Survey of Blood Parasites in Black Vultures and Turkey Vultures from South Carolina
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1 2005 SOUTHEASTERN NATURALIST 4(2): Survey of Blood Parasites in Black Vultures and Turkey Vultures from South Carolina STEPHEN L. WEBB 1, ALAN M. FEDYNICH 1,*, SAMANTHA K. YELTATZIE 1, TRAVIS L. DEVAULT 2, AND OLIN E. RHODES, JR. 2 Abstract - Black Vultures (Coragyps atratus) and Turkey Vultures (Cathartes aura) are found throughout many parts of southeastern North America, but relatively little is known about the factors that may negatively impact their populations. We surveyed both species for blood parasites to learn more about factors that may influence their health. During , 22 Black Vultures and 11 Turkey Vultures were live-captured at the Savannah River Site in South Carolina. Two blood smears from each bird were made on microscope slides, stained, and examined at 1000x magnification. A Haemoproteus sp. was found in blood smears of one Turkey Vulture and microfilariae were detected in smears of one Black and two Turkey Vultures. We did not detect Leucocytozoon or Plasmodium in our samples, even though they have been reported in vultures from other parts of eastern North America. Introduction The Black Vulture (Coragyps atratus Bechstein 1793) and Turkey Vulture (Cathartes aura Linnaeus 1758) are new world vultures that play important roles in ecosystem function as a result of their scavenging behavior (del Hoyo et al. 1994). Although Black Vultures co-occur with Turkey Vultures in the southern United States, Central, and South America, relatively little is known about factors that may negatively impact their populations such as predation, diseases, and parasites (Buckley 1999, Kirk and Mossman 1998). Blood parasites are known to cause morbidity and mortality in various avifauna (Atkinson 1991, Forrester 1991, Greiner 1991). Often, bloodinhabiting protozoans are considered non-lethal at low levels of infection; however, they can cause anemia and possibly overwhelm a host s immune system at high levels of infection, thereby increasing susceptibility to other pathogens or predation. There are few published reports of blood parasites in Black Vultures. Robinson (1954) found microfilariae in four of four Black Vultures from Ohio, while Forrester et al. (1994) did not detect blood parasites in two Black Vultures from Florida. More recently, Forrester and Spalding (2003) reported results from 211 Black Vultures sampled in Florida between The single bird that was positive for blood parasites had concurrent Plasmodium elongatum Huff, 1930 and Leucocytozoon toddi Sambon, 1907 infections. 1 Caesar Kleberg Wildlife Research Institute, Texas A&M University-Kingsville, Kingsville, TX Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN * Corresponding author - alan.fedynich@tamuk.edu.
2 356 Southeastern Naturalist Vol. 4, No. 2 Blood parasite surveys of Turkey Vultures have been more extensive, ranging from 1 79 birds sampled in Georgia, Ohio, District of Columbia, New Jersey, Maryland, and Florida (Forrester and Spalding 2003; Forrester et al. 1994; Love et al. 1952; Robinson 1954, 1961; Wetmore 1941; Williams and Bennett 1978). Based on those studies that reported infections, Leucocytozoon sp., L. toddi, Haemoproteus sp., P. elongatum, and microfilariae occur in Turkey Vultures from North America. We initiated this study to learn more about the occurrence of blood parasites in Black Vultures and Turkey Vultures. Our objective was to determine if Black Vultures and Turkey Vultures sampled from the Savannah River Site (SRS) in South Carolina were infected with blood parasites. Study Area The SRS is a United States Department of Energy limited-access nuclear production and research facility located in Aiken County, SC. Trap sites were located near R Reactor, which is an abandoned nuclear reactor near the center of the SRS that now serves as a large communal roost for Black Vultures and Turkey Vultures. A detailed description of the plant communities and geographical features of the SRS is presented in White and Gaines (2000). Methods Vultures were captured during October December 2000 and June September 2001 using baited live traps and rocket nets for a concurrent study on vulture home range and movement patterns by two of the authors (T.L. DeVault and O.E. Rhodes, Jr.). We captured and sampled 22 Black Vultures and 11 Turkey Vultures. Of these, 12 adult Black Vultures were sampled during October December 2000 and 10 Black Vultures (three juveniles and seven adults) were sampled during June September One adult Black Vulture was recaptured during the second trapping period and was resampled (yielding 23 sets of slides for Black Vultures). One juvenile Turkey Vulture was sampled in winter 2000 and 10 (three juveniles and seven adults) were sampled in summer Each bird was aged according to feather characteristics, head coloration, and degree of wrinkling observed on the head (Buckley 1999, Kirk and Mossman 1998). We attached a backpack-mounted radio transmitter to each vulture, took blood samples, and released the bird at the trap site. For determining blood parasite infection, two thin blood smears were made from each bird using blood from the brachial vein obtained by venipuncture. Each blood smear was air-dried, preserved in 100% methanol for one minute, and stained using Diff-Quik. Each blood smear was examined for 15 minutes (total exam time was 30 minutes per bird) with a light microscope at 1000x magnification (Glass et al. 2002). Blood protozoan density was estimated using one of the two smears from the positive bird, in which 10,000 erythrocytes were counted in 100 replicates of 100 each, following protocols of Godfrey et al. (1987).
3 2005 S.L. Webb, A.M. Fedynich, S.K. Yeltatzie, T.L. DeVault, and O.E. Rhodes, Jr. 357 Vultures were trapped, handled, and radio-marked according to the protocols of the United States Fish and Wildlife Service (Permit No. MB ) and South Carolina Department of Natural Resources (Permit No. G-00-17). This study was approved by the Purdue University Animal Care and Use Committee (No ). Results No blood protozoans were observed on blood smears of the Black Vultures. However, a microfilaria was found in one Black Vulture sampled during winter One juvenile Turkey Vulture sampled in June 2001 was concurrently infected with Haemoproteus sp. and microfilariae, and one adult was infected with microfilariae. Density of Haemoproteus sp. was 2 per 10,000 erythrocytes. Protocols for quantifying density of microfilariae in blood smears have not been developed and, therefore, were not attempted. The adult Black Vulture that was captured twice was negative on both occasions. Discussion Microfilariae are motile embryos of filariid nematodes that occur in a wide range of avian species (Greiner et al. 1975) and include several genera such as Ornithofilaria, Sarconema, and Splendidofilaria (Cohen et al. 1991, McDonald 1969, Sonin 1966). No attempts were made to further identify microfilariae because identification typically requires the adult nematode (Saunders 1959, Sonin 1966). Typically, microfilariae occur in the circulatory system where they are acquired by blood feeding vectors. In our study, microfilariae prevalences of 5% (1 of 22) in Black Vultures and 18% (2 of 11) in Turkey Vultures were lower than those reported by Robinson (1954), who found prevalences of 100% (4 of 4) in Black Vultures and 66% (2 of 3) in Turkey Vultures from southeastern Georgia. Robinson (1961) also reported that one Turkey Vulture sampled in Ohio was infected. Wetmore (1941) examined 79 Turkey Vultures in the Washington, DC, area and found nine (11%) infected with microfilariae. In our study, no Haemoproteus sp. or Leucocytozoon sp. were found in blood smears of Black Vultures, although a Haemoproteus sp. was observed on both blood smears of one Turkey Vulture. Darling (1912) found what he believed to be Haemoproteus danilewskyi Kruse, 1890 in several Turkey Vultures from the Canal Zone in Panama; however, this species occurs only in the Corvidae (Bishop and Bennett 1990) and was likely misidentified (Wetmore 1941). The blood protozoan found in our study was not identified to species, as no taxonomic description to species in New World vultures currently exists. It should be noted that examination of blood smears for blood protozoans may result in increased false negatives, because this method only samples for those stages of protozoans that occur in the blood (i.e., in leucocytes and
4 358 Southeastern Naturalist Vol. 4, No. 2 erythrocytes). Thus, this method would miss those infected hosts that were not demonstrating infections in the blood or those that had extremely low densities circulating in the blood when sampled. We believe the latter possibility was minimized as smears of each bird were examined for 30 minutes. Examination of impression smears of organs might demonstrate exoerythrocytic schizonts, which could reduce the number of false negatives of certain species of protozoans resulting from using blood smears exclusively. However, this method requires killing the host, which was not possible for our study. Of the 79 Turkey Vultures examined by Wetmore (1941), 14 (18%) individuals were infected with a Haemoproteus sp. and two (3%) individuals were infected with a Leucocytozoon sp. Additionally, Williams and Bennett (1978) found two birds infected with a Haemoproteus sp. and one bird infected with a Leucocytozoon sp. from a sample of nine Turkey Vultures from Maryland and New Jersey. Of the 11 Turkey Vultures reported in Forrester and Spalding (2003), one was infected with P. elongatum. In spite of small sample sizes in these studies, parasites representing three major groups of blood protozoans have been found, suggesting that they have relatively high prevalence. By contrast, prevalence and diversity of blood protozoans in Black Vultures appears to be low with only one bird infected with both L. toddi and P. elongatum out of a sample of 211 reported in Forrester and Spalding (2003) and 22 in our study. In conclusion, our findings suggest that blood parasites were uncommon in Black Vultures and Turkey Vultures occurring at the SRS, or at least they were not demonstrating active infections in the peripheral blood when the birds were sampled during either winter 2000 or summer Based on the findings reported in studies conducted in North America, Haemoproteus sp. is noticeably absent in Black Vultures, whereas Leucocytozoon sp., Plasmodium sp., and microfilariae have been found in both host species, but with marked differences in prevalence. These findings provide opportunity for future research directed at determining the causes and consequences of blood parasite patterns in Black Vultures and Turkey Vultures from North America. Acknowledgments Funding was provided by the Caesar Kleberg Wildlife Research Institute and by contract DABT63-96-D-0006 between Purdue University and the United States Air Force Bird/Wildlife Aircraft Strike Hazard Team. We also acknowledge the support of the Purdue University Department of Forestry and Natural Resources, and the United States Department of Energy through contract DE-FC09-96SR18546 with the University of Georgia s Savannah River Ecology Laboratory. We thank A.L. Bryan, B.D. Reinhart, J.L. Weston, and I.L. Brisbin, Jr. for help on various aspects of this project. This is manuscript number of the Caesar Kleberg Wildlife Research Institute.
5 2005 S.L. Webb, A.M. Fedynich, S.K. Yeltatzie, T.L. DeVault, and O.E. Rhodes, Jr. 359 Literature Cited Atkinson, C.T Vectors, epizootiology, and pathogenicity of avian species of Haemoproteus (Haemosporina: Haemoproteidae). Bulletin of the Society for Vector Ecology 16: Bishop, M.A., and G.F. Bennett The haemoproteids of the avian families Corvidae (crows and jays) and Sturnidae (starlings and mynas) (Passeriformes). Canadian Journal of Zoology 68: Buckley, N.J Black Vulture (Coragyps atratus). In A. Poole and F. Gill (Eds.). The Birds of North America, No The Birds of North America, Inc., Philadelphia, PA. 24 pp. Cohen, S., M.T. Greenwood, and J.A. Fowler The louse Trinoton anserinum (Amblycera: Phthiraptera), an intermediate host of Sarconema eurycerca (Filarioidea: Nematoda), a heartworm of swans. Medical and Veterinary Entomology 5: Darling, S.T Some blood parasites (Haemoproteus and Haemogregarina). Bulletin de la Societe de Pathologie Exotique et de ses Filiales 5: del Hoyo, J., A. Elliott, and J. Sargatal (Eds.) Handbook of the Birds of the World. Vol. 2. New World Vultures to Guineafowl. Lynx Ediciones, Barcelona, Spain. 638 pp. Forrester, D.J The ecology and epizootiology of avian pox and malaria in Wild Turkeys. Bulletin of the Society for Vector Ecology 16: Forrester, D.J., and M.G. Spalding Parasites and Diseases of Wild Birds in Florida. University Press of Florida, Gainsville, FL pp. Forrester, D.J., S.R. Telford, Jr., G.W. Foster, and G.F. Bennett Blood parasites of raptors in Florida. Journal of Raptor Research 28: Glass, J.W., A.M. Fedynich, M.F. Small, and S.J. Benn Characteristics of the haemosprote community in an expanding White-winged Dove population. Journal of Parasitology 88: Godfrey, Jr., R.D., A.M. Fedynich, and D.B. Pence Quantification of hematozoa in blood smears. Journal of Wildlife Diseases 23: Greiner, E.C Leucocytozoonosis in waterfowl and wild galliform birds. Bulletin of the Society for Vector Ecology 16: Greiner, E.C., G.F. Bennett, E.M. White, and R.F. Coombs Distribution of the avian hematozoa of North America. Canadian Journal of Zoology 53: Kirk, D.A., and M.J. Mossman Turkey Vulture (Cathartes aura). In A. Poole and F. Gill (Eds.). The Birds of North America, No The Birds of North America, Inc., Philadelphia, PA. 32 pp. Love, G.J., S.A. Wilkin, and M.H. Goodwin, Jr Incidence of blood parasites in birds collected in southwestern Georgia. Journal of Parasitology 38: McDonald, M.E Catalogue of helminths of waterfowl (Anatidae). Bureau of Sport Fisheries and Wildlife, Special Scientific Report Wildlife No. 126, Washington, DC. 692 pp. Robinson, Jr., E.J Notes on the occurrence and biology of filarial nematodes in southwestern Georgia. Journal of Parasitology 40: Robinson, Jr., E.J Incidence of microfilariae in some Ohio birds and data on the habits of a possible vector. Journal of Parasitology 47: Saunders, D.C Microfilariae and other blood parasites in Mexican wild doves and pigeons. Journal of Parasitology 45:69 75.
6 360 Southeastern Naturalist Vol. 4, No. 2 Sonin, M.D Filariata of Animals and Man and Diseases Caused by Them, Part One: Aproctoidea. Essentials of Nematodology, Vol. 17. Translated from Russian by Israel Program for Scientific Translations Keter Publishing House Jerusalem Ltd., Jerusalem, Israel. 365 pp. Wetmore, P.W Blood parasites of birds of the District of Columbia and Patuxent Research Refuge vicinity. Journal of Parasitology 27: White, D.L., and K.F. Gaines The Savannah River Site: Site description, land use, and management history. Studies in Avian Biology 21:8 17. Williams, N.A., and G.F. Bennett Hematozoa of some birds of New Jersey and Maryland. Canadian Journal of Zoology 56:
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