American Society Symposium 44:529–537, 2004 © 2004 by the American Fisheries Society

Evaluating and Understanding Fish Health Risks and Their Consequences in Propagated and Free-Ranging Fish Populations

CHRISTINE M. MOFFITT1 USGS, Cooperative Fish and Wildlife Research Unit Department of Fish and Wildlife Resources, University of Idaho Moscow, Idaho 83844-1136, USA

ALF H. HAUKENES2 Department of Fish and Wildlife Resources, University of Idaho Moscow, Idaho 83844-1136, USA

CHRISTOPHER J. WILLIAMS Department of Statistics, University of Idaho, Moscow, Idaho 83844-1104, USA

Abstract.— managers and resource conservationists are increasingly interested in understand- ing the fish health and disease risks of free-ranging fishes and whether propagated fishes or features and practices used at fish culture facilities pose a health risk to free-ranging populations. Disease agents are present in most both captive and all free-ranging fish populations, but the consequences and extent of in free-ranging populations are often difficult to measure, control, and understand. Sampling methods, protocols, and assay techniques developed to assess the health of captive populations are not as applicable for assessments of free-ranging fishes. The use of chemicals and therapeutics to control diseases and parasites in propagated fishes likely reduces the risk of introducing specific pathogens into the environment, but control measures may have localized effects on the environment surrounding fish culture facilities. To understand health risks of propa- gated and free ranging fishes, we must consider fish populations, culture facilities, fish releases, and their interactions within the greater geospatial features of the aquatic environment.

Introduction: Quantifying Diseases in more readily monitored over time because individuals Free Ranging and Propagated Fish in the population are accessible. However, measuring and understanding the disease status of free-ranging In this paper, we review some of the challenges of populations, and measuring the impact of diseases in a measuring and interpreting the health status of propa- population, are difficult as sick fish are often removed gated and free-ranging fish populations. We propose a by predators, the populations are dispersed across space, framework to improve interpretations of the risks of and portions of the population may migrate to other disease and disease control in propagated and free- areas bringing new diseases and parasites with them. ranging fish populations. In propagated fishes, stresses associated with cap- We know much more about diseases and disease tivity and the close proximity of individuals in the processes of fish held in captivity than in free-ranging rearing environment can increase the vulnerability of fishes. The disease status of captive populations can be fish to and result in pathogen amplification and increased opportunities for disease transmission. 1 E-mail: [email protected] On the other hand, in controlled rearing systems, wa- 2 Present address: University of Alaska-Fairbanks, School of ter treatments and physical modifications can improve Fisheries and Ocean Sciences, Fishery Industrial Technology water quality and limit the exposure of propagated Center, Kodiak, Alaska 99615, USA fish to other fish, invertebrates, or pathogens. Cov- 529 530 MOFFITT ET AL. ered rearing containers can exclude predators and other affect pathogen development, survival rates, transmis- biological or physical vectors that may transmit patho- sion, and susceptibility (Harvell et al. 2002). gens or serve as intermediate hosts. Biological, physi- It is likely that the spread of whirling disease, cal, and chemical control measures are often used in caused by cerebralis, was through planting fish culture to modify water quality and to enhance of pathogen positive fish by management agencies or resistance to infectious diseases and reduce pathogen by unapproved releases of positive fish (Nehring and loads and their effect on propagated fish (Winton Walker 1996; Bartholomew and Reno 2002). With 2001). Treatment of hatchery effluents containing , there are other habitat compo- chemicals, nutrients, and pathogens reduces the im- nents that are independent of the fish host that can be pact of culture systems on the receiving environment affected by anthropogenic activities such as increased (Aitcheson et al. 2001; Boyd 2003; MacMillan et al. siltation, impounded waters, and other changes that 2003; Tacon and Forster 2003). change the host environment and pathogen relation- Management decisions regarding the siting of fish ships for native species and can multiply the risks of culture facilities are often made with a goal of mini- infections (Baldwin et al. 2000; Hiner and Moffitt mizing the risks of disease in the propaged fish species 2002; Kerans and Zale 2002). through water source and quality. Fish diseases are Infectious diseases within a population can be part of natural population dynamics (Coutant 1998), modeled with epidemiological models of a popula- and studies have documented a variety of parasites, tion, such as those presented by Anderson and May viral, fungal, and bacterial pathogens in free-ranging (1979) and May and Anderson (1979), to include fishes (e.g., Yamamoto 1975; Grischkowsky and dynamic processes for the number of susceptible, im- Amend 1976; Ellis et al. 1978; Deardorff and Kent mune, and removed individuals (Reno 1998). Pat- 1989; Sakai et al. 1992; Mellergaard and Spanggaard terns of host density and distribution of asymptomatic 1997; Baldwin et al. 1998). carriers are critical limitations in these models. If there Stresses in any environment will increase the like- are intermediate hosts or vectors modeling disease rela- lihood of disease to be expressed (Snieszko 1974; tionships is more complex (Hiner and Moffitt 2002; Wedemeyer 1996; Mesa et al. 2000). No population Kerans and Zale 2002). The disease process in free- of free-ranging fishes can be considered free from the ranging populations has been modeled for the fungal stress of human and habitat alterations associated with parasite Ichthyophonus hoferi in the Atlantic global climate change, effluents from human and in- (also known as North sea herring) Clupea harengus dustrial sewage and non point source discharges, har- (Patterson 1996; Mellergaard and Spanggaard 1997), vest, alterations of flow regimes, and habitat (Rapport using inference from samples of fish populations and et al. 1982; Krishnakumar et al. 1999; Arkoosh et al. separating natural and parasite induced mortality from 2001; Harvell et al. 2002). mortality (Haddon 2001). Interest in diseases in fish and wildlife popula- Fish pathogens can spread in both free-ranging tions has increased. Emerging diseases defined by and captive populations, but few studies have made Kiesecker et al. (2004) are those that have increased in observations over a wide geography and over any length incidence, virulence, or geographic range; have shifted of time (Moffitt et al. 1998; LaPatra 2003). A limited hosts; or have recently evolved new strains. Diseases number of studies provided assessments of a selected emerge when a new pathogen is introduced into a parasite, virus, or bacteria in free-ranging and captive naïve host population or when an external factor some- populations on a larger geographic scale (Ching and how increases the vulnerability of current hosts. Munday 1984; Baldwin et al. 1998; Kent et al. 1998; Some exotic pathogens can produce serious health Bruneau et al. 1999a; Kurath et al. 2003; Murray et effects in both propagated and free ranging stocks al. 2003). (Naylor et al. 2001). Movement of water or fish can Propagated fishes have been documented respon- spread exotic pathogens (Lilley et al. 1997, 1998; sible for the spread of some fish diseases especially Blazer et al. 1999; Goodwin 2002). Harvell et al. when the surrounding populations were naïve. Johnsen (1999) reviewed the disease outbreaks in the marine and Jensen (1994) studied the spread of the disease environment and illustrated new diseases emerging furunculosis in salmonids in Norwegian fish farms through host or range shifts of known pathogens. They and rivers and attributed this introduction of infected associated these shifts with climate and human activi- hatchery rainbow mykiss from ties that accelerate global transport of species. Climate Denmark. From 1985 to 1992, the number of cases change poses many potential synergisms that could of furunculosis at marine and freshwater farms in- EVALUATING AND UNDERSTANDING FISH HEALTH RISKS AND THEIR CONSEQUENCES 531 creased from 16 to 550, and the authors attributed techniques and sampling protocols can show different the rapid spread to escaped fish from infected farms trends over time. Murray et al. (2003) monitored Scot- and transportation of infected fish between farms. tish farms from 1996 to 2001 for infectious pancre- In most circumstances, the pathogens that occur atic necrosis virus (IPNV) in Atlantic . They in cultured fishes are also present in the free-ranging used culture and enzyme-linked immunosorbent fishes of the region. Noakes et al. (2000) reviewed the assays on pooled samples and reported that prevalence disease cases in salmon propagation facilities over a 22- increased over time, but they did not adjust for effect year period and found that length of time in captive of pooled samples, and as a consequence, true preva- conditions was proportional to the risk of infection of lence was likely overestimated (Williams and Moffitt any disease. Noakes et al. (2000) concluded that 2001). pathogens found in farmed salmon were of the same Inference from detection must consider whether suite as those in free-ranging in British Co- the presence of clinical disease is determined or merely lumbia. Meyers et al. (1993) evaluated the prevalence the disease agent (LaPatra 2003). Cell culture often of bacterial kidney disease in wild and hatchery stocks shows different results from genetic assays. Dixon et in Alaska to find that the pathogen was widespread in al. (2003) reported results of cell culture of hemor- propagated and free ranging or wild stocks. rhagic septicemia virus (VHSV) in selected marine Bakke and Harris (1998) reviewed the diseases species collected off the coast of the United Kingdom and parasites of wild populations and from 1995 to 1998. For two of these years, they ana- found that the myxozoans, furunculosis and Gyrodac- lyzed fish with both cell culture and polymerase chain tylus salaris, and Argulus sp. were the pathogens most reaction (PCR). Although few of the fish examined likely to threaten both wild and managed stocks, but showed gross external signs of disease, and few were little was known on their impact. They noted that the positive by tissue culture, they found diverse transfer of sea lice (Argulus) was enhanced by groups for the pathogen at sites. All inference was the close proximity of fish in net pens. limited by small sample sizes and lack of agreement Understanding the prevalence and impact of dis- between the two methods of interrogation. eases in most natural populations is complicated by a Scientists and managers are often not prepared lack of long-term monitoring, consistent sampling ahead of time with adequate data sets and sampling methods, and adequate sampling designs (Williams designs for management decisions regarding the im- and Moffitt 2001, 2003). Even when sampling is portance and risks of emerging diseases. Historical planned, a variety of techniques are used to search for records are often problematic, as they frequently rep- the disease agent or disease because of availability of resent an array of assay techniques and sampling de- laboratory resources, costs, and study objectives. Num- signs. Intelmann (2001) compiled more than 18,000 bers of fish sampled for a disease agent is critical to the records of fish health testing by public agencies in level of inference that can be extracted. Assays results the states of , Idaho, , , and can be simply positive or negative or they may show a from agency records. He found that the range of response that helps to describe the intensity most extensive data were for assays of M. cerebralis, of infection. the cause of salmonid whirling disease, and these records Even within one species of fish, the inference constituted 32% of the total samples of free-ranging from samples is limited by several criteria: (1) Are mea- fishes. The next most commonly reported fish patho- sures made of the agent or of the disease that results? gen in these databases was , the (2) Are samples from one point in time or over time? cause of furunculosis. Using these databases for retro- (3) How many samples are collected and analyzed? (4) spective analyses when these data were not collected for Are samples individual or pooled? (5) What are the that purpose could be risky. For example, many of the sensitivity and specificity of methods used to find the assessments of M. cerebralis were made on fish samples disease or agent? that were pooled, and sometimes the size of the pool Interpretations made from data collected at dif- was not reported. Pooled samples are appropriate to ferent times of the year can affect the inference. Dou- reduce effort of analysis and screen greater number of glas-Helders et al. (2003) measured , but number of fish pooled is essential to calcu- in the summer and winter and at various distances late prevalence. from sea cage and farming sites. Water temperature, Techniques and sample sizes recommended by salinity, and availability of food were major factors the American Fisheries Society Blue Book (Thoesen affecting the distribution of disease. Different assay 1994; American Fisheries Society Fish Heath Section 532 MOFFITT ET AL.

2003) were developed primarily for monitoring propa- (Kerry et al. 1994; DePaola et al. 1995; Capone et al. gated fishes with a concern for keeping certain high- 1996; Weston et al. 1998). The fates of other drugs risk pathogens out of culture systems. With pooled such as sulfadimethoxine and ormetoprim have been samples, the confidence of estimates decreases when documented in the natural environment and in vitro prevalence increases. Williams and Moffitt (2001) (Cooper et al. 1993; Bakal and Stoskopf 2001). provided a sample program to calculate maximum like- critics have written in popular lit- lihood based confidence intervals for pooled samples. erature and reports criticizing chemical and antibiotic However, the confidence of these estimates is affected treatments as a risk to the environment and human by the testing assay specificity and sensitivity safety (Goldburg and Triplett 1997; Benbrook 2002). (Thorburn 1996; Bruneau et al. 1999b). Williams However, chemical treatments for bacterial and para- and Moffitt (2003) used Gibbs sampling and Baye- sitic diseases are highly regulated in the United States sian analysis to estimate the prevalence and confidence and Canada, and in contrast with other farm- limits from samples with imperfect sensitivity and speci- ing (McEwen and Fedorka-Cray 2002), antibiotics ficity to illustrate how the confidence of estimates is are not used as growth promoters. influenced by these parameters. Incorporation of in- Vaccines are an important tool used to control fish formation on sensitivity and specificity are possible disease amplification in propagated fishes and when with known laboratory data or sometimes with expert effective vaccines reduce antibiotic use. When the At- opinion if no data are available. lantic salmon industry developed in Norway in the Recently genetic typing allows scientists to deter- 1980s, antibiotic use increased with production (Grave mine the origin of specific strains of pathogens in the et al. 1990). However, as the control of most bacterial geographical landscape (Troyer et al. 2000; St-Hilaire diseases was accomplished with vaccine programs (Grave et al. 2002; Kurath et al. 2003). The increased use of et al. 1999; Horsberg 2001), use of oxytetracycline gene sequences in larger data sets can show likely routes dropped from 5,014 kg in 1989 to 25 kg in 1999. Use of transfer from one location to another, and similarity of oxolenic acid in Norway also dropped from 12,630 of strains can be used to resolve questions of mutation kg to 494 kg in the same period. and radiation, but assessment of disease will still need Antibiotic therapy can increase the frequency of to be made with clinical observations. resistant bacteria in and surrounding a treated facility, and transfer of resistant bacteria and resistance Disease Control in Propagated Fishes from aquaculture environments to humans may occur through consumption of antimicrobial resistant bacte- In captive rearing, control of diseases is accomplished ria in fish or associated products (Inglis et al. 1993; by a combination of management techniques, includ- Andersen and Sandaa 1994; Sandaa and Enger 1996; ing biosecurity management practices, use of vaccines, Petersen et al. 2002). In food animals, antimicrobial chemicals, and application of therapeutic substances resistance has emerged in zoonotic enteropathogens such (Plumb 1999; Winton 2001). Controlling the am- as Salmonella spp. and Camphylobacter spp. and in com- plification of disease agents in propagated fishes re- mensal bacteria such as Escherichia coli, but prevalence duces the risks of releasing fish pathogens into the of resistance varies (McEwen and Fedorka-Cray 2002). environment from effluents or stocking. Recent reports provided evidence of resistant and multi- In the United States, only a few therapeutants drug resistant strains in aquaculture and the aquatic are approved for use in aquaculture, including one environment (Sandaa et al. 1992; Rhodes et al. 2000; anesthetic, a hormone (gonadotropin), a fungus and Schmidt et al. 2001; Yoo et al. 2003). However, the parasite treatment (formalin), and three antibiotic feed lack of a good database and monitoring effort limits the additives used to control various gram negative bacte- inference from these observations. rial infections: oxytetracycline, sulfadimethoxine Understanding the effects of chemotherapeutics ormetoprim, and sulfamerizine (Winton 2001). Other on the bacterial ecology of fish and fish rearing waters antibiotics and chemical treatments used are available has received little attention (DePaola et al. 1995). There in a limited manner with veterinary extra label author- are no established and validated protocols for collect- ity or Investigational New Animal Drug (INAD) per- ing and processing samples, and because of a hetero- mits provided by the U.S. Food and Drug Admini- geneous environment, improper sampling can lead to stration. In all of aquaculture, the most widespread misleading conclusions (Zitko 2001). antibiotic used is oxytetracycline. The environmental At the University of Idaho, our effort to gain fate and effects of this compound have been described regulatory approval of erythromycin to control - EVALUATING AND UNDERSTANDING FISH HEALTH RISKS AND THEIR CONSEQUENCES 533 nid bacterial kidney disease through a regional INAD ing fishes require also that hatchery locations and re- permit (Moffitt and Haukenes 1995; Moffitt 1998) leases be placed within the greater geographical context mandates that we keep records of drug use. From 1992 of aquatic systems. McArthur and Tuckfield (2000) to 2001, the annual use of erythromycin at the 60– described spatial patterns in antibiotic resistance in two 100 participating hatcheries ranged from 916 to 1,799 Georgia streams and found the highest frequency of kg. Most use was for O. tshawytscha resistance in the tributary draining a nuclear reactor and juveniles released as smolts in the Columbia River ba- industrial complex and were unrelated to . sin. By adjusting use during this decade by the number In human epidemiology, spatial tools are being of salmon smolts released in the Columbia basin, these applied to investigate clustering of diseases and ex- data can be placed in a spatial context to show drug use planatory relationships (Olsen et al. 1996; Lawson scattered throughout the drainage (Figure 1). 2001). To adequately assess risks, information from a Effluents from fish propagation facilities must be variety of sources is needed to create integrated placed within a context relative to other point and geospatial databases that provide details about the nonpoint effluents that introduce a wide array of chemi- environment surrounding fish culture facilities. Us- cals through sewage, and from runoff from farm animal ing these databases, we need to begin to apply meth- production facilities. Kolpin et al. (2002) found eryth- ods and models of spatial epidemiology to fish in romycin or its metabolites present in 21.6% of all water aquatic ecosystems. Only if the cumulative effects of samples tested across the nation. Evaluating and under- multiple alterations are considered can the correct risks standing the health risks for propagated and free-rang- to free-ranging populations be calculated.

Figure 1. Patterns of erythromycin use (mg erythromycin /yearling Chinook salmon released) at fish hatcheries in the Columbia River basin in Washington, Oregon, and Idaho. The extent of the basin in the United States is outlined with a dashed line. The annual erythromycin use was calculated for 1991–2001 from records maintained at the University of Idaho under INAD 6013. Use patterns for hatcheries within individual hydrologic units of the drainage are coded as one of three categories: <50 (slight gray), <100 (gray), and >100 (black) mg/fish released. The numbers of fish released at hatcheries were obtained from the Fish Passage Center and distributed via the internet by the School of Fisheries, University of Washington (www.cqs.washington.edu/dart/dart.html). The yearling Chinook salmon releases in the spring were appropriately lagged to correspond with erythromycin use the previous year of hatchery rearing. 534 MOFFITT ET AL.

Acknowledgments tions. Journal of Veterinary Diagnostic Investiga- tion 12:312–321. This is contribution 991 of the Idaho Forestry Wild- Bartholomew, J. L., and P. W. Reno. 2002. The history life and Range Experiment Station. Support was pro- and dissemination of whirling disease. Pages 3–24 vided in part by the Fish and Wildlife Program, in J. L. Bartholomew and J. C. Wilson, editors. Bonneville Power Administration and by the Depart- Whirling disease: reviews and current topics. Ameri- ment of Agriculture, Western Regional Aquaculture can Fisheries Society, Symposium 29, Bethesda, Center. Kara Anlauf, University of Idaho, provided Maryland. assistance with graphics. Benbrook, C. M. 2002. Antibiotic drug use in U.S. aquac- ulture. The Northwest Science and Environmental Policy Center, Sandpoint, Idaho. References Blazer, V. S., W. K. Vogelbein, C. L. Densmore, E. B. Aitcheson, S. J., J. Arnett, K. R. Murray, and J. Zhang. May, J. H. Lilley, and D. E. Zwerner. 1999. 2001. Removal of aquaculture therapeutants by car- Aphanomyces as a cause of ulcerative skin lesions bon adsorption 2: multicomponent adsorption and of menhaden from Chesapeake Bay tributaries. Jour- the equilibrium behaviour of mixtures. Aquaculture nal of Aquatic Animal Health 11:340–349. 192:249–264. Boyd, C. E. 2003. Guidelines for aquaculture effluent American Fisheries Society Fish Health Section. 2003. management at the farm-level. Aquaculture 226:101– Suggested procedures for the detection and identifi- 112. cation of certain finfish and shellfish pathogens, Bruneau, N. N., M. A. Thorburn, and R. M. W. (Blue Book), 5th edition. American Fisheries Soci- Stevenson. 1999a. Occurrence of Aeromonas ety, Bethesda, Maryland. salmonicida, Renibacterium salmoninarum, and Anderson, R. M., and R. M. May. 1979. Population infectious pancreatic necrosis virus in Ontario salmo- biology of infectious diseases: part I. Nature (Lon- nid populations. Journal of Aquatic Animal Health don) 280:361–367. 11:350–357. Andersen, S. R., and R. A. Sandaa. 1994. Distribution Bruneau, N. N., M. A. Thorburn, and R. M. W Stevenson of tetracycline resistance determinants among gram- 1999b. Use of the Delphi method to assess expert negative bacteria isolated from polluted and unpol- perception of the accuracy of screening test system luted sediments. Applied Environmental Microbi- for infectious pancreatic necrosis virus and infec- ology 60:908–912. tious hematopoeitic necrosis virus. Journal of Arkoosh, M. R., E. Casillas, E. Clemons, P. Huffman, Aquatic Animal Health 11:139–147. A. J. Kagley, T. Collier, and J. E. Stein. 2001. In- Capone, D. G., D. P. Weston, V. Miller, and C. Shoe- creased susceptibility of juvenile chinook salmon maker. 1996. Antibacterial residues in marine sedi- (Oncorhynchus tshawytscha) to disease after expo- ments and invertebrates following chemotherapy in sure to chlorinated and aromatic compounds found aquaculture. Aquaculture 145:55–75. in contaminated urban estuaries. Journal of Aquatic Ching, H. L., and D. R. Munday. 1984. Geographic and Animal Health 13:257–268. spatial distribution of the infectious stage of Bakke, T. A., and P. D. Harris. 1998. Diseases and para- Ceratomyxa Shasta Noble, 1950, a Myxozoan sites in wild Atlantic salmon (Salmo salar) popula- salmonid pathogen in the Fraser River system. Ca- tions. Canadian Journal of Fisheries and Aquatic nadian Journal of Zoology 62:1075–1080. Sciences 55(Supplement 1):247–266. Cooper, R. K., C. E. Starliper, E. B. Shotts, and P. W. Bakal, R. S., and M. K. Stoskopf. 2001. In vitro stud- Taylor. 1993. Comparison of plasmids isolated from ies of the fate of sulfadimethoxine and ormetoprim Romet-30 resistant Edwardsiella ictaluri and in the aquatic environment. Aquaculture 195:95– tribrissen resistant Escherichia coli. Journal of 102. Aquatic Animal Health 5:9–15. Baldwin, T. J., J. E. Peterson, G. C. McGhee, K. D. Coutant, C. C. 1998. What is “normative” for fish patho- Staigmiller, E. S. Motteram, C. C. Downs, and D. gens? A perspective on the controversy over inter- R. Stanek. 1998. Distribution of Myxobolus actions between wild and cultured fish. Journal of cerebralis in salmonid fishes in Montana. Journal Aquatic Animal Health 10:101–106. of Aquatic Animal Health 10:361–371. Deardorff, T. L., and M. L. Kent. 1989. Prevalence of Baldwin, T. J., Vincent, E. R., Silflow, R. M., and D. R. larval simplex in pen-reared and wild- Stanek. 2000. Myxobolus cerebralis infection in rain- caught salmon (Salmoniidae) from Puget Sound, bow trout (Oncorhynchus mykiss) and Washington. Journal of Wildlife Diseases 25:416– (Salmo trutta) exposed under natural stream condi- 419. EVALUATING AND UNDERSTANDING FISH HEALTH RISKS AND THEIR CONSEQUENCES 535

DePaola, A., J. T. Peeler, and G. E. Rodrick. 1995. Ef- Hiner, M., and C. M. Moffitt. 2002. Modeling Myxobolus fect of oxytetracycline-medicated feed on antibiotic cerebralis infections in trout: associations with habi- resistance of gram-negative bacteria in catfish ponds. tat variables. Pages 167–179 in J. L. Bartholomew Applied and Environmental Microbiology 61:2335– and J. C. Wilson, editors. Whirling disease: reviews 2340. and current topics. American Fisheries Society, Dixon, P. F., S. Avery, E. Chambers, S. Feist, H. Symposium 29, Bethesda, Maryland. Mandhar, L. Parry, D. M. Stone, H. K. Strmmen, J. Horsberg, T. 2001. Food safety aspects of aquaculture K. Thurlow, C. T Lui, and K. Way. 2003. Four products in Norway. Speaking notes from How to years of monitoring for viral haemorrhagic septi- Farm the Seas: the science, economics and politics caemic virus in marine waters around the United of aquaculture. 28–30 September 2000, Montague, Kingdom. Diseases of Aquatic Organisms 54:175– PEI Canada. Atlantic Institute of Market Studies, 186. Halifax, Nova Scotia. Douglas-Helders, G. M., D. P. O-Brien, B. E. Johnsen, B. O., and A. J. Jensen. 1994. The spread of McCorkell, D. Zilberg, A. Gross, J. Carson, and B. furunculosis in salmonids in Norwegian rivers. Jour- F. Nowak. 2003. Temporal and spatial distribution nal of Fish Biology 45:47–55. of paramoebae in the water column – a pilot study. Inglis, V., E. Yimer, E. J. Bacon, and S. Ferguson. 1993. Journal of Fish Diseases 26:231–240. Plasmid-mediated antibiotic resistance in Aeromo- Ellis, R. W., A. J. Novotny, and L. W. Harrell. 1978. nas salmonicida isolated from Atlantic salmon, Case report of kidney disease in a wild chinook Salmo salar L., in Scotland. Journal of Fish Dis- salmon, Oncorhynchus tshawytscha, in the sea Jour- ease 16:593–599. nal of Fish Diseases 14:120–123. Intelmann, S. S. 2001. A retrospective summary of the Goldburg, R., and T. Triplett. 1997. Murky waters: en- pathogen and disease monitoring of salmonid fishes vironmental effects of aquaculture in the United across the intermountain west states. Master’s the- States. The Environmental Defense Fund, Wash- sis. University of Idaho, Moscow. ington D.C. Kent, M. L., G. S. Traxler, D. Kieser, J. Richard, S. C. Goodwin, A. E. 2002. First report of spring viremia of Dawe, R. W. Shaw, G. Prosperi-Porta, J. Ketcheson, carp virus (SVCV) in North America. Journal of and T. P. T. Evelyn. 1998. Survey of salmonid patho- Aquatic Animal Health 14:161–164. gens in ocean-caught fishes in British Columbia, Grave, K., M. Englestad, N. E. Soli, and T. Hastein. Canada. Journal of Aquatic Animal Health 10:211– 1990. Utilization of antibacterial drugs in salmonid 219. farming in Norway during 1980–1988. Aquacul- Kerans, B. L., and A. V. Zale. 2002. The ecology of ture 86:347–358. Myxobolus cerebralis. Pages 145–166 in J. L. Grave, K., E. Lingaas, M. Bangen, and M. Ronning. Bartholomew and J. C. Wilson, editors. Whirling 1999. Surveillance of the overall consumption of disease: reviews and current topics. American Fish- antibacterial drugs in humans, domestic animals and eries Society, Symposium 29, Bethesda, Maryland. farmed fish in Norway in 1992 and 1996. Journal Kerry, J., M. Kiney, R. Coyne, D. Cazabon, S. of Antimicrobial Chememotherapy 43:243–252. NicGabhainn, and P. Smith. 1994. Frequency and Grischkowsky, R. S., and D. F. Amend. 1976. Infec- distribution of resistance to oxytetracycline in mi- tious hematopoietic necrosis virus: prevalence in cro-organisms isolated from marine fish farm sedi- certain Alaskan , Oncorhynchus ments following therapeutic use of oxytetracycline. nerka. Journal of the Fisheries Research Board of Aquaculture 123:43–54. Canada 33:186–188. Kiesecker, J. M. L. K Belden, K. Shea, and M. J. Rubbo. Haddon, M. 2001. Modeling and quantitative methods 2004. Amphibian decline and emerging disease. in fisheries. CRC Press, Boca Raton, Florida. American Scientist 92:138–147. Harvell, C. D., K. Kim, J. M. Burkholder, R. R. Colwell, Kolpin, D. W., E. T. Furlong, M. T. Meyer, E. M. P. R. Epstein, D. J. Grimes, E. E. Hofmann, E. K. Thurman, S. D. Zaugg, L. B. Barber, and H. T. Lipp, A. D. M. E. Osterhaus, R. M. Overstreet, J. Buxton. 2002. Pharmaceuticals, hormones, and other W. Porter, G. W. Smith, and G. R. Vasta. 1999. organic wastewater contaminants in U. S. stream, Emerging marine diseases – climate links and an- 1999–2000: a national reconnaissance Environmen- thropogenic factors. Science 285:1505–1510. tal Science and Technology 36:1202–1211. Harvell, C. D., C. E. Mitchell, J. R. Ward, S. Altizer, A. Krishnakumar, P. K. E. Casillas, R. G. Snider, A. N. P. Dobson, R. S. Ostfeld, and M. D. Samuel. 2002. Kagley, and U. Varanasi. 1999. Environmental con- Climate warming and disease risks for terrestrial taminants and the prevalence of hemic neoplasia (leu- and marine biota. Science 296:2158–2162. kemia) in the common mussel (Mytilus edulis 536 MOFFITT ET AL.

complex) from Puget sound, Washington, USA. Moffitt, C. M. 1998. Field trials of investigational new Journal of Invertebrate Pathology 73:135–146. animal drugs. Veterinary and Human Toxicology Kurath, G., K. A. Graver, R. M. Troyer, E. J. 40:48–52. Emmenenegger, K. Einer-Jensen, and E. D. Ander- Moffitt, C. M., and A. H. Haukenes. 1995. Regional son. 2003. Phylogeography of infectious haemato- investigational new animal drug permits for eryth- poietic necrosis virus in North America. Journal of romycin as a feed additive and injectable drug. Pro- General Virology 84:803–814. gressive Fish-Culturist 57:97–101. LaPatra, S. E. 2003. The lack of scientific evidence to Moffitt, C. M., B. C. Stewart, S. E. LaPatra, R. D. support the development of effluent limitations Brunson, J. L. Bartholomew, L. E. Peterson, and K. guidelines for aquatic animal pathogens. Aquacul- H. Amos. 1998.: Pathogens and diseases of fish in ture 226:191–199. aquatic ecosystems: implications in fisheries man- Lawson, A. B. 2001. Statistical methods in spatial epide- agement. Journal of Aquatic Animal Health 10:95– miology. Wiley, New York. 100. Lilley, J. H., D. Hart, R. H. Richards, R. J. Roberts, L. Murray, A. G., C. D. Busby, and D. W. Bruno. 2003. Cerenius, and K. Soderahall. 1997. Pan-Asian Infectious pancreatic necrosis virus in Scottish At- spread of single fungal clone results in large scale lantic salmon farms, 1996–2001. Emerging Infec- fish kills. Veterinary Record 140:653–654. tious Diseases 9:455–460. Lilley, J. H., R. B. Callinan, S. Chinabut, S. Kanchana- Naylor, R. L., S. L. Williams, and d. R. Strong. 2001. khan, I. H. MacRae, and M. J. Phillips. 1998. Epi- Aquaculture – a gateway for exotic species. Science zootic ulcerative syndrome (EUS) technical 294:1655–1656. handbook. Aquatic Animal Health Research Insti- Nehring, R. B., and P. G. Walker. 1996. Whirling dis- tute, Bangkok, Thailand. ease in the wild: the new reality in the intermountain MacMillan, J. R., T. Huddleston, M. Woolley, and K. west. Fisheries 21(6):28–31. Fothergill. 2003. Best management practice devel- Noakes, D. J., R. J. Beamish, M. L. Kent. 2000. On the opment to minimize environmental impact from large decline of Pacific salmon and speculative links to flow-through trout farms. Aquaculture 226:91–99. salmon farming in British Columbia. Aquaculture May, R. M., and R. M. Anderson. 1979. Population 183:363–386. biology of infectious diseases: part II. Nature (Lon- Olsen, S. F., M. Martuzzi, and P. Elliott. 1996. Cluster don) 280:455–461. analysis and disease mapping- why, when, and how? McArthur, J. V., and R. C. Tuckfield. 2000. Spatial pat- A step by step guide. British Medical Journal terns in antibiotic resistance among stream bacteria: 313:863–866. effects of industrial pollution. Applied and Envi- Patterson, K. R. 1996. Modelling the impact of disease- ronmental Microbiology 66:3722–3726. induced mortality in an exploited population: the McEwen, S. A., and P. J. Fedorka-Cray. 2002. Antimi- outbreak of the fungal parasite Ichthyophonus hoferi crobial use and resistance in animals. Clinical Infec- in the North Sea herring (Clupea harengus). Cana- tious Diseases 34(Supplement 3):93–106. dian Journal of Fisheries and Aquatic Sciences Mellergaard, S., and B. Spanggaard. 1997. An Ichthy- 53:2870–2887. ophonus hoferi epizootic in herring in the North Sea, Petersen, A., J. Andersen, T. Kaewmak, T. Somsiri, and the Skagerrak, the Kattegat and the Baltic Sea. Dis- A. Dalsgaard. 2002. Impact of integrated fish farm- eases of Aquatic Organisms 28:191–199. ing on antimicrobial resistance in a pond environ- Mesa, M. G., A. G. Maule, and C. B. Schreck. 2000. ment. Applied and Environmental Microbiology Interaction of infection with Renibacterium 68:6036–6042. salmoninarum and physical stress in juvenile Chi- Plumb, J. A. 1999. Health maintenance and principal nook salmon: physiological responses, disease pro- microbial diseases of cultured fishes. Iowa State gression, and mortality. Transactions of the American University Press, Ames. Fisheries Society 129:158–173. Rapport, D. J., H. A. Regier, and C. Thorpe. 1982. Di- Meyers, T. R., S. Short, C. Farrington, K. Lipson, H J. agnosis, prognosis and treatment of ecosystems Geiger, and R. Gates. 1993. Comparison of the en- under stress. Pages 269–280 in G. W. Barrett and zyme-linked immunosorbent assay (ELISA) and R. Rosenberg, editors. Stress effects on natural eco- fluorescent test (FAT) for measuring the systems. John Wiley, New York. prevalences and levels of Renibacterium salmoni- Reno, P. 1998. Factors involved in the dissemination of narum in wild and hatchery stocks of salmonid disease in fish populations. Journal of Aquatic Ani- fishes in Alaska, USA. Diseases of Aquatic - mal Health 10:160–171. isms 16:181–189. Rhodes, G., G. Huys, J. Swings, P. McGann, M. Hiney, EVALUATING AND UNDERSTANDING FISH HEALTH RISKS AND THEIR CONSEQUENCES 537

P. Smith, and R. W. Pickup. 2000. Distribution of Thorburn, M. A. 1996. Apparent prevalence of fish patho- oxytetracycline resistance plasmids between gens in asymptomatic salmonid populations and its Aeromonads in hospital and aquaculture environ- effect on misclassifying population infection status. ments: implication of Tn1721 in dissemination of Journal of Aquatic Animal Health 8:271–277. the tetracycline resistance determinant Tet A. Ap- Troyer, R. M., S. E. LaPatra, and G. Kurath. 2000. plied and Environmental Microbiology 66:3883– Genetic analyses reveal unusually high diversity of 3890. infectious haematopoietic necrosis virus in rainbow Sakai, M., S. Atsuta, and M. Kobayashi. 1992. Detec- trout anquaculture. Journal of General Virology tion of Renibacterium salmoninarum antigen in 81:2823–2832. migrating adult (Oncorhynchus keta) Wedemeyer, G. A. 1996. Physiology of fish in intensive in . Journal of Wildlife Diseases 28:110–112. culture systems. Chapman and Hall, New York. Sandaa, R.-A. V. L. Torsvik, and J. Goksoyr. 1992. Trans- Weston, D., B. Dixon, and C. Forney. 1998. Fate and ferable drug resistance in bacteria from fish-farm microbial effects of aquacultural drug residues in the sediments. Canadian Journal of Microbiology environment. University of , Berkeley. 38:1061–1065. Williams, C. J., and C. M. Moffitt. 2001. A critique of Sandaa, R. -A., and Ø. Enger. 1996. High frequency methods of sampling and reporting pathogens in transfer of a broad host range plasmid present in an populations of fish. Journal of Aquatic Animal atypical strain of the fish pathogen Aeromonas Health 13:300–309. salmonicida. Diseases of Aquatic Organisms 24:71– Williams, C. J., and C. M. Moffitt. 2003. Bayesian esti- 75. mation of fish disease prevalence from pooled Schmidt, A. S., M. S. Bruun, I. Dalsgaard, and J. L. samples incorporating sensitivity and specificity. Larsen. 2001. Incidence, distribution and spread of Pages 39–51 in C. J. Williams, editor. Bayesian in- tetracycline resistance determinants and integron- ference and maximum entropy methods in science associated antibiotic resistance genes among motile and engineering. American Institute of Physics, aeromonids from a fish farming environment. Ap- College Park, Maryland. plied and Environmental Microbiology 67:5675– Winton, J. 2001. Fish health management. Pages 559– 5682. 639 in G. A. Wedemeyer, editor. Fish Hatchery Snieszko, S. F. 1974. The effects of environmental stress Management, 2nd edition. American Fisheries So- on outbreaks of infectious diseases of fishes. Jour- ciety, Bethesda, Maryland. nal of Fish Biology 6:197–208. Yamamoto, T. 1975. Frequency of detection and sur- St-Hilaire, S. C. S. Ribble, C. Stephen, E. Anderson, G. vival of infectious pancreatic necrosis virus in a Kurath, and M. L. Kent. 2002. Epidemiological in- carrier population of ( vestigation of infectious hematopoietic necrosis vi- fontinalis) in a lake. Journal of the Fisheries Re- rus in salt water net-pen reared Atlantic salmon in search Board of Canada 32(4):568–570. British Columbia, Canada. Aquaculture 212:49–67. Yoo, M. H., M. Huh, E. Kim, H. Lee, and H. D. Jeong. Tacon, A. G. J., and I. P. Forster. 2003. Aquafeeds and 2003. Characterization of chloramphenical acetyl- the environment: policy implications. Aquaculture transferase gene by multiplex polymerase chain re- 226:181–189. action in multidrug-resistant strains isolated from Thoesen, J. C., editor. 1994. Suggested procedures for aquatic environments. Aquaculture 217:11–21. the detection and identification of certain finfish and Zitko, V. 2001. Analytical chemistry in monitoring the shellfish pathogens, 4th edition. American Fisher- effects of aquaculture: one laboratory’s perspective. ies Society, Bethesda, Maryland. ICES Journal of Marine Science 58:486–491.