Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds

Abstract

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.

Ecology and Dynamics of the Blood Parasite, Hepatozoon Tuatarae (Apicomplexa), in Tuatara (Sphenodon Punctatus) on Stephens Island, New Zealand

“…The negative relationship between tuatara size and Ht prevalence contrasts with most other studies of reptilian blood parasites, which report that smaller or younger individuals were less likely to be infected with blood parasites because cumulative exposure to sources of infection increases with host age (Hepatozoon: Salkeld and Schwarzkopf, 2005;Plasmodium: Schall and Marghoob, 1995;Staats and Schall, 1996;haemogregarines: Sorci, 1996;Amo et al, 2004;Brown et al, 2006). However, the negative relationship between tuatara size and Ht intensity was consistent with numerous studies of reptilian blood parasites showing a decline in infection intensity of infected individuals with increased host size or age (Bromwich and Schall, 1986;Sol et al, 2003;Madsen et al, 2005;Brown et al, 2006) because younger individuals have had less opportunity to acquire immunity than older hosts (Hudson and Dobson, 1997;Sol et al, 2003).…”

“…Infection prevalence can vary with fluctuations in vector abundance, both seasonally (Bennett and Cameron, 1974) and spatially (Merila et al, 1995;Sol et al, 2000;Bajer et al, 2006), whereas patterns of infection within exposed populations can vary with host sex, body size, and reproductive status. The level of exposure to vectors can vary between host sexes if they differ in homerange size or activity rates (Krasnov et al, 2005).…”

“…The exposure of hosts to infected vectors can increase with host age, leading to a positive relationship between host age and infection prevalence (Allander and Bennett, 1994;Sorci, 1996;Amo et al, 2004;Salkeld and Schwarzkopf, 2005). However, lower levels of acquired immunity can lead to higher infection intensity in younger, infected hosts (Allander and Bennett, 1994;Hudson and Dobson, 1997;Sol et al, 2003). Thus, insights into the factors influencing the transmission of blood parasites and the levels of host immunity can be inferred from patterns of infection in natural populations.…”

Associations between malaria and MHC genes in a migratory songbird

“…A number of studies from wild bird populations have shown that there are severe fitness costs associated with the acute phase of avian malaria (Richner et al 1995;Oppliger et al 1996;Atkinson et al 2001;Sol et al 2003). In the great tit (Parus major), females with Plasmodium malaria infections lay smaller egg clutches (Richner et al 1995;Oppliger et al 1996).…”

Syncuaria squamata (Linstow, 1883) (Nematoda: Acuariidae) in the Great Cormorant [Phalacrocorax carbo sinensins (Blumenbach, 1798)] in northern Poland

“…For this reason, both the young and the adult cormorants are exposed to identical invasive forms of parasites occurring in their food. Consequently, the presence of most S. squamata in the immature birds is most likely a result of a much higher food uptake (related to high energy demand) by the immature birds during growth (Sitko, 1993) or the deficiency of their incompletely developed immunological system (Ros et al, 1997;Sol et al, 2003), or a combination of the two factors. However, effects of other environmental variables cannot be excluded.…”