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Occurrence of the Parasitic Copepod Ergasilus labracis on Threespine Sticklebacks from the South Coast of Newfoundland a
b
Alexandra A. Eaves , Keng Pee Ang & Harry M. Murray
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Stantec Consulting, Ltd., 141 Kelsey Drive, St. John's, Newfoundland A1B 0L2, Canada
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Cooke Aquaculture, Inc., 1 Fundy Bay Drive, St. George, New Brunswick E5C 3E2, Canada
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Fisheries and Oceans Canada, Aquatic Resources Division, Science Branch, Aquaculture, Biotechnology, and Aquatic Animal Health Section, 80 East White Hills Road, Post Office Box 5667, St. John's, Newfoundland A1C 5X1, Canada Published online: 16 Oct 2014.
To cite this article: Alexandra A. Eaves, Keng Pee Ang & Harry M. Murray (2014) Occurrence of the Parasitic Copepod Ergasilus labracis on Threespine Sticklebacks from the South Coast of Newfoundland, Journal of Aquatic Animal Health, 26:4, 233-242, DOI: 10.1080/08997659.2014.938871 To link to this article: http://dx.doi.org/10.1080/08997659.2014.938871
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Journal of Aquatic Animal Health 26:233–242, 2014 C American Fisheries Society 2014 ISSN: 0899-7659 print / 1548-8667 online DOI: 10.1080/08997659.2014.938871
ARTICLE
Occurrence of the Parasitic Copepod Ergasilus labracis on Threespine Sticklebacks from the South Coast of Newfoundland Alexandra A. Eaves Stantec Consulting, Ltd., 141 Kelsey Drive, St. John’s, Newfoundland A1B 0L2, Canada
Keng Pee Ang Downloaded by [Lakehead University] at 13:52 28 October 2014
Cooke Aquaculture, Inc., 1 Fundy Bay Drive, St. George, New Brunswick E5C 3E2, Canada
Harry M. Murray* Fisheries and Oceans Canada, Aquatic Resources Division, Science Branch, Aquaculture, Biotechnology, and Aquatic Animal Health Section, 80 East White Hills Road, Post Office Box 5667, St. John’s, Newfoundland A1C 5X1, Canada
Abstract A study conducted from August to October 2013 surveyed Threespine Sticklebacks Gasterosteus aculeatus (n = 822) for the presence of parasitic copepods in the vicinity of large sea-cage salmonid farms in Bay d’Espoir, Newfoundland. The majority of parasitic copepods surveyed were Ergasilus labracis (n = 4,684). Other parasitic copepods observed on Threespine Sticklebacks during the survey included chalimus-stage Lepeophtheirus spp. (n = 3), adult Argulus alosae (n = 2), and a single Thersitina gasterostei. This represents a new host record for E. labracis. The copepods were present on fish collected in a broad range of temperatures (6.9–17.7◦ C) and salinities (10.2–30.2 [Practical Salinity Scale]). The parasitic copepods were most commonly found on larger hosts estimated to be age 1 or older. Surprisingly, the highest infestations (approximately 65%) were found on regions of the hosts outside of the gills (behind the pectoral fins and pelvic spines); in some cases, the copepods had inflicted significant damage to the skin of their hosts. Among host fish with evidence of an additional infection, such as microsporidian tumors (xenomas) or hemorrhagic-like symptoms (dark red abdomens and bloody mucus), the prevalence of E. labracis was significantly higher (43.4%) than among healthy fish (28.9%) despite there being no significant difference in size between the two fish health groups. In contrast, intensity (mean number of individual parasites per host) was significantly higher among healthy hosts (23.6) than among unhealthy ones (7.63). Although this parasite has been listed as present in Newfoundland previously, it has a broad host range and has been reported to be pathogenic to farmed salmonids. Therefore, its potential impact on wild and farmed fish populations around Newfoundland should not be underestimated.
Parasitic copepods are a persistent global problem affecting wild and farmed fish alike (Johnson et al. 2004; Costello 2009; Saksida et al. 2011). There are several species of parasitic copepods, many with broad host specificity (Costello 2009), but the majority of studies have focused on species of ecological
or commercial interest, particularly those affecting aquaculture operations (reviewed by Pike and Wadsworth 1999; Johnson et al. 2004). A broader knowledge of the dynamics of parasitic copepods infecting both wild and cultured fishes would improve our understanding of how epidemics develop and persist in the
*Corresponding author: [email protected] Received March 28, 2014; accepted June 16, 2014
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marine environment and assist with the development of strategies for reducing their negative impacts (Costello 2009; Bellay et al. 2013). Ergasilid copepods are an important group of parasites that occur globally in marine, brackish, and freshwater habitats (Wilson 1911; Bere 1930; Hudson et al. 1994; Paperna 1996; Kilian and Avenant-Oldewage 2013). So far as is known, ergasilid copepods remain free-swimming for the entire lifecycle of males and all developmental stages of females (Wilson 1911; Kabata 1988; Hogans 1991). Only the adult females are parasitic, and they have disproportionately large second antennae which function as claws for grasping the host, most commonly by the gill lamellae (Wilson 1911; Kabata 1988). The parasitic females use their oral appendages for grazing on the epithelium, mucosal glands, and blood of the gills (Wilson 1911; Einzporn 1965). Prolific ergasilids are pathogenic to their hosts, causing destruction of gill tissue, emaciation, and sometimes death (reviewed by Paperna and Zwerner 1982). Many common food fishes are suitable hosts on which parasitic adult females can be found in abundance (Wilson 1911; Paperna and Zwerner 1976a; Hogans 1991). Thus, due to their low host specificity and tolerance of a broad range of environmental conditions, ergasilids pose a potential threat to both wild and farmed fish stocks (Johnson and Rogers 1973; Hogans 1989; Johnson et al. 2004; Dezfuli et al. 2011). Recently, Threespine Sticklebacks Gasterosteus aculeatus in the Northeast Pacific were found to harbor higher abundances of developing parasitic copepods (Lepeophtheirus and Caligus spp.) than were found on wild salmon Oncorhynchus spp. in the same area (Jones et al. 2006; Jones and Prosperi-Porta 2011). Jones and Prosperi-Porta (2011) hypothesized that these fish serve as a sentinel species for the abundance and diversity of parasitic copepods in coastal ecosystems. Threespine Sticklebacks have a nearly circumpolar distribution (Williams and Delbeek 1989), and most populations are anadromous: adults migrate into freshwater to breed in the spring, and surviving adults and young of the year return to the marine environment in the late summer (Williams and Delbeek 1989). Threespine Sticklebacks are planktivorous predators (Peltonen et al. 2004) and are not regarded to be highly active swimmers (Williams and Delbeek 1989). In addition, they are host to several species of parasites throughout their range (Hanek and Threlfall 1970a; McDonald and Margolis 1995). The fish parasites endemic to Newfoundland and Labrador are relatively poorly known (Hanek and Threlfall 1970a). Freshwater species of ergasilids, such as Ergasilus auritus, E. luciopercarum, and another unidentified species, are known to parasitize landlocked populations of Rainbow Smelt Osmerus mordax, Brook Trout Salvelinus fontinalis, Atlantic Salmon Salmo salar, Brown Trout Salmo trutta, and Threespine Stickleback (Sandeman and Pippy 1967; Hanek and Threlfall 1970b; Threlfall 1981; Cone and Ryan 1984; McDonald and Margolis 1995). However, there have been scant reports of this family of parasitic copepods occurring in Newfoundland’s marine en-
vironment (Kabata 1988; McDonald and Margolis 1995) and no information detailing the effects of infestation on the host. Moreover, due to the expansion of finfish aquaculture on the south coast of Newfoundland in the last two decades, it is imperative to understand the parasite ecology of this region (Khan 2009), but there are no published reports of parasitic copepods on farmed salmonids for this area. In response to this knowledge gap, we examined resident nonsalmonid finfish (primarily Threespine Sticklebacks) to identify potential sentinel species for monitoring the presence and effects of parasitic copepods on host fish in the vicinity of aquaculture operations off southern Newfoundland and possibly other areas in the North Atlantic.
METHODS Field sampling.—Sampling was conducted in the Bay d’Espoir region of the south coast of Newfoundland (Figure 1). Three sampling trips were made between August and October 2013: August 22–24, October 1–2, and October 29–30. For each trip, 2 d of sampling were conducted; on day 1 beach seining was done with a 1-m × 6-m pole seine (Wildlife Supply Company), and on day 2 trawls were made using a 1.5-m2 small pelagic seine (Filmar, Inc.). Seining was conducted according to beach accessibility as determined by weather and tides (beach 2 was only sampled on trip 3), and pelagic trawls were made adjacent to two salmonid marine production sites. After collection, fish were bagged collectively at each location on the first trip and individually on trips 2 and 3. All samples were frozen at −20◦ C until examination in the laboratory. Temperature and salinity were recorded for each location with a YSI Castaway (CTD) device. Salinities were recorded in terms of the Practical Salinity Scale, which defines salinity according to a dimensionless conductivity ratio instead of by weight (pounds of salt per thousand pounds of seawater [‰]); the numerical values are similar between the two, however (UNESCO 1981). Parasitic copepod and fish health survey.—In the laboratory fish were thawed, then total body length and weight were measured. Fish were examined with the aid of a dissecting microscope (Leica Wild MZ8) at 10 × magnification and illuminated with a fiber optic light source (Cole Palmer 9745-00). Fish were placed into one of two categories according to their relative health status: (1) healthy, i.e., having no external evidence of deformities, lesions, or disease (this category included healthy reproductive adults) or (2) unhealthy, i.e., having external evidence of deformity or disease such as microsporidian tumors (xenomas) or hemorrhagic-like symptoms (bloody mucus and inflamed, dark red abdomens) (Figure 2). Fish were also surveyed for the presence and number of parasitic copepods as well as their locations on the host. Only copepods with grasping claws firmly attached to host tissue were counted. All fish and copepods were inventoried and stored in 95% ethanol. Identification of parasitic copepods was made according to Kabata (1988) and Hogans (1991).
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FIGURE 1. Map of the Bay d’Espoir region on the south coast of Newfoundland. The sites at which beach seining was conducted (circles) are as follows: (1) Hardy Cove, (2) Raymond Point, (3) Day Cove, (4) Brimball Harbour, and (5) Furbey Cove. Pelagic trawls were conducted at Atlantic Salmon farm sites (squares [6–7]).
Digital imaging.—Images of parasitic copepods on hosts were recorded with a Leica MZ6 dissecting microscope equipped with an Olympus Q Color 5 camera. The morphological features of the parasitic copepods were documented with a Zeiss AX10 compound microscope with a Nikon Coolpix 4500 camera. Image plates were assembled using Adobe Photoshop CS 5 version 12.1. Statistical analyses.—Due to limited sample sizes and the inconsistent presence of fish at sites (i.e., n = 8 for all pelagic trawls adjacent to finfish farming sites), all fish were pooled per collection trip for analysis. Prevalence and mean intensity (mean number of individual parasites per host) as defined by Bush et al. (1997) were used in the analysis. Mean prevalence and intensity and their 95% confidence intervals were calculated according to Rozsa et al. (2000) using QPweb (Reiczigel et al. 2013). Comparisons of host size and the intensity of parasitic copepod infections were made using the nonparametric Kruskal–Wallis test and the pairwise multiple comparison procedure (Dunn’s method); Fisher’s exact test was employed for comparison of prevalences. Differences for which there were P-values 100 lice/fish) (Paperna and Zwerner 1982) also had large lesions on the skin, but whether or not this was a moribund condition for the host could not be determined postmortem. Regardless, the potential consequences of skin lesions associated with the site of ergasilid attachment may be similar to those described for other parasitic copepods, such as Lepeophtheirus salmonis, whose dermal grazing habits compromise the osmoregulation and swimming ability of host Atlantic Salmon (Wagner et al. 2003) as well as increasing secondary infections, stress, and loss of growth (Pike and Wadsworth 1999; Johnson et al. 2004). On Atlantic Salmon infested by L. salmonis, the parasitic copepods are most commonly found on regions of the host with thin skin that are devoid of scales, such as the head and the regions between the dorsal and adipose fins and the perianal region (Wootten et al. 1982; J´onsd´ottir et al. 1992; summarized by Mustafa et al. 2000). These regions of the host are typified as having thin, soft skin and no scales, and parasitic copepods were most commonly found attached to the same tissue type on Threespine Sticklebacks in the present study (i.e., from the soft mucous-secreting regions at the base of the fins and on the abdomen under the base of the pelvic girdle). This raises the question why this pattern of Ergasilus distribution has not been more commonly reported on host fish. Are hosts with suitable outer tissues limited to a single freshwater and marine parasite host combination (Rogers and Hawke 1978; present study)? Another possibility is sampling bias; previous studies of Ergasilus spp. largely report dissecting out the gills without
TABLE 2. Prevalence, intensity, and abundance of Ergasilus labracis on Threespine Sticklebacks in Bay d’Espoir according to the health appearance of hosts. Within columns, means with significant differences (P < 0.05) are indicated different lowercase letters.
Ergasilids (means and 95% confidence intervals)
Fish (means ± SEs) Host appearance Healthy Unhealthy
n
Length (mm)
Weight (g)
Prevalence (%)
Intensity
557 265
35.3 ± 0.6 z 32.9 ± 0.6 z
0.640 ± 0.041 z 0.368 ± 0.030 z
28.9 (25.2–32.8) y 43.4 (37.5–49.4) z
23.6 (19.7–28.9) z 7.63 4.78–12.5) y
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examining the rest of the host fish’s body (i.e., Paperna and Zwerner 1976b, 1982; Hogans 1989, 1991; Dezfuli et al. 2011; Kilian and Avenant-Oldewage 2013).
Prevalence of Ergasilus labracis by Host Size and Health Among the Threespine Sticklebacks we surveyed there was a significant positive correlation between host size and the intensity of parasitic copepods. The average size of fish infected with gill lice was significantly larger than that of uninfected fish (45.6 ± 1.0 mm versus 29.0 ± 0.3 mm). Cope (1959) also found that Threespine Sticklebacks without ergasilid infestation in a freshwater stream in Alaska were relatively small (average size, 35.8 mm). This disparity in average size likely represents different age-classes of fish; Reimchen (1990) and Barber (2003) classify Threespine Sticklebacks less than 40 mm as young of the year and those greater than 40 mm as age 1 or older. Generally, larger fish harbor more parasitic copepods (Pike and Wadsworth 1999), and with respect to E. labracis on wild fish in particular, Paperna and Zwerner (1976b) reported the prevalence of infection on all Striped Bass over 1 year old (n = 192) and from all collecting localities to have exceeded 90%. To date, the highest reported infection intensity of E. labracis on a wild fish involved an age-1 White Perch that had 2,757 individuals parasitizing its gills (Paperna and Zwerner 1976a). However, during an outbreak of E. labracis that killed several thousand parr-sized farmed Atlantic Salmon in only a few days, Hogans (1989) reported a prevalence of 100% and an intensity of 84.6 E. labracis per host; the highest number of parasitic copepods infesting a single fish was 2,229. Not only can the immediate pathological effects of parasitic copepod infestation be detrimental to hosts, heavily infected hosts are less likely to withstand environmental challenges such as oxygen depletion, algal blooms, and pollution (Paperna and Zwerner 1976b; Lafferty and Kuris 1999). Host health also had a significant effect on parasitic copepod infestation levels. When the infestation levels of healthy and unhealthy host groups were compared, we observed that the prevalence of parasitic copepod infestation was greater among unhealthy fish. In contrast, the intensity of infection was significantly lower among unhealthy fish despite there being no significant difference in host size. Parasitic copepod infestation may render hosts more susceptible to secondary infection (Pike and Wadsworth 1999; Mustafa et al. 2000; Wagner et al. 2003) or be a vector for the transmission of microsporidian, viral, and bacterial pathogens (Weissenberg 1968; Nylund et al. 1994; Barker et al. 2009; Jakob et al. 2011; Oelckers et al. 2014). However, simultaneous infections have a significant effect on the available resources of the host (Threlfall 1968; Ward et al. 2005). So even though lice infestation could increase the likelihood of a fish’s becoming infected by another pathogen, parasitic copepods may have greater infestation success (i.e., achieve higher infestation intensities) on healthy hosts. The influence of simultaneous host health afflictions on parasitic copepod infestation warrants fur-
ther investigation, as do the dynamics of co-occurring epizootic events among fish populations. Occurrence of Ergasilus labracis with Regard to Temperature and Salinity Hogans (1991) suggested that E. labracis are an estuarine or freshwater parasite which is unlikely to survive the transition to a marine environment on an anadromous host. However, fish infested with E. labracis have been collected from a broad range of environmental conditions, ranging in temperature from 0–24◦ C and salinities ranging from 0–32‰ (Paperna and Zwerner 1976b; Frimeth 1987; Hogans 1989). Paperna and Zwerner (1976b, 1982) describe these parasitic copepods to be as euryhaline as their anadromous hosts. The present study supports the conclusion that E. labracis are indeed tolerant of a broad range of environmental conditions, having found them among fish collected in water temperatures ranging from 6.9◦ C to 17.7◦ C and salinities of 10.2–30.2 (Practical Salinity Scale). Consistent with these observations, in a study of fish assemblages in a Newfoundland estuary Methven et al. (2001) reported no correlation between salinity and the abundance of Threespine Sticklebacks. However, considering that the majority of the female ergasilid developmental life cycle and the entirety of the males’ is spent free swimming (Wilson 1911; Kabata 1988), other oceanographic factors such as current pattern, speed, wind influence, and site flushing (Revie et al. 2003) should be examined as potential parameters affecting the distribution of this species of parasite. Lastly, the comparatively small sample size (n = 39) on trip 3 corresponded to a marked decline in the temperature range in the near-surface sampling environment. Threespine Sticklebacks drop down to slightly deeper water in winter (Jones and John 1978); despite this, the prevalence of parasitic copepods among the fish sampled remained high (79.5%). As described above, E. labracis are tolerant of colder temperatures and can overwinter on hosts and even continue to produce egg strings (albeit at a slower rate) during the coldest months of the year (Paperna and Zwerner 1976a, 1976b, 1982). Conclusions The parasitic copepod E. labracis appears to be widespread among the Threespine Sticklebacks surveyed in the south coast region of Newfoundland. This raises the specter that this species might serve as a reservoir for E. labracis in the western North Atlantic, similar to their role in the Northeastern Pacific (Jones and Prosperi-Porta 2011). Considerable research will be required to understand the dynamics of these parasitic copepods and Threespine Stickleback ecology (Jones et al. 2006) and host health (presented here). In addition, E. labracis are known to infest farmed salmonids in another region of the North Atlantic (Hogans 1989; O’Halloran et al. 1992). Both the presence of this parasite on farmed fish in Newfoundland and the potential for transmission between wild and farmed fish populations needs to be investigated. Ergasilus labracis are not as rare or host
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specific as previously thought (Hogans 1989). Moreover, they have the capacity to exploit more regions of the host and inflict far greater damage to fish than has been previously recognized. Given this and their tolerance of a broad range of aquatic environmental conditions, the potential impact of this parasite on wild and farmed fish populations should not be underestimated.
ACKNOWLEDGMENTS The authors are grateful to Dwight Drover, Curtis Pennell, and Sharon Kenny for technical assistance with field sampling; to the farm operators and boat crew of Cooke Aquaculture, Inc. (Cold Ocean Salmon Ltd.), for conducting the trawls; to Sebastien Donnet for processing CTD data; and to Pierre Goulet for preparing the map images used in Figure 1. This work was funded by the Department of Fisheries and Oceans (DFO), Aquaculture Collaborative Research and Development Program, and Cooke Aquaculture, Inc. (Cold Ocean Salmon Ltd.). An earlier version of this manuscript benefitted from comments by John Brattey at DFO and two anonymous reviewers.
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Revie, C. W., G. Gettinby, J. W. Treasurer, and C. Wallace. 2003. Identifying factors affecting sea lice Lepeophtheirus salmonis abundance on Scottish salmon farms using general linear models. Diseases of Aquatic Organisms 57:85–95. Rogers, W. A., and J. P. Hawke. 1978. The parasitic copepod Ergasilus from the skin of the Gizzard Shad Dorosoma cepedianum. Transactions of the American Microscopical Society 97:244. Rozsa L., J. Reiczigel, and G. Majoros. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86:228–232. Saksida, S. M., D. Morrison, M. Sheppard, and I. Keith. 2011. Sea lice management on salmon farms in British Columbia, Canada. Pages 235–278 in S. Jones and R. Beamish, editors. Sea lice: an integrated approach to understanding parasite abundance and distribution. Wiley, Toronto. Sandeman, I. M., and J. H. C. Pippy. 1967. Parasites of freshwater fishes (Salmonidae and Coregonidae) of insular Newfoundland. Journal of the Fisheries Research Board of Canada 24:1911–1943. Threlfall, W. 1968. A mass die-off of Three-Spined Sticklebacks (Gasterosteus aculeatus L.) caused by parasites. Canadian Journal of Zoology 46:105–106. Threlfall, W. 1981. Metazoan parasites of two populations of Rainbow Smelt in Newfoundland, Canada. Journal of Parasitology 67:129–131. UNESCO (United Nations Educational, Scientific, and Cultural Organization). 1981. Tenth report of the Joint Panel on Oceanographic Tables and Standards. Technical Papers in Marine Science 36. Wagner, G. N., R. S. McKinley, P. A. Bjørn, and B. Finstad. 2003. Physiological impact of sea lice on swimming performance of Atlantic Salmon. Journal of Fish Biology 62:1000–1009. Ward, A. J. W., A. J. Duff, J. Krause, and I. Barber. 2005. Shoaling behaviour of sticklebacks infected with the microsporidian parasite, Glugea anomala. Environmental Biology of Fishes 72:155–160. Weissenberg, R. 1968. Intracellular development of the microsporidian Glugea anomala Moniez in hypertrophying migratory cells of the fish Gasterosteus aculeatus L., an example of the formation of “xenoma” tumors. Journal of Protozoology 15:44–57. Williams, D. D., and J. C. Delbeek. 1989. Biology of the Threespine Stickleback, Gasterosteus aculeatus, and the Blackspotted Stickleback, G. wheatlandi, during their marine pelagic phase in the Bay of Fundy, Canada. Environmental Biology of Fishes 24:33–41. Wilson, C. B. 1911. North American parasitic copepods belonging to the family Ergasilidae. Proceedings of the United States National Museum 39:263–400. Wilson, C. B., 1932. The copepods of the Woods Hole region, Massachusetts. Bulletin of the United States National Museum 158. Wootten, R., J. W. Smith, and E. A. Needham. 1982. Aspects of biology of the parasitic copepods Lepeophtheirus salmonis and Caligus clemensi on farmed salmonids, and their treatment. Proceedings of the Royal Society of Edinburgh, Section B 81:185–197. Yamashita, K. 1980. Parasitic copepod (Ergasilus sp.) found on the epidermis of the larval fish of Red Seabream (Pagrus major). Fish Pathology 15:91–94. Yamashita, K. 1981. Correction of the report entitled “The parasites found on the epidermis of the larval fish of Red Seabream (Pagrus major)” in Fish Pathology 15:91–94. Fish Pathology 16:55.
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Occurrence of the Parasitic Copepod Ergasilus labracis on Threespine Sticklebacks from the South Coast of Newfoundland a
b
Alexandra A. Eaves , Keng Pee Ang & Harry M. Murray
c
a
Stantec Consulting, Ltd., 141 Kelsey Drive, St. John's, Newfoundland A1B 0L2, Canada
b
Cooke Aquaculture, Inc., 1 Fundy Bay Drive, St. George, New Brunswick E5C 3E2, Canada
c
Fisheries and Oceans Canada, Aquatic Resources Division, Science Branch, Aquaculture, Biotechnology, and Aquatic Animal Health Section, 80 East White Hills Road, Post Office Box 5667, St. John's, Newfoundland A1C 5X1, Canada Published online: 16 Oct 2014.
To cite this article: Alexandra A. Eaves, Keng Pee Ang & Harry M. Murray (2014) Occurrence of the Parasitic Copepod Ergasilus labracis on Threespine Sticklebacks from the South Coast of Newfoundland, Journal of Aquatic Animal Health, 26:4, 233-242, DOI: 10.1080/08997659.2014.938871 To link to this article: http://dx.doi.org/10.1080/08997659.2014.938871
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Journal of Aquatic Animal Health 26:233–242, 2014 C American Fisheries Society 2014 ISSN: 0899-7659 print / 1548-8667 online DOI: 10.1080/08997659.2014.938871
ARTICLE
Occurrence of the Parasitic Copepod Ergasilus labracis on Threespine Sticklebacks from the South Coast of Newfoundland Alexandra A. Eaves Stantec Consulting, Ltd., 141 Kelsey Drive, St. John’s, Newfoundland A1B 0L2, Canada
Keng Pee Ang Downloaded by [Lakehead University] at 13:52 28 October 2014
Cooke Aquaculture, Inc., 1 Fundy Bay Drive, St. George, New Brunswick E5C 3E2, Canada
Harry M. Murray* Fisheries and Oceans Canada, Aquatic Resources Division, Science Branch, Aquaculture, Biotechnology, and Aquatic Animal Health Section, 80 East White Hills Road, Post Office Box 5667, St. John’s, Newfoundland A1C 5X1, Canada
Abstract A study conducted from August to October 2013 surveyed Threespine Sticklebacks Gasterosteus aculeatus (n = 822) for the presence of parasitic copepods in the vicinity of large sea-cage salmonid farms in Bay d’Espoir, Newfoundland. The majority of parasitic copepods surveyed were Ergasilus labracis (n = 4,684). Other parasitic copepods observed on Threespine Sticklebacks during the survey included chalimus-stage Lepeophtheirus spp. (n = 3), adult Argulus alosae (n = 2), and a single Thersitina gasterostei. This represents a new host record for E. labracis. The copepods were present on fish collected in a broad range of temperatures (6.9–17.7◦ C) and salinities (10.2–30.2 [Practical Salinity Scale]). The parasitic copepods were most commonly found on larger hosts estimated to be age 1 or older. Surprisingly, the highest infestations (approximately 65%) were found on regions of the hosts outside of the gills (behind the pectoral fins and pelvic spines); in some cases, the copepods had inflicted significant damage to the skin of their hosts. Among host fish with evidence of an additional infection, such as microsporidian tumors (xenomas) or hemorrhagic-like symptoms (dark red abdomens and bloody mucus), the prevalence of E. labracis was significantly higher (43.4%) than among healthy fish (28.9%) despite there being no significant difference in size between the two fish health groups. In contrast, intensity (mean number of individual parasites per host) was significantly higher among healthy hosts (23.6) than among unhealthy ones (7.63). Although this parasite has been listed as present in Newfoundland previously, it has a broad host range and has been reported to be pathogenic to farmed salmonids. Therefore, its potential impact on wild and farmed fish populations around Newfoundland should not be underestimated.
Parasitic copepods are a persistent global problem affecting wild and farmed fish alike (Johnson et al. 2004; Costello 2009; Saksida et al. 2011). There are several species of parasitic copepods, many with broad host specificity (Costello 2009), but the majority of studies have focused on species of ecological
or commercial interest, particularly those affecting aquaculture operations (reviewed by Pike and Wadsworth 1999; Johnson et al. 2004). A broader knowledge of the dynamics of parasitic copepods infecting both wild and cultured fishes would improve our understanding of how epidemics develop and persist in the
*Corresponding author: [email protected] Received March 28, 2014; accepted June 16, 2014
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marine environment and assist with the development of strategies for reducing their negative impacts (Costello 2009; Bellay et al. 2013). Ergasilid copepods are an important group of parasites that occur globally in marine, brackish, and freshwater habitats (Wilson 1911; Bere 1930; Hudson et al. 1994; Paperna 1996; Kilian and Avenant-Oldewage 2013). So far as is known, ergasilid copepods remain free-swimming for the entire lifecycle of males and all developmental stages of females (Wilson 1911; Kabata 1988; Hogans 1991). Only the adult females are parasitic, and they have disproportionately large second antennae which function as claws for grasping the host, most commonly by the gill lamellae (Wilson 1911; Kabata 1988). The parasitic females use their oral appendages for grazing on the epithelium, mucosal glands, and blood of the gills (Wilson 1911; Einzporn 1965). Prolific ergasilids are pathogenic to their hosts, causing destruction of gill tissue, emaciation, and sometimes death (reviewed by Paperna and Zwerner 1982). Many common food fishes are suitable hosts on which parasitic adult females can be found in abundance (Wilson 1911; Paperna and Zwerner 1976a; Hogans 1991). Thus, due to their low host specificity and tolerance of a broad range of environmental conditions, ergasilids pose a potential threat to both wild and farmed fish stocks (Johnson and Rogers 1973; Hogans 1989; Johnson et al. 2004; Dezfuli et al. 2011). Recently, Threespine Sticklebacks Gasterosteus aculeatus in the Northeast Pacific were found to harbor higher abundances of developing parasitic copepods (Lepeophtheirus and Caligus spp.) than were found on wild salmon Oncorhynchus spp. in the same area (Jones et al. 2006; Jones and Prosperi-Porta 2011). Jones and Prosperi-Porta (2011) hypothesized that these fish serve as a sentinel species for the abundance and diversity of parasitic copepods in coastal ecosystems. Threespine Sticklebacks have a nearly circumpolar distribution (Williams and Delbeek 1989), and most populations are anadromous: adults migrate into freshwater to breed in the spring, and surviving adults and young of the year return to the marine environment in the late summer (Williams and Delbeek 1989). Threespine Sticklebacks are planktivorous predators (Peltonen et al. 2004) and are not regarded to be highly active swimmers (Williams and Delbeek 1989). In addition, they are host to several species of parasites throughout their range (Hanek and Threlfall 1970a; McDonald and Margolis 1995). The fish parasites endemic to Newfoundland and Labrador are relatively poorly known (Hanek and Threlfall 1970a). Freshwater species of ergasilids, such as Ergasilus auritus, E. luciopercarum, and another unidentified species, are known to parasitize landlocked populations of Rainbow Smelt Osmerus mordax, Brook Trout Salvelinus fontinalis, Atlantic Salmon Salmo salar, Brown Trout Salmo trutta, and Threespine Stickleback (Sandeman and Pippy 1967; Hanek and Threlfall 1970b; Threlfall 1981; Cone and Ryan 1984; McDonald and Margolis 1995). However, there have been scant reports of this family of parasitic copepods occurring in Newfoundland’s marine en-
vironment (Kabata 1988; McDonald and Margolis 1995) and no information detailing the effects of infestation on the host. Moreover, due to the expansion of finfish aquaculture on the south coast of Newfoundland in the last two decades, it is imperative to understand the parasite ecology of this region (Khan 2009), but there are no published reports of parasitic copepods on farmed salmonids for this area. In response to this knowledge gap, we examined resident nonsalmonid finfish (primarily Threespine Sticklebacks) to identify potential sentinel species for monitoring the presence and effects of parasitic copepods on host fish in the vicinity of aquaculture operations off southern Newfoundland and possibly other areas in the North Atlantic.
METHODS Field sampling.—Sampling was conducted in the Bay d’Espoir region of the south coast of Newfoundland (Figure 1). Three sampling trips were made between August and October 2013: August 22–24, October 1–2, and October 29–30. For each trip, 2 d of sampling were conducted; on day 1 beach seining was done with a 1-m × 6-m pole seine (Wildlife Supply Company), and on day 2 trawls were made using a 1.5-m2 small pelagic seine (Filmar, Inc.). Seining was conducted according to beach accessibility as determined by weather and tides (beach 2 was only sampled on trip 3), and pelagic trawls were made adjacent to two salmonid marine production sites. After collection, fish were bagged collectively at each location on the first trip and individually on trips 2 and 3. All samples were frozen at −20◦ C until examination in the laboratory. Temperature and salinity were recorded for each location with a YSI Castaway (CTD) device. Salinities were recorded in terms of the Practical Salinity Scale, which defines salinity according to a dimensionless conductivity ratio instead of by weight (pounds of salt per thousand pounds of seawater [‰]); the numerical values are similar between the two, however (UNESCO 1981). Parasitic copepod and fish health survey.—In the laboratory fish were thawed, then total body length and weight were measured. Fish were examined with the aid of a dissecting microscope (Leica Wild MZ8) at 10 × magnification and illuminated with a fiber optic light source (Cole Palmer 9745-00). Fish were placed into one of two categories according to their relative health status: (1) healthy, i.e., having no external evidence of deformities, lesions, or disease (this category included healthy reproductive adults) or (2) unhealthy, i.e., having external evidence of deformity or disease such as microsporidian tumors (xenomas) or hemorrhagic-like symptoms (bloody mucus and inflamed, dark red abdomens) (Figure 2). Fish were also surveyed for the presence and number of parasitic copepods as well as their locations on the host. Only copepods with grasping claws firmly attached to host tissue were counted. All fish and copepods were inventoried and stored in 95% ethanol. Identification of parasitic copepods was made according to Kabata (1988) and Hogans (1991).
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FIGURE 1. Map of the Bay d’Espoir region on the south coast of Newfoundland. The sites at which beach seining was conducted (circles) are as follows: (1) Hardy Cove, (2) Raymond Point, (3) Day Cove, (4) Brimball Harbour, and (5) Furbey Cove. Pelagic trawls were conducted at Atlantic Salmon farm sites (squares [6–7]).
Digital imaging.—Images of parasitic copepods on hosts were recorded with a Leica MZ6 dissecting microscope equipped with an Olympus Q Color 5 camera. The morphological features of the parasitic copepods were documented with a Zeiss AX10 compound microscope with a Nikon Coolpix 4500 camera. Image plates were assembled using Adobe Photoshop CS 5 version 12.1. Statistical analyses.—Due to limited sample sizes and the inconsistent presence of fish at sites (i.e., n = 8 for all pelagic trawls adjacent to finfish farming sites), all fish were pooled per collection trip for analysis. Prevalence and mean intensity (mean number of individual parasites per host) as defined by Bush et al. (1997) were used in the analysis. Mean prevalence and intensity and their 95% confidence intervals were calculated according to Rozsa et al. (2000) using QPweb (Reiczigel et al. 2013). Comparisons of host size and the intensity of parasitic copepod infections were made using the nonparametric Kruskal–Wallis test and the pairwise multiple comparison procedure (Dunn’s method); Fisher’s exact test was employed for comparison of prevalences. Differences for which there were P-values 100 lice/fish) (Paperna and Zwerner 1982) also had large lesions on the skin, but whether or not this was a moribund condition for the host could not be determined postmortem. Regardless, the potential consequences of skin lesions associated with the site of ergasilid attachment may be similar to those described for other parasitic copepods, such as Lepeophtheirus salmonis, whose dermal grazing habits compromise the osmoregulation and swimming ability of host Atlantic Salmon (Wagner et al. 2003) as well as increasing secondary infections, stress, and loss of growth (Pike and Wadsworth 1999; Johnson et al. 2004). On Atlantic Salmon infested by L. salmonis, the parasitic copepods are most commonly found on regions of the host with thin skin that are devoid of scales, such as the head and the regions between the dorsal and adipose fins and the perianal region (Wootten et al. 1982; J´onsd´ottir et al. 1992; summarized by Mustafa et al. 2000). These regions of the host are typified as having thin, soft skin and no scales, and parasitic copepods were most commonly found attached to the same tissue type on Threespine Sticklebacks in the present study (i.e., from the soft mucous-secreting regions at the base of the fins and on the abdomen under the base of the pelvic girdle). This raises the question why this pattern of Ergasilus distribution has not been more commonly reported on host fish. Are hosts with suitable outer tissues limited to a single freshwater and marine parasite host combination (Rogers and Hawke 1978; present study)? Another possibility is sampling bias; previous studies of Ergasilus spp. largely report dissecting out the gills without
TABLE 2. Prevalence, intensity, and abundance of Ergasilus labracis on Threespine Sticklebacks in Bay d’Espoir according to the health appearance of hosts. Within columns, means with significant differences (P < 0.05) are indicated different lowercase letters.
Ergasilids (means and 95% confidence intervals)
Fish (means ± SEs) Host appearance Healthy Unhealthy
n
Length (mm)
Weight (g)
Prevalence (%)
Intensity
557 265
35.3 ± 0.6 z 32.9 ± 0.6 z
0.640 ± 0.041 z 0.368 ± 0.030 z
28.9 (25.2–32.8) y 43.4 (37.5–49.4) z
23.6 (19.7–28.9) z 7.63 4.78–12.5) y
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examining the rest of the host fish’s body (i.e., Paperna and Zwerner 1976b, 1982; Hogans 1989, 1991; Dezfuli et al. 2011; Kilian and Avenant-Oldewage 2013).
Prevalence of Ergasilus labracis by Host Size and Health Among the Threespine Sticklebacks we surveyed there was a significant positive correlation between host size and the intensity of parasitic copepods. The average size of fish infected with gill lice was significantly larger than that of uninfected fish (45.6 ± 1.0 mm versus 29.0 ± 0.3 mm). Cope (1959) also found that Threespine Sticklebacks without ergasilid infestation in a freshwater stream in Alaska were relatively small (average size, 35.8 mm). This disparity in average size likely represents different age-classes of fish; Reimchen (1990) and Barber (2003) classify Threespine Sticklebacks less than 40 mm as young of the year and those greater than 40 mm as age 1 or older. Generally, larger fish harbor more parasitic copepods (Pike and Wadsworth 1999), and with respect to E. labracis on wild fish in particular, Paperna and Zwerner (1976b) reported the prevalence of infection on all Striped Bass over 1 year old (n = 192) and from all collecting localities to have exceeded 90%. To date, the highest reported infection intensity of E. labracis on a wild fish involved an age-1 White Perch that had 2,757 individuals parasitizing its gills (Paperna and Zwerner 1976a). However, during an outbreak of E. labracis that killed several thousand parr-sized farmed Atlantic Salmon in only a few days, Hogans (1989) reported a prevalence of 100% and an intensity of 84.6 E. labracis per host; the highest number of parasitic copepods infesting a single fish was 2,229. Not only can the immediate pathological effects of parasitic copepod infestation be detrimental to hosts, heavily infected hosts are less likely to withstand environmental challenges such as oxygen depletion, algal blooms, and pollution (Paperna and Zwerner 1976b; Lafferty and Kuris 1999). Host health also had a significant effect on parasitic copepod infestation levels. When the infestation levels of healthy and unhealthy host groups were compared, we observed that the prevalence of parasitic copepod infestation was greater among unhealthy fish. In contrast, the intensity of infection was significantly lower among unhealthy fish despite there being no significant difference in host size. Parasitic copepod infestation may render hosts more susceptible to secondary infection (Pike and Wadsworth 1999; Mustafa et al. 2000; Wagner et al. 2003) or be a vector for the transmission of microsporidian, viral, and bacterial pathogens (Weissenberg 1968; Nylund et al. 1994; Barker et al. 2009; Jakob et al. 2011; Oelckers et al. 2014). However, simultaneous infections have a significant effect on the available resources of the host (Threlfall 1968; Ward et al. 2005). So even though lice infestation could increase the likelihood of a fish’s becoming infected by another pathogen, parasitic copepods may have greater infestation success (i.e., achieve higher infestation intensities) on healthy hosts. The influence of simultaneous host health afflictions on parasitic copepod infestation warrants fur-
ther investigation, as do the dynamics of co-occurring epizootic events among fish populations. Occurrence of Ergasilus labracis with Regard to Temperature and Salinity Hogans (1991) suggested that E. labracis are an estuarine or freshwater parasite which is unlikely to survive the transition to a marine environment on an anadromous host. However, fish infested with E. labracis have been collected from a broad range of environmental conditions, ranging in temperature from 0–24◦ C and salinities ranging from 0–32‰ (Paperna and Zwerner 1976b; Frimeth 1987; Hogans 1989). Paperna and Zwerner (1976b, 1982) describe these parasitic copepods to be as euryhaline as their anadromous hosts. The present study supports the conclusion that E. labracis are indeed tolerant of a broad range of environmental conditions, having found them among fish collected in water temperatures ranging from 6.9◦ C to 17.7◦ C and salinities of 10.2–30.2 (Practical Salinity Scale). Consistent with these observations, in a study of fish assemblages in a Newfoundland estuary Methven et al. (2001) reported no correlation between salinity and the abundance of Threespine Sticklebacks. However, considering that the majority of the female ergasilid developmental life cycle and the entirety of the males’ is spent free swimming (Wilson 1911; Kabata 1988), other oceanographic factors such as current pattern, speed, wind influence, and site flushing (Revie et al. 2003) should be examined as potential parameters affecting the distribution of this species of parasite. Lastly, the comparatively small sample size (n = 39) on trip 3 corresponded to a marked decline in the temperature range in the near-surface sampling environment. Threespine Sticklebacks drop down to slightly deeper water in winter (Jones and John 1978); despite this, the prevalence of parasitic copepods among the fish sampled remained high (79.5%). As described above, E. labracis are tolerant of colder temperatures and can overwinter on hosts and even continue to produce egg strings (albeit at a slower rate) during the coldest months of the year (Paperna and Zwerner 1976a, 1976b, 1982). Conclusions The parasitic copepod E. labracis appears to be widespread among the Threespine Sticklebacks surveyed in the south coast region of Newfoundland. This raises the specter that this species might serve as a reservoir for E. labracis in the western North Atlantic, similar to their role in the Northeastern Pacific (Jones and Prosperi-Porta 2011). Considerable research will be required to understand the dynamics of these parasitic copepods and Threespine Stickleback ecology (Jones et al. 2006) and host health (presented here). In addition, E. labracis are known to infest farmed salmonids in another region of the North Atlantic (Hogans 1989; O’Halloran et al. 1992). Both the presence of this parasite on farmed fish in Newfoundland and the potential for transmission between wild and farmed fish populations needs to be investigated. Ergasilus labracis are not as rare or host
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specific as previously thought (Hogans 1989). Moreover, they have the capacity to exploit more regions of the host and inflict far greater damage to fish than has been previously recognized. Given this and their tolerance of a broad range of aquatic environmental conditions, the potential impact of this parasite on wild and farmed fish populations should not be underestimated.
ACKNOWLEDGMENTS The authors are grateful to Dwight Drover, Curtis Pennell, and Sharon Kenny for technical assistance with field sampling; to the farm operators and boat crew of Cooke Aquaculture, Inc. (Cold Ocean Salmon Ltd.), for conducting the trawls; to Sebastien Donnet for processing CTD data; and to Pierre Goulet for preparing the map images used in Figure 1. This work was funded by the Department of Fisheries and Oceans (DFO), Aquaculture Collaborative Research and Development Program, and Cooke Aquaculture, Inc. (Cold Ocean Salmon Ltd.). An earlier version of this manuscript benefitted from comments by John Brattey at DFO and two anonymous reviewers.
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