Range Expansion of Fascioloides magna in North Carolina

Transcription

1 Range Expansion of Fascioloides magna in North Carolina Author(s): April D. Boggs, Christopher S. DePerno and James R. Flowers Source: Southeastern Naturalist, 17(2): Published By: Eagle Hill Institute URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 SOUTHEASTERN Southeastern Naturalist NATURALIST 17(2): Range Expansion of Fascioloides magna in North Carolina April D. Boggs 1,*, Christopher S. DePerno 1, and James R. Flowers 2 Abstract - In North Carolina, Odocoileus virginianus (White-tailed Deer) are the definitive natural hosts of Fascioloides magna (Giant Liver Fluke). Previous research identified the enzootic range of Giant Liver Fluke in North Carolina to be within the Tar River and Roanoke River Basins in Halifax and neighboring counties. Recent Giant Liver Fluke infections of Ovis aries (Domestic Sheep), Capra hircus (Domestic Goat), Lama glama (Llama), Vicugna pacos (Alpaca), and Bos taurus (Cattle) outside the historic enzootic range prompted us to investigate the current range of Giant Liver Fluke in North Carolina. From September 2014 to January 2015, we examined livers from hunter-harvested Whitetailed Deer within 16 North Carolina counties. We detected Giant Liver Fluke in livers from 5 counties, with an overall prevalence of 10.3%. Besides reporting the first Giant Liver Fluke infections of livestock in North Carolina, we documented new geographic localities (Cabarrus, Franklin, Mecklenburg, Union, Wake, and Washington counties) for Giant Liver Fluke. An increased impact on North Carolina livestock is likely with the possible range expansion of Giant Liver Fluke, which may be related to the increase in populations of White-tailed Deer. Introduction Fascioloides magna (Bassi) (Giant Liver Fluke) is a parasite of North American wild and domestic ruminants. Odocoileus virginianus (Zimmermann) (White-tailed Deer) is the definitive host of Giant Liver Fluke (Pybus 2001), but little pathology occurs in this host species. However, infections in domestic livestock cause death or condemnation of livers (Davidson 2006, Králová-Hromadová et al. 2016, Pybus 2001, Swales 1935). Only 3 studies (Flowers 1996, Harlow and Jones 1965, Pursglove et al. 1977) have reported Giant Liver Fluke from North Carolina. In 2013, a fatal case of Giant Liver Fluke was diagnosed in a Lama glama L. (Llama) from Cabarrus County, NC (NCDA Griffin Diagnostic Laboratory, Monroe, NC). In 2014, two fatal cases of Giant Liver Fluke in Vicugna pacos (L.) (Alpaca) were diagnosed from Franklin County, NC, and in 2016, an Ovis aries L. (Domestic Sheep) from Wake County, NC died from a Giant Liver Fluke infection (NCDA Rollins Diagnostic Laboratory). In addition, a Capra hircus L. (Domestic Goat) infection and numerous Bos taurus L. (Cattle) infections have been detected in Washington County (NCDA Rollins Diagnostic Laboratory). Livestock may experience morbidity and mortality from liver fluke disease; thus, the range expansion of Giant Liver Fluke is of concern, especially where wild hosts share habitat 1 North Carolina State University, Department of Forestry and Environmental Resources, Fisheries, Wildlife, and Conservation Biology, 110 Brooks Avenue, Raleigh, NC North Carolina State University, College of Veterinary Medicine, Department of Population Health and Pathobiology, 1060 William Moore Drive, Raleigh, NC * Corresponding author - adboggs@ncsu.edu. Manuscript Editor: Roger Applegate 365

3 with livestock. Significant financial losses can affect livestock producers; therefore, our objective was to document and report an increase in the historic distribution of White-tailed Deer infected with Giant Liver Fluke in North Carolina. Methods From September 2014 to January 2015, we collected 165 livers from hunter-harvested White-tailed Deer within 16 counties in North Carolina (Fig. 1). Collections were opportunistic, based on hunter participation, and included contributions from 4 hunt clubs (Washington, Halifax, and Stanly counties), 3 nature preserves (Mecklenburg County), 1 research station (Washington County), 1 custom processing center (various counties), and donations from private citizens (various counties). Our research team received White-tailed Deer livers from hunters that were either freshly harvested or that had been stored on ice or in freezers. Livers from the custom processor were donated directly to our research team, placed in a cooler for transport back to our North Carolina State University (NCSU) laboratory, and necropsied within 24 h. Livers collected in Mecklenburg County were placed on ice, transported back to NCSU, and necropsied weekly. Other livers were collected by hunters or hunt clubs, stored in freezers, transported to NCSU, thawed and necropsied monthly or after the end of the hunting season. At the NCSU laboratory, we examined the livers for signs of Giant Liver Fluke or other parasites. Besides the number of flukes detected in each liver, we also noted pathologic signs characteristic of Giant Liver Fluke infections, such as melanoid and fibrous tracks in the liver tissue, liver damage, and the number of fluke pockets (Králová-Hromadová et al. 2016, Pursglove 1977, Pybus 2001, Pybus et al. 2015, Swales 1935). We deposited specimens (HWML ) in the Harold W. Manter Laboratory of Parasitology. Our parasite host statistical analyses (prevalence and intensity) followed Bush et al. (1997). Results We collected 165 livers from 16 counties and detected Giant Liver Fluke in 17 livers (10.3%) from 5 of the counties sampled (Table 1, Fig. 1). The average number of liver flukes per infected liver was 5.4; the highest number of liver flukes was 29 in a single liver from Mecklenburg County (Table 1). Discussion Harlow and Jones (1965) reported a prevalence of 11.5% out of 87 North Carolina White-tailed Deer infected with Giant Liver Fluke; however, they did not report the counties of collection. In the 1960s and 1970s, parasitologists from North Carolina State University conducted various surveys of helminth parasites of wildlife in North Carolina. Giant Liver Fluke had been detected in White-tailed Deer from hunting clubs near the towns of Roanoke Rapids and Scotland Neck, in Halifax County (Fig. 1), but had not been detected at Fort Bragg hunting clubs in Cumberland County (G. Miller, Emeritus, North Carolina State University, Raleigh, NC, 366

4 pers. comm.). Within the Roanoke River basin of North Carolina, Pursglove et al. (1977) reported enzootic areas with prevalence of 56% in Halifax County, 63% in Bertie County, and 80% in Northampton County, and a focus of infection in Bladen County (29%) within the Cape Fear River Basin (Fig. 1). Later, Flowers (1996) reported 73% prevalence in White-tailed Deer from a hunting club in Halifax County, near Fishing Creek, a tributary of the Tar River in North Carolina (Fig. 1). The prevalence of Giant Liver Fluke from our study (10.3%) was similar to the prevalence (12.8%) detected by Pursglove et al. (1977) in their study of 13 southeastern states. However, in North Carolina, Pursglove et al. (1977) reported Giant Liver Fluke from only 4 of 22 locations, with no Giant Liver Fluke detected east of Bertie County or west of Bladen County (Fig.1). Our research identified Giant Liver Fluke infections in Washington County, ~84 km (~52 mi) east of the Halifax enzootic area; in Wake and Franklin counties, ~101 km (~63 mi) west of the Halifax enzootic area; and in Cabarrus, Union, and Mecklenburg counties, ~322 km (~200 mi) southwest of the Halifax enzootic area (Table 1, Fig. 1). Of special interest is the continued enzootic status of Halifax County, in North Carolina s Upper Coastal Plain. The prevalence of Giant Liver Fluke in Whitetailed Deer from Halifax County has been reported as 56% (Pursglove et al. 1977), 73% (Flowers 1996), and 70% (present study). Halifax County is bordered to the north by the Roanoke River and only 12.5 miles to the south by Fishing Creek, a major tributary of the Tar River. This physiography results in lowland to swampy habitat throughout much of the county, which is excellent for the endemicity of Giant Liver Fluke, providing browse and cover for the definitive host (i.e., Whitetailed Deer), and slow-moving to stagnant aquatic habitat for its lymnaeid snail host, Pseudosuccinea columnella (Say) (Mimic Lymnaea) (Flowers and Miller 1993, Walter 1954). Similar habitats, including marshlands, moist lowlands, and swamps associated with major river drainages, have been reported as enzootic habitats for Giant Liver Fluke (Pursglove et al. 1977, Pybus 2001, Pybus et al. 2015, Vanderwaal et al. 2014, Vannatta 2016). Pybus et al. (2015) described the Giant Figure 1. Collection sites of White-tailed Deer livers from September 2014 to January 2015, and locations of previously reported Fascioloides magna (Giant Liver Fluke) infections in North Carolina. 367

5 Liver Fluke s habitat tolerances to be relatively broad and characterized by standing water, ubiquitous aquatic snails, and emergent vegetation. Pursglove et al. (1977) reported Giant Liver Fluke from the Halifax enzootic region but did not detect this fluke from collection sites outside this region (Fig. 1). The present study reports new geographic locales, which may indicate a range expansion of this fluke. Our White-tailed Deer and livestock reports of Giant Liver Fluke from Franklin and Wake counties, as well as Washington County suggests expansion west and east, respectively, from the Halifax enzootic region. Our reports of this fluke from Cabarrus, Mecklenburg, and Union counties suggest the Giant Liver Fluke may have dispersed into North Carolina from populations reported by Pursglove et al (1977) in South Carolina s Chester and Union counties. Range expansions of the Giant Liver Fluke in North Carolina would unlikely be due to recent expanded distributions of snail hosts, as the Mimic Lymnaea, likely the fluke s main snail host in North Carolina, has historically been common, ubiquitous, and widespread (Adams et al. 1990, Flowers 1996, Flowers and Miller 1993, Turgeon et al. 1998, Walter 1954). Although marshland habitats are important for Giant Liver Fluke enzootic regions, Peterson et al. (2013) concluded the occurrence of Giant Liver Fluke in Alces alces (L.) (Moose) populations was more correlated to the population density of White-tailed Deer than the proportion of wetland habitats. In North Carolina, White-tailed Deer populations have increased from 1976 to 2015 (NCWRC 2015), and have the potential to spread parasites and diseases, such as the Giant Liver Fluke and tick-borne pathogens (Paddock and Yabsley 2007). Future research is necessary to determine if the Giant Liver Fluke has expanded to other locations in North Carolina and to understand financial impacts that infections may have on livestock producers. Table 1. Fascioloides magna (Giant Liver Fluke) from 17 of 165 Odocoileus virginianus (Whitetailed Deer) collected from September 2014 to January 2015 in North Carolina. Intensity County Livers examined Prevalence (%) Mean Range Beaufort Chatham Columbus Franklin Granville Halifax Lee Mecklenburg Moore Nash Stanly Union Vance Wake Warren Washington

6 Acknowledgments We thank J. Tetterton, J. Bland, J. Giles, G. Marshall, J. Johnson, Pearce s Custom Processing, Mecklenburg Parks and Recreation, NCDA Tidewater Research Station, B. Sherrill, M. Lashley, C. Chitwood, F. Worley, G. Gardner, T. Boggs, B. Johnson, and B. Blackmon for helping with collecting and delivering the livers. We are grateful to hunters from Old Church Hunt Club, Ridge Hunt Club, and Westside Hunting Club, as well as hunters and staff at the Fork Farm, for collecting livers for the study. Also, gratitude is extended to the NCDA Griffin Diagnostic Laboratory of Monroe, NC, and the NCDA Rollins Diagnostic Laboratory of Raleigh for providing data on livestock cases. This project was funded by North Carolina State University, the Fisheries, Wildlife, and Conservation Biology Program, and the Department of Population Health and Pathobiology. Literature Cited Adams, W.R, J.M. Alderman, R.G. Biggins, A.G. Gerberich, E.P. Keferl, H.J. Porter, and A.S. Van Devender A report on the conservation status of North Carolina s freshwater and terrestrial molluscan fauna. The Scientific Council on Freshwater and Terrestrial Mollusks, Raleigh, NC. 246 pp. Bush, A.O., K.D. Lafferty, J.M. Lotz, and A.W. Shostak Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: Davidson, W.R Field Manual of Wildlife Diseases in the Southeastern United States, 3 rd Editon. Southeastern Cooperative Wildlife Disease Study, The College of Veterinary Medicine, The University of Georgia, Athens, GA. 448 pp. Flowers, J.R Notes on the life history of Fascioloides magna (Trematoda) in North Carolina. Journal of the Elisha Mitchell Scientific Society 112: Flowers, J.R., and G.C. Miller Molluscs from Swift Creek, Wake, and Johnston counties, North Carolina. Proceedings of the Annual Conference of the Southeastern Association of Fish and Wildlife Agencies 47: Harlow, R.F., and F.K. Jones Jr The White-Tailed Deer in Florida. Technical Bulletin No. 9. Florida Game Fresh Water Fish Commission, Tallahassee, FL. 240 pp. Králová-Hromadová, I., L. Juhásová, and E. Bazsalovicsová The Giant Liver Fluke, Fascioloides magna: Past, Present, and Future Research. SpringerBriefs in Animal Sciences. Springer International Publishing, Basel, Switzerland. 106 pp. North Carolina Wildlife Resources Commission (NCWRC) Reported deer harvest by county Available online at Deer Harvest by County pdf. Accessed 15 November Paddock, C.D., and M.J. Yabsley Ecological havoc, the rise of White-tailed Deer, and the emergence of Amblyomma americanum-associated zoonoses in the United States. Current Topics in Microbiology and Immunology 315: Peterson, W.J., M.W. Lankester, J.G. Kie, and R.T. Bowyer Geospatial analysis of Giant Liver Flukes among Moose: Effects of White-tailed Deer. Acta Theriologica 58: Pursglove, S.R., A.K. Prestwood, T.R. Ridgeway, and F.A. Hayes Fascioloides magna infection in White-tailed Deer of southeastern United States. Journal of the American Veterinary Medical Association 171: Pybus, M.J Liver Flukes. Pp , In W.M. Samuel, M.J. Pybus, and A.A. Kocan (Eds.). Parasitic Diseases of Wild Mammals, 2 nd Edition. Iowa State University Press, Ames, IA. 559 pp. 369

7 Pybus, M.J., E.W. Butterworth, and J.G. Woods An expanding population of the Giant Liver Fluke (Fascioloides magna) in Elk (Cervus canadensis) and other ungulates in Canada. Journal of Wildlife Diseases. 51: Swales, W.E The life cycle of Fascioloides magna (Bassi, 1875), the large liver fluke of ruminants in Canada. Canadian Journal of Research 12: Turgeon, D.D., J.F. Quinn, Jr., A.E. Bogan, E.V. Coan, F.G. Hochberg, Jr., W.G. Lyons, P.M. Mikkelsen, R.J. Neves, C.F.E. Roper, G. Rosenberg, B. Roth, A. Scheltema, F.G. Thompson, M. Vecchione, and J.D. Williams Common and Scientific Names of Aquatic Invertebrates from the United States and Canada: Mollusks, 2 nd Edition. American Fisheries Society Special Publication 26. American Fisheries Society, Bethesda, Md. 536 pp. Vanderwaal, K.L., S.K. Windels, B.T. Olson, J.T. Vannatta, and R. Moen Landscape influence on spatial patterns of meningeal worm and liver-fluke infection in White-tailed Deer. Parasitology. 142: Vannatta, J.T The Giant Liver Fluke: A review, intermediate host habitat, and infection in a White-tailed Deer population in Minnesota. M.Sc. Thesis. University of Minnesota, Duluth, MN. 137 pp. Walter, W.M Mollusks of the upper Neuse River, North Carolina. Ph.D. Dissertation. Duke University, Durham, NC. 219 pp. 370