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

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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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Contents

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

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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 1.4. The orientation and bottom depths for the Hardangerfjord numerical fjord model grid with an 800-m horizontal resolution.

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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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Introduction: Lepeophtheirus salmonis— A Remarkable Success Story

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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 (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 ( 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 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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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



64

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Salmon Lice

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

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