Veterinary Parasitology 140 (2006) 35–43 www.elsevier.com/locate/vetpar
Culicoides bottimeri as a vector of Haemoproteus lophortyx to quail in California, USA B.A. Mullens a,*, C.J. Cardona b, L. McClellan c, C.E. Szijj a, J.P. Owen a a
b
Department of Entomology, University of California, Riverside, CA 92521, USA Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA c K and L Quail, 26 Thompson Flat Road, Oroville, CA 95965, USA
Received 23 January 2006; received in revised form 3 March 2006; accepted 8 March 2006
Abstract Arthropod sampling via periodic direct bird examination and regular light trapping was conducted between June 2000 and October 2002 to survey for potential vectors of Haemoproteus lophortyx to nonnative, captive-raised bobwhite quail (Colinus virginianus) in northern California, USA. Examination of individual bobwhite quail (from 5 weeks of age through adult, total n = 76) was conducted on several dates during the transmission period (June–October). No ectoparasites, including hippoboscid flies (reported as Haemoproteus vectors to wild quail in early literature), were collected from the birds. Trapping with ultraviolet light suction traps near the quail revealed nine species of biting midges (Culicoides spp.). Of these, 94% were C. bottimeri, which was abundant near the birds, and 65% of collected C. bottimeri were engorged with blood. C. bottimeri adult activity began in late-April, slightly before the onset of disease in the quail. Activity peaked between July and late-September, coincident with maximum reported transmission, and adult activity ceased by early-November. Nonengorged C. bottimeri had a parity rate of 43.6% overall, suggesting excellent survival for biological transmission of a pathogen like H. lophortyx. A controlled study was done injecting a macerated slurry of pooled, nonengorged, wild-caught C. bottimeri into the peritoneum of 1-day-old bobwhite quail hatchlings held in insect-proof containers. Blood smears 13–19 days later confirmed H. lophortyx infection in zero controls but all insect-injected quail. Biting midges, especially C. bottimeri, transmit H. lophortyx to captive quail and probably are the dominant vector to native California quail (Callipepla californica) as well. # 2006 Elsevier B.V. All rights reserved. Keywords: Haemoproteus; Quail; Bobwhite quail; California quail; Malaria; Culicoides; Ceratopogonidae; Hippoboscidae
1. Introduction
* Corresponding author. Tel.: +1 951 827 5800; fax: +1 951 827 3086. E-mail address:
[email protected] (B.A. Mullens).
Avian haematozoa (e.g. Haemoproteus, Leucocytozoon and Plasmodium spp.) are very common nearly worldwide (Greiner et al., 1975; White et al., 1978; Bennett et al., 1992; Valkiunias, 1997). In North
0304-4017/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2006.03.015
36
B.A. Mullens et al. / Veterinary Parasitology 140 (2006) 35–43
America, species of the genus Haemoproteus frequently infect 10–50% of individuals in susceptible host species, and they are reported in at least 23 bird families (Greiner et al., 1975). While often regarded as rather nonpathogenic (perhaps because hosts become chronic carriers after recovery from acute infection), a number of instances of disease have been associated with members of this genus (see reviews by Atkinson, 1991; Garvin et al., 2003). Haemoproteus spp. are transmitted either by louse flies (Hippoboscidae) or by biting midges in the genus Culicoides (Ceratopogonidae), but vectors have been investigated for fewer than 10% of Haemoproteus spp. (Atkinson, 1991). It is thought that a particular species of Haemoproteus is likely to be transmitted by either louse flies or ceratopogonids, but probably not both (Atkinson, 1991). As discussed by Atkinson (1991), however, epidemiological evidence suggests that certain species such as H. columbiae may be transmitted by both groups (e.g. Greiner, 1975). California quail, Callipepla californica, are frequently infected by Haemoproteus lophortyx (O’Roke, 1930, 1932; Herman and Bischoff, 1949; Tarshis, 1955). The infection sometimes can cause anemia, prostration, or death in wild quail. More recently, high levels of infection, morbidity, and mortality in nonnative, captive bobwhite quail (Colinus virginianus) also have been documented (Cardona et al., 2002). In bobwhite quail, disease signs and symptoms include enlarged and darkened spleens and livers, hemorrhagic streaks (megaloschizonts) in skeletal muscles (particularly thighs and legs), erythrocyte destruction (hemolysis), and nervous system involvement leading to inability to stand (Cardona et al., 2002). Early work implicated two hippoboscids found on California quail, Lynchia hirsuta and Stilbometopa impressa, in transmission of H. lophortyx (O’Roke, 1930; Herman and Bischoff, 1949; Tarshis, 1955). Despite significant effort, however, the hippoboscid transmission of H. lophortyx was only marginally successful, with one reported transmission via sporozoite injection from L. hirsuta (O’Roke, 1930), one transmission by injection of sporozoites from S. impressa (Herman and Bischoff, 1949), and several cases of transmission by bite of S. impressa (Tarshis, 1955). At the time, the research community was unaware of the widespread involvement of
ceratopogonids in Haemoproteus spp. transmission, which was first recognized in the late 1950s (e.g. Fallis and Bennett, 1960). The present work was initiated to investigate potential vectors of H. lophortyx in a known, very active transmission setting in northern California (Cardona et al., 2002).
2. Materials and methods 2.1. Study site The study site was at the eastern edge of the northern Central Valley, at an elevation of 138 m in the foothills of the Sierra Nevada Mountain range near Oroville, Butte County, CA, USA (398320 N, 1218350 W latitude). The site had a permanent stream, with a pond and marshy area
