Infections by Renibacterium salmoninarum and Nanophyetus salmincola Chapin are associated with reduced growth of juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Northeast Pacific Ocean Sandell, T. A., Teel, D. J., Fisher, J., Beckman, B., & Jacobson, K. C. (2015). Infections by Renibacterium salmoninarum and Nanophyetus salmincola Chapin are associated with reduced growth of juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Northeast Pacific Ocean. Journal of fish diseases, 38(4), 365-378. doi:10.1111/jfd.12243 10.1111/jfd.12243 John Wiley & Sons Ltd. Version of Record http://cdss.library.oregonstate.edu/sa-termsofuse Journal of Fish Diseases 2015, 38, 365–378 doi:10.1111/jfd.12243 Infections by Renibacterium salmoninarum and Nanophyetus salmincola Chapin are associated with reduced growth of juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Northeast Pacific Ocean T A Sandell1, D J Teel2, J Fisher3, B Beckman4 and K C Jacobson5 1 Department of Microbiology, Oregon State University, Corvallis, OR, USA 2 NOAA Fisheries, Northwest Fisheries Science Center, Manchester Research Laboratory, Manchester, WA, USA 3 Cooperative Institute for Marine Resources Studies, Oregon State University, Newport, OR, USA 4 NOAA Fisheries, Northwest Fisheries Science Center, Seattle, WA, USA 5 NOAA Fisheries, Northwest Fisheries Science Center, Newport, OR, USA first year at sea has been linked to survival for Abstract some stocks of Chinook salmon, the infections We examined 1454 juvenile Chinook salmon, may therefore play a role in regulating these pop- Oncorhynchus tshawytscha (Walbaum), captured in ulations in the Northeast Pacific Ocean. nearshore waters off the coasts of Washington and Keywords: disease ecology, survival, parasite, Oregon (USA) from 1999 to 2004 for infection pathogen. by Renibacterium salmoninarum, Nanophyetus sal- mincola Chapin and skin metacercariae. The prev- alence and intensities for each of these infections were established for both yearling and subyearling Introduction Chinook salmon. Two metrics of salmon growth, Pathogens and parasites can regulate host popula- weight residuals and plasma levels of insulin-like tions through direct mortality, by affecting the host growth factor-1, were determined for salmon organism’s ability to compete intra- or interspecifi- infected with these pathogens/parasites, both indi- cally and by affecting fitness or growth. Once con- vidually and in combination, with uninfected fish sidered to play a minor role in ecological used for comparison. Yearling Chinook salmon communities, parasites have been observed to have infected with R. salmoninarum had significantly density-dependent effects and thus may influence reduced weight residuals. Chinook salmon the density of a species. Aquatic pathogens can reg- infected with skin metacercariae alone did not ulate fish populations via host mortality and have significantly reduced growth metrics. Dual reduced fecundity (Lester 1984), particularly when infections were not associated with significantly pathogen transfer rates are high, as among farmed more severe effects on the growth metrics than or captive fish populations (Sindermann 1987). single infections; the number of triple infections Patterson (1996) modelled effects of the parasite was very low and precluded statistical comparison. Ichthyophonus hoferi Plehn & Mulsow on North Sea Overall, these data suggest that infections by these herring, Clupea harengus Linnaeus, and estimated organisms can be associated with reduced juvenile that the population size was reduced by 10–20% Chinook salmon growth. Because growth in the during epizootics. A field study that analysed the influences of an ectoparasite on the bridled goby, Coryphopterus glaucofraenum Gill, showed that Correspondence T A Sandell, Department of Microbiology, Oregon State University, Corvallis, OR 97331, USA infected individuals had significantly reduced (e-mail: [email protected]) growth, gonad mass and higher instantaneous Ó 2014 John Wiley & Sons Ltd 365 Journal of Fish Diseases 2015, 38, 365–378 T A Sandell et al. Infections affect salmon growth mortality (Finley & Forrester 2003). The effect of trematodes are also acquired in fresh water and these infections on growth is of interest because persist for a minimum of several months (Fergu- numerous studies have demonstrated that size can son et al. 2010) to years (Hoffmann & Putz be a critical factor in the survival of juvenile fish in 1965) and may persist for the entire lifespan of their first year at sea (Sogard 1997; Zabel & Achord the infected salmon host. Species identification 2004; Van Doornik et al. 2007; Duffy & Beau- can be difficult because the morphology of the champ 2011). Parasitic infections that reduce metacercariae is variable; ‘Neascus’ is a larval form juvenile growth can reduce survival and thus may common to the families Strigeidae and Diplos- play a role in regulating fish populations, including tomatidae and may refer to several species (Olson Chinook salmon. et al. 2003). Thus, we refer to cases of black spot The pathogenic bacterium Renibacterium salmon- infection simply as ‘skin metacercariae’. Acute, inarum, metacercarial stages of the trematode Nan- heavy infections with A. donicus were shown to ophyetus salmincola Chapin and metacercarial stages cause mortality in small coho salmon, O. kisutch of the trematodes causing ‘black spot’ disease (either (Walbaum) (6 cm in length) (Niemi & Macy Neascus or Apophallus sp.) have been documented 1974), and Ebersole et al. (2006) noted lower- in many coastal rivers and estuaries of the Pacific than-expected overwintering survival in coho sal- Northwest (Arkoosh et al. 2004). All are acquired mon smolts parasitized by Apophallus spp. These in fresh water and persist in the host after ocean results were confirmed by Ferguson et al. (2010), entry. Renibacterium salmoninarum is the causative who reported dramatic declines in the abundance agent of bacterial kidney disease (BKD) in suscepti- of Apophallus spp. between the parr and smolt ble salmonids. The infection is typically acquired in stages in coho salmon, suggesting parasite-related the fresh water phase of the salmonid life cycle and mortality. is transmitted both vertically (in ovo) and horizon- Few studies have examined the effects of infec- tally (fish-to-fish, via the faecal–oral route) within tions on juvenile salmon growth during their mar- populations (Evelyn, Prosperi-Porta & Ketchenson ine phase. The goal of this study was to determine 1986; Balfry, Albright & Evelyn 1996; McKibben the prevalence (percentage infected) and intensity & Pascho 1999). Studies by Rhodes et al. (2006, (number of parasites) of these common infections 2011) suggest that the infection can also be passed and to determine whether juvenile Chinook salmon horizontally among juvenile salmon in salt water. with single or multiple infections have reduced Infection with R. salmoninarum can cause epizoot- growth early in marine residency. We tested for cor- ics, particularly in hatcheries where fish densities are relations between infection intensity and the growth high (Banks 1994), but more typically leads to metrics and looked for evidence that multiple infec- chronic infections with persistent low-level mortal- tions resulted in increased mortality. This research ity. There is some evidence of recovery from the was part of a larger study of juvenile salmon ecology infection in fresh water (Bruno & Munro 1986; off the Oregon and Washington coast (Peterson Pascho, Elliot & Streufert 1991; Cvitanich 2004; et al. 2010) in areas where juvenile Chinook sal- Turgut et al. 2008). mon are predominately from the Columbia River The trematode N. salmincola infects juvenile sal- Basin (Fisher & Pearcy 1995; Daly et al. 2012). mon as a second intermediate host in fresh water. Our study comprised 6 years of sampling and, in The encysted metacercariae survive for the life of the case of R. salmoninarum, utilized newer and the salmon (Bennington & Pratt 1960; Farrell, more sensitive detection assays, providing the most Lloyd & Earp 1964) or until the fish is eaten by the comprehensive study to date on the role of these parasite’s definitive host, either a mammal (Mille- common infections in juvenile Chinook salmon mann & Knapp 1970) or piscivorous bird (Farrell growth. et al. 1964). Several studies have demonstrated the ability of N. salmincola to increase mortality in infected juvenile salmonids (Baldwin, Milleman & Methods Knapp 1967; Butler & Milleman 1971; Newcomb, Fish capture, storage and classification Snell & Waknitz 1991; Jacobson et al. 2008). Metacercarial stages of the trematodes which Juvenile salmon were captured by surface trawl in cause ‘black spot’ disease encyst in the salmon nearshore marine waters in May, June and Sep- host’s skin or subcutaneous muscle. These tember of 1999–2004. Although variations Ó 2014 John Wiley & Sons Ltd 366 Journal of Fish Diseases 2015, 38, 365–378 T A Sandell et al. Infections affect salmon growth occurred due to daylight and weather, we typically they were stored at À80 °C at the conclusion of sampled three transects in May and eight transects each sampling cruise. in June and September (Fig. 1). These transects ranged from Tatoosh Island, WA (48.337N; Juvenile salmon age class determination and À124.718W) south to Newport, Oregon jack exclusion (44.40N; À124.4W). Along each transect, stations were typically sampled from 1 to a maximum of Because sexually precocious salmon (‘jacks’) are 25 nautical