatments application of, 189 bath treatments of, 57, 86, 168, 189–90 cascade use of, 184 case studies on L. salmonis treatment with, 170–73 choosing, 165 evaluating, 169 in feed, 166, 168, 189, 222, 271 for L. salmonis, 164–73, 184, 191 methods for use of, 166, 167t, 168–69 properties of L. salmonis treatment, 166f synchronized approaches for L. salmonis treatment with, 170 topical, 165, 168 underdosing and, 189, 195 Methods L. salmonis management, 177–201 for medicinal use, 166, 167t, 168–69, 186 for planktonic louse distribution determination, 34–39, 36f, 38f wrasse used as biological control, 190 Migration diel vertical, 137–38 of L. salmonis, 5 protection of salmon during, 296 routes of salmon, 106–8 Models, 145 atmospheric, 37 Bergen Ocean, 37 biological particle, 69–70 coastal ocean, 37 of dispersal in Loch Torridon of L. salmonis, 68–74, 73f–74f Finite Volume Coastal Ocean, 119, 145

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fjord, 37–38, 38f, 42–43, 43f, 44t hydrodynamic, 68–69, 73f infection pressure maps and, 72–73 of L. salmonis distribution and abundance in Norway, 31–49 of L. salmonis production and concentrations in Broughton Archipelago, 117–47 mathematical, 226 numerical, 35 numerical circulation, 119–28 quantitative epidemiology and, 217–27, 218f–219f, 220t, 223t, 224f–226f results of distribution and abundance of planktonic salmon lice, 39–47, 40f–43f, 44t, 45f, 47f salmon lice growth and advection, 38–39, 44–47, 45f–47f validated, 35 Monitoring Atlantic salmon, 292–94 developing Norwegian programs for, 160, 289–91 government auditing of industry L. salmonis, 266–67 Irish national program for, 181–86, 185t, 200 of L. salmonis, 160–61, 287–88 objectives of, 181–82 routine L. salmonis, 239 Morphology, of L. salmonis, 7 Mortality, 295 in farmed salmon from L. salmonis, 180–81 L. salmonis hosts, 1 parasitic diseases and, 287–88 of pink salmon, 324 of planktonic louse, 135–38, 136f of sea trout, 285 Movement modeling particles, 71–72, 73f particles’ horizontal, 71 particles’ vertical, 71–72 National Animal Health Authority, 161 Neguvon, 159 Nets. See also Open net pen farming cages of floating, 83 plankton, 36 stress to fish from, 189 tows, 141–44, 142f, 143f

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New Brunswick ABMAs in, 105, 105f L. salmonis abundance on farmed salmon in southwestern, 86–99, 88f–93f, 94f, 96f–99f, 100t, 101–2, 101f–102f L. salmonis interactions between farmed salmon and wild fish in southwestern, 106–9 Letang area salmon farms in, 87 management actions for controlling sea lice in southwestern, 102–6, 104f–105f outbreaks of L. salmonis in, 85–86 salmon farms in, 83–84, 84f–85f water temperatures in, 93–95, 94f, 96f Norway, 221. See also Norwegian Ecological Model System; Norwegian Food Safety Authority advection of coastal waters in, 293 Altafjord system in, 290–91 approaches to L. salmonis management in, 162–73, 166f, 167t, 171f case studies of L. salmonis treatment in, 170–73 coast of, 31–32, 32f, 153, 281–98 coordinated sea lice areas and zones in, 174 export value of salmon in, 153 fjords in, 173–74, 287–94 growth of salmon farming in, 153–54 L. salmonis as main Atlantic salmon parasite in, 34 law on fish health in, 161 maximum thresholds of L. salmonis in, 239 modeling distribution and abundance of L. salmonis’ planktonic larval stages in, 31–49 monitoring programs as developed in, 160, 289–91 national action plan against L. salmonis, 160–61 national salmon watercourses in, 173–74 prescription for L. salmonis treatment in, 159 present status/implications of L. salmonis on wild salmonids in coastal zones of, 281–98 regulations and licensing in, 156–58, 157f, 157t salmon farming statistics in, 153 salmon farms in, 15, 153–56, 155f–156f, 174–75

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Norway (Continued ) salmonid farming industry in, 153–56, 155f–156f, 282 salmon in rivers along coast of, 34 salmon louse management on farmed salmon in, 153–75 sea trout on coast of, 281 Vik watershed in, 288 wild salmonids’ population regulation in, 294–96, 297f wild salmon in, 173–74, 281–92 Norwegian Ecological Model System, 37 Norwegian Food Safety Authority, 159 Nutrition, of L. salmonis, 6–7 Observations of environment conditions, 35–36, 109–10 of L. salmonis, 36 of L. salmonis in Atlantic Canada, 83–84 plankton nets for, 36 Occurrence of C. elongatus, 15, 89, 93 of L. salmonis, 14–16 Ocean Fish Lift, 292 Oceanography of Broughton Archipelago, 117, 119 of fjords, 31 Oceans. See Atlantic ocean; Pacific ocean Open net pen farming, xiii. See also Salmon farms Overfishing, 173 Pacific ocean L. salmonis in, xii, 8–9 L. salmonis on farmed salmon in, 267 L. salmonis on salmonids in northeast, 307–25 salmon farming in, xii, 267 wild salmon in, xii Pancreas disease, 192 Parasites. See also Lepeoptheirus salmonis; Sea lice of Canada, 16 diseases and, 287–88 feeding activities of, 10 relationships of hosts and, 9–19 spread of, xi Particles horizontal movement of, 71 modeling biological, 69–70 movement modeling, 71–72, 73f

release locations of, 139–40 release schedule of, 139–40 tracking of, 128–30, 129f vertical movement of, 71–72 Passamaquoddy Bay, 83, 90, 93 Pathology, of L. salmonis infections, 282–86, 283f, 286 Patterns copepodids behavior patterns, 138, 140 L. salmonis’ spatial and temporal, 314 PCR. See Polymerase Chain Reaction Pest. See also Integrated Pest Management Irish improved control of, 195–99, 199f Physiology, of L. salmonis infections, 282–86, 283f Pink salmon, 14, 238–39 abundance of L. salmonis on, 315, 325 collapse in popular abundance of, 325 debates around, 108 interactions between L. salmonis and, 307 interannual variation of L. salmonis on, 314–15 juvenile, 316–18, 317t locations of, 310 mortality of, 324 population biology of, 309–13, 311f–312f, 312t as produced, 310–12, 312t spawning, 309, 313 species of, 309f Plankton blooms, 194 nets, 36 net tows, 141–44, 142f, 143f sampling, 61 Planktonic louse behavior of, 135–38, 136f development, 135–38, 136f, 145–46 distribution in Norway of, 31–49 growth and advection model of, 38–39, 44–47, 45f–47f maturation of, 139 methods determining distribution/abundance of, 34–39, 36f, 38f model results of distribution and abundance of, 39–47, 40f–43f, 44t, 45f, 47f mortality of, 135–38, 136f sampling for, 61–65, 62f

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simulations and, 138–39 spread of, 39, 44–47, 45f–47f, 48f, 49, 102–3, 186 Plasma chloride, 286 Polymerase Chain Reaction (PCR), 216 Population biology of pink salmon, 309–13, 311f–312f, 312t collapse of pink salmon, 325 dynamics of sea lice, 19 host, 60–61 increases, xi level studies of L. salmonis, 307 in Loch Torridon, 60–61 of Pacific salmon, 324–25 regulation of wild salmonids in Norway by L. salmonis, 294–96, 297f Predators, 287 Prescriptions, for L. salmonis treatment, 159 Problems with husbandry, xi osmoregulatory, 284 with treatments, 225–26, 226f Production costs, 154 efficiency, 154 of farmed salmon in Ireland, 180 on farms of sea lice eggs, 131–35, 133f–134f, 139–40 of L. salmonis eggs, 34, 119, 130–31, 145, 147 modeling L. salmonis production, 117–47 modeling sea lice, 117–47 of pink salmon, 310–12, 312f Programs. See also Integrated Pest Management; Marine Institute Sea Lice Monitoring Programme fjords trawl, 293–94, 294f monitoring, 160, 181–86, 185t, 200, 289–91 Protection of Atlantic salmon, 159 during migration of salmon, 296 Protocol, sampling, 221–22 Pumps, fish, 271 Rae, Gordon, 205, 222 early data collected by, 206–11 on L. salmonis eggs, 206–7, 206f treatment data from, 209 Rain, acid, 173

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Rainbow trout, 153, 177, 179 Recapture, 295–96 Regions L. salmonis abundances variation and farming, 269–70 of salmon farming in Ireland, 177, 178f–179f Regulations osmotic and ionic, 283–84 on salmon farming in Norway, 156–58, 157f, 157t of wild salmon populations by L. salmonis, 294–96, 297f Rejection, of sea lice, 14 Relationships host-parasite, 9–19 of L. salmonis with other sea lice, 9 Reporting on farmed Pacific salmon, 267 L. salmonis data, 239 Resistance as defined, 323 to L. salmonis, 323–24 of sea lice, 216–17 Response C. elongatus’ immune, 13 salmon’s immune, 12–13, 190 Restrictions, on catch size, xi Risk factors and abundance of L. salmonis, 220–21, 220t of L. salmonis introduced to Southern Hemisphere, 16 River Balgy, 60 Rivers habitat modification and destruction, 173 salmon in, 34, 106 Routes, salmon migration, 106–8 Routine, monitoring of L. salmonis, 239 Safety. See also Norwegian Food Safety Authority measures, 169 Salinity of Broughton Archipelago, 127 changes in, 270 climatology of, 121–22 L. salmonis tolerance of, 4–5 levels of, 74, 95, 97f measures of, 35 as varying in regions, 270

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Salmon. See also Atlantic salmon; Farmed salmon; Pink salmon; Wild salmon C. clemensi on juvenile Pacific, 323 chinook, 235 chum, 316–17 coho, 15, 235 early marine survival of, xiii export value in Norway of, 153 immune response of, 12–13, 190 impact of L. salmonis on Juvenile Pacific, 323–24 impact of L. salmonis on populations of Pacific, 324–25 interactions between L. salmonis and Pacific, 309 migration, 296 nearshore habitats’ L. salmonis on juvenile, 313–19 in Norway’s coastal rivers, 34 in rivers near Bay of Fundy, 106 selective breeding of, 14 sockeye, 313 swimming performance of, 284 Salmon farms. See also Marine fish farming arguments over, xi around Vancouver Island, 236 in Broughton Archipelago, 117, 118f, 238–39 buffer zone free of, 159–60 diseases and, 159 economic benefits of, xi, 179–80 economic significance of L. salmonis infestations in, 18 floating net cages for, 83 immediate concerns for British Columbia’s, 272–723 improved pest control strategy on Irish, 195–99, 199f industry in Norway of, 153–56, 154f–156f, 282 Irish regions of, 177, 178f–179f L. salmonis dynamics on, 222–23 L. salmonis management in British Columbia, 235–75 L. salmonis passed to wild salmon from, xi locations of, xii in New Brunswick, 83–84, 84f–85f, 86–99, 88f–93f, 94f, 96f–99f, 100t, 101–2, 101f–102f, 109–10 in Norway, 15, 153–56, 155f–156f, 174–75 as not isolated, xi

opposition to, 307 outbreaks of L. salmonis after establishment of, 15 parasites plaguing, xi proximity of, 95, 98f regulations in Norway on, 156–58, 157f, 157t in Scottish sea lochs, 51 sea lice epidemiology on Scottish, 217–27, 218f–219f, 220t, 223t, 224f–226f temperature for Atlantic, 31–32 tidal excursion areas of, 100t Salmon lice. See Lepeoptheirus salmonis Salmon louse. See Lepeoptheirus salmonis Sampling bias and, 221 coastal larval lice, 61 for larval lice, 61–67, 62f lice counts from wild fish, 65–66, 66f offshore larval lice, 62–63 plankton, 61 protocol, 221–22 for salmonids in fjords, 288 sentinel cages for, 66–67 SBM. See Single Bay Management Scotland. See also Loch Torridon AMAs in, 222 coastal exposure of L. salmonis in, 220 coastal waters of, 50–53, 75 control of lice in Scottish aquaculture, 57–59 data collection on L. salmonis in, 205–6 L. salmonis in, 53, 54f, 55–59 L. salmonis management on farmed salmon in, 205–27 medicated feed in, 222 returning wild salmon in, 214–15 salmon farms in sea lochs of, 51 sea lice epidemiology on salmon farms in, 217–27, 218f–219f, 220t, 223t, 224f–226f sea lochs in, 51–53 wild sea trout in, 214–16 Sea lice. See also Lepeoptheirus salmonis basic biology of, 2–6, 211 clinical signs of infection of, 10–11 epizootiological studies on, 18–19 L. salmonis’ relationship with other, 9 modeling production of, 117–47 population dynamics, 19 rejecting, 14

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Sea lochs. See also Loch Shieldaig; Loch Torridon circulation, 52–53 Loch Torridon system of, 59–60 salmon farms in Scottish, 51 wind and, 53 Sea louse. See Lepeoptheirus salmonis Sea Louse Management Zones, 103–5 Sea trout, 7 capturing, 287 L. salmonis infection of, 281 L. salmonis on, 215–16 monitoring L. salmonis on, 287 mortality of, 285 on Norwegian coast, 281 in Norwegian fjords, 288–92 physiology/pathology of L. salmonis infections in, 282–86 plasma chloride levels on, 286 wild, 213–14 Selection breeding and, 14 of hosts, 9–10 Sentinel cages data on, 173 layout of, 36f observations of L. salmonis with, 36 sampling of larval lice with, 66–67 Single Bay Management (SBM), 199 development of, 186, 196 husbandry practices in, 186 L. salmonis as impacted by, 187–88 strategic treatments under, 190–91 Size restrictions on catch, xi of salmon farming industry in British Columbia, 235 Skin, erosions, 1, 10 Sognefjord, 34 Southern Hemisphere, L. salmonis in, 15 Spawning, 309, 313 channels, xii Speed, swimming, 12, 138 Spread of diseases, xi in fjords of L. salmonis, 44–47, 45f–47f of L. salmonis, 39, 102–3 of parasites, xi of planktonic louse, 39, 44–47, 45f–47f, 48f, 49, 102–3, 186 variability of L. salmonis, 39, 47, 48f, 49 Status, of L. salmonis in Norway, 281–98

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Sticklebacks, xii, 1, 16, 109, 320 Stocking, 220 Strategies for bay management, 196–98 Irish improved pest control, 195–99, 199f under SBM, 190–91 treatment, 188–91, 191t, 212–13 Stress, 271 to fish from nets, 189 handling, 267 hormones, 180 osmotic, 284 Surface, circulation, 120–21 Swimming, 131 copepodids as free, 4 performance, 284 speeds, 12, 138 stage of L. salmonis, 146 vertical, 40 water flow change causing bursts of, 5 Tagging, 295 Tarpaulin, 168–69, 189 Teflubenzuron, 106 Temperature for Atlantic farmed salmon, 31–32 of Broughton Archipelago, 127, 128f changes in, 270 climatology of, 121–22 L. salmonis development and water, 3–4, 135–36, 211 measures of, 35 of Scottish coastal waters, 51 water, 2–4, 93–95, 94f, 96f, 192–93 Tides, 100t, 120 Time, generation, 4 Timing, of treatments, 213 Transmission currents and L. salmonis, 185 L. salmonis’ successful, 313–14 vertical and lateral L. salmonis, 183 water circulation and L. salmonis, 95, 97, 99–102 Trawling, 293–94, 294f Treatments alternative, 189 animal welfare act and L. salmonis, 159 for C. elongatus, 168 case studies on L. salmonis medicinal, 170–73 chemical, 57, 86, 103, 223–24 development in strategies of, 188–91, 191t

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Treatments (Continued ) with fish pump, 271 with hydrogen peroxide, 190 ineffective, 194 infestation as impacted by L. salmonis, 219 of L. salmonis, 57, 86, 159, 164–73, 166f, 186–88, 191–95, 192f–194f, 271–74, 271f medicinal, 95, 164–69 new issues for L. salmonis, 191–95, 192f, 194f problems with, 225–26, 226f Rae’s data on, 209 rotation of L. salmonis, 188 strategic, 190–91, 212–13 subtle effects of, 219 synchronized winter, 172–73 tarpaulin, 168–69 timing and, 213 topical/bath, 57, 86, 168, 189–90 types of, 189 well boats used for, 190 Trends, of L. salmonis abundance, 88 Tripartite Working Group, 58–59 Trout. See also Sea trout rainbow, 153, 177, 179 Underdosing medicated feed and, 195 medicines, 189, 195 Value, export, 153 Variation interannual, 314–16 of L. salmonis abundance, 268–70 spatial, 318–19 Water. See also Watercourses advection of Norwegian, 293 circulation, 95, 97, 99–102, 321

copepodids responding to accelerations of, 5 fresh, 120 Scotland’s coastal, 50–53, 75 temperature, 2–4, 93–95, 94f, 96f, 135–36, 192–93, 211 Watercourses, Norwegian national salmon, 173–74 Watersheds, 288 Weather, 183 Welfare, animal, 149, 159, 183 Well boats hydrogen peroxide treatments with, 190 used in medicinal treatments, 190 Wild salmon data on sea louse abundance on, 108 factors adversely effecting, xii interactions between farmed and, 17–18, 53, 54f, 55–56, 106–9 L. salmonis’ effects on, xii L. salmonis levels in Ireland on, 177–78 L. salmonis passed from salmon farms to, xi in Norway, 173–74, 281–92 in Pacific ocean, xii population regulation of, 294–96, 297f returning in Scotland, 214–15 statistical description of loads on, 56–57 Wind, 126 circulation from, 271 sea lochs and, 53 surface circulation influenced by, 120–21 Wrasse as biological control method, 190 cultured, 190 Zones. See also Sea Louse Management Zones buffer, 159–60 Norwegian coordinated sea lice, 174

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Chapter 10

Lepeophtheirus salmonis on Salmonids in the Northeast Pacific Ocean Simon R.M. Jones and Richard J. Beamish

Introduction Systematic, population level studies of salmon louse (Lepeophtheirus salmonis) infections on Pacific salmon (Oncorhynchus spp.) in the coastal waters of western North America started in 2003. The earlier work in this region focused mainly on questions of parasite taxonomy and on parasite interactions with individual salmon. While louse infections on adult salmon migrating back to coastal waters are common and unremarkable, there were virtually no reports of the infections on juvenile Pacific salmon in the coastal areas of the ocean. It is not known whether this absence was related to a generally lower surveillance effort directed at this life history stage, particularly of pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon, or whether it reflected a naturally low prevalence of the parasite. Small abundances of sea lice have always occurred on juvenile Pacific salmon (Z. Kabata, personal communication). It was the association of sea lice with the developing salmon farming industry, specifically that infections on farmed salmon were speculated to give rise to unnaturally high levels of infection on wild juvenile salmon, which highlighted the poor understanding of the population dynamics of sea lice. Various organizations have opposed salmon farming on many fronts, but the possible negative impacts on Pacific salmon have alarmed the general public. Critics of salmon farming maintain that sea lice are spread from farms and kill juvenile Pacific salmon. Thus, when there were observations of salmon lice on a large percentage of juvenile pink salmon in the Broughton region of British Columbia in 2001 there was no way of assessing how the infection started or its effect on juvenile Pacific salmon. The Broughton region is an area of coastal British Columbia east of Queen Charlotte Strait that includes Broughton Island and the islands that surround it (Figure 10.1). The observation of a large infection with sea lice also preceded a large decline in the strength of the same cohort that returned to the area to spawn in 2002. Inevitably, there was concern and speculation that the louse infections were derived from farmed salmon and that they played a significant role in the stock decline (Pacific Fisheries Resource Conservation Council 2002). At the time, scientific literature consisted largely of European reports documenting impacts of L. salmonis on coastal populations of juvenile Atlantic salmon (Salmo salar) and sea-run brown trout (Salmo trutta). In Norway, Scotland, Salmon Lice: An Integrated Approach to Understanding Parasite Abundance and Distribution, First Edition. Edited by Simon Jones and Richard Beamish.  C 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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Figure 10.1. Map of British Columbia coast (A) and the Broughton region (B) showing locations mentioned in the chapter. Black dots indicate location of three salmon farms used in the study.

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and Ireland the farmed salmon vastly outnumber the wild salmonids and the negative impacts of the parasite on wild salmon and trout populations in Norwegian fjords with high densities of salmon farms were well documented. In British Columbia, given the diversity and abundance of wild Pacific salmon, there was concern that the European literature did not accurately reflect population level effects of the salmon louse. Interactions between anadromous Pacific salmon and L. salmonis occur in two broad ecological domains: the high seas, primarily involving subadult and adult salmon; and in coastal or nearshore habitats, involving mature salmon returning to spawn and juvenile salmon shortly after entry into the ocean (Beamish et al. 2005). This chapter reviews salmon louse research conducted in each of these domains and uses this information to assess the impacts of the salmon louse on pink salmon at the population level.

The Population Biology of Pink Salmon Pink salmon are the most abundant of all anadromous Pacific salmon. They enter the ocean in the spring a few days to weeks after the eggs hatch in freshwater. Most juvenile pink salmon die in the ocean and all pink salmon die after spawning. An estimate of their average marine survival ranges from about 1.7 to 4.7% with a mean value of about 3% (Heard 1991). In contrast to other Pacific salmon species, pink salmon have a fixed, 2-year life history strategy that results in the complete isolation of populations that spawn in adjacent years in the same river (Figure 10.2). Pink salmon spawn in

Average age

Range

Pink salmon (O. gorbuscha)

2 years

(2 years)

Chum salmon (O. keta)

4 years

(3–6 years)

Sockeye salmon (O. nerka)

4 years

(4–6 years)

Coho salmon (O. kisutch)

3 years

(2–4 years)

Chinook salmon (O. tshawytscha)

4 years

(1–7 years)

Figure 10.2. The five main species of Pacific salmon found on the British Columbia coast and their average age at maturity.

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consecutive years in some rivers, while in other rivers, they spawn in alternate years. For example, the largest population of pink salmon in British Columbia spawns in the Fraser River in alternate years that end in an odd number. By convention, these are called odd-year pink salmon. Fish spawning in even-numbered years are called evenyear pink salmon. No one understands why some rivers have only one type or why there are significant differences in the abundances of odd- and even-year types or brood lines within the same river. To further complicate the understanding of the population dynamics of pink salmon, there are examples of large and sudden collapses of one type followed by a gradual increase in abundance of the other type in the same river (Bugayev 2002; Gritsenko 2002). Again, there are no scientifically based explanations for these changes, although there is speculation that when abundances of pink salmon fry reach a high density, reduced carrying capacity in the early marine period can result in massive mortalities (Gritsenko 2002). Pink salmon are also produced in hatcheries and “enhanced” by creating more spawning habitat in artificial spawning channels. Spawning channels greatly increase the egg to fry survival rate compared to the survival rates in natural spawning areas. There is a substantial literature that indicates that hatchery-produced or spawning channel-produced Pacific salmon replace or reduce the productivity of wild Pacific salmon (Hilborn 1992; Meffe 1992; Levin et al. 2001; Zaporozhets and Zaporozhets 2004) although this interpretation is not without challenge (Wertheimer et al. 2001). The methodology used to determine how many Pacific salmon return from the high seas as adults each year is also important to this discussion. The estimate of abundance of spawning Pacific salmon used by all investigators is termed escapement. Escapement numbers are mainly visual estimates of the abundance of fish of a particular species in a particular river. In many cases, the visual estimate is for a species that is mixed into schools of several species. The estimate is made by observers that are experienced at recognizing a species from a distance and at estimating the number of individuals in a school. The estimates are almost never verified by direct counts and virtually never assigned error limits. Escapement estimates, therefore, are approximations of the abundance of spawning fish. However, these estimates are the only numbers that exist. There are 27 rivers and streams in the Broughton region that produce pink salmon. There are artificial spawning channels associated with two of these rivers (Figure 10.1B; Beamish et al. 2007). The spawning channel on the Glendale River was completed in 1988 and pink salmon have spawned in the channel since that date (Figure 10.3). Most pink salmon enter this river and the channel in August and spawn from September to October. When the channel contains approximately 60,000–70,000 fish, it is closed and the remaining pink salmon spawn in the Glendale River. It is interesting that local residents report that the number of grizzly bears feeding on pink salmon in the river and around the spawning channels increased from just a few before the channel was built to about 40 in recent years, suggesting that there has been a substantial change in the local population ecology of pink salmon (Figure 10.4). The other spawning channel is on the Kakweiken River and was finished in 1989. Apparently, it was not well populated with Pacific salmon and our inspection of the channel in the spawning period in recent years did not detect any fish. The pink salmon fry that are produced in the Glendale River and spawning channel are an essential part of the population dynamics of all pink salmon populations in the area. The average number of pink salmon fry produced each year between 1990 and

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Figure 10.3.

311

Aerial view of Glendale spawning channels.

2007 in the Glendale River and spawning channel calculated according to the methods in Beamish et al. (2006) is 37,639,000; 57,684,000 in odd-numbered years (1991–2007) and 17,593,000 pink fry in even-numbered years (1990–2006; Table 10.1). Beamish et al. (2006) estimated the marine survival for the six major populations of pink salmon in the Broughton region because the numbers were reliable and represented 95% of all pink salmon production in this area. In recent years (2003–2007), pink fry production from the Glendale River and spawning channel has been a large percentage (85% in odd-numbered years and 64% in even-numbered years) of total fry production

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Figure 10.4.

Grizzly bear feeding in the Glendale River.

Table 10.1. Pink salmon (Oncorhynchus gorbuscha) fry production from the Glendale River and spawning channel. Fry enter the ocean in the year after the spawning year.

Spawning year

Year of ocean entry

Number of fry

1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007

1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008

14,608,000 730,000 29,217,000 8,348,000 8014,000 3,339,000 17,947,000 13,356,000 20,869,000 409,929,000 31,721,000 56,347,000 760,000 6,756,000 27,612,000 9,326,000 7,589,000 11,028,000

Average (all years) Average (odd-numbered years) Average (even-numbered years)

37,639,000 57,684,000 17,593,000

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Figure 10.5. The percentage of pink salmon juveniles produced in the Glendale River and spawning channel in relation to the total fry production from the six major populations in the Broughton area. Data for 1999 are unreliable (Beamish et al. 2006) and are omitted. Juveniles enter the ocean in the year following the spawning year and return to spawn in the next year.

from the six major rivers (Figure 10.5). Thus, the production of pink salmon fry from the Glendale River and spawning channel is very substantial and is relevant to any assessment of the population dynamics of pink salmon in the Broughton region. There is a possibility that the production of pink salmon from the Glendale River and spawning channel is gradually dominating all pink salmon production in the area by reducing the marine survival of smaller populations. Hilborn (1992) and West and Mason (1987) reported a 40% decline in the smaller populations of sockeye salmon (Oncorhynchus nerka) as a consequence of the spawning channel enhancement of Babine Lake sockeye salmon. The mechanism could be related to a limited capacity of the ocean to provide prey in the early marine period of the pink salmon fry. Thus, the population dynamics of the pink salmon in other rivers in the Broughton region is unlikely to be independent of the production from the spawning channels.

L. salmonis on Juvenile Salmon in Nearshore Habitats The fundamental dilemma faced by L. salmonis is the challenge of successful transmission because of the anadromous behavior of the host. Parasite reproduction must occur prior to host migration into a freshwater environment that is lethal to the parasite. Depending on the species, Pacific salmon spend 1–5 years in the ocean before returning to spawn; however, ages of the parasites are not known and some reinfection occurs on the high seas (Nagasawa 1987, 2001; Nagasawa et al. 1993; Beamish et al. 2005). Adult Pacific salmon were captured during their coastal migration and examined for sea lice in two marine areas in the central coast area of British Columbia. Virtually all salmon had sea lice. Pink, chum, and sockeye salmon had average intensities ranging from 41.5 to 52.0 sea lice. Chinook (Oncorhynchus tshawytscha) and coho

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(Oncorhynchus kisutch) salmon had average intensities ranging from 16.1 to 18.5 sea lice. L. salmonis were about twice as numerous as Caligus clemensi. Most C. clemensi were in the chalimus stage and most L. salmonis were in the mobile stage. Gravid female L. salmonis represented 33.3% of all mobile stages. The similar intensities of sea lice on Pacific salmon returning to the coastal areas of British Columbia is an indication that large numbers of L. salmonis may be transported into all coastal areas (Beamish et al. 2005). The cues used by L. salmonis to initiate ovulation and optimize reproductive success are poorly understood. Although the high proportion of adult parasites on the returning salmon suggests that sexual maturity of the parasite may be coordinated with that of the host, ovigerous lice are also observed on juvenile and immature salmon suggesting it is unlikely that maturation of the host is an important trigger. It is more likely that fertilized female lice continually produce egg strings (see the introductory chapter contributed by Hayward et al.) and that reproductive success relies on maximizing larval output as host biomass increases in coastal waters during the spawning migration, as recently proposed by Beamish et al. (2007). The working hypothesis concerning continuity of L. salmonis populations on anadromous salmon is that larvae produced from the infections on returning adult salmon form the basis, directly or indirectly, of infections that occur on the succeeding host generation. According to the life history strategy of Beamish et al. (2007), transmission of L. salmonis to the next host generation is maximized in late summer or early autumn when outmigrating juvenile pink, chum, and sockeye salmon encounter returning adult salmon. L. salmonis on younger juvenile coho and chinook salmon that remain in nearshore habitats after adult salmon enter freshwater, help to carry the infections over the winter and into the following year. This is important because of the relatively short developmental time for infective copepodid production relative to the interval between host spawning and fry migration to the ocean. During this interval, which can range from 2 to 5 months depending on the locality, parasites must be sustained over winter on host populations in coastal or nearshore waters. The term migratory allopatry was defined as “a period of spatial separation between adults and juvenile hosts, which is caused by host migration and which prevents parasite transmission from adult to juvenile hosts” (Krkoˇsek et al. 2007a). However, this is obviously a successful parasite and Beamish et al. (2007) argued that there must be an advantage to the parasite to maintain a life history strategy in which it is transported in high abundance into the coastal areas immediately before the host entered freshwater. There has been considerable effort in recent years to document biological, environmental, and anthropogenic factors influencing the winter abundance of L. salmonis populations in the nearshore of coastal British Columbia. Two questions drive sea lice research in this region: (1) what are the factors that influence the abundance of infective copepodids in coastal waters and (2) what is the impact of L. salmonis on juvenile Pacific salmon? Spatial and temporal patterns in the distribution of L. salmonis in western Canada obtained to date are largely based on observations of infections on migratory (wild) or stationary (farmed) populations of salmon. Parker and Margolis (1964) described mixed infections with L. salmonis and another siphonostomoid copepod C. clemensi on juvenile pink salmon shortly after they had entered the ocean on the central coast of British Columbia, north of Vancouver Island. More recently, L. salmonis has been documented on postemergent pink and chum salmon from two coastal regions of British Columbia: (1) adjacent to the mouth of the Skeena River and Chatham Sound

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on the north coast of British Columbia and (2) in the Broughton region (Morton and Williams 2004; Morton et al. 2004; Jones and Hargreaves 2007; Krkoˇsek et al. 2007a, 2007b). Similarly, L. salmonis and C. clemensi were reported on juvenile sockeye salmon in the Discovery Islands, east of Vancouver Island (Morton et al. 2008). All studies documented differences in L. salmonis levels suggesting both spatial and temporal patterns of abundance as well as significant interannual differences. Fisheries and Oceans Canada monitored levels of L. salmonis and C. clemensi on juvenile pink and chum salmon in the Broughton region of British Columbia between 2003 and 2009. Several collections were made at monthly intervals after the fish entered the ocean in late February to early March. Descriptions of the survey, including gear used and sampling methodologies are reported in Jones and Nemec (2004); Jones et al. (2006a); Jones and Hargreaves (2007).

Interannual Variation Year-to-year differences in the prevalence and abundance of L. salmonis on juvenile pink and chum salmon in spring samples were statistically significant. In the Broughton region there was an increase in 2004 followed by consistently decreasing levels between 2005 and 2009 (Jones and Hargreaves 2007, 2009). Over 60% of pink salmon and over 70% of chum salmon were infected early in May 2004 whereas in 2008, only 3.8% and 5.9% were infected (Table 10.2). An absence of salmon lice on the pink salmon collected during March 2008, for the first time in the study, further reinforced the decreasing trend (Jones and Hargreaves 2009). Interannual differences in the levels of L. salmonis on juvenile pink and chum salmon have also been documented by other workers in the Broughton region and further north along the British Columbia coast. In Smith and Rivers inlets, an area with no fish farms, immediately north of the Broughton region, Beamish et al. (2005, 2007) recorded relatively large abundances of L. salmonis on adult Pacific salmon that were returning to their natal rivers. Using only the chalimus stages, Beamish et al. (2007) recorded prevalences on juvenile pink, chum, sockeye, coho, and chinook salmon of 33.3%, 22.0%, 60.7%, 14.3%, and 3.1%, respectively. Most of these juveniles were migrating into the open ocean and most likely would carry these sea lice with them. The abundance of L. salmonis was monitored on juvenile pink salmon collected from the ocean near the Skeena River and Chatham Sound between 2004 and 2006 (Krkoˇsek et al. 2007a). In contrast to the Broughton region, approximately 450 km to the south, the abundance of L. salmonis on the more northern pink salmon gradually increased between 2004 and 2006 (Figure 10.6). The abundance of the parasite on pink salmon in the Skeena and Nass rivers region in 2006 was comparable to that observed in the Broughton region in 2007 and 2008 (Figure 10.7). Furthermore, although detailed prevalence data are not available in Krkoˇsek et al. (2007a), the authors reported that prevalence was “approximately 2–3% during the first three months of marine life of pink salmon.” This too is similar to the prevalence of L. salmonis observed on juvenile pink salmon in the Broughton region in 2008 (Jones and Hargreaves 2009), despite the absence of farmed salmon in the northern region. In these localities, year-to-year differences are most likely the result of interacting factors including the abundance of the overwintering louse population, temperature, and salinity levels in surface seawaters during and preceding the migration of juvenile salmon into the ocean. The rate of development and therefore

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(A)

(B)

Figure 10.6. Abundance (lice/fish) of Lepeophtheirus salmonis on juvenile pink salmon Oncorhynchus gorbuscha collected from the Broughton region (A) and the Skeena Rivers—Chatham Sound region (B). Bars in each year represent samples collected in March, April, May, June, and July of each year. In 2004, no samples were collected in March and April; and in 2007, 2008, and 2009 no samples were collected in July. (Data in (A) are from Jones and Hargreaves (2007, 2009). Data in (B) are from Krkoˇsek et al. (2007a).) (A)

(C)

(B)

(D)

Figure 10.7. Lepeophtheirus salmonis: proportion of copepodid and motile developmental stages on pink (A, C) and chum (B, D) salmon collected from the Broughton region of British Columbia. Bars in each year represent samples collected in March, April, May, June, and July, respectively. In 2004, no samples were collected in March and April; and in 2007, 2008, and 2009, no samples were collected in July. (Data from Jones and Hargreaves 2007, 2009.)

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the timing of emergence of salmon larvae are strongly influenced by temperature during incubation in the gravel. Thus, interannual variation in the timing of pink and chum salmon fry emergence and outmigration is driven by winter temperatures. In addition, surface seawater in the Broughton region was warmer in 2004 compared with either 2003 or 2005, and salinity was higher in 2005 compared with 2004 during the outmigration of the juvenile salmon (Jones and Hargreaves 2007). Precisely how these oceanographic variables interact to affect parasite prevalence and abundance is not clear. Changes in salmon louse management practices on farmed salmon in the Broughton region may have also influenced interannual trends in the levels of L. salmonis observed on juvenile salmon (Jones 2009; Marty et al. 2010).

Temporal Variation Juvenile pink and chum salmon migrate downstream immediately following emergence from gravel spawning beds in late February to early March. At this time they are ca. 35 mm in length and weigh 0.3 g or less. The juveniles occur first in nearshore habitats in large schools and only move out of the nearshore areas once they have attained weights of several grams. Juvenile pink and chum salmon can spend several months in coastal areas before migrating off shore to open ocean (Beamish et al. 2006). During this nearshore residence, they grow rapidly, undergoing shifts in feeding preference and associated changes in behavior and habitat utilization (Heard 1991; Salo 1991). Infections with L. salmonis have been observed on individual salmon of both species at weights less than 0.3 g, indicating that the initial exposure to infection occurs very soon after the fish enter the ocean (Table 10.2; Jones and Nemec 2004; Jones and Hargreaves 2009). Therefore, densities of infective copepodids sufficient to cause measurable infections also occur in this shallow, nearshore habitat. With few exceptions, infections with L. salmonis are similar on juvenile pink and chum salmon during this early migratory phase. In the Broughton region, the prevalence of L. salmonis tends to be low shortly after the salmon enter the ocean, peaks in April to May and declines as the fish leave the study area. It was not clear why between June and July, 2004, while the prevalence on chum salmon decreased from 61 to 24%, prevalence remained from 59 to 69% on pink salmon (Jones and Hargreaves 2007). In the Skeena River—Chatham Sound region of British Columbia, the abundance of L. salmonis appears to spike in July, an effect attributed to new infections transmitted from adult chinook salmon returning to spawn (Krkoˇsek et al. 2007a; Gottesfeld et al. 2009). Infections with L. salmonis on juvenile pink and chum salmon observed in late March predominantly consist of copepodids and first stage chalimus, reflecting recent exposures to the parasite (Figure 10.7). In the Broughton region, the number of these early stages as a percent of all stages ranged from 39.1% (2005) to 95.2% (2007) on pink salmon and from 44.5% (2005) to 83.0% (2006) on chum salmon. By late June, these early stages on pink salmon had declined in abundance, ranging from 0.5% (2007) to 16.2% (2004). Similarly on chum salmon, the early stages in late June ranged from 2.6% (2007) to 38.5% (2004). Conversely, the proportion of more fully developed parasites (motile preadult and adult stages of both genders) was low in March shortly after pink salmon (range: zero in 2007 to 6.7% in 2006) and chum salmon (range: 0.9% in 2005 to 7.0% in 2007) entered the ocean. By June, virtually

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Table 10.2. Prevalence and mean intensity of Lepeophtheirus salmonis on juvenile chum salmon (Oncorhynchus keta) from the Broughton Archipelago. Year

Month

Number of fish

Prevalence (95% CI)

Mean intensity (max.)

2004

May June July

1,136a 890a 484a

71.8 (69.1–74.4)a 60.9 (57.7–64.1)a 23.6 (19.9–27.6)a

13.7 (132) 11.1 (175) 4.1 (58)

2,510

58.6 (56.7–60.6)

12.0 (175)

265 620 660a 459a 312a

25.3 (20.4–30.9) 31.3 (27.7–35.1) 29.7 (26.3–33.3)a 23.7 (20.0–27.9)a 8.0 (5.4–11.7)a

3.3 (11) 2.1 (10) 2.8 (30) 2.3 (12) 1.4 (6)

Annual total

2,316

25.5 (23.8–27.3)

2.4 (30)

2006

502 1,008 1,134 823 604

7.4 (5.4–10.0) 22.0 (19.6–24.7) 16.6 (14.5–18.9) 17.3 (14.8–20.0) 13.2 (10.8–16.2)

1.3 (4) 1.5 (5) 1.2 (5) 1.5 (6) 1.5 (10)

Annual total

4,071

16.4 (15.3–17.6)

1.4 (10)

2007

791 1,489 907 1,456

7.2 (5.6–9.2) 14.6 (12.9–16.5) 36.6 (33.5–39.8) 8.4 (7.1–9.9)

1.3 (3) 1.5 (7) 1.8 (8) 1.6 (7)

Annual total

4,643

15.7 (14.7–16.8)

1.6 (8)

2008

277 583 1,692 1,126

0.7 (0.1–2.6) 1.7 (0.9–3.1) 5.9 (4.9–7.2) 8.8 (7.3–10.6)

1.0 (1) 1.0 (1) 1.6 (8) 1.3 (4)

Annual total

3,678

5.7 (5.0–6.5)

1.4 (8)

2009

253 1,005 1,036 997

0 2.4 (1.6–3.6) 4.4 (3.3–5.9) 3.3 (2.4–4.6)

0 1.0 (1) 1.1 (2) 1.1 (3)

3,291

3.1 (2.6–3.8)

1.1 (3)

Annual total 2005

March April May June July March April May June July March April May June March April May June March April May June

Annual total a Data

previously reported in Jones and Hargreaves (2007).

all parasites on pink salmon had matured to motile stages (range: 82.3% in 2004 to 97.0% in 2007), whereas the proportion of mature stages on chum salmon at this time was significantly lower (range: 34.0% in 2004 to 71.0% in 2007) (Figure 10.7). In the Skeena River—Chatham Sound region, no consistent trend in the proportion of immature parasite stages (copepodid and chalimus 1) was evident in 2004 and 2005, probably due to the overall low abundance of the parasite. In 2006, immature lice accounted for 56% of all stages in May, decreasing to 19.4% in July. The proportion of motile stages in 2006 increased from zero in May to approximately 70% in July (Krkoˇsek et al. 2007a). In coastal British Columbia, infections with L. salmonis were

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acquired shortly after juvenile pink and chum salmon enter the ocean. On the pink salmon, there was evidence that relatively few subsequent new infections occur and that the development of the parasite parallels the rapid growth of the host during the following 3 or 4 months. Chum salmon also grew very quickly during this interval; however, the proportion of immature parasites remained relatively elevated and that of the mature stages relatively depressed. This suggested either that chum salmon continued to acquire new infections during the coastal migration or that a measurable proportion of chum salmon with mature parasites were no longer available for capture. These observations may reflect the difference in susceptibility to L. salmonis between these salmon species (Jones et al. 2007).

Spatial Variation Infections with L. salmonis on juvenile salmon display significant patterns of spatial variation. In the Broughton region, these patterns occur on scales ranging from kilometers to tens of kilometers and appear to be similar on migrating juvenile pink and chum salmon and on resident three-spine sticklebacks (Gasterosteus aculeatus). Jones et al. (2006a) and Jones and Hargreaves (2007) reported that on all three host species, the abundance of L. salmonis was consistently higher in Tribune Channel than in adjacent water bodies in the Broughton region. In addition, in all years of the survey the overall abundance of L. salmonis and that of C. clemensi was higher in the western portion of the region. Generally, spatial trends in L. salmonis infections will reflect differences in the distribution and abundance of ovigerous lice, in the capacity of the water to support the survival, development and advection of planktonic stages, and in the migratory behavior of the juvenile salmon hosts. In addition, salmon farms in well-established locations within the Broughton region are known to support populations of salmon lice (Beamish et al. 2006; Saksida et al. 2007). Some authors argued that spatial patterns of L. salmonis infection were explainable solely by the proximity or recent proximity of host fish to one or more salmon farms (Morton et al. 2004; Krkoˇsek et al. 2005, 2006, 2007b). The challenge faced when interpreting the spatial trends is to reconcile the concurrent effects of proximity to a source of unknown magnitude, along with salinity and temperature gradients and local water currents in the vicinity of the source. Recent evidence indicates that in the Broughton region the number of female L. salmonis on farmed salmon accounts for 98% of the variation in prevalence of the parasite on outmigrating juvenile salmon (Marty et al. 2010).

Overwintering Hosts of L. salmonis The occurrence of a population of ovigerous lice must exist coincident with or shortly before pink and chum salmon are infected with L. salmonis in shallow nearshore waters of the Broughton shortly after entering the ocean in late February and early March. The ovigerous lice, the result of infections sustained in the area since the return of adult salmon the previous autumn fall into three categories: those occurring on wild resident salmonids; on nonsalmonid species, particularly three-spine sticklebacks; and those occurring on farmed Atlantic salmon. Most migratory anadromous Pacific salmon have already spawned by mid- to late-November and surveys of the abundance

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and distribution of resident salmonids over the winter months in the Broughton region did not catch any Pacific salmon (Beamish et al. 2011). Infections with motile L. salmonis were observed on approximately 80% of juvenile coho and chinook salmon collected from Queen Charlotte Strait, west of the Broughton region between November 30 and December 5, 2004 (Beamish et al. 2007). In another study, Trudel et al. (2006) documented the occurrence of L. salmonis on ocean age 1 pink salmon and on ocean age 1 and 1+ chum, coho, and chinook salmon resident in coastal waters from Oregon to Alaska during the winter months. The prevalence and abundance were significantly higher on the larger size class salmon of all species. Together, these studies indicate insufficient evidence to support a role of wild salmonids as a major host population capable of supporting overwintering L. salmonis infections in the Broughton region. The high abundance of sea lice on three-spine sticklebacks was one of the most surprising observations made during the 7-year surveillance of juvenile salmon in the Broughton region. Sticklebacks are common in the shallow nearshore waters of lower Knight Inlet and Tribune Channel during the time that these channels are occupied by migrating juvenile pink and chum salmon. In the Broughton region, infections with L. salmonis and C. clemensi occur on as many as 90% of sticklebacks at intensities that are five- to tenfold higher than occur on the juvenile salmon (Jones and Nemec 2004; Jones et al. 2006a; Jones and Prosperi-Porta 2011). The salmon louse was subsequently reported from sticklebacks in the Skeena River—Chatham Sound region (Krkoˇsek et al. 2007a). More recently, sea lice belonging to another species, Lepeophtheirus cuneifer, were found to be common parasites of the stickleback in the region (Jones and Prosperi-Porta 2011). While finding L. salmonis on sticklebacks was novel, the ecological significance of the finding is not well understood because adult parasites, regardless of species, are rarely found on this host, either in nature or in laboratory infections (Jones et al. 2006b). Thus, it is unlikely that sticklebacks are a significant source of infective copepodids. However, the possibility that motile stages of the parasite are able to relocate from sticklebacks to a more competent host was previously discussed (Jones et al. 2006a). Motile stages of L. salmonis, particularly males, move among hosts (Ritchie 1997) and the recently discovered flipping behavior displayed by motile L. salmonis as it moves from prey to predator host species (Connors et al. 2008) appears to further define conditions under which host transfer occurs. It has been suggested that sticklebacks may be valuable sentinels for the abundance of sea lice that are parasites of commercially valuable species (Jones et al. 2006a; Jones and Prosperi-Porta 2011). Farmed salmon represent the third category, serving as possible overwinter hosts of L. salmonis infections in the Broughton region. The levels of L. salmonis on farmed fish during the time that juvenile pink and chum migrate through the Broughton region can be both high and variable (Beamish et al. 2006; Saksida et al. 2007). Beamish et al. (2011) followed the developing lice infection on three farms that are the farthest up an inlet and the first farms encountered by most of the juvenile pink salmon that are migrating to the open ocean (Figure 10.1B). While sea lice may be observed on the farmed salmon throughout the year, an increase in the infection of the chalimus stage at a rate of 0.03 lice/day occurred in late November at a surface salinity of 30 and a temperature of 7◦ C. An increase in the development of mobile stages followed about 4 weeks later. The timing of the increase in the abundance of gravid lice probably started in late January but

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Figure 10.8. The combined abundances of all species of all stages of sea lice from the DFO study (squares) and the farm staff estimates (circles) at the Sargeaunt Pass farm, compared to the temperature (thick line) and salinity (thin line) readings in the net pen area. The dashed R . Note that temperature and vertical line indicates when the fish were treated with SLICE salinity have the identical scale. R was difficult to precisely document because the farms were treated with SLICE in early February (Figure 10.8). Increased infection of the farms in the winter has been associated by some authors with the increased salinity (Brooks 2005). A salinity higher than 30 may be associated with increased survival of larval and early parasitic stages during the winter, but the hosts of the infections contributing the relatively large numbers of copepodids needed to start the winter infections on the farms had not been identified (Beamish et al. 2011). As mentioned above, sticklebacks carry heavy louse burdens coincident with juvenile salmon migration; however, levels of overwintering infections were not known. Thus, sticklebacks appeared to be a key to identifying the source and timing of the infection. Sticklebacks captured in the trawl surveys in the area in the winter of 2007/2008 were heavily infected with juvenile lice belonging to L. salmonis and C. clemensi, indicating a continuous source of infection. Sticklebacks were also the most abundant species in the trawl catch even though they were small and could easily move through the meshes of most of the net. The R in early January and in March a sample of farmed fish were treated with SLICE 412 three-spine sticklebacks collected nearby included 248 that were infected. The prevalence, intensity, and abundance of all stages of both species of lice were 60.2%, 2.1, and 1.3, respectively. There were 115 L. salmonis of which 94.8% were in the chalimus stage. From these observations, it was concluded that there was a persistent source of infection over the winter that continued after the farms were treated with R . SLICE The ocean circulation in the area is known as an estuarine-type circulation. As freshwater from the rivers flowing into the inlet leave on the surface, there is a compensating in-flowing current below the surface (Freeland and Farmer 1980; Foreman et al. 2006; see Chapter 4 contributed by Stucchi et al.). Beamish et al. (2011) proposed two, but not mutually exclusive, hypotheses to explain the origin of the lice that were infecting the farmed fish in early winter. In the first, the distance and surface flow characteristics of Knight Inlet predicted a source of infection up-inlet. Fall chum salmon return to spawn at Glendale River from mid-October to early-November.

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At this time, surface seawater is approximately 7◦ C and L. salmonis larvae hatched at this temperature require approximately 6.4 days to mature to infective copepodids (Brooks 2005), which then remain viable for approximately 7 days (Tucker et al. 2000). Given a mean westerly surface flow of 10 cm s−1 , particles released at the Glendale River would take ca. 7 days to reach the first salmon farm. Thus, larvae released from L. salmonis infecting chum salmon that are preparing to enter the Glendale River will have an opportunity to molt to copepodids during early November as they drift toward the salmon farm. Annual variation in the temperature, salinity, and estuarine flow characteristics and in the timing, abundance, and infection status of returning fall chum salmon will all influence the size, viability, and timing of the drifting population of L. salmonis larvae. The second hypothesis predicts that larvae were coming into the area in deeper water representing the returning estuarine flow. The deeper water moves up the inlet, past the farms and up encounters a sill that rises to 63 m from the surface. It is well known that this sill results in the deeper water finding its way to the surface and thus can be transported back down the inlet and into the farm area. If this proposed explanation is correct, the source of the lice could be farms farther down the inlet and wild Pacific salmon that were outside of the survey area. Movement into the deeper water may occur during the vertical diurnal behavior displayed by larval L. salmonis. If this is the process that is responsible for the winter infection, it may be important in the spring when juvenile pink salmon are passing the farms and when the estuarine circulation is the strongest. It is interesting that there was a very poor relationship between the number of gravid L. salmonis on the three farms in March, April, and May of 2005, 2006, and 2007, and the number of chalimus stages of L. salmonis on the juvenile pink salmon in the farm area. This surprising lack of correlation indicates that there is considerable variation in the factors affecting the infection of the juvenile pink salmon, that sources additional to the immediate farms are important, or both (Figure 10.9).

Occurrence of C. clemensi on Juvenile Pacific Salmon The body of water separating Vancouver Island from mainland British Columbia is called the Strait of Georgia. The Fraser River is the most significant source of juvenile salmon that migrate into the Strait of Georgia in the spring, including chinook, coho, sockeye, chum, and as mentioned above, pink salmon in even-numbered years. The Gulf Islands form an archipelago in the Strait of Georgia adjacent to the southeast coast of Vancouver Island opposite the mouth of the Fraser River (Figure 10.1A). Several species of juvenile salmon inhabit the waterways surrounding the Gulf Islands in the spring and early summer. Other species of fish occur here coincidentally with the salmon including Pacific herring (Clupea pallasi) and three-spine sticklebacks. The nearest salmon farms are located in Puget Sound, Washington State (U.S.A.), approximately 100 km to the south. A recent study identified infections with C. clemensi on juvenile salmon that had only recently entered the ocean (Beamish et al. 2009). The prevalence (greater than 70%) and abundance of the C. clemensi infections (2.9 lice per fish) were higher than previously reported for this species on salmon. The abundance of C. clemensi exceeded that of L. salmonis on all fish species by approximately 60-fold. Virtually all young-of-the-year and spawning herring concurrently sampled from this area were infected with C. clemensi at abundances almost twice those measured for

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Figure 10.9. The number of gravid L. salmonis on farms in the Broughton region in March, April, and May of 2005, 2006, 2007, and the number of chalimus stages of L. salmonis on the juvenile pink and chum salmon captured within a 30- km radius of these farms. The expected relationship (dashed line) would occur if the lice on the salmon only came from the three farms. The deviation from the expected relationship indicates that there is either considerable variation in the factors affecting the infection of juvenile Pacific salmon or that sources of sea lice, additional to the immediate farms, are important, or both.

the infections on salmon. A study in the Discovery Passage region to the northwest of the Strait of Georgia (Figure 10.1A), found the abundance of C. clemensi on juvenile sockeye salmon exceeded that of L. salmonis by approximately threefold (Morton et al. 2008). These data suggest that C. clemensi is a common parasite of juvenile sockeye salmon in the Strait of Georgia and that herring are a source of this infection. Herring are also a source of C. clemensi in the Broughton Region as they move into

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the area in the winter as adults and rear in the area as juveniles (Beamish et al. 2011). It is possible that these herring are a major source of sea lice.

Impacts of L. salmonis on Juvenile Pacific Salmon Infections on Pacific salmon generally display patterns consistent with enhanced host resistance relative to those observed on salmonids (Salmo spp.) in the Atlantic Ocean (see also the introductory chapter contributed by Hayward et al. for a review of impacts to species of salmonids in the Atlantic Ocean (Salmo spp., Salvelinus alpinus), see Chapter 9 contributed by Finstad and Bjørn). Resistance is defined as the capacity of the host to limit the intensity of sea lice infections. However, controlled laboratory studies have documented significant variation in resistance among salmon species such that coho salmon were found to be most resistant followed by chinook then Atlantic salmon (Johnson and Albright 1992a). Fast et al. (2002) also found coho salmon to be more resistant to L. salmonis than either Atlantic salmon or rainbow trout (Oncorhynchus mykiss) and pink salmon were more resistant than chum salmon (Jones et al. 2006b, 2007). Comparative resistance among host species has been inferred from the number of lice per fish shortly after laboratory exposure, from louse rejection rates on different hosts, from comparative histopathological changes at or near the site of louse attachment, or from measurements of immunological parameters including the expression of proinflammatory genes. It is evident that resistance among some Oncorhynchus spp. is associated with the ability to mount a rapid cutaneous and systemic inflammatory response following exposure (Johnson and Albright 1992b; Fast et al. 2006; Jones et al. 2007). Conversely, susceptible species such as Atlantic salmon appear unable to mount a vigorous cutaneous inflammatory response, possibly because they are sensitive to immunosuppressive factors present in salivary secretions of the parasite (Fast et al. 2006). Furthermore, there was evidence of a stress response in the susceptible chum and Atlantic salmon but not in the more resistant pink salmon, suggesting the possibility of immunosuppression in the former two species (Jones et al. 2007). More recent work has shown that the resistance to L. salmonis is first manifested in pink salmon at a weight of 0.7 g and these small pink salmon remain resistant despite deprivation of food (Jones et al. 2008a, 2008b). Some subsequent researchers estimated impacts to juvenile pink and chum salmon by documenting the proportion of infections that exceeded 1.6 lice per gram. Over 90% of the pink salmon were found to have been at risk when the threshold developed for Salmo spp. was used (Morton and Williams 2004; Morton et al. 2004). Later work compared the mortality of naturally infected pink salmon that had been partitioned into barrels according to level of infection (Morton and Routledge 2005). In the latter study, the majority of fish infected with motile louse stages died and it was concluded that short-term mortality of juvenile pink and chum salmon was increased by infections with one to three lice (Morton and Routledge 2005). Although the latter study provided neither data on fish size nor controls for alternative causes of mortality, this and a related study (Krkoˇsek et al. 2006) concluded a high proportion of the juvenile salmon were at risk of sea lice associated mortality (Krkoˇsek et al. 2007b). Subsequent research has found that host size plays an important role in the resistance of pink salmon to L. salmonis infection. Postemergent pink salmon fry derived

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from two separate stocks were exposed to a range of copepodid concentrations in a controlled laboratory environment when they weighed 0.3 g, 0.7 g, and 2.5 g (Jones et al. 2008b). Following the heaviest exposure, approximately 33% of the 0.3 g fish died, 5% of the 0.7 g fish died, and none of the 2.5 g fish died. In contrast to the studies cited in Chapter 9 contributed by Finstad and Bjorn, over 80% of the lice on the dead pink salmon were chalimus stages. It is evident that susceptibility was greatest in pink salmon weighing less than 0.7 g and that mortality was influenced by the severity of the copepodid challenge. The requirement to consider both size and exposure dose led to a recommendation of 7.5 lice per gram to estimate the threshold of lethal infection density on wild pink salmon weighing less than 0.7 g. In the Broughton region, the percent of these smallest pink salmon with L. salmonis infections that exceeded the threshold was 4.5% in 2005 (n = 956), 0.8% in 2006 (n = 1,097), 0.4% in 2007 (n = 2,079), and 0% in 2008 (n = 1,447) (Jones and Hargreaves 2009). From these data it was possible to conclude that pink salmon were at greatest risk of exceeding the lethal threshold within a month of entering the ocean, but only in those years when the copepodid challenge was sufficiently high.

Impacts of L. salmonis on Populations of Pacific Salmon Morton et al. (2004) reported that a pronounced reduction in adult pink salmon returns to the Broughton region was caused by an infection of sea lice that originated from salmon farms. Krkoˇsek et al. (2007b) went further with a prediction that there could be a 99% collapse of pink salmon populations in the same area in four generations (8 years) due to the mortalities caused by sea lice. These were alarming statements that were taken seriously by the reviewers and editors of the two respected journals that published the papers. The paper by Krkoˇsek et al. (2007b) that modeled a 99% collapse in pink salmon population abundance in four salmon generations excluded the pink salmon production from the Glendale River and spawning channel “because any increased salmon abundances in these rivers confound our estimates of natural changes in abundance.” The inclusion of the salmon produced in the Glendale River and spawning channel is important because they also have to swim by the salmon farms in the area, depending on their migration route, and thus are an excellent indicator of the impacts of sea lice. How the juveniles were produced is not relevant to the impacts of their exposure to the farms and there is laboratory evidence that the effect of sea lice on juvenile pink salmon from the Glendale River and spawning channel is similar to that on Quinsam River pink salmon (Jones et al. 2008b). There is no reason to expect that pink salmon from the populations included in the Krkoˇsek et al. (2007b) paper would be affected differently. The paper by Krkoˇsek et al. (2007b) excluded the “fallow year” 2003 from their analysis. Beamish et al. (2006) was cited to support their decision that the high marine survival of the juvenile pink salmon in 2003 resulted from the fallowing of farms and the creation of a migration corridor that appears to have been interpreted as a safe refuge. Beamish et al. (2006) reported that the levels of sea lice on juvenile pink salmon in 2003 ranged from a prevalence of 13.1% in March to 30.3% in June, with an intensity ranging from 1.6 to 1.9. This level of infection could not have been harmful at the population level for the exceptionally high pink salmon marine survivals to have

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been achieved. Furthermore, Jones and Hargreaves (2007) showed that abundances of L. salmonis on juvenile pink and chum salmon in the Broughton region in 2005 were significantly lower than in 2004, in the absence of prescribed fallowing. Thus, it was not the fallowing of four of 20 farms that was most relevant to the report of the very high marine survival; rather it was the sea lice infection levels. Marty et al. (2010) have examined the relationship between pink salmon escapement in the Broughton region, lice levels on farmed Atlantic and juvenile wild salmon and production biomass of the farmed salmon. They were unable to find a relationship between lice levels, whether on farmed or juvenile wild salmon and the strength of the spawning population. Understanding the impact of sea lice on the dynamics of pink salmon at the population level is difficult because of the poor understanding of the natural dynamics of this species and because of the construction of the spawning channel in the Glendale River. Thus, all information needs to be considered, especially the pink salmon produced in the Glendale River and spawning channel, when attempting to assess the impact of sea lice infections at the population level. The interpretations of current observations are limited by this lack of knowledge. However, in the meantime, fish farming and aquaculture are important industries for British Columbia. An approach of monitoring wild Pacific salmon escapements and continuing to carry out the research that will identify the sources of marine mortalities of Pacific salmon, including the impacts of man-made interventions such as open net-pen aquaculture, hatcheries, spawning channels, and fishing, will help ensure that wild Pacific salmon are managed sustainably at the population level.

References Beamish, R.J., Neville, C., Sweeting, R., and Ambers, N. 2005. Sea lice on adult Pacific salmon in the coastal waters of central British Columbia, Canada. Fisheries Research 76: 198–208. Beamish, R.J., Jones, S., Neville, C., Sweeting, R., Karreman, G., Saksida, S., and Gordon, E. 2006. Exceptional production of pink salmon in 2003/2004 indicates that farmed salmon and wild Pacific salmon can coexist successfully in a marine ecosystem on the Pacific coast of Canada. ICES Journal of Marine Science 63: 1326–1337. Beamish, R.J., Neville, C.M., Sweeting, R.M., Jones, S.R.M., Ambers, N., Gordon, E.K., Hunter, K.L., McDonald, T.E., and Johnson, S.C. 2007. A proposed life history strategy for the salmon louse, Lepeophtheirus salmonis in the subarctic Pacific Ocean. Aquaculture 264: 428– 440. Beamish, R., Wade, J., Pennell, W., Gordon, E., Jones, S., Neville, C., Lange, K., and Sweeting, R. 2009. A large, natural infection of sea lice on juvenile Pacific salmon in the Gulf Islands area of British Columbia, Canada. Aquaculture 297: 31–37. Beamish, R., Gordon, E., Wade, J., Pennell, B., Neville, C., Lange, K., Sweeting, R., and Jones, S. 2011. The winter infection of sea lice on salmon in farms in a coastal inlet in British Columbia and possible causes. Journal of Aquaculture Research and Development 2: 107. doi:10.4172/2155-9546.1000107. Brooks, K.M. 2005. The affects of water temperature, salinity and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada. Reviews in Fisheries Science 13: 177–204. Bugayev, V.F. 2002. On pink salmon (Oncorhynchus gorbuscha) abundance influence on Asian sockeye salmon (Oncorhynchus nerka) abundance. North Pacific Anadromous Fish Commission Document 628: 11.

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Connors, B.M., Krkoˇsek, M., and Dill, L.M. 2008. Sea lice escape predation on their host. Biological Letters 4: 455–457. Fast, M.D., Muise, D.M., Easy, R.E., Ross, N.W., and Johnson, S.C. 2006. The effects of Lepeophtheirus salmonis infections on the stress response and immunological status of Atlantic salmon (Salmo salar). Fish and Shellfish Immunology 21: 228–241. Fast, M.D., Ross, N.W., Mustafa, A., Sims, D.E., Johnson, S.C., Conboy, G.A., Speare, D.J., Johnson, G., and Burka, J.F. 2002. Susceptibility of rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar and coho salmon Oncorhynchus kisutch to experimental infection with sea lice Lepeophtheirus salmonis. Diseases of Aquatic Organisms 52: 57–68. Foreman, M.G.G., Stucchi, D.J., Zhang, Y., and Baptista, A.M. 2006. Estuarine and tidal currents in the Broughton Archipelago. Atmospheric-Oceans 44: 47–63. Freeland, H.J. and Farmer, D.M. 1980. Circulation and energetics of a deep, strongly stratified inlet. Canadian Journal of Fisheries and Aquatic Sciences 37: 1398–1410. Gottesfeld, A.S., Proctor, B., Rolson, L.D., and Carr-Harris, C. 2009. Sea lice, Lepeophtheirus salmonis, transfer between wild sympatric adult and juvenile salmon on the north coast of British Columbia, Canada. Journal of Fish Diseases 32: 45–57. Gritsenko, O.F. (ed) 2002. Atlas of Distribution in the Sea of Different Schools of Pacific Salmon in the Period of Spring-Summer Feeding Migration and Prespawning Migrations, VNIRO. [in Russian] Heard, W.R. 1991. Life history of pink salmon (Oncorhynchus gorbuscha). In: Pacific Salmon Life Histories (eds C. Groot and L. Margolis), pp. 121–230. UBC Press, Vancouver. Hilborn, R. 1992. Institutional learning and spawning channels for sockeye salmon (Oncorhynchus nerka). Canadian Journal of Fisheries and Aquatic Sciences 49: 1126–1136. Johnson, S.C. and Albright, L. J. 1992a. Comparative susceptibility and histopathology of the response of na¨ıve Atlantic, Chinook and coho salmon to experimental infection with Lepeophtheirus salmonis (Copepoda: Caligidae). Diseases of Aquatic Organisms 14: 179–193. Johnson, S.C. and Albright, L.J. 1992b. Effects of cortisol implants on the susceptibility and histopathology of the responses of na¨ıve coho salmon Oncorhynchus kisutch to experimental infection with Lepeophtheirus salmonis (Copepoda: Caligidae). Diseases of Aquatic Organisms 14: 195–205. Jones, S.R.M. 2009. Controlling salmon lice on farmed salmon and implications for wild salmon. CAB Reviews: Perspectives in Agriculture, Veterinary Sciences, Nutrition and Natural Resources 4(048): 1–13. Jones, S.R.M. and Hargreaves, N.B. 2007. The abundance and distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on pink Oncorhynchus gorbuscha and chum O. keta salmon in coastal British Columbia. Journal of Parasitology 93: 1324–1331. Jones, S.R.M. and Hargreaves, N.B. 2009. Infection threshold to estimate Lepeophtheirus salmonis associated mortality among juvenile pink salmon. Diseases of Aquatic Organisms 84: 131–137. Jones, S. and Nemec, A. 2004. Pink Salmon Action Plan: Sea lice on juvenile salmon and on some non-salmonid species caught in the Broughton Archipelago in 2003. Pacific Scientific Advice Review Committee, PSARC Working Paper H2004–105: 83 p. Jones, S.R.M. and Prosperi-Porta, G. 2011. The diversity of sea lice (Copepoda: Caligidae) parasitic on three-spined sticklebacks Gasterosteus aculeatus in coastal British Columbia. Journal of Parasitology 97: 399–405. Jones, S.R.M., Prosperi-Porta, G., Kim, E., Callow, P., and Hargreaves, N.B. 2006a. The occurrence of Lepeophtheirus salmonis and Caligus clemensi (Copepoda: Caligidae) on threespine stickleback Gasterosteus aculeatus in coastal British Columbia. Journal of Parasitology 92: 473–480. Jones, S.R.M., Kim, E., and Dawe, S. 2006b. Experimental infections with Lepeophtheirus salmonis (Krøyer) on threespine sticklebacks, Gasterosteus aculeatus L. and juvenile Pacific salmon, Oncorhynchus spp. Journal of Fish Diseases 29: 489–495.

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Jones, S.R.M., Fast, M.D., Johnson, S.C., and Groman, D.B. 2007. Differential rejection of Lepeophtheirus salmonis by pink and chum salmon: disease consequences and expression of proinflammatory genes. Diseases of Aquatic Organisms 75: 229–238. Jones, S.R.M., Fast, M.D., and Johnson, S.C. 2008a. Influence of reduced feed ration on Lepeophtheirus salmonis infestation and inflammatory gene expression in juvenile pink salmon. Journal of Aquatic Animal Health 20: 103–109. Jones, S., Kim, E., and Bennett, W. 2008b. Early development of resistance to the salmon louse Lepeophtheirus salmonis (Krøyer) in juvenile pink salmon Oncorhynchus gorbuscha (Walbaum). Journal of Fish Diseases 31: 591–600. Krkoˇsek, M., Lewis, M.A., and Volpe, J.P. 2005. Transmission dynamics of parasitic sea lice from farm to wild salmon. Proceedings of the Royal Society B 272: 689–696. Krkoˇsek, M., Lewis, M.A., Morton, A., Frazer, L.N., and Volpe, J.P. 2006. Epizootics of wild fish induced by farm fish. Proceedings of the National Academy of Science USA 103: 15506–15510. Krkoˇsek, M., Gottesfeld, A., Proctor, B., Rolston, D., Carr-Harris, C., and Lewis, M.A. 2007a. Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations. Proceedings of the Royal Society B 274: 3141–3149. Krkoˇsek, M., Ford, J.S., Morton, A., Lele, S., Myers, R.A., and Lewis, M.A. 2007b. Declining wild salmon populations in relation to parasites from farm salmon. Science 318: 1772– 1775. Levin, P.S., Zabel, R.W., and Williams, J.G. 2001. The road to extinction is paved with good intentions: negative association of fish hatcheries with threatened salmon. Proceedings of the Royal Society of London B, Biological Science 268: 1153–1158. Marty, G.D., Saksida, S.M., and Quinn II, T.J. 2010. Relationship of farm salmon, sea lice, and wild salmon populations. Proceedings of the National Academy of Sciences of the U.S.A. Meffe, G.K. 1992. Techno-arrogance and halfway technologies: Salmon hatcheries on the Pacific Coast of North America. Conservation Biology 6: 350–354. Morton, A. and Routledge, R. 2005. Mortality rates for juvenile pink Oncorhynchus gorbuscha and chum O. keta salmon infested with sea lice Lepeophtheirus salmonis in the Broughton Archipelago. Alaska Fisheries Research Bulletin 11: 146–152. Morton, A.B. and Williams, R. 2004. First report of a sea louse, Lepeophtheirus salmonis, infestation on juvenile pink salmon, Oncorhynchus gorbuscha, in nearshore habitat. Canadian Field-Naturalist 117: 634–641. Morton, A., Routledge, R., and Krkoˇsek, M. 2008. Sea louse infestation in wild juvenile salmon and Pacific herring associated with fish farms off the east-central coast of Vancouver Island, British Columbia. North American Journal of Fisheries Management 28: 523–532. Morton, A., Routledge, R., Peet, C., and Ladwig, A. 2004. Sea lice (Lepeophtheirus salmonis) infection rates on juvenile pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon in the nearshore marine environment of British Columbia, Canada. Canadian Journal of Fisheries and Aquatic Sciences 61: 147–157. Nagasawa, K. 1987. Prevalence and abundance of Lepeophtheirus salmonis (Copepoda: Caligidae) on high-seas salmon and trout in the North Pacific Ocean. Nippon Suisan Gakkaishi 53: 2151–2156. Nagasawa, K. 2001. Annual changes in the population size of the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae) on high-seas Pacific salmon (Oncorhynchus spp.) and relationship to host abundance. Hydrobiologia 453/454: 411–416. Nagasawa, K., Ishida, I., Ogura, M., Tadokoro, K., and Hiramatsu, K. 1993. The abundance of distribution of Lepeophtheirus salmonis (Copepoda: Caligidae) on six species of Pacific salmon in offshore waters of the North Pacific Ocean and Bering Sea. In: Pathogens of Wild and Farmed Fish: Sea Lice (eds G.A. Boxshall and D. Defaye), pp. 166–178. Ellis Horwood, London. Parker, R.R. and Margolis, L. 1964. A new species of parasitic copepod, Caligus clemensi sp. nov. (Caligoida: Caligidae), from pelagic fishes in the coastal waters of British Columbia. Journal of the Fisheries Research Board of Canada 21: 873–889.

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