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Helminth parasites of two species of Lepomis (Osteichthyes: Centrarchidae) from an urban watershed and their potential use in environmental monitoring.

ABSTRACT

We provide a checklist of the common parasites of bluegill (Lepomis macrochirus) and redbreast sunfish (Lepomis auritus) collected from eight creeks within an urban watershed located in Columbus, Georgia. A total of 12 parasite species were observed from 427 fish dissected. Bluegill (n = 222) were infected with 11 species, which included five species of larval helminths (Proteocephalus sp., Bothriocephalus sp., Posthodiplostomum minimum, Diplostomulum sp. and Clinostomum complanatum), one adult trematode (Pisciamphistoma stunkardi), four adult nematodes (Philometra sp., Philometra intraoculus, Spinetectus carolini and Camallanus oxycephalus) and one adult acanthocephalan (Neochinorhynchus cylindratus). Redbreast sunfish (n = 205) were infected with the same parasite species, except for the absence of larval Bothriocephalus sp. and the presence of an adult trematode (Crepidostomum cooperi). Metacercariae of the trematode P. minimum were the most common parasite in both fish species. Similar parasite communities in these sunfishes suggest that these species share similar microhabitats within the watershed, food resources and foraging sites. Seasonal comparison between the number of summer and winter parasites indicate a greater mean number of parasites per host in summer. We discuss the utility of such baseline parasite data in the potential environmental monitoring of the Bull and Upatoi Creeks watershed.

Key Words: Checklist, trematodes, nematodes, cestodes, acanthocephalans, sunfish, Centrarchidae, Lepomis macrochirus, Lepomis auritus, Muskogee County.

INTRODUCTION

Parasite assemblages of sunfishes (Lepomis) have received much interest and have been extensively surveyed (McDaniel 1963, McGraw and Allison 1967, Harley and Keefe 1970, Meade and Bedinger 1972, McDaniel and Bailey 1974, Cloutman 1975, Deselle et al. 1978, Jilek and Crites 1980, Fiorillo and Font 1996, Wilson et al. 1996, Muzzall and Peebles 1998, Fiorillo and Font 1999) thus making them a good investigative model. However, parasite community structure in fishes can vary greatly with environment and geographic region (Holmes and Price 1986). While regional variation in parasite communities of Lepomis is well documented in the literature, environmental influences on temporal variation of parasites within a region or locality may be of specific interest for environmental monitoring (e.g., Lafferty 1997, Kennedy 1997, Sures 2004). However, such monitoring is only possible with a baseline assessment of typically occurring parasites and their abundance. By documenting what parasites infect specific host fishes and their abundance in a natural system, investigators may be able to monitor ecosystem health and identify environmentally-induced disease (Overstreet 1997).

The use of parasites as a bioindicator of ecosystem health is not novel and has been reviewed extensively (Adams 1990, Marcogliese 2005). Parasites may be particularly useful in monitoring anthropogenic related pollution (Khan and Billiard 2007), as increased parasitism is often observed as host defense mechanisms are compromised by certain pollutants. For example, toxic chemicals impair mucus production in fishes, making them more susceptible to gill ciliates (e.g. Khan et al. 1994). In addition, most helminth parasites of fish rely on multiple hosts, connected through the food web or other ecological interactions, for completing their complex life cycles and thus their presence or absence may provide useful information about the ecological integrity of an aquatic system. By establishing baseline data, potential increases (or decreases, see Marcogliese 2004) in parasite richness and abundance could be used by future investigators as a mechanism for environmental monitoring (Lafferty 1997, Kennedy 1997, Sures 2004). Furthermore, both the presence of parasites and their abundance within a host individual (or population) may be costly and can be characterized specifically as disease. Such epidemiological information regarding disease and parasitism is becoming more common in monitoring the health of biological and aquatic systems (e.g., Kennedy 1997, Hoffman 1999, Sures 2004).

A specific aquatic system of interest, the Bull and Upatoi creeks watershed, consists of eight creeks located within and just east of Columbus, Georgia (Figure 1). Both urban development and rapid changes in land-use are predicted to influence the environmental quality of this aquatic system. Additionally, potential land-use change along the northern boundary of Fort Benning has been of great interest and a stimulus for this funded study (ERDC-CERL Contract #DACA 4200-C-0047). This study and another investigation of fish diversity (Martin and Lutterschmidt 2013) were aimed at investigating how urbanization and land-use type may influence biological diversity. Biodiversity and identification of potential indicator species could be used as ecological drivers in the application of the Land use Evolution and impact Assessment Model (LEAM) at Fort Benning. LEAM was developed with funding from the National Science Foundation and simulates changes in land use across a landscape that may result from spatial and dynamic interactions among economic, ecological, and social systems (Deal 2001). Insight gained from LEAM simulations would inform environmental policy and planning and has been used with other models (Wang et al. 2005) to help in land-use management decisions.

Here we surveyed the parasites of bluegill (Lepomis macrochirus) and redbreast sunfish (Lepomis auritus) to: (1) inventory and provide a checklist of the parasites found in the Bull and Upatoi Creeks watershed, Muskogee County, Georgia, (2) compare seasonal variation in parasite richness and abundance, within a host species, (3) compare variation in parasite richness and abundance between host species, and (4) calculate indices of parasite biodiversity to potentially serve as an indicator (Marcogliese 2005) and ecological driver in future land-use models. These data may ultimately provide investigators with information on the parasites of two common fishes and needed baseline data to evaluate potential changes in environmental quality due to land-use change, urbanization, or pollution within an urban watershed of Columbus, Georgia.

MATERIALS AND METHODS

A total of 222 bluegill (Lepomis macrochirus) and 205 redbreast sunfish (Lepomis auritus) were collected from eight small creeks (Lindsey, Cooper, Flatrock, Bull, Dozier, Randall, Kendall and Baker) within the Bull and Upatoi Creeks watershed, Muskogee County, Georgia. Creeks are located perpendicular to Macon Road (U.S. Highway 22) east of Columbus, Georgia, and just north of the northern boundary of Fort Benning (Figure 1). We accessed each creek from Macon Road and sampled fish from stream pools and mns both north and south of where each creek intersects Macon Road. A backpack electro-fisher (Smith-Root[R] Inc.) was used to collect fishes which were transported live to our field laboratory and euthanized prior to dissection. Individuals that could not be freshly dissected, were frozen for transport and later dissection at Sam Houston State University, Huntsville, Texas. Fish were collected in February (winter) and August (summer) 2002, six months apart, to investigate potential temporal variation in host parasite communities. All field research, specimen collection, and dissections were conducted in accordance with the methods and protocols outlined by the American Society of Icthyologists and Herpetologists (1987) Guidelines for the Use of Fishes in Field Research. All fish were collected under a permit (29-WMB-01-147) issued to William I. Lutterschmidt by the Georgia Department of Natural Recourses.

Body mass (g) and standard length (mm) of hosts were measured prior to dissection. The eyes, eye cavities, viscera (heart, spleen, liver, kidney and gonads), and intestinal tract (intestinal mesentery, intestinal lumen, pyloric ceca and stomach) were examined for helminth parasites. Gills were not examined for parasites (e.g., Monogenes). All parasites were identified to the lowest possible taxon (Hoffman 1999). Trematodes were fixed in Berland's solution (9 parts acetic acid, 1 part 37% formaldehyde) and stored in alcohol-formalin-acetic acid (AFA). Nematodes were fixed in Berland's solution and placed in glycerine alcohol. Acanthocephalans were refrigerated in distilled water overnight to extrude the proboscis, and several small holes were made in the body wall with fine dissecting pins prior to fixation in AFA. Trematodes and acanthocephalans were stained with Semichon's Carmine procedure (Meyer and Olsen 1975), dehydrated in a graded alcohol series, cleared in xylene, and using gum damar, mounted on slides for positive identification. Nematodes were cleared and examined as temporary mounts in glycerine jelly.

Nematodes and acanthocephalans were observed only for presence or absence due to their low occurrence. Trematodes and cestodes were most abundant and therefore the seven species in these two groups were used in our community analyses to summarize species richness, total parasites, and the mean number of parasites per host. We used Shannon-Weiner indices of diversity (Shannon 1948 as cited in Zar 1999) to calculate species diversity (H') and evenness (J' = H'/H'max). Trematode and cestode counts were used to calculate percent similarity index (PSI) between fish species and all parasites species (n = 12) were used to calculate the Jaccard community coefficient (Table I). We used SigmaPlot[c] Version 11.0 and SPSS[c] Version 22 to run a 2 x 2 factorial, two-way analysis of variance with both species (bluegill and redbreast sunfish) and season (winter and summer) as independent factors and total parasite load per host fish as the dependent factor. Total parasite load data were corrected for normality and equal variance using the square-root transformation. All results are considered significant at P [less than or equal to] 0.05.

RESULTS AND DISCUSSION

Parasites (Table I) collected from bluegill (Lepomis macrochirus) and redbreast sunfish (L. auritus) from eight creeks of the Bull and Upatoi creeks watershed (Figure 1) have been previously documented in these hosts (see Hoffman 1999). Bluegill (n = 222, mean body mass ([+ or -] SE) = 11.0 [+ or -] 0.54 g, mean standard length = 84.6 [+ or -] 1.35 mm) were infected with 11 parasites species including five larval helminths (Proteocephalus sp., Bothriocephalus sp., Posthodiplostomum minimum, Diplostomulum sp. and Clinostomum complanatum), one adult trematode (Pisciamphistoma stunkardi), four adult nematodes (Philometra sp., Philometra intraoculus, Spinetectus carolini and Camallanus oxycepha/us) and an adult acanthocephalan (Neochinorhynchus cylindratus). Redbreast sunfish (n = 205, mean body mass = 14.6 [+ or -] 0.85 g, mean standard length = 88.4 [+ or -] 1.64 mm) were infected with the same parasites, except for the absence of larval Bothriocephalus sp. and the presence of an adult trematode (Crepidostomum cooperi).

Bluegill prey mostly on aquatic insect larvae, microcrustaceans, fallen terrestrial insects and occasionally plant matter/algae, which they likely consume accidentally while foraging for aquatic insects (Etnier 1971, Sadzikowski and Wallace 1976), and redbreast sunfish feed on surface dwelling invertebrates, insect larvae, crayfish, gastropods and fishes (Goldstein 2000, Murphy et al. 2005). From stomach contents of hosts, we found primarily finger-nail clams, freshwater snails, insect larvae, and algae in bluegill. We observed fewer of these prey in redbreast sunfish and noted partially digested fishes (Cyprinidae) suggesting that redbreast sunfish in this system are feeding on larger prey, including vertebrates. We might expect the parasites of these two Lepomis species to differ due to their differences in trophic strategies. While bluegill are generalists, other sunfishes (e.g., redbreast sunfish and pumpkinseed) are considered specialists in their feeding ecology (e.g., Goldstein 2000, Robinson et al. 1993). Regardless of these apparent differences in feeding strategies, these hosts shared 10 of the 12 helminth species observed in this study (Table I) and their parasite communities were similar (percent similarity index = 99.49%, Jaccard community coefficient = 0.833, Table I) which suggests that bluegill and redbreast sunfish may share foraging sites and food resources, as nine of the 12 helminths infect fish through the food web. However, the high degree of similarity between these two parasite communities is likely due to the high abundance of P. minimum representing 99% of all helminths. This parasite infects fish by penetrating through a host's skin and encysting in its visceral organs. It is likely that both bluegill and redbreast sunfish co-occur in areas where physid snails, first intermediate host in the life cycle of this trematode, are actively shedding the parasite.

We found both low and similar parasite diversity (H') and evenness (J') for the two species of Lepomis, mostly due to the dominant abundance of P. minimum in both hosts (Tables I and II). Although more fish were collected in the winter (n = 241) than summer (n = 186) sample, the winter sample showed lower total parasites and greater difference in parasite diversity and evenness between host fishes (Table II). This might suggest that summer samples may be more repeatable and useful in the development of environmental monitoring regimes. With increased activity and frequent feeding during summer, fishes are more likely to acquire a parasite community that is more fully representative of the total helminth fauna available in the environment.

Although the parasite richness between these host fish species is similar, we found significant differences in the total parasites infecting bluegill and redbreast sunfish (F = 7.44; df = 1, 423; P = 0.007, Table III) with bluegill also harboring significantly more metacercariae of P. minimum (t = 4.038, df = 425, P = 0.042). However, both hosts appear to be equally exposed to snails shedding P. minimum cercariae, as prevalence of this parasite in both hosts is quite similar (Table I). Posthodiplostomum minimum shows preference, among centrarchid fishes, for Lepomis spp. suggesting this trematode may be less of a generalist than previously reported (Lane et al. 2015). Similarly, Fellis and Esch (2004) showed that green sunfish (L. cyanellus) are typically found in the littoral zone and presumably in closer proximity of snails shedding P. minimum cercariae than bluegill. However, green sunfish harbored significantly less worms than bluegill suggesting that green sunfish may be less susceptible to infection. Assuming both bluegill and redbreast sunfish have similar probability of encounter with this parasite, bluegill appear to be the preferred host in this watershed. Further laboratory studies are needed to critically examine a "differential susceptibility" versus a more parsimonious "differential exposure" hypothesis to explain these observed differences in how P. minimum parasitizes Lepomis species.

We also found significant differences between the winter and summer samples (F = 67.98; df = 1, 423; P = 0.001, Table III), suggesting that the use of parasites for environmental monitoring must control for seasonal effects. A non-significant interaction between fish species and season indicate that both host fishes experience similar changes in seasonally dependent parasite loads (Table III). Bluegill and redbreast sunfish were each more heavily parasitized in summer than in winter, with fish collected in winter harboring less than half the number of parasites infecting fish collected in summer (Table II). These data suggests greater winter mortality for fishes that are heavily parasitized. Lemly and Esch (1983, 1984a and 1984b) showed a similar pattern as bluegills infected with more than 50 metacercariae of Uuulifer ambloplitis, a close relative of P. minimum, suffered significantly higher winter mortality than less infected conspecifics. Like U. ambloplitis, P. minimum metacercariae are not lost once recruited, which leads to an accumulating worm burden and the potential for heavily infected individuals which may be more susceptible to environmental stressors (see Lutterschmidt et al. 2007). Previous studies (e.g. Spall and Summerfelt 1970, Amin 1984, Amin 1990, and Wilson and Camp 2003) have found substantial variation in the prevalence, abundance, and mean intensity of P. minimum over several geographic regions but P. minimum metacercariae are typically the dominant parasite. Because of the high abundance of P. minimum across creeks within this urban watershed, this parasite species may serve as good response variable for environmental monitoring. Metacercariae of this parasite in both fish species infected the pericardial sac of the heart, liver, spleen, kidney, gonads, and mesenteries of the peritoneal cavity.

Both field and laboratory studies suggest that there are 2 subspecies of P. minimum which infect North American freshwater fishes. Posthodiplostomum minimum minimum infect minnows (Cyprinidae), while P. minimum centrarchi infects fishes in the family Centrarchidae (Hoffman 1999). However because P minimum has such a wide distribution and can infect so many different fish hosts, absolute identification to species can be obtained only from molecular techniques or from adult parasites recovered from experimental infection with the metacercariae.

Pisciamphistoma stunkardi was the second most common parasite in both fish species and was observed in the intestinal lumen and pyloric ceca. Proteocephalus sp. was observed in the liver and associated connective tissues of both fish species, Diplostomulum sp. was found in the aqueous humor and lens of the eye in both fish species, while Crepidostomum cooperi was observed in the digestive tract and Bothriocephalus sp. was recovered from the liver in only the redbreast sunfish.

There may be numerous abiotic and biotic considerations for the temporal changes in parasite diversity and abundance, and the assumption that infection increases/decreases with environmental pollution and stress (Schwaiger 2001) must be carefully evaluated (Sures 2004, Marcogliese 2005). However, there is overwhelming evidence that parasites abundance may serve as an excellent metric for the monitoring of environmental change (e.g., Mackenzie 1999, Lafferty 1997, Overstreet 1997, Sures et al. 1999, Sures 2001). Although parasites are not classically viewed as sentinel or indicator species, as are macro-invertebrates (Rosenburg and Resh 1993) and some fishes (Chovanec et al. 2003), the advantages of parasites are both numerous and great (Sures 2004, Marcogliese 2005). Additionally, both the presence and abundance of gill parasites (e.g., monogenes) might serve as an additional indicator for environmental quality as they have direct interface with both the host and the environment. Monogenes were not investigated here due to our limited expertise with this group.

Here we establish a baseline for the parasites and their abundance in two common host fishes, the bluegill and redbreast sunfish, within eight creeks of the Bull and Upatoi Creeks watershed, Muskogee County, Georgia. Because this watershed is subject to future land-use change and anthropogenic disturbances associated with urbanization, we hope these data may serve future investigators and provide baseline data for the potential establishment or enhancement of environmental monitoring protocols and programs for the creeks of Columbus, Georgia.

ACKNOWLEDGEMENTS

We thank Laurieanne Dent, Daniel S. Millican, and Dennis K. Wasco for their dedicated field assistance as paid technicians on this project. We also acknowledge a research grant awarded to William I. Lutterschmidt by the Engineer Research and Development Center (ERDC) and the Civil Engineering Research Laboratory (CERL) of the US Army Corps of Engineers (ERDC-CERL Contract #DACA 42-00-C-0047). We acknowledge the assistance provided by Gordon A. Plishker and all personnel of the Texas Research Institute for Environmental Studies (TRIES) at Sam Houston State University. Special thanks to David R. Hoffpauir (Operations Manager of the TRIES GIS Laboratory) for his assistance in GIS mapping. We also thank Hugh Westbury of the Strategic Environmental Research and Development Program (SERDP), Ecosystem Management Project (SEMP), and Harold (Hal) Balbach of the US Army ERDC and CERL for their dedicated interest in and support of this project. Our sincere thanks to Julia C. Buck, William F. Font and Autumn Smith-Herron for their reviews of this manuscript.

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Sidney M. Anderson [1], Riccardo A. Fiorillo [2] *, Tamara J. Cook [3] and William I. Lutterschmidt [3,4] *

[1] Texas Veterinary Medical Diagnostic Laboratory Texas A&M University, College Station, Texas 77843

[2] School of Science and Technology Georgia Gwinnett College, Lawrenceville, Georgia 30043

[3] Department of Biological Sciences Sam Houston State University, Huntsville, Texas 77341

[4] Texas Research Institute for Environmental Sciences Sam Houston State University, Huntsville, Texas 77341

* Corresponding Authors: rfiorill@ggc.edu, lutterschmidt@shsu.edu

Table I. A checklist of the parasites of the bluegill (Lepomis
macrochirus) and redbreast sunfish (L. auritus) sunfishes within the
Bull and Upatoi creeks watershed. Parasites are listed in order of
greatest to least abundance. Either counts, presence (X), or absence
(-) are indicated and followed by (prevalence) for each parasite
species. Due to low occurrence, nematodes and acanthocephalans counts
are not included. Trematode and cestode counts were used to calculate
percent similarity index (PSI = 99.49%) between fish species, and all
parasites species (n = 12) were used to calculate Jaccard community
coefficient (J = 0.833). Asterisk (*) indicates larval form of the
parasite.

                                                          Redbreast
                                          Bluegill         Sunfish
Parasite Species (n)                   L. macrochirus    L. auritus

Trematodes

Posthodiplostomum minimum * (26742)    15810 (94.5%)    10932 (94.6%)
Diplostomulum sp. * (84)                 18 (4.9%)        66 (8.2%)
Pisciamphistoma stunkardi (31)           12 (3.6%)        19 (6.8%)
Clinostomum complanatum * (7)             3 (0.4%)        4 (1.9%)
Crepidostomum cooperi (3)                    --           3 (0.9%)

Cestodes

Proteocephalus sp. * (73)                50(12.1%)        23 (6.8%)
Bothriocephalus sp. * (1)                 1 (0.4%)           --

Nematodes

Philometra intraoculis                       X                X
Philometra sp.                               X                X
Spinetectus carolini                         X                X
Camallanus oxycephalus                       X                X

Acanthocephalans
Neochinorhynchus cylindratus                 X                X

Table II. Summary of species richness, total parasites, mean
([+ or -] standard error, SE) parasites per fish host, mean ([+ or -]
standard error, SE) P. minimum per fish host, species diversity (H')
and species evenness (J') for bluegill (L. macrochirus, Lm) and
redbreast sunfish (L. auritus, La) sunfishes collected in winter and
summer 2002. Due to low occurrence, nematodes and acanthocephalans
were included in the calculation of species richness only.

                              Parasite Data

                                            Mean (SE)
                    Species      Total      Parasites
Season   Host (n)   Richness   Parasites     per Host

Winter   Lm (132)      5         6524       49.4 (7.9)
         La (109)      4         3591       32.9 (8.2)
Summer   Lm (90)       4         9370      104.1 (13.3)
         La (96)       5         7456       77.7 (8.9)

                             Parasite Data

                     Mean (SE)      Species    Species
                     P. minimum    Diversity   Evenness
Season   Host (n)     per Host       (H')        (J')

Winter   Lm (132)    49.3 (7.9)     0.0068      0.0098
         La (109)    32.7 (8.2)     0.0181      0.0300
Summer   Lm (90)    103.3 (13.3)    0.0225      0.0374
         La (96)     76.6 (8.9)     0.0343      0.0490

Table III. Summary statistics of a 2 x 2 factorial, two-way analysis
of variance showing significance differences between host fish
species (bluegill and redbreast sunfish) and season (winter and
summer) for total parasite load.

Source of Variation      df      SS        MS        F       P

Species                   1    144.84    144.84    7.44    0.007
Season                    1    1323.04   1323.04   67.98   0.001
Interaction (Species x    1     7.57      7.57     0.39    0.533
  Season)
Residual                 423   8232.79    19.46
Corrected Total          426   9659.97    22.67
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Author:Anderson, Sidney M.; Fiorillo, Riccardo A.; Cook, Tamara J.; Lutterschmidt, William I.
Publication:Georgia Journal of Science
Article Type:Report
Date:Jun 22, 2015
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