Ticks (Ixodes sp.) and blood parasites (Haemoproteus spp.) in New Holland Honeyeaters (Phylidonyris novaehollandiae): evidence for site specificity and fitness costs

The degree to which widespread avian blood parasites in the genera Plasmodium and Haemoproteus pose a threat to novel hosts depends in part on the degree to which they are constrained to a particular host or host family. We examined the host distribution and host-specificity of these parasites in birds from two relatively understudied and isolated locations: Australia and Papua New Guinea. Using polymerase chain reaction (PCR), we detected infection in 69 of 105 species, representing 44% of individuals surveyed (n = 428). Across host families, prevalence of Haemoproteus ranged from 13% (Acanthizidae) to 56% (Petroicidae) while prevalence of Plasmodium ranged from 3% (Petroicidae) to 47% (Ptilonorhynchidae). We recovered 78 unique mitochondrial lineages from 155 sequences. Related lineages of Haemoproteus were more likely to derive from the same host family than predicted by chance at shallow (average LogDet genetic distance = 0, n = 12, P = 0.001) and greater depths (average distance = 0.014, n = 11, P < 0.001) within the parasite phylogeny. Within two major Haemoproteus subclades identified in a maximum likelihood phylogeny, host-specificity was evident up to parasite genetic distances of 0.029 and 0.007 based on logistic regression. We found no significant host relationship among lineages of Plasmodium by any method of analysis. These results support previous evidence of strong host-family specificity in Haemoproteus and suggest that lineages of Plasmodium are more likely to form evolutionarily-stable associations with novel hosts.

An important pattern in host-parasite assemblages is a higher intensity of parasites in juveniles than in adults, but the reasons for these differences remain obscure. Three non-mutually exclusive hypotheses have been proposed: (1) heavily parasitized juveniles die before being recruited into the adult population ('selection' hypothesis); (2) the development of an acquired immunity by the host in front of the parasite reduces the intensity of the parasite in adult hosts ('immunity' hypothesis); and (3) differences in behavior makes adults less exposed to the parasite than juveniles ('vector exposure' hypothesis). Having rejected the 'vector exposure' hypothesis in a previous study, here we tested the 'selection' and 'immunity' hypotheses in feral pigeons (Columba livia) infected by the blood parasite Haemoproteus columbae. In agreement with the 'selection' hypothesis, young (but not adult) pigeons that were highly parasitized had a lower probability of surviving until adulthood, independent of their body condition. However, selection was not strong enough to account for the observed differences in parasite intensity between age-classes, and after selection parasite intensity of survivors still remained 85% higher in juveniles than in adults. In contrast, the 'immunity' hypothesis offered a greater explanatory power. The intensity of blood parasites in young pigeons, but not in adults, decreased over time so dramatically that by the time they had become adults their intensities were indistinguishable from that typically seen in adults. Therefore, while selection against highly parasitized juveniles can contribute to some extent to a reduction in parasitism seen in the adult population, age-specific blood parasitism in feral pigeons is best explained as a transitory phase just before the host develops an effective immune response.

Both reproduction and parasite defense can be costly, and an animal may face a trade-off between investing in offspring or in parasite defense. In contrast to the findings from nonexperimental studies that the poorly reproducing individuals are often the ones with high parasite loads, this life-history view predicts that individuals with high reproductive investment will show high parasite prevalence. Here we provide an experimental confirmation of a positive association between parental investment levels of male great tits Parus major and the prevalence of Plasmodium spp, a hematozoa causing malaria in various bird species. We manipulated brood size, measured feeding effort of both males and females, and assessed the prevalence of the hemoparasite from blood smears. In enlarged broods the males, but not the females, showed significantly higher rates of food provisioning to the chicks, and the rate of malarial infection was found to be more than double in male, but not female, parents of enlarged broods. The findings show that there may be a trade-off between reproductive effort and parasite defense of the host and also suggest a mechanism for the well documented trade-off between current reproductive effort and parental survival.