Effects of hematozoan parasites on condition and return rates of American Kestrels

ABSTRACT.-We evaluated the relationship between blood parasites and body condition of American Kestrels (Falco sparverius) during the breeding season. Females that were infected with at least one species of parasite were in poorer condition than those without parasites during incubation but not prior to egg laying. We suggest that the relationship between parasitism and condition was masked before laying because of large increases in body mass of females during egg formation. Reduced condition of males during incubation also was associated with higher intensity of infections by Haemoproteus in one of two years. The negative association between condition and intensity of infection suggests that blood parasites impose costs on kestrels owing to competition for nutrients or allocation of energy by hosts to immune function or tissue repair Alternatively, kestrels in poor condition may be more likely to have relapses of chronic infections, or they may be less able to control new infections because of resource limitations. In contrast to results during incubation, during the prelaying period the prevalence of parasites tended to be higher, and in one year infections were more intense, among males in good condition. One possible explanation for these results is that body condition of males during courtship is an important determinant of the quality of mate they are able to obtain, and males may be accumulating body reserves at the expense of decreased immune function. Return rates of female kestrels to the study area declined as the intensity of their Haemoproteus infections increased, suggesting that blood parasitism is associated with reduced survival or increased dispersal probability. Received 30 September 1998, accepted 1 October 1999.

THEORY SUGGESTS that host-parasite interactions are responsible for substantial genetic variation within host populations (Anderson and May 1982), the evolution and maintenance of sexual reproduction and certain sexually selected traits (Hamilton 1980, Hamilton and Zuk 1982), and the complexity of parasite-resistance mechanisms (Anderson and May 1982, Behnke et al. 1992). Although such arguments are based on the premise that parasites reduce the fitness of their hosts (Combes 1997, Goater and Holmes 1997), the effects of parasites on hosts remain controversial. Diseased or moribund animals rarely are observed in nature, and finding parasites with commensal or amensal associations with hosts also is rare (Price 1980, Anderson and May 1982). Without knowledge of the effects of a specific parasite on a host species, it is impossible to evaluate the importance of the parasite as an evolutionary force (Price 1980).

Hematozoa are protozoan blood parasites whose life cycles have both sexual and asexual stages in an arthropod vector, and asexual stages in a vertebrate host (Desser and Bennett 1993). Detrimental effects on hosts can occur at several stages of the parasite's life cycle. Tissue damage to the host's liver, kidney, spleen, lungs, or other organs can occur when the vector injects sporozoites that enter host cells to develop into meronts (Desser and Bennett 1993, Peirce et al. 1997). The reinvasion of host cells by asexually produced merozoites also can cause damage, as can meronts that produce gametocytes. Gametocytes entering circulating erythrocytes may impair oxygen-carrying capacity or cause cells to rupture, resulting in host anemia (Kocan and Clark 1966, Maley and Desser 1977). We tested whether the presence (prevalence) and number (intensity) of circulating gametocytes were associated with body condition of breeding American Kestrels (Falco sparverius). We also tested whether prevalence and intensity of hematozoan infections were associated with return rates of kestrels to the study area from one year to the next.

STUDY AREA AND METHODS

We quantified hematozoa in a wild population of American Kestrels that bred in nest boxes near Besnard Lake (55N, 106W) in north-central Saskatchewan, Canada, during 1994 and 1995. Kestrels arrived on our study area in mid- to late April and began laying eggs in mid-May (Bortolotti 1994). Adult kestrels were first captured during the prelaying period using bal-chatri traps or nest-box traps. We captured adults again during incubation in nest boxes.

Blood collected from the brachial vein or the jugular vein was used to make blood smears (Bennett 1970). We air-dried and fixed smears in 100% ethanol immediately after obtaining each sample. Smears were stained with Giemsa and sent to the International Reference Centre for Avian Haematozoa at Memorial University, St. John's, Newfoundland, where G. F. Bennett quantified prevalence and intensity of hematozoa by counting the number of parasites in 100 microscope fields under oil, using a 100x objective for Haemoproteus and Plasmodium and a 40x objective for Leucocytozoon and Hepatozoon.

We banded each bird, weighed it to the nearest gram, and measured length of the unflattened wing chord, 10th primary outer rectrix, central rectrix, and culmen, and width of the tarsus. We obtained an index of body size using the first component of a principal components analysis (PCA). We used the six linear measurements for the PCA, performing separate analyses for females (n = 454) and males (n = 336; see Bortolotti and Iko 1992). Body mass is partly a function of an animal's structural size, so to obtain an index of condition we removed the effect of body size by regressing mass against PC1 and used the residuals as our measure of condition.