Seasonal prevalence of a haematozoan parasite of Red-bellied Woodpeckers (Melanerpes carolinus) and its association with host condition and overwinter survival

The Auk 120(1):130-137, 2003

ABSTRACT.-We examined seasonal prevalence of a haematozoan parasite (Haemoproteus velans) of the Red-bellied Woodpecker (Melanerpes carolinus) in the Apalachicola National Forest, northern Florida. We also investigated how infection with H. velans was associated with host mass, body condition, and overwinter survival. Analysis of blood smears taken from individual woodpeckers between May 2000 and July 2001 indicated that prevalence of H. velans peaked in July 2000, at ~80% of individuals sampled, decreased to 0% in January and February 2001, and peaked again in July 2001, at ~50% of individuals. Infection with H. velans was associated with low mass and poor body condition in males. Infection showed no association with female mass. In addition, infection with H. velans showed no relationship with overwinter survival. Our data reemphasize the importance of considering seasonal variation in parasite prevalence during testing for haematozoa. In addition, our data suggest that, although infection with H. velans is associated with poorer host condition, it does not negatively affect host survival. Received 15 March 2002, accepted 22 October 2002.

INTEREST IN THE potential role of parasites in the evolution and ecology of their hosts has grown substantially since Hamilton and Zuk (1982) proposed that mate choice based on parasite resistance is an important mechanism in sexual selection. Hamilton and Zuk's (1982) hypothesis proposed that females choose mates on the basis of condition-dependent secondary sexual characters that advertise parasite-resistant genotypes. That hypothesis was based on data suggesting a positive correlation between plumage brightness and the prevalence of protozoan blood parasites (haematozoa) in passerine birds. Much debate has followed about the evidence for Hamilton and Zuk's hypothesis (Hamilton and Zuk 1989, Read and Harvey 1989, Zuk 1989) and the practical issues involved in testing it (Cox 1989; Weatherhead and Bennett 1991, 1992). Part of that debate concerns the potential for haematozoan parasites to affect host fitness and the ability of researchers to detect chronic haematozoan infections (Cox 1989, Weatherhead and Bennett 1991). More recently, a trade-off between reproductive effort and resistance to haematozoan parasites has been proposed as a physiological mechanism potentially involved in mediating the cost of reproduction in birds (Norris et al. 1994, Richner et al. 1995, Oppliger et al. 1997, Nordling et al. 1998). That trade-off is thought to arise when limited resources must be partitioned between reproductive effort (i.e. number of offspring) and disease resistance. Growing evidence for a parasite-mediated cost of reproduction in birds has caused ecologists to reconsider the role of disease in population dynamics and life-history evolution (Price 1991).

Although the role of haematozoan parasites in avian evolutionary ecology has engendered much interest, the biology of haematozoa in the wild has not been well studied. Much of what is known about avian haematozoa has been learned from laboratory studies of domestic animals or from studies of the effects of haematozoa on novel hosts (van Riper et al. 1986, Atkinson and van Riper 1991). Poor understanding of haematozoan biology in wild populations of natural host species has raised doubts about the role of those parasites in the ecology and evolution of their hosts. Specifically, seasonal variation in parasite prevalence and the paucity of evidence for fitness effects have caused some authors to question the utility of using haematozoa to test for parasite-mediated sexual selection and life-history trade-offs (Cox 1989; Weatherhead and Bennett 1991, 1992; Sheldon and Verhulst 1996).

Several studies have demonstrated the tendency of haematozoan infections to increase in frequency during the breeding season (for example, Weatherhead and Bennett 1991, Hatchwell et al. 2000). That trend is often referred to as the spring relapse and is thought to occur when hormone activity or the physiological stress associated with breeding causes relapse of chronic infections (Atkinson and van Riper 1991). Weatherhead and Bennett (1992) have suggested that spring relapse hinders the ability of researchers to determine accurately, from a blood smear, whether an individual is infected. Blood smears can only be used to detect circulating haematozoa, but noncirculating chronic infections may persist in the livers of infected hosts (Jarvi et al. 2001). Noncirculating chronic infections may not be detected from blood smears if the individual is sampled before or after the peak of the relapse. Therefore, we must understand how parasite prevalence varies seasonally to maximize our ability to detect infections from blood smears.

The existence of parasite-mediated sexual selection or a parasite-mediated cost of reproduction requires that the parasites involved negatively affect host fitness (Hamilton and Zuk 1982, Sheldon and Verhulst 1996). Laboratory studies on domestic species have shown haematozoa to have significant pathological effects on their hosts (Atkinson and van Riper 1991). In addition, Plasmodium, the haematozoan parasite that causes avian malaria, has been shown to limit the geographic distribution and abundance of Hawaiian land birds (van Riper et al. 1986). Few studies have assessed the effect of haematozoa on host fitness in the wild, however, and evidence for negative associations between haematozoan infection and measures of host condition, which are often thought to reflect fitness, is mixed. Some studies have found no effect of haematozoa on survival rates or condition (reviewed by Bennett et al. 1988, 1993; Davidar and Morton 1993), whereas other studies have shown haematozoan parasites to affect negatively the immune and condition indices and the reproductive success of their hosts (Ots and Horak 1998, Merino et al. 2000).