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Black-Flies and Leucocytozoon Spp. As Causes of Mortality in Juvenile Great Horned Owls in the Yukon, Canada

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Black-Flies and Leucocytozoon Spp. As Causes of Mortality in Juvenile Great Horned Owls in the Yukon, Canada Black-flies and Leucocytozoon spp. as Causes of Mortality in Juvenile Great Horned Owls in the Yukon, Canada D. Bruce Hunter1, Christoph Rohner2, and Doug C. Currie3 ABSTRACT.—Black fly feeding and infection with the blood parasite Leucocytozoon spp. caused mortality in juvenile Great Horned Owls (Bubo virginianus) in the Yukon, Canada during 1989-1990. The mortality occurred during a year of food shortage corresponding with the crash in snowshoe hare (Lepus americanus) populations. We postulate that the occurrence of disease was mediated by reduced food availability. Rohner (1994) evaluated the numerical re- black flies identified from Alaska, USA and the sponse of Great Horned Owls (Bubo virginianus) Yukon Territory, Canada, 36 percent are orni- to the snowshoe hare (Lepus americanus) cycle thophilic, 39 percent mammalophilic and 25 from 1988 to 1993 in the Kluane Lake area of percent autogenous (Currie 1997). Numerous southwestern Yukon, Canada. The survival of female black flies were obtained from the car- juvenile owls was very high during 1989 and casses of the juvenile owls, but only 45 of these 1990, both years of abundant hare populations. were sufficiently well preserved for identifica- Survival decreased in 1991, the first year of the tion. They belonged to four taxa as follows: snowshoe hare population decline (Rohner and Helodon (Distosimulium) pleuralis (Malloch), 1; Hunter 1996). Monitoring of nest sites Helodon (Parahelodon) decemarticulatus combined with tracking of individuals by radio- (Twinn), 3; Simulium (Eusimulium) aureum Fries telemetry provided us with carcasses of 28 ju- complex, 3; and Simulium (Eusimulium) venile owls found dead during 1990 and 1991 canonicolum (Dyar and Shannon) complex, 38 (Rohner and Doyle 1992). Although we (Hunter et al. 1997). observed a variety of causes of death in these carcasses including trauma and bacterial Black flies are pool feeders that penetrate the infections, 13 of the 28 owls died from severe skin and produce small craterous lesions using anemia, dehydration and extensive skin lesions a slashing or biting action involving the stylets attributed to feeding by ornithophilic black flies and labium (Sutcliffe and McIver 1984). Black (Diptera: Simulidae) and in several birds, fly saliva containing anticoagulants, enzymes internal lesions caused by heavy concurrent and histamine, is mixed with the blood pre- infections with Leucocytozoon spp. (Rohner and venting clotting until it is ingested by the fly. Hunter 1996, Hunter et al. 1997). This was the Black fly bites cause localized tissue damage first record of black flies from Great Horned and if the number of feeding flies is sufficient, Owls and provided evidence of black flies as they may produce a blood-loss anemia. In potential pathogens for young owls (Hunter et addition, the host’s reaction to fly attacks may al. 1997). include systemic illness, allergic reactions or even death; these reactions presumably Black flies are abundant throughout north- mediated by histamine. Harwood and James western North America. Of the 70 species of (1979) refer to a systemic reaction to black fly bites in humans known as “black fly fever” 1 Department of Pathobiology, Ontario Veterin- characterized by headaches, fever, nausea, ary College, University of Guelph, Guelph, adenitis, generalized dermatitis, and allergic Ontario, Canada N1G 2W1. asthma. In Alberta and Saskatchewan (Can- 2 Centre for Biodiversity Research, Department ada), intense black fly attacks have caused of Zoology, University of British Columbia, hysteria, systemic disease, and mortality in Vancouver, BC, Canada V6T 1Z4. cattle (Fredeen 1969, Harwood and James 3 Centre for Biodiversity and Conservation 1979). The pathogenicity of black flies for birds Biology, Royal Ontario Museum, 100 Queen’s has not been well established. Edgar (1953) Park, Toronto, Ontario, Canada M5S 2C6. reported egg production drops in laying 243 2nd Owl Symposium chickens tormented by black flies. We could al. 1993 ), or basic behaviors such as nest only find a single report of black fly induced defense activity (Ilmonen pers. comm.). pathology in raptorial birds. S. Cain (unpubl. data) observed mortality and premature evacu- That subclinical disease can affect reproductive ation of nests by Red-tailed Hawk (Buteo jamai- performance, life history strategies, and censis) chicks in Wyoming (USA) due to black survival in wild bird populations is not fly attacks. Black flies are also the main vector surprising if one considers the large body of for the blood parasite Leucocytozoon spp. information available in the domestic poultry literature. In growing commercial poultry, Although Leucocytozoon spp. can be a serious subclinical disease, regardless of the etiologic pathogen in immunologically naive captive or agent, results in decreased growth rates, domestic waterfowl, turkeys and chickens reduced feed consumption and feed conversion (Bennett et al. 1993), rarely has it been asso- rates, retarded physiologic maturation leading ciated with clinical disease or mortality in wild to slow feathering patterns, and reduced birds (Herman et al. 1975). Leucocytozoon spp. immune competence etc., without causing infection is common in raptorial birds (Peirce overt clinical disease or mortality. Any of these 1981) but documentation of clinical disease sorts of physiologic changes induced by and mortality is lacking. The fledgling owls in subclinical diseases in wild species must our study had massive parasitemias and wide- reduce the chances of juvenile survival. In spread tissue lesions associated with concur- adult breeder or commercial laying hens, the rent Leucocytozoon spp. infection which we first indication of subclinical disease is a believe contributed to the mortality. reduction or complete cessation of egg production. Parasites and most pathogens Interestingly, mortality from parasitism only compete for critical resources and during occurred in 1991, the year of the crash in periods resource decline, for example during a snowshoe hare populations. We have no reason period of declining food availability, the host to believe that the owls were not equally para- maintains itself at the expense of reproduction sitized in the previous years of the study, yet in or offspring survival. This strategy makes these years clinical disease or mortality due to sense in species with a relatively long parasitism was not observed. reproductive life span. We suspect that almost every northern Great In our Great Horned Owl study, black fly Horned Owl chick is exposed to black flies and feeding, the effects of infection with that most become infected with Leucocytozoon Leucocytozoon spp., and likely other spp. Under normal conditions and during unrecognized subclinical disease occurrences years of adequate food supply, as occurred in all compete for host resources. We suspect 1989 and 1990, young birds were able to that even in years when mortality due to successfully fight infection, recover from the parasitism is low, black fly feeding may anemia and fledgling survival remained high. influence other aspects of Great Horned Owl We propose that the occurrence of clinical behavior such as nest site selection, timing of disease and mortality in 1991 was mediated by nesting, and roost site selection of fledglings. reduced food availability and possibly other The recognition and biologic importance of factors. subclinical disease has received little attention by researchers, yet may yield interesting and Most wildlife managers recognize that disease important biological information about the life is endemic in wildlife populations, but there is history strategies of wild species. a tendency to think of disease in terms of indi- vidual mortality events or isolated dieoffs. Our LITERATURE CITED understanding of the subclinical effects of disease on individuals or populations is very Bennett, G.P.; Peirce, M.A.; Ashford, R.W. limited. There is an increasing number of 1993. Avian haematozoa: mortality and reports demonstrating that subclinical disease pathogenicity. Journal of Natural History. in wildlife may affect biological processes such 27: 993-1001. as predator avoidance (Hudson et al. 1992, Temple 1987) or reproductive success by in- Clayton, D.H. 1991. The influence of parasites fluencing mate selection (discussed by Clayton on host sexual selection. Parasitology 1991), clutch size (Rohner 1994, Korpimäki et Today. 7: 329-334. 244 Currie, D.C. 1997. Black flies (Diptera: Simu- Peirce, M.A. 1981. Current knowledge of the liidae) of the Yukon, with reference to the haematozoa of raptors. In: Cooper, J.E.; black fly fauna of northwestern North Greenwood, A.G., eds. Recent advances in America. In: Downes, J.A.; Danks, H.V., the study of raptor diseases. Keighley, West eds. Insects of the Yukon. Ottawa, Canada: Yorkshire, England: Chiron Publications: Biological Survey of Canada (Terrestrial 15-19. Arthropods). In press. Rohner, C.; Doyle, F.I. 1992. Methods of Edgar, S.A. 1953. A field study of the effect of locating Great Horned Owl nests in the black fly bites on egg production of laying boreal forest. Journal of Raptor Research. hens. Poultry Science. 32: 779-780. 26: 33-35. Fredeen, F.J.H. 1969. Outbreaks of the black Rohner, C. 1994. The numerical response of fly Simulium articum (Malloch) in Alberta. Great Horned Owls to the snowshoe hare Quaestiones Entomologicae. 5: 341-72. cycle in the boreal forest. Vancouver, BC: University of British Columbia. Ph.D. Harwood, R.F.; James, M.T. 1979. Gnats, black
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