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Impact of a Gill Parasite Upon the Minnow Notropis telescopus
Andrew B. Adrian, Brittany Holmes, and Bruce W. Stallsmith

Southeastern Naturalist, Volume 11, Issue 1 (2012): 23–34

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2012 SOUTHEASTERN NATURALIST 11(1):35–42 Impact of a Gill Parasite Upon the Minnow Notropis telescopus Andrew B. Adrian1,2, Brittany Holmes1, and Bruce W. Stallsmith1,* Abstract - Dactylogyrus is a holarctic genus of monogene flatworms that infects the gills of cyprinid fishes. Dactylogyrus species are usually highly host specific, and little is known about their life history in North America. The purpose of this study was twofold: to determine 1) whether Dactylogyrus exhibits seasonality in its life cycle, and 2) if there is any potential effect upon reproductive effort of the host as a result of Dactylogyrus infection. Over a 12-month period, 967 Dactylogyrus were found on the gills of 383 Notropis telescopus (Telescope Shiner), a cyprinid fish collected in the upper Paint Rock River system in northeastern Alabama. A significant positive relationship was found between prevalence of infection and host somatic weight and gonadosomatic index (GSI). The assumptions that parasite presence is evenly distributed among individual host fish and within each month were rejected by chi square tests, with the months of March through July as a peak for the extent of Dactylogyrus infection. These months are the time of gonadal development and reproduction in Telescope Shiners. Introduction Dactylogyrus Diesing (Phylum Platyhelminthes: Class Monogenoidea) is a holarctic genus of flatworm gill flukes that infect freshwater fishes, primarily Cypriniformes. These highly host-specific gill flukes attach to host gills with the use of their unique haptor, armed with a series of 14 hooks and 2 large anchors (Mueller 1936). They irritate gill tissues, causing significant mortalities in aquaculture and the ornamental fish industry. Dactylogyrus have a direct life cycle, with no intermediate host. New hosts are infected by free-swimming larvae, and at 20 °C, European Dactylogyus species hatch in five days and mature in six to ten days, with the life cycle completing in 18 to 20 days (Olsen 1986). There are no data describing reproductive impacts of Dactylogyrus species upon any North American fish, and, with the exception of Knipes and Janovy (2009), no studies reporting seasonality. Dactylogyrus spatulus Cloutman, has been found upon the gills of Notropis telescopus Cope (Telescope Shiner) (Cloutman 1988). The Telescope Shiner occurs throughout the river drainages of the Tennessee River on the Cumberland Plateau of eastern North America, and within the White and Black river systems in Arkansas and Missouri (Mettee et al. 1996). Where found, it is a common species that prefers small to medium-sized upland streams in flowing water near riffles over gravel or rock substrates. Its reproductive biology in Alabama was 1Department of Biological Sciences, University of Alabama in Huntsville, Huntsville, AL 35899. 2Department of Biological Sciences, University of Iowa, Iowa City, IA 52242- 1324. *Corresponding author - stallsb@uah.edu. 36 Southeastern Naturalist Vol. 11, No. 1 recently described (Holmes et al. 2010), and its diet consists of small terrestrial insects and aquatic insect larvae (Mettee et al. 1996). Parasites play an important role in the biology of animals. They often are responsible for host mortality and may attenuate success or alter timing of reproduction (review in Michalakis and Hochberg 1994). Interactions between hosts and parasites have been cited as major evolutionary forces, providing for the maintenance of sex and greatly influencing rates of speciation (review in Hudson and Greenman 1998). Although ecologists acknowledge the importance of parasites in communities, their effects remain under-investigated (Thomas et al. 2000). The purpose of this study is to elucidate the host-parasite interaction between the Telescope Shiner and Dactylogyrus parasites, specifically, the seasonal prevalence and abundance of gill flukes upon the host, and whether increased prevalence of infection may coincide with peak reproductive potential. Field-Site Description Fish used in this study were collected from two sites: Estill Fork of the Paint Rock River, Jackson County, AL (34°57'54"N, 86°09'14"W), and Hurricane Creek, also a tributary to the Paint Rock River, Jackson County, AL (34º59'12"N, 86º05'41"W). The latter is within the Walls of Jericho tract of Alabama’s Forever Wild land holdings. These streams are clear, shallow riffle and run systems over gravel, sand, and cobble. They range from 10–15 m wide and rarely more than 1 m deep. Both run through narrow incised valleys between ridges about 350 m high. Materials and Methods Collection of fish Fish collections were performed using seine nets (3 m long x 1.3 m deep; 3-mm mesh). Monthly collections were made in late morning. Fish were not selected by size or sex. Water temperature (°C) was recorded during each collection. Monthly collections made at Hurricane Creek (Feb 2007–Sep 2007) consisted of ≈30 Telescope Shiners (as per our permit), which were euthanized using MS-222 (tricaine methanesulfonate) and immediately transferred to Sörensen’s solution for fixation (Weydert and Cullen 2010). Fish collected from Estill Fork (Oct 2008–Jan 2009) were euthanized with MS-222 and then placed on ice for an hour until being fixed in Sörensen’s solution. Gill inspection Visual inspections were performed on removed gill arches from the collected fish. To remove gill arches, the operculum was forced anteriorly, and each gill arch was removed with forceps. All gill arches from the right and left sides of each fish were removed and examined. Intact gill arches were stained in a 1% acetocarmine solution for 24 to 48 hours before being inspected under a dissecting microscope at 30X magnification. Parasites were counted by feathering through the gill filaments with a dissecting needle on both sides of each gill arch to ensure all of the parasites on a given arch were counted. Approximately 15 parasites 2012 A.B. Adrian, B. Holmes, and B.W. Stallsmith 37 were examined for species determination, and all showed the characteristics of D. spatulus as described by Cloutman (1988). Because such a small number of the total parasites counted were identified to species, this study refers to all observed parasites simply as Dactylogyrus, although no other species of Dactylogyrus are known to occur on Telescope Shiners. Length and mass data collection and determination of sex and gonadal condition of fish Standard length (nearest 0.01 mm) was recorded for each fish with digital calipers. Individuals were weighed after blotting to remove excess fluid. Gonads were removed, and gonad mass was recorded to 0.01 g. Sex was determined through visual gonadal examination. The gonadosomatic index (GSI) was calculated as: (gonad mass/somatic mass) x 100. An Ohaus Explorer balance (Pine Brook, NJ) was used for the collection of all mass data. These methods follow those described in Holmes et al. (2010). Statistical analysis The terminology of Bush et al. (1997) is used to describe the percentage of hosts infected with one or more parasites (prevalence) and the number of individual parasites in an infected host (intensity of infection). The abundance of infection per fish was organized into a frequency distribution for each month, and the monthly counts were totaled over the entire year to give a frequency distribution for the entire year. To determine if parasites infect Telescope Shiner individuals at random, the yearly distribution of parasites per fish was compared with that of the expected Poisson distribution. The expected values were calculated by the equation Expected = nke-n/k!*N, where n equals the average number of parasites per fish, N equals the total number of fish examined, and k equals the number of parasites found for the frequency being examined. These calculated expected values were compared to the observed yearly distribution through a chi square analysis. In order to keep expected values greater than 1 for this calculation, the fish with more than 8 parasites were combined into one category of 8 or more parasites. Because the prevalence appeared to increase during the Telescope Shiner breeding season (Holmes et al. 2010), the percentage of infected and non-infected individuals in both breeding and non-breeding seasons were compared using a chi square contingency analysis. In order to determine what is related to whether an individual is infected by parasites, a binary logistic regression was performed in the software program SPSS. The initial independent variables used to create the logistic model were standard length, GSI, and somatic weight, a calculated weight adjusted by removing the weight of the gonad for each individual fish. The dependent variable was infection, where 0 was used to represent a fish that was non-infected, and 1 represented infected. 38 Southeastern Naturalist Vol. 11, No. 1 Table 1. Summary of intensity, mean abundance, and prevalence and calculated expected values for the Poisson distribution based on the observed total distribution for Dactylogyrus infecting Telescope Shiners. Data are separated into breeding and non-breeding seasons to show the differences in parasite intensity. Hurricane Creek, breeding season Estill Fork, non-breeding season Intensity of infection per fish Feb March April May June July Aug Sept Oct Nov Dec Jan Total Exp 0 13 10 9 3 3 10 18 17 9 12 25 11 140 30.67 1 7 1 1 1 2 4 15 10 3 6 8 3 61 77.43 2 7 3 4 4 9 3 5 8 5 1 4 1 54 97.75 3 2 5 1 4 5 3 1 2 1 1 2 0 27 82.27 4 0 4 2 1 5 2 0 0 1 0 2 3 20 51.93 5 1 2 7 2 6 2 0 0 1 1 0 0 22 26.22 6 1 4 3 1 3 2 0 0 0 0 0 0 14 11.03 7 1 0 1 3 0 0 0 1 0 0 2 0 8 3.98 ≥8 0 4 5 0 3 1 0 0 0 0 0 0 37 1.26 Total fish 32 37 39 25 42 29 39 38 20 20 42 18 383 Total parasite 45 149 194 147 183 80 28 39 25 11 35 31 967 Average parasite 1.41 4.03 4.97 5.88 4.36 2.76 0.72 1.03 1.25 0.55 0.83 1.55 2.52 %infected 59 73 77 88 93 66 54 55 55 40 40 39 63 2012 A.B. Adrian, B. Holmes, and B.W. Stallsmith 39 Results A total of 967 Dactylogyrus were counted on the gills of 383 individual Telescope Shiners, for an overall mean abundance of 2.52 ± 0.54 SE parasites per fish. Mean abundance was higher than the annual average from March through July (highest in May) and lower during August through February (lowest in November) (Table 1). If it can be assumed that parasites would be equally likely to develop an association with any Telescope Shiner individual, there should be a random assortment of parasites per fish, which can be tested against the Poisson distribution of the yearly parasite intensity counts (Table 1). The chi square test (χ2 5 = 1493, P < 0.001) was found to be statistically significant, showing that the abundance of parasites does not appear to be random. Fewer fish than expected had 2 parasites, three times fewer fish than expected had 3 parasites, and about 2.5 times fewer fish than expected had 4 parasites. Greater than four times more fish than expected had no parasites, two times more fish than expected had 7 parasites, and significantly more fish than expected had 8 or more parasites. The observed number of fish having 1, 5, or 6 parasites were close to the expected intensity of infection. The chi square analysis of the contingency table (Table 2) comparing the number of infected and non-infected fish during the breeding and non-breeding seasons was statistically significant (χ2 1 = 22.40, P < 0.01), showing that the prevalence of infection differs strongly between breeding season and non-breeding seasons. The chi square analysis also showed that there were almost 2 times more non-infected fish during the non-breeding season than expected, while there were about twothirds as many infected fish during the non-breeding season as expected. This finding supports the idea that parasite infection of Telescope Shiners is more likely to occur during the breeding season than the non-breeding season. An initial binary logistic regression using length, somatic weight, and GSI as independent variables indicated that length was not significantly related to presence or absence of Dactylogyrus. The regression was run without length as a variable (Table 3) and determined that presence or absence of infection was Table 2. Comparison of Dactylogyrus parasitizing Telescope Shiners during the breeding versus non-breeding season (χ2 1 = 22.40). Bold values are statistically significant (P < 0.05). Hurricane Creek, breeding season Estill Fork, non-breeding season Observed Expected Chi square Observed Expected Chi square Non-infected 83 102.72 3.78 57 37.28 10.43 Infected 198 178.28 2.18 45 64.72 6.01 Table 3. Results of binary logistic regression showing the relationships of somatic weight and GSI of Telescope Shiners with presence or absence of infection of Dactylogyrus. B S.E. df P Exp(B) Somatic weight 1.369 0.405 1 0.001 3.930 GSI 0.074 0.033 1 0.027 1.077 Constant -1.213 0.525 1 0.021 0.297 40 Southeastern Naturalist Vol. 11, No. 1 statistically significant when incorporating the variables of somatic weight and GSI of examined fish. The overall equation Log (Presence of Infection) = 1.369(Somatic Weight) + 0.074(GSI) – 1.213 showed that the largest contribution to infection was somatic weight. This variable might be attributed to the age or overall health of individual fish, since sex and time of year were removed from this variable. Discussion Parasite abundance in the host Telescope Shiners showed a strong seasonal pattern, with low abundance from August to February followed by higher abundance from March to July. Stream water temperatures varied from a low of 9 ºC in February to a high of 24 ºC in July. While the Dactylogyrus life cycle is known to be somewhat temperature dependent (Olsen 1986), the temperature maximum in July does not correspond with peak parasite abundance. The months of peak abundance coincided with reproductive effort of the host Telescope Shiners as observed through GSI and gonadal condition (Holmes et al. 2010). This general seasonal Dactylogyrus abundance pattern was found by Knipes and Janovy (2009) in the cyprinid host Pimephales promelas Rafinesque, although the seasonal fluctuations in abundance were not as pronounced as those in this study. Such close association with reproductive timing has been attributed to coevolutionary processes whereby the parasites have matched their reproduction with the time when the host is least capable of fighting off the infection due to the dramatic energy costs of reproduction (Lamková et al. 2007). A significant correlation between fish weight and the prevalence of infection (Table 3) can be attributed to higher gill surface area of older, larger fish. Elevated prevalence of infection by Dactylogryus is positively correlated with the GSI of Telescope Shiners (Table 3), indicating that when fish are reproductive, the parasite prevalence increases. This result raises the question of the effects of parasite infection on the host’s reproductive effort, since an individual’s GSI is a good measure of reproductive effort. It is unclear whether Dactylogyrus preferentially infects certain individuals, or if the infection of an individual is due to a series of purely random factors. Laboratory studies with the Trinidadian Guppy, Poecilia reticulata Peters, have shown that different Guppy populations vary in their resistance to monogene trematodes (van Oosterhout et al. 2003), and individual Guppy’s resistance to infection is replicable (Cable and van Oosterhout 2007a). This finding strongly suggests that the action of parasite-mediated selection on host immunity can be a major influence on the ecology and evolution of freshwater fishes including the Telescope Shiner and its congeners (Cable and van Oosterhout 2007b). Although not determined in the present study, the presence of Dactylogyrus during May at the peak of Telescope Shiner gonadal development may impact gonad development as the intensity and prevalence of infection also peak 2012 A.B. Adrian, B. Holmes, and B.W. Stallsmith 41 (Table 1; Holmes et al. 2010). Diminished GSI and heightened Dactylogyrus intensity of infection during the spawning season was found in the European cyprinid Leuciscus cephalus L. by Lamková et al. (2007). It is likely that such a relationship exists between other North American cyprinids and their specific Dactylogyrus parasites. Acknowledgments Part of this work was performed in the Walls of Jericho state lands tract with a permit from the State Lands Division of the Alabama Department of Conservation and Natural Resources. We wish to thank Nick Sharp of the State Lands Division for his assistance acquiring and using that permit. Taito Eguchi and James Swarthout assisted with much of the field and laboratory work. Literature Cited Bush, A.O., K.D. Lafferty, J.M. Lotz, and A.W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575–583. Cable, J., and C. van Oosterhout. 2007a. The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biological Journal of the Linnean Society 90:647–655. Cable, J., and C. van Oosterhout. 2007b. 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Guegan, Y. Michalakis, and F. Renaud. 2000. Parasites and host lifehistory traits: Implications for community ecology and species co-existence. International Journal for Parasitology 5:669–674. van Oosterhout, C., P.D. Harris, and J. Cable. 2003. Marked variation in parasite resistance between two wild populations of the Trinidadian Guppy, Poecilia reticulata (Pisces: Poeciliidae). Biological Journal of the Linnean Society 79:645–651. Weydert, C.J., and J.J. Cullen. 2010. Measurement of superoxide dismutase, catalase, and glutathione peroxidase in culture cells and tissue. Nature Protocols 5:51–66.