2010 NORTHEASTERN NATURALIST 17(2):211–222 Giant Kidney Worms in Mink from New York: Prevalence, Distribution, and Health Implications Jefferey J. Loukmas1,*, David T. Mayack2, and Milo E. Richmond3 Abstract - We examined 612 wild Neovison vison (Mink) carcasses collected during 1998–2002 from New York State for presence of Dioctophyme renale (Giant Kidney Worm). Twenty-three Mink (15 males and 8 females) contained the parasite in the right kidney. The percentage of infected Mink (3.8%) was considerably lower than was found in Ontario (48%) and Minnesota (27%), but higher than in Manitoba (1%) and North Dakota (less than 1%). We found a clustered distribution of Giant Kidney Worms in Mink; all infections were located in the northern and central areas of the state and were restricted to a few physiographic and hydrological regions. Left kidneys were enlarged in parasitized Mink, but other condition measures (body and omentum weights, body weight:length ratio, and hepatic metal concentrations) did not differ between infected and non-infected animals when adjusted for gender, age, and capture location. This assessment indicated that Giant Kidney Worms have a minimal impact on Mink health; however, it should be viewed with caution because animals severely affected by infection may have been less susceptible to trapping. Future research should focus on the impact of infections on long-term health and mortality of Mink and the ecological requirements of Giant Kidney Worms and hosts to understand why infections are clustered in certain areas. Introduction Dioctophyme renale Goeze (Giant Kidney Worm) is a large, dioecious parasitic nematode that primarily infects Neovison vison Schreber (Mink) and is occasionally found in a variety of carnivorous mammals, including other mustelids such as Lontra canadensis Shreber (River Otter), Martes americana Turton (American Marten), and Mustela spp. (weasels) (Anderson 1992). Giant Kidney Worms typically occupy only the right kidney of Mink, but on occasion are observed in the abdominal cavity (Mech and Tracy 2001). When the kidney is infected, the parenchyma is destroyed, resulting in the elimination of renal function (Anderson 1992). Often the kidney is infected with multiple worms, and a concurrent infection of both a male and female worm is necessary for egg fertilization. Fertilized eggs are passed to the environment via the urinary tract (Measures 2001). After entering an aquatic system, the eggs embryonate at 15–30 °C and then are consumed by Lumbriculus variegatus (Blackworm), an aquatic oligochaete known as the only intermediate host (Mace and Anderson 1975). This oligochaete is commonly 1New York State Department of Environmental Conservation, 625 Broadway, Albany, NY 12233-4753. 2New York State Department of Environmental Conservation, Hale Creek Field Station, Gloversville, NY 12078. 3New York Cooperative Fish and Wildlife Research Unit, Cornell University, USGS—BRD, Ithaca, NY 14853. *Corresponding author - jjloukma@gw.dec.state.ny.us. 212 Northeastern Naturalist Vol. 17, No. 2 ingested by paratenic hosts (frogs and fish) that are important sources of food for Mink, making this species particularly vulnerable to infection (Mace and Anderson 1975, Measures 2001, Measures and Anderson 1985). Giant Kidney Worms have been recorded in wild Mink in many areas of eastern and central North America (Crichton and Urban 1970, Hallberg 1953, Jorde 1980, Mace and Anderson 1975, Mech and Tracy 2001, Wren et al. 1986). Infected Mink were uncommon in North Dakota (<1% of examined Mink were infected) and Manitoba (1%), more numerous in Minnesota (27%), and relatively frequent in Ontario (48%). Previously reported cases of Giant Kidney Worm infections indicated that some Mink in the northern region of the New York State harbored the parasite (O’Connor and Nielsen 1981, Stone 1997); however, these were cursory reports and were limited in ecological scope. A high prevalence of the parasite may constitute an important mortality factor or may affect health. Graves (1937) and Meyer and Witter (1950) implicated Giant Kidney Worm infections as a cause of death in ranched Mink, and experimental infection with Giant Kidney Worm larvae has resulted in mortality (Mace and Anderson 1975). Mink may survive infections that only destroy one kidney as long as the other kidney compensates and remains healthy (Measures 2001). However, Wren et al. (1986) suggested that the health of Mink may be impaired because the loss of one kidney may decrease the ability to excrete toxins. The long-term impacts of Giant Kidney Worm infection on the heath of individual Mink and the status of Mink populations are largely unknown. To understand the implications of the Giant Kidney Worm to Mink in New York State, we documented the distribution and prevalence of infections throughout the state and examined several aspects of condition that may reflect the impact of infection on the health of Mink. Methods During 1998–2002, we collected skinned Mink carcasses from fur trappers throughout most of New York State during trapping seasons and several road-killed Mink at various times of the year. Capture locations and dates were provided by trappers. We stored carcasses frozen at -20 °C until necropsies were performed. We mapped and categorized capture locations according to several geographic classifications including general region (northern or southern; Will et al. 1982), physiographic zone (Dickinson 1983, Reschke 1990, Will et al. 1982), and hydrological unit (New York State Master Habitat Database [NY DEC 2003]) for ecological and spatial comparisons. We calculated capture location elevations as the mean of elevations for United States Geological Survey contour lines (NY DEC 2003) immediately above and below the location. All data were imaged using ArcView GIS 3.2 software (Environmental Systems Research Institute 1996). We determined gender, age class, and body length (without tail) and weight (without pelt) for nearly all Mink, and omentum and left kidney 2010 J.J. Loukmas, D.T. Mayack, and M.E. Richmond 213 weights for subsets of Mink. Abdominal cavities and kidneys of each carcass were examined for the presence of Giant Kidney Worms. Worms were removed from infected kidneys, counted, measured for length, and classified by gender. Lower canine teeth were extracted from each Mink and sent to an independent laboratory (Matson’s Laboratory, Milltown, MT) where age was determined from cementum annuli. Livers of selected Mink were collected, homogenized, and stored at -20 °C prior to analysis for cadmium (Cd), mercury (Hg), and lead (Pb). Liver samples were analyzed for metals by two laboratories: (1) Frontier Geosciences, Inc. (Seattle, WA) analyzed samples from the Northern Hudson River hydrological unit; and (2) the Analytical Services Unit of the New York State Department of Environmental Conservation (ASU NYS DEC, Gloversville, NY) analyzed samples from the St. Regis, Raquette, Oneida River, and Mid-Northern Lake Ontario units. All samples were digested in concentrated, high-purity nitric acid and diluted. Cold vapor-atomic spectrophotometry was used for Hg analysis. Either inductively coupled plasma-mass spectrometry (northern Hudson River unit samples) or graphite furnace-atomic absorption spectrophotometry (other samples) was used to analyze Cd and Pb. Frontier Geosciences analyzed 9–13 samples of a certified reference material DOLT-2 (National Research Council of Canada) and 23–25 duplicate samples for each metal. The ASU NYS DEC analyzed 7–8 samples of certified reference materials SRM 2976, SRM 1577b (US National Institute of Standards and Technology) and DORM-2 (National Research Council of Canada) for Pb, Cd, and Hg, respectively, and 15 duplicates. Lead was not at measurable levels for one or both of 9 duplicates analyzed by the ASU NYS DEC. Percent recoveries (mean ± standard deviation) were similar between laboratories: 96 ± 17.1 versus 99 ± 7.7, 94 ± 10.8 versus 95 ± 7.0, and 97 ± 4.8 versus 93 ± 4.5 for Pb, Cd, and Hg, respectively. Relative percent differences for duplicates with measurable levels were also similar: 10 ± 10.0 versus 9 ± 8.7, 7 ± 10.3 versus 7 ± 8.8, and 8 ± 8.9 versus 6 ± 6.4 for Pb, Cd, and Hg, respectively. All samples had measurable levels of Hg and Cd; however, Pb levels were below the method detection limit (0.029 μg/g) in 15 samples. We used half the detection limit for non-measurable levels in the statistical analysis of Pb concentrations. We selected five condition factors to evaluate health: body weight, body weight:length ratio, relative omentum weight (omentum weight/body weight x 100), relative left kidney weight (left kidney weight/body weight x 100) and liver metal concentrations (μg/g, wet-weight basis). Body weight, body weight:length ratio, and relative omentum weight were statistically evaluated for Mink captured from three locations with kidney worm infections: (1) the St. Regis, Raquette, and Northern Hudson River hydrological units comprising an “Adirondack” location; (2) the Mid-Northern Lake Ontario and Oneida River units comprising an “Eastern Lake Ontario” location; and (3) the Unadilla and East Branch Delaware River units comprising a “Southern Tier” location. The Eastern Lake Ontario, Adirondack, and 214 Northeastern Naturalist Vol. 17, No. 2 Southern Tier locations included body weights for 58 (10 infected), 95 (10 infected), and 30 (3 infected) Mink, respectively; body weight:length ratios for 53 (9 infected), 93 (8 infected) and 30 (3 infected) Mink, respectively; and relative omentum weights for 34 (7 infected), 84 (10 infected), and 4 (0 infected) Mink, respectively. Age class was lacking for four, two, and one Mink analyzed for body weight, body weight:length ratios, and relative omentum weight, respectively, from the Eastern Lake Ontario location and two Mink analyzed for each condition factor from the Adirondack location. The evaluation of relative left kidney weight and metal concentrations was restricted to Mink from the Adirondack and Eastern Lake Ontario locations. Relative left kidney weights and metal concentrations were available for 80 (6 infected) and 37 (10 infected) Mink, respectively, from the Adirondack location and 3 (1 infected) and 30 (8 infected) Mink, respectively, from the Eastern Lake Ontario location. Age class was lacking for two Mink analyzed for kidney weight from the Adirondack location and one Mink analyzed for metals from the Eastern Lake Ontario location. We used one-way analysis of variances (ANOVAs) to compare the number of worms between genders and the elevation of capture locations of infected vs. non-infected Mink. Metal concentrations were multiplied by 1000 and transformed to a base10 logarithm for statistical analysis. One-way ANOVAs also were used to compare condition factors and transformed metal concentrations between infected and non-infected Mink, with gender, age class, and location as covariates. Not significant as covariates in initial models were: gender for relative omentum weight (P = 0.180) and all metals (P = 0.075, P = 0.595, and P = 0.1003 for Hg, Cd, and Pb, respectively); age class for relative left kidney weight (P = 0.983) and Pb (P = 0.500); and location for relative omentum weight (P = 0.353), Cd (P = 0.786), and Pb (P = 0.888). Non-significant covariates were removed in subsequent reduced models. Reported means related to the effect of kidney worms were adjusted for significant covariates, and metals data were back-transformed for presentation. Summary statistics (means, standard errors [SE], and ranges), and ANOVAs were calculated with the MEANS and GLM procedures, respectively, within the Statistical Analysis System (SAS Institute 1985) using analytical methods by Freud and Littell (1986), Freud et al. (1986), and Hatcher and Stephanski (1994). Probability of a greater F value for factorial effects and covariates were considered significant for P < 0.05. Results We examined 612 Mink (436 males, 175 females, and 1 of unknown gender; age class was not available for 11 males and 1 female) for Giant Kidney Worms; 3.8% (15 males and 8 females) were infected. Infection rates were only slightly different between males (3.4%) and females (4.6%). One-year males were infected at twice the rate of less-than-oneyear males (6 of 99 [6.1%] vs. 8 of 251 [3.2%], respectively); older males (2–6 year) were infected at a lower rate (1 of 75; 1.3%). Less-than-one2010 J.J. Loukmas, D.T. Mayack, and M.E. Richmond 215 year females were infected at a rate (7 of 131; 5.3%) greater than older (1–4 year) females (1 of 43; 2.3%). We found 55 worms (32 females and 23 males), all in the right kidney. Male worms ranged in length from 115–276 mm (mean = 164 ± 7.9 mm). Female worms were 200–535 mm long (mean = 362 ± 16.3 mm). The number of kidney worms in each Mink varied from 1–9 (mean = 2.6 ± 0.40). The mean number of worms in male Mink (mean = 2.7 ± 0.62) was not different from that in females (mean = 2.5 ± 0.88; P = 0.802). The gender ratio also was similar for kidney worms in male (1.5:1 female to male worms) and female (1.2:1 female to male worms) Mink. Only 6 of 23 infected Mink (26%) contained both sexes of worms; therefore, most cases were not reproductively viable. Most infected Mink (18 of 23; 78%) occurred in the northern region of the state (Fig. 1). The infection rate for the northern region (18 of 254; 7.1%) was considerably greater than for the southern region (5 of 356; 1.4%). Infected Mink were located in 7 of 25 surveyed physiographic zones (Fig. 1). The combined infection rate for physiographic zones where kidney worms were detected was 7.7% (23 of 300). Infected Mink were most prevalent in the Oswego Lowland and Tug Hill Transition physiographic zones (10 of 54; 19% infection rate) in the north-central area of the state. Most of the remaining infected Mink were located in the greater Adirondack Mountain region, with 5 of 65 in the Central Adirondacks (7.7% infection rate), 4 of 27 in the Western Adirondack Foothills (15% infection rate), and 1 of 45 in the Eastern Adirondack Foothills (2.2% infection rate). Also, several occurred near the Pennsylvania–New York State border in the Central Appalachian and Delaware Hills physiographic zones. Of note, 272 Mink from 11 physiographic zones throughout the western, middle, and eastern regions of the state were not infected. Seven of 34 surveyed hydrological units contained Mink infected with Giant Kidney Worms (Fig. 1). The combined infection rate for hydrological units where kidney worms were detected was 12% (23 of 185). Infected Mink were concentrated in the Mid-Northern Lake Ontario and Oneida River (10 of 58, 17% infection rate). The Northern Hudson, St. Regis, and Raquette Rivers contained the other infected Mink (10 of 96, 10% infection rate) in the northern region of the state. The three remaining infected Mink occurred in the East Branch Delaware and Unadilla Rivers. Within hydrological units, the distribution of infected Mink was generally localized with multiple captures of infected Mink from the same location or locations in close proximity (Fig. 2). Of note, 216 of the Mink collected from three adjacent, connected hydrological units, the Mohawk, Mid-Hudson, and Mid- Northern Hudson Rivers were not infected. Elevation of capture locations was not significantly different between infected (mean = 284 ± 29.9 m) and non-infected Mink (mean = 255 ± 6.13 m; P = 0.353). However, no infected Mink was captured below 117 m, while 124 non-infected Mink were collected below that level. However, in 216 Northeastern Naturalist Vol. 17, No. 2 2010 J.J. Loukmas, D.T. Mayack, and M.E. Richmond 217 hydrological units where Giant Kidney Worms were found, with the exception of the St. Regis River, infected Mink were usually captured at relatively low elevations within the hydrological unit (Fig. 3). Of the condition factors analyzed, only relative left kidney weight was related to kidney worm infection; it was greater in Mink with infections (mean = 0.837 ± 0.039) compared to those without (mean = 0.504 ± 0.009; P < 0.001). Gender and location were significant covariates; relative left kidney weight was greater in females (mean = 0.569 ± 0.031) than males (mean = 0.518 ± 0.014; P = 0.011) and greater in the Adirondack (mean = 0.533 ± 0.014) than Eastern Lake Ontario location (mean = 0.500 ± 0.103; P = 0.013). Relative omentum weight of infected Mink (mean = 0.347 ± 0.0395) was not different from that of Mink without infection (mean = 0.359 ± 0.016; P = 0.777). However, relative omentum weight was greater in juveniles (mean = 0.382 ± 0.020) than adults (mean = 0.310 ± 0.022; P = 0.022). Body weight and mean body weight:length ratios were also not different between infected (mean = 623 ± 23.7 g and 1.72 ± 0.057, respectively) and non-infected Mink (mean = 6.08 ± 9.1 g, and 1.68 ± 0.021; P = 0.561 and P = 0.420, respectively). Gender and age class were significant covariates: body weight and body weight:length ratios were greater for male (mean = 701 ± 12.3 g and 1.86 ± 0.027, respectively) than female Mink (mean = 423 ± 8.2 g and 1.30 ± 0.022, respectively; P < 0.001) and were significantly greater for adults (mean = 675 ± 23.8 g and 1.80 ± 0.050, respectively) than juveniles (mean = 579 ± 14.9 g and 1.62 ± 0.032, respectively; P = 0.003 and 0.011, respectively). Body weight and body weight:length ratios from the Southern Tier location (mean = 716 ± 39.0 g and 1.88 ± 0.081, respectively) were greater than those from Eastern Lake Ontario (mean = 609 ± 23.6 g and 1.65 ± 0.050, respectively) and Adirondack (mean = 586 ± 15.2 g and 1.65 ± 0.034, respectively) locations, but the differences were not significant (P = 0.056 and 0.420, respectively). Concentrations of metals were not different between infected and noninfected Mink. Means (- SE, + SE) for infected vs. non-infected Mink were: 1.21 (1.04, 1.41) vs. 1.01 (0.91, 1.11; P = 0.315) μg/g for Hg; 0.10 (0.08, 0.12) vs. 0.12 (0.10, 0.13; P = 0.390) μg/g for Cd; and 0.03 (0.03, 0.04) vs. 0.04 (0.04, 0.05; P = 0.221) μg/g for Pb. Age and location were significant as covariates for Hg: concentrations were greater in adults (1.44 [1.23, 1.68] μg/g) than juveniles (0.90 [0.81, 1.00] μg/g; P = 0.021) and were greater in Figure 1 (opposite page). Capture locations of 610 Mink relative to New York State hydrological units and physiographic zones. Capture locations of two Mink collected from the greater Appalachian Plateau could not be assigned a specific location. The bold line separates northern vs. southern regions of New York State. Solid circles indicate capture locations of 23 Mink infected with kidney worms; a number of circles are hidden due to close proximity or multiple captures at locations. Numbers without parentheses indicate Mink collected from a geographic unit; numbers in parentheses indicate infected Mink. 218 Northeastern Naturalist Vol. 17, No. 2 the Adirondack (1.38 [1.21, 1.56] μg/g) than the Eastern Lake Ontario location (0.72 [0.65, 0.81] μg/g; P = 0.001). Similarly, age was significant as a covariate for Cd: concentrations were greater in adults (0.17 [0.14, 0.21] μg/g) than juveniles (0.09 [0.08, 0.10] μg/g; P = 0.003). Figure 2. Capture locations of Mink collected within hydrological units that had two or more Mink infected with kidney worms. Numbers without parentheses indicate Mink collected from a geographic unit; numbers in parentheses indicate infected Mink. Solid circles indicate capture locations of 22 infected Mink. The Eastern Branch of the Delaware River hydrological unit with two Mink (one infected) was not presented. Open circles indicate locations for non-infected Mink. A number of open circles are hidden due to multiple captures at locations. 2010 J.J. Loukmas, D.T. Mayack, and M.E. Richmond 219 Discussion Statewide, Mink infected with Giant Kidney Worms were uncommon. The 3.8% infection rate was much lower than that in Ontario (48%; Mace and Anderson 1975) and Minnesota (27%; Mech and Tracy 2001), but slightly higher than reports from North Dakota (<1%; Jorde 1980) and Manitoba (1%; Crichton and Urban 1970). While not found throughout much of the state, clusters of Giant Kidney Worm infections were found in several areas. The prevalence of infected Mink was higher in the northern part of the state and is coincident with previous reports (O’Connor and Nielson 1981, Stone 1997). Localized concentrations of the parasite were spread among a diverse array of physiographic zones, hydrological units, and elevations; consequently, the distribution pattern of infection could not be explained at a landscape level. We suspect that smaller-scale ecological factors need to be examined in order to determine the conditions favoring infection. Mace and Anderson (1975) suggested that the presence of appropriate paratenic hosts in association with Blackworm was key for transmission of this parasite. An evaluation of differences in the distribution of potential paratenic hosts (frogs and fish) relative to Blackworm and in the dependency of Mink or their prey on aquatic food chains may offer possible explanations for regional disparities in the prevalence of kidney worm infection in Mink. The mean number of worms in each infected Mink (2.7 in males, 2.5 in females) was similar to that found in Minnesota (2.5 in males, 1.8 in females; Mech and Tracy 2001) and Ontario (2.5 in males, 2.8 in females; Mace and Figure 3. Rank-order distribution of Mink by elevation for five hydrological units with one or more Mink infected with kidney worms. Solid symbols indicate infected Mink. Not graphed are two Mink from the East Branch Delaware River: one was infected, both collected at an elevation of 273 m; and two Mink from the Raquette River: both were infected and collected at an elevation of 513 m. Sample sizes were 8, 14, 29, 44, and 86 for the St. Regis River, Oneida River, Unadilla River, Mid- Northern Lake Ontario, and Northern Hudson River, respectively. 220 Northeastern Naturalist Vol. 17, No. 2 Anderson 1975). Infections in our study, however, were different from other studies in several respects. We found a lower ratio between the percentage of infected males to the percentage of infected females (0.8:1 vs. 1.8:1 in Minnesota and 1.5:1 in Ontario). Mech and Tracy (2001) speculated that dietary differences between males and females may be a reason for their observed differences in infection rate. Similar infection rates observed between genders in this study suggest these differences were not an issue. We also found that the prevalence of Giant Kidney Worm infections increased with age in male Mink, whereas Mech and Tracy (2001) reported no difference between juvenile and adult males. In addition, the percentage of infections that were considered fertile (i.e., infections with both male and female worms) was much lower in our study (29%) than reported by Mace and Anderson (1975) for Ontario (54%). The low prevalence of fertile infections may explain, in part, the overall low prevalence of kidney worm infections in Mink from New York. The limited distribution and overall low prevalence of infections indicates that the Giant Kidney Worm may not be important to the health or mortality of Mink in New York. However, because infected Mink were clustered in several areas, impacts may be evident at a local level. Left kidneys in infected Mink were hypertrophied, an indication of compensation for loss of renal function on the right side. The loss of one kidney did not signifi- cantly increase hepatic retention of potentially toxic metals (Hg, Cd, and Pb) in Mink from New York State. However, renal function compromised by kidney worms may impact the overall ability to excrete metals in some populations. Indeed, Capodagli (2002) found that Mink infected with Giant Kidney Worms had higher metal burdens than non-infected Mink in Ontario. A lack of an effect of kidney worm infection on the retention of metals in this study does not rule out that infections may exacerbate the risk of certain toxins to the health of Mink, a species highly sensitive to many environmental contaminants (Wren 1991). We did not find differences in other condition factors between infected and non-infected Mink, suggesting that Giant Kidney Worms have little impact on Mink health. However, the lack of a health effect might be a biased observation because Mink in poor health may not survive harsh fall and winter weather conditions or may be less susceptible to trapping due to reduced mobility. Giant Kidney Worms are widely distributed throughout North America, but are abundant only in certain enzootic regions (Measures 2001). Localized clusters of infected Mink were observed in our study, but the reasons for this remain unknown. The elucidation of ecological factors that limit Giant Kidney Worms and regulate parasite-host relationships might provide an explanation for the observed pattern of distribution. Further knowledge about the health and mortality implications of infections and the overall infection potential of an area to Mink and other susceptible mammals would be beneficial for the management of these species. 2010 J.J. Loukmas, D.T. Mayack, and M.E. Richmond 221 Acknowledgments This project was supported by the Hudson River Estuary Program, the New York Natural Resources Damage Assessment Fund and Federal Aid for the Restoration of Wildlife to New York State, Project WE-173-G. We thank the Mink trappers of New York State who contributed to our study, especially members of the Adirondack Foothills Trapping Club and the Dutchess County Trapping Club. L. Capodagli made important contributions with Mink collections and necropsies. Laboratory assistance was provided by K.C. Geesler and K.L. Hellijas. C.J. Balk provided considerable assistance with Mink carcass acquisition. We thank F. DeSantis, Jr. and S. Fonda for contributing to data management and A. Lorefice for assisting in the production of Figures 1 and 2. We also thank the staff at Matson’s Laboratory for conducting Mink age analyses and the staff at Frontier Geosciences, Inc. and A. Gudlewski and B. Buanno of NYS DEC for metals analysis. Literature Cited Anderson, R.C. 1992. The family Dioctophymatidae, Dioctophyme. Pp. 533–535, In R.C. Anderson (Ed.). Nematode Parasites of Vertebrates: Their Development and Transmission. CAB International, Cambridge, UK. Capodagli, L. 2002. 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