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Home , Ancylostoma, Black Rock Forest, Capillaria aerophila, Capillaria plica

Journal of Wildlife Diseases, 39(3), 2003, pp. 712–717 ᭧ Wildlife Disease Association 2003

A Survey of the Parasites of (Canis latrans) in based on Fecal Analysis

Matthew E. Gompper,1,8 Rachel M. Goodman,2 Roland W. Kays,3 Justina C. Ray,4 Christine V. Fiorello,5,7 and Susan E. Wade61 Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, Missouri 65211, USA; 2 Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996, USA; 3 New York State Museum, CEC 3140, Albany, New York 12230, USA; 4 Wildlife Conservation Society, Faculty of , University of Toronto, 33 Willcocks Street, Toronto, Ontario, M5S 3B3, Canada and 2300 Southern Blvd., Bronx, New York 10460, USA; 5 Center for Environmental Research and Conservation, , New York, New York 10027, USA; 6 New York State Health Diagnostic Laboratory, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, USA; 7 Current address: Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, PO Box 100126, Gaines- ville, Florida 32610, USA; 8 Corresponding author (email: [email protected])

ABSTRACT: Coyotes (Canis latrans) have colo- tential risks that range expansion nized northeastern only within represent to , domestic , the past 10–80 yr. We examined feces of coy- otes in 2000–01 at three sites in New York and wildlife of the region. (USA) to survey parasites in the region. Two Much of what we know about parasites cestodes, nine , five protozoa, one of coyotes comes from the western and trematode, and two arthropods were identified southeastern (Custer and from 145 coyote fecal samples. Parasite com- Pence, 1981a, b; Pence and Custer, 1981; ponent community diversity was higher (nϭ16 Van Den Bussche et al., 1987). In the east- ) in southern New York than in middle and northern sites (nine species each) and in- ern United States the most northern ex- fracommunity species richness was greater in amination of coyote parasites was a small southern New York than at the other sites. (nϭ16 fecal sample) study in southern These differences may reflect the variable diets Pennsylvania (USA; Bixel, 1995). It is un- of coyotes, as well as recent colonization of the clear how transferable these findings are region and the mixing of component commu- nities from expanding coyote populations. to the very different environment of the Key words: Canis latrans, coyotes, para- northeast, especially given previous find- sites, New York, survey. ings demonstrating substantial dissimilarity of coyote parasite faunas from across geo- Coyotes (Canis latrans) first colonized graphic regions (Custer and Pence, northeastern North America in the 1940s 1981a). when animals moved from Que´bec (Can- The goal of this study was to survey the ada) into northern New York (USA), and parasites of coyotes from New York, based then steadily expanded into surrounding on fecal samples collected from a series of states and provinces such that by the late transects at three sites (Fig. 1): the north- 1990s the species was virtually ubiquitous ern Adirondacks (ADK) across a large area throughout the northeast (Parker, 1995; in Franklin, Essex, and Clinton counties Fener, 2001; Gompper, 2002a). While (44Њ09ЈN, 74Њ18ЈW); the 12 km2 Albany heartworms, sarcoptic mange mites, ca- Pine Bush Preserve (PBP) between the nine distemper virus, and rabies virus are cities of Albany and Schenectady known to infect and cause clinical disease (42Њ42ЈN, 73Њ52ЈW); and the 15 km2 Black and mortality in coyotes in the northeast Rock Forest (BRF) in the Hudson High- (Agostine and Jones, 1982; Okoniewski lands of southern New York between the and Stone, 1983) no broad examination of towns of Cornwall and West Point occurrence of enteric parasites of coyotes (41Њ45ЈN, 74Њ01ЈW). Coyotes have inhab- in the northeast has been published ited these sites for approximately 60, 40, (Gompper, 2002b). Such information is and 20 yr, respectively (Fener, 2001). Al- important for understanding coyote pop- though all transects were located in for- ulation limitation and understanding po- ested sites, the landscapes in which they

712 SHORT COMMUNICATIONS 713

USA). Prevalence was calculated as the ra- tio of the number of fecal samples infected to the total number examined. Species ac- cumulation curves and the non-parametric Chao2 estimator were used to calculate species richness of parasite component communities (the community of parasites associated with a regional subset of hosts; Bush et al., 1997). The Chao2 estimator has been shown to have excellent predic- tive power when data are in the form of presence-absence and sample sizes are small (Colwell and Coddington, 1994). Calculations were performed using FIGURE 1. Map of New York showing the three EstimateS version 6.0b1 (Colwell, 2001). study sites. Sample order was randomized 100 times without replacement and mean (ϮSD) were situated covered a wide spectrum in species richness estimated for each sample housing density and general devel- accumulation level. opment, with ADK the least developed, Nineteen species of parasites were iden- PBP situated in a suburban setting, and tified from 145 coyote fecal samples (Table BRF situated in a rural region 80 km north 1). All observed species have previously of New York City. been reported from coyotes elsewhere in During 2000 and 2001, fecal samples their range. Forty-four percent (nϭ64) of were collected at all three sites by walking the samples contained no parasite species transects of variable lengths (5–40 km) on of coyotes. While it is typical for a signifi- unpaved roads and in each re- cant percent of the population to be un- gion. Fresh feces (estimated Յ4 days old) parasitized, it is also possible that some of were collected and preserved in 10% for- our samples may have suffered from deg- malin acetate within 12 hr and stored at radation. However, 13% of these did con- room temperature until analysis. Species tain eggs or cysts of prey species eaten by origin of the sample was determined by coyotes, suggesting that degradation of the size, shape, and a detailed knowledge of samples does not explain the absence of the fauna of each site based on extensive coyote parasites in all fecal samples. use of motion detection cameras (M. Ova of nine species of nematodes were Gompper, R. Kays, and J. Ray, unpubl. observed, including aerophila data). To avoid confusion between and C. putorii, at all three sites, and C. (Vulpes vulpes) and coyote feces, we only plica at ADK. Prevalence of C. aerophilia selected large samples (Ͼ2 cm diameter) was relatively high in ADK (35%), but low- for analysis. er in PBP and BRF (13–14%). If the rate All fecal samples were processed using of occurrence observed in these three sites standard sugar and zinc sulfate centrifu- is representative of the true prevalence in gation concentration flotation techniques the Northeast, it is unlikely that Capillaria (Bowman, 1999). Ova, oocysts, and larvae infection is a significant morbidity or mor- were identified by morphologic character- tality risk to coyotes in southern New York, istics and linear measurements. A subset but it may be important in northern New of samples was tested for Giardia spp. us- York. ing an enzyme-linked immunosorbent as- Uncinaria stenocephala was found in say (ELISA; ProSpecT Giardia Microplate over a third of BRF samples, but was rare Assay, Alexon-Trend, Ramsey, Minnesota, elsewhere. Samuel et al. (1978) reported 714 JOURNAL OF WILDLIFE DISEASES, VOL. 39, NO. 3, JULY 2003

TABLE 1. Endoparasites of coyote fecal samples from three sites in New York. Values are prevalence esti- mates excluding samples for which no parasites of coyotes were observed, suggesting degradation. Values in parentheses are prevalence estimates including all samples. For Giardia, values represent ELISA-based prev- alence with number of samples tested in parentheses.

Northern Pine Bush, Black Rock Adirondacks Albany Forest, Cornwall Total (n ϭ 54) (n ϭ 68) (n ϭ 23) (n ϭ 145)

Arthropods Trichodectes canis 6.3 (4.4) 1.1 (0.7) Demodex sp. 6.8 (4.4) 6.3 (4.4) 4.5 (2.8) Cestodes Spirometra sp. 10.3 (5.6) 3.4 (2.1 Taenia sp. 41.4 (22.2) 6.8 (4.4) 6.3 (4.4) 18.0 (11.0) Nematodes Capillaria aerophila 34.5 (18.5) 13.6 (8.8) 12.5 (8.2) 20.2 (12.4) Capillaria putorii 3.5 (1.9) 2.3 (1.5) 12.5 (8.2) 4.5 (2.8) Capillaria plica 3.5 (1.9) 1.1 (0.7) Crenosoma sp. 10.3 (5.6) 2.3 (1.5) 6.3 (4.4) 5.6 (3.5) Physaloptera sp. 6.3 (4.4) 1.1 (0.7) Spirurida 6.3 (4.4) 1.1 (0.7) Toxascaris leonina 12.5 (8.7) 2.3 (1.4) Toxocara canis 12.5 (8.7) 2.3 (1.4) Uncinaria stenocephala 3.5 (1.9) 2.3 (1.5) 37.5 (26.1) 9.0 (5.5) Protozoans Giardia spp. 15.2 (46) 13.3 (30) 16.6 (18) 14.9 (94) Isospora canis 6.3 (4.4) 1.1 (0.7) Isospora (Hammondia) heydorni 18.8 (13.0) 3.4 (2.0) Isospora ohioensis 25.0 (17.4) 4.5 (2.8) Sarcocystis sp. 6.9 (3.7) 45.5 (29.4) 12.5 (8.7) 27.0 (16.6) Trematodes Digenea 18.2 (11.8) 9.0 (5.5) similarly high Uncinaria prevalence (28%) population, especially among young indi- in southwestern Manitoba. in- viduals with lower levels of immunity. Sim- fection can cause varying severity of dis- ilarly, the common canid parasites, Toxas- ease, from unapparent infection or mild caris leonina and Toxocara canis were only anemia to fatal exsanguination, depending identified at BRF. The later species can be on virulence of the parasitic species, the quite pathogenic to domestic puppies age and health of the host, and acquired (Bowman, 1999). immunity of the host. Uncinaria infects Two parasites of domestic were the small intestines of carnivores and is identified. Ova of T. cati in one sample less pathogenic than the common canid from PBP and Aelurostrongylus larvae in hookworm, (Bow- one sample from BRF. Both are likely spu- man, 1999), which was not observed in this rious prey parasites gained from ingesting survey. Both species have been observed a domestic , as the sample from which in eastern coyotes as far north as southern T. cati was identified also contained the re- Pennsylvania (Bixel, 1995). While disease mains of a domestic cat. Coyote due to U. stenocephala is perhaps less se- on domestic cats is not unusual, and do- vere than that due to A. caninum, the high mestic cat hair has been found in coyote prevalence of U. stenocephala suggests it feces collected from all three study sites could be an important stressor on the BRF (M. Gompper and R. Kays, unpubl. data). SHORT COMMUNICATIONS 715

Two cestodes were identified; Spirome- tra sp. was observed from ADK and Tae- nia sp. was identified at all three sites, al- though prevalence was higher at ADK. Taeniids generally cannot be identified to species based on ova alone (Bowman, 1999), and at least nine species of Taenia have been reported in necropsies of coy- otes (Custer and Pence, 1981b). In Feb- ruary 2001 we necropsied four adult ADK FIGURE 2. Species accumulation curves for par- coyotes killed by a trapper ca. 20 km NW asite component communities (excluding Giardia and ectoparasites) in A) Black Rock Forest, B) Pine Bush of Paul Smiths and found adult T. pisifor- Preserve, C) Northern Adirondacks, and D) all sites mis in the intestines of two coyote. Previ- combined. Lower curve is based on observed data. ous studies of coyotes have found this spe- Upper curve is the results of the Chao2 non-para- cies ubiquitous (Custer and Pence, metric estimator of species richness based on succes- 1981b). sively greater numbers of samples from the data set. For both curves each point represents the mean of Five species of protozoa were identified. 100 estimates using randomized accumulation order Giardia sp. and Sarcocystis sp. occurred at of fecal samples. all three sites, while three Isospora spp. occurred only at BRF where the genus oc- curred in 35% of samples. No sample, 9.9 and 11.5 species for ADK and PBP, however, had Ͼ1 Isospora species. Preva- respectively. However the shape of the lence of Sarcocystis, for which coyotes are curve for PBP, and the large standard de- definitive hosts (Dubey et al., 1989), was viation (Ϯ7.2) for ADK indicate that an ex- high (46%) in PBP but far lower at the act estimate for these sites necessitates ad- other sites. Sarcocystis has been previously ditional sampling. reported in coyotes from the western and Of the 145 fecal samples, 44.1% con- southeastern United States (Conder and tained one species, 9.0% contained two Loveless, 1978; Davidson et al., 1992; species, 1.4% contained three species, and Holzman et al., 1992). 1.4% contained five species (Fig. 3). The Species accumulation curves and esti- overall distribution of number of parasitic mates of species richness indicate a maxi- species per fecal sample showed a negative mal sampled parasite community of ap- binomial distribution, although the distri- proximately 18 species, based on fecal flo- bution pattern for the individual sites var- tations and excluding ectoparasites (Fig. ied. There were significant differences in 2). The number of observed species (16) the size of the infracommunities (the par- and the mean Chao2 estimate for all 145 asite community within a particular host; samples (18.2Ϯ5.3) suggest that this sur- Bush et al., 1997) at the three sites (Krus- vey has identified most of the fecal para- kal-Wallis One-Way ANOVA; Pϭ0.049) sites in these regions, and that the analysis due to the higher species richness of BRF of additional samples would not greatly in- infracommunities. Samples from ADK and crease estimates of species richness. The PBP had similar means of 0.61 (range 0– BRF component community appears to be 2) and 0.59 (0–3) species per sample, re- well sampled, with the observed species spectively. In contrast, BRF had a mean of richness (13) and estimated species rich- 1.30 (0–5) species per sample, with 13% ness (14.7Ϯ3.0 for all samples) curves of samples containing Նthree species, de- meeting. However, the richness of the spite a small sample size relative to ADK component communities of ADK, and es- and PBP. Across the three sites, mean in- pecially PBP, remain inexact. The Chao2 fracommunity richness was 0.71 species. estimator indicates a species richness of The parasite component community of 716 JOURNAL OF WILDLIFE DISEASES, VOL. 39, NO. 3, JULY 2003

cluding these species, overlap in commu- nity composition was 39–47% between both BRF and the other sites. In contrast, overlap in the ADK and PBP communities was 64% (Table 2). While this survey has likely identified the majority of gastrointestinal parasites present in coyotes in the Northeast, there were significant differences in the parasite communities of the three study sites. The basis for these differences in infracom- munity and component community struc- ture, especially in southern New York, are unclear. The differences could be due to dietary variation among the hosts or to en- vironmental differences between the sites, FIGURE 3. Distribution of the number of parasite perhaps including differences in the ecol- species identified per sample. A. Northern Adiron- ogy of domestic in and near the sites. ϭ ϭ dacks (n 54). B. Pine Bush Preserve (n 68). C. In addition the pattern and process of col- Black Rock Forest (nϭ23). D. All sites combined (nϭ145). onization of the northeast by coyotes may also have played a role in structuring the parasite community. Coyotes only arrived BRF differed from that of PBP and ADK. in the southern New York region within Two species of parasites were found only the past two decades, and the colonizing in ADK and one only in PBP. In contrast, animals may have entered from multiple nine species were unique to BRF. These fronts, including not only northern New differences may reflect sampling error, as York but also northeastern Pennsylvania sample sizes were relatively small and sam- and northwestern New Jersey (USA) ple collection was opportunistic. In addi- (which represent separate colonization tion, seasonal variation in worm burden, fronts from the New York front; Parker, egg output, rates of hatching, and rates of 1995). The current southern New York degradation of parasite ova were unac- coyote population and its parasite compo- counted for. Nonetheless, the BRF para- nent community may therefore represent site component community stands out in an interface between that found in upstate its higher parasite richness (14 endopara- New York and that found in more south- site species versus nine at ADK and eight ern regions. Indeed, of the five species of at PBP) which was detected in a relatively parasites identified by Bixel (1995) in small sampling effort. Seven parasite spe- Pennsylvania, only one (an Ancylostoma cies were common to all three sites. In- species) is absent from the southern New

TABLE 2. Overlap in the parasite component communities of three study sites in New York. Values above the diagonal represent absolute number of species shared between the sites. Values below the diagonal represent the proportion (%) of total number of identified species (n) shared among the two sites.

Black Rock Northern Pine Bush, Forest, Adirondacks Albany Cornwall

Northern Adirondacks n/a 7 7 Pine Bush, Albany 63.6% (n ϭ 11) n/a 8 Black Rock Forest, Cornwall 38.9% (n ϭ 18) 47.1% (n ϭ 17) n/a SHORT COMMUNICATIONS 717

York site examined in this study, while ings, J. A. Chapman and D. Pursley (eds.). Frost- three are absent from the central and burg, Maryland, R. R. Donelley and Sons, Falls Church, Virginia, pp. 730–759. northern New York sites. These prelimi- DAVIDSON, W. R., M. J. APPEL,G.L.DOSTER,O.E. nary findings suggest further study for the BAKER, AND J. F. BROWN. 1992. Diseases and idea of mixing parasite fronts is warranted. parasites of red , gray foxes, and coyotes Funding for this study came from the from commercial sources selling to fox-chasing Wildlife Conservation Society, Geraldine enclosures. Journal of Wildlife Diseases 28: 581– 589. R. Dodge Foundation, Columbia Univer- DUBEY, J. P., C. A. SPEER, AND R. FAYER 1989. Sar- sity, University of Missouri, New York cocystosis of animals and man. CRC Press, Boca State Museum, and New York Biodiversity Raton, Florida, 215 pp. Research Institute. Thanks to A. Wright, FENER, H. M. 2001. Coyote (Canis latrans) coloni- D. Bogan, J. Bopp, E. Hellwig, S. LaPoint, zation of New York: The influence of human- induced landscape changes. M.A. Thesis, Colum- and D. Ruggeri for help with sample col- bia University, New York, New York, 64 pp. lection. GOMPPER, M. E. 2002a. Top carnivores in the sub- urbs? Ecological and conservation issues raised LITERATURE CITED by colonization of northeastern North America AGOSTINE, J. C., AND G. S. JONES. 1982. Heartworms by coyotes. Bioscience 52: 185–190. (Dirofilaria immitis) in coyotes (Canis latrans)in . 2002b. The ecology of northeast coyotes: New England. Journal of Wildlife Diseases 18: Current knowledge and priorities for future re- 343–345. search. Wildlife Conservation Society Working BIXEL, K. D. 1995. Survey of the endoparasites of Paper 17: 1–48. south central Pennsylvania coyotes using fecal HOLZMAN, S., M. J. CONROY, AND W. R. DAVIDSON. analysis. Journal of the Pennsylvania Academy of 1992. Diseases, parasites and survival of coyotes Science 69: 17–21. in south-central Georgia. Journal of Wildlife Dis- BOWMAN, D. D. 1999. Georgis’ parasitology for vet- eases 28: 572–580. erinarians, 7th Edition, W. B. Saunders Compa- OKONIEWSKI, J. C., AND W. B. STONE. 1983. Causes ny, Philadelphia, Pennsylvania, 430 pp. of morbidity and mortality in coyotes in New BUSH, A. O., K. D. LAFFERTY,J.M.LOTZ, AND A. W. York. New York Fish and Game Journal 30: 224– SHOSTAK. 1997. Parasitology meets ecology on 27. its own terms: Margolis et al. revisited. Journal PARKER, G. R. 1995. Eastern coyote. Nimbus Pub- of Parasitology 83: 575–583. lishing, Halifax, Nova Scotia, Canada, 254 pp. COLWELL, R. K. 2001. EstimateS: Statistical estima- PENCE,D.B.,AND J. W. CUSTER. 1981. Host-para- tion of species richness and shared species from site relationships in the wild Canidae of North samples. Version 6.0b1, http://viceroy.eeb.uconn. America. 2. Pathology of infectious diseases in edu/EstimateS. the genus Canis. In Proceeding of the worldwide , AND J. A. CODDINGTON. 1994. Estimating furbearer conference, J. A. Chapman and D. terrestrial biodiversity through extrapolation. Pursley (eds.). Frostburg, Maryland. R.R. Don- Philosophical Transactions of the Royal Society nelley and Sons, Falls Church, Virginia, pp. 760– of London B 345: 101–118. 845. CONDER, G. A., AND R. M. LOVELESS. 1978. Para- SAMUEL, W. M., S. RAMALINGAM, AND L. N. CARBYN. sites of the coyote (Canis latrans) in central 1978. Helminths in coyotes (Canis latrans Say), Utah. Journal of Wildlife Diseases 14: 247–249. (Canis lupus L.), and red foxes (Vulpes CUSTER,J.W.,AND D. B. PENCE. 1981a. Ecological vulpes L.) of southwestern Manitoba. Canadian analyses of helminth populations of wild canids Journal of Zoology 56: 2614–2617. from the Gulf Coastal Prairies of Texas and Lou- VAN DEN BUSSCHE, R. A., M. L. KENNEDY, AND W. isiana. Journal of Parasitology 67: 289–307. E. WILHELM. 1987. Helminth parasites of the , AND . 1981b. Host-parasite relation- coyote (Canis latrans) in Tennessee. Journal of ships in the wild Canidae of North America. I. Parasitology 73: 327–332. Ecology of helminth infections in the genus Ca- nis. In Worldwide furbearer conference proceed- Received for publication 7 August 2002.