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Journal of Parasitology 2021 107(4) 600–605 Ó American Society of Parasitologists 2021 Published 3 August 2021 Contents and archives available through www.bioone.org or www.jstor.org Journal of Parasitology journal homepage: www.journalofparasitology.org DOI: 10.1645/19-138 GAPEWORM (SYNGAMUS SPP.) PREVALENCE IN WISCONSIN GREATER PRAIRIE Downloaded from http://meridian.allenpress.com/journal-of-parasitology/article-pdf/107/4/600/2901038/i0022-3395-107-4-600.pdf by guest on 02 October 2021 CHICKENS (TYMPANUCHUS CUPIDO PINNATUS) J. A. Shurba1,2, R. A. Cole3, M. S. Broadway1,4, C. L. Roderick3, J. D. Riddle1, S. A. Dubay1, and S. Hull5 1 University of Wisconsin–Stevens Point, College of Natural Resources 800 Reserve Street, Stevens Point, Wisconsin 54481. 2 Department of Forestry and Environmental Conservation, Clemson University 261 Lehotsky Hall, Box 340317, Clemson, South Carolina 29634. 3 U.S. Geological Survey–National Wildlife Health Center, 6006 Schroeder Road, Madison, Wisconsin 53711. 4 Indiana Department of Natural Resources Division of Fish and Wildlife, 402 W. Washington Street, Indianapolis, Indiana 46204. 5 Wisconsin Department of Natural Resources, 101 S. Webster Street, PO Box 7921, Madison, Wisconsin 53707. Correspondence should be sent to J. A. Shurba (https://orcid.org/0000-0002-1895-4158) at: [email protected] or to R. A. Cole (https://orcid.org/ 0000-003-2923-1622) at: [email protected] KEY WORDS ABSTRACT Gapeworm Under Wisconsin state law, the greater prairie chicken (GRPC; Tympanuchus cupido pinnatus) has Greater prairie chicken been listed as a threatened species since 1976. In 2014–15, we conducted a pilot study to determine Syngamus spp. the prevalence and intensity of gapeworms (Syngamus spp.) in female Wisconsin GRPCs collected Tympanuchus cupido pinnatus from 2 monitored populations. We captured 62 female GRPCs using walk-in-style traps for females and night lighting for juveniles 45 days of age. From these individuals, we collected 15 carcasses of Wisconsin radio-marked birds, most of whom died due to predation events. Through dissection, we identified gapeworm in 20% of examined carcasses and report an intensity ranging between 4 and 74 worms. Greater prairie chickens (GRPCs; Tympanuchus cupido pinna- from yolk that was ectopically located in the body cavity (yolk tus) are grassland obligates once ubiquitous in mixed and tallgrass peritonitis) and heavy infection of the trachea and bronchi with prairies. However, habitat loss and fragmentation have resulted in Syngamus spp. (n ¼ 74) that resulted in chronic-active pleuro- GRPC declines (Ross et al., 2006), population isolation, and pneumonia and bronchitis. subsequent extirpations throughout endemic ranges (Westemeier Because there are no data on the extent of Syngamus spp. in et al., 1998). As a result of this decline in numbers, this species was GRPC, our goal was to collect recently deceased birds from 2 listed as threatened species by Wisconsin in 1976 (Sverdarsky et Wisconsin GRPC populations and examine them for Syngamus al., 2000). Similarly, expansive grassland and early successional spp. and to identify them via genetic analyses to expound on habitats provided nesting and brood-rearing cover before current genetic and morphological findings. We hypothesized conversion of lands to agriculture, which contributed to juvenile birds would have a higher prevalence of gapeworms Wisconsin GRPC population declines (Svedarksy et al., 2000). based on previous accounts provided by Goebel and Kutz (1945) Currently, Wisconsin GRPC populations are limited to grassland and Soulsby (1965), who reported that juvenile birds had a higher patches interspersed throughout the Central Wisconsin Grassland prevalence of infection of parasites based on their age and Conservation Area (CWGCA). The CWGCA is located in an resulting immature immune system. area of Wisconsin comprising mostly private farmland, where We trapped and banded 74 and 68 individual GRPCs on several sportsman’s clubs and game farms release pen-reared lekking grounds in 2014 and 2015, respectively. We radio-collared pheasants for hunting. During our study, mean lekking male 9 and 11 females at Paul Olson and 23 and 19 females at Buena counts were between 82 and 90 at the Paul J. Olson Wildlife Area Vista in 2014 and 2015, respectively. No stress-related mortalities (POWA, 4483101900 N, 8985200400 W) in Wood County in 2014 and were recorded, and birds were immediately released at capture 110–133 at the Buena Vista Wildlife Area (BVWA, 4483103800 N, sites after radio-collaring and processing. We monitored female 8983800000 W) in Portage County in 2015. prairie chickens via telemetry to determine breeding season and In 2015, one dead banded and radio-collared adult female nest survival as described in Broadway (2015). Females were GRPC from POWA was submitted frozen to the USGS National tracked until collar failure or mortality with carcass collection and Wildlife Health Center (NWHC) (Case 26614-001) to determine freezing usually within 24-hr post-mortem. the cause of death after noting uncharacteristic swelling to the Of the 15 radio-collared females recovered and necropsied, 14 crop and throat area during a regular telemetry check. died from natural causes (e.g., predation) and 1 likely died from Pathologists determined the bird was in good body condition, asphyxiation related to an impacted crop due to poor radio-collar but 2 disease processes were observed: acute coelomitis resulting fit. One bird was necropsied by a board-certified veterinary 600 This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. SHORT COMMUNICATION 601 pathologist at the NWHC, where worms were removed and fixed Hasegawa-Kishino-Yano plus G as the appropriate model. in warm 10% neutral buffered formalin, then preserved in 70% Statistical support for groupings was estimated by bootstrap ethanol, while 3 were fixed and stored in 100% ethanol. The analysis with 2,000 replications (Fig. 3). Not unexpectedly based remaining birds were necropsied at the University of Wisconsin– on results in Table II, PX1117 did not cluster with the other Stevens Point using the methods below. During the processing of GRPC nematodes in this study but clustered with S. merulae. carcasses, mass and body length to the nearest gram and Morphologically, female worm PX1117 was similar to S. merulae centimeter were recorded. The presence or absence of ectopara- females with respect to total worm length and anterior-vulva sites was noted by rubbing the carcass feathers to remove length (Baylis, 1926). However, spicule lengths, presence of a head ectoparasites. Additionally, superficial indicators of the potential collar (present in all, but not discernable for female PX 1211), and cause of death (puncture wounds, abrasions, etc.) were noted. lack of pronounced female tail appendage were similar to the After external examination, a single ventral incision was made, other GRPC specimens (PX1141, 1142, 1212, and 1264), not S. Downloaded from http://meridian.allenpress.com/journal-of-parasitology/article-pdf/107/4/600/2901038/i0022-3395-107-4-600.pdf by guest on 02 October 2021 and the trachea and lungs were removed. The trachea was opened merulae (unfortunately bursal rays were not visible in PX1117). via an incision along its entire length, and lungs were opened PX1141, 1142, 1212, and 1264 had some similar morphometrics along bronchi into bronchioles and examined for nematodes using and dorsal bursal ray morphology (Figs. 1, 2; Table I) and a dissection microscope. Nematodes were removed, counted, and overlapped considerably with Syngamus trachea (Madsen, 1950; preserved in 10% neutral buffered formalin. Barus, 1964). The dorsal bursal rays of these 4 worms also were Six mature, in copula worms in good condition were cleared in similar to those of Syngamus skrjabinomorpha that are found in lactophenol, and male and female were separated and examined domestic geese and chickens in the country of Georgia (Rizhikov, (Olympus BX 50F microscope; Olympus, Center Valley, Penn- 1949); however, the measurements were not in agreement on most sylvania) to observe taxonomically relevant characters (Cram, structures. Neither the morphometrics of the 4 worms nor the 1927; Madsen, 1950; Barus, 1964; Kanarek et al., 2016), which COI sequences agreed with any published data. The low number were photographed using a microscope-mounted Insight CMOS of worms collected in good condition along with the unsettled camera and SPOT 5.2 digital imaging software (Figs. 1, 2; Spot taxonomy of the species of Syngamus and the fact that the Imaging, Sterling Heights, Michigan). Measurements of each morphological characters are highly elastic and variable within a worm are presented in millimeters (mm) (Table I). Hologeno- species, and even within a single host (Lewis, 1928; Madsen, 1950; phore, paragenophore, and extracted DNA vouchers were Barus, 1964; Kanarek et al., 2016), prevented a robust description deposited in the Museum of Southwest Biology, University of of a new species. New Mexico, Albuquerque, New Mexico (MSB: Para: 30725- In total, 15 GRPC carcasses (4 juveniles, 11 adults) were 30731) and the Harold W. Manter Laboratory, University of examined, including the individual necropsied by NWHC. Of Nebraska, Lincoln, Nebraska (HWML 110419). A 2-mm piece of these, 5 still had a leg band at the time of necropsy with 3 midsection from each of the 6 female worms was removed, soaked collected from POWA and 2 from BVWA. Three

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