Links between blood parasites, blood chemistry, and the survival of nestling American crows

Abstract

Many studies have used the avian hemosporidians (Leucocytozoon, Plasmodium, and Hemoproteus) to test hypotheses of host–parasite co‐evolution, yet documented health and survival consequences of these blood parasites vary among studies and generalizations about their pathogenicity are debatable. In general, the negative effects of the hemosporidians are likely to be greatest during acute infections of young birds, yet most previous studies in wild passerines have examined chronic effects in adults. Here, we evaluated responses of nestling American crows (Corvus brachyrhynchos) to acute infection (prevalence and burden), as well as its short‐ and long‐term survival consequences. We used panel of nine hematological and biochemical parameters that are regularly used to evaluate the health of domestic animals, including leukocyte profiles, hematocrit, and plasma proteins. We assessed the effects of infection on survival in a mark‐recapture framework. Overall, 56% of crows (n = 321 samples) were infected by at least one of the three genera. Infections by all genera were associated with elevated plasma proteins and globulins, which could indicate an adaptive immune response. However, only Plasmodium infections were associated with low hematocrit (anemia) and lower fledging success, possibly mediated by the negative effect of low hematocrit values on body condition. Moreover, early Plasmodium infection (<40 days of age) had long‐term survival implications: it was associated with lower apparent survival probability within 3 years after fledging. These results suggest that young crows mounted an adaptive immune response to all three genera. Short‐ and long‐term pathological effects, however, were only apparent with Plasmodium infections.

Low heterozygosity is associated with vector‐borne disease in crows

“…Some avian taxa in North America do appear to mount a protective immune response against Plasmodium, as evidenced by specific alleles associated with resistance (Loiseau et al 2011, Sepil et al 2013, combined with apparent local adaptation to sympatric strains (Sarquis-Adamson and MacDougall-Shackleton 2016). Likewise, we found some evidence for an adaptive immune response to Plasmodium infection among crows in the Davis, California population: Globulins (the fraction of the plasma protein that contains parasite-specific antibodies) were elevated in Plasmodium-infected crows (Townsend et al 2018a).…”

“…In crows, inbreeding does appear to be associated with a suppressed or altered immune response. Likewise, we found some evidence for an adaptive immune response to Plasmodium infection among crows in the Davis, California population: Globulins (the fraction of the plasma protein that contains parasite-specific antibodies) were elevated in Plasmodium-infected crows (Townsend et al 2018a). However, the hypothesis that a suppressed immune response among inbred birds increases their infection risk assumes that crows can mount an effective immune response against Plasmodium and WNV.…”

“…Molecular scoring of Plasmodium followed methods and modified PCR conditions described in Freund et al (2016). Although this assay also screened for two other haemosporidian parasites (Leucocytozoon and Haemoproteus), the current study was focused on confirmed pathogens, and-unlike Plasmodium-Leucocytozoon and Haemoproteus did not have detectable negative health consequences in crows (Townsend et al 2018a). We identified Plasmodium in samples with parasite cyt b amplification by sequencing the fragments bidirectionally using the BigDye version 1.1 sequencing kit (Applied Biosystems, Foster City, California, USA) on an ABI PRISM3100 automated sequencer (Applied Biosystems).…”

“…Sequences were edited in Sequencher 4.9 (GeneCodes, Ann Arbor, Michigan, USA), aligned by eye, and then subjected to a BLAST search to ensure that Plasmodium was amplified. Although this assay also screened for two other haemosporidian parasites (Leucocytozoon and Haemoproteus), the current study was focused on confirmed pathogens, and-unlike Plasmodium-Leucocytozoon and Haemoproteus did not have detectable negative health consequences in crows (Townsend et al 2018a). However, for the purpose of comparison with other studies that have evaluated these genera, we present their relationship with heterozygosity in Appendix S1: Fig.…”

“…Here, we examined the relationship between heterozygosity in American crows (Corvus brachyrhynchos; "crows" hereafter) and three of their most commonly documented pathogens in Davis, California: (1) West Nile virus (WNV), an emerging, mosquito-borne flavivirus associated with high mortality rates in crows (Yaremych et al 2004, Reisen et al 2006, LaDeau et al 2007); (2) Plasmodium spp., a widespread mosquito-borne avian protozoal parasite that has been linked to anemia, poor condition, and lower survival in crows (Townsend et al 2018a); and (3) Campylobacter jejuni, a common and widespread bacterial pathogen with a fecal-oral transmission route (Waldenstr€ om and Griekspoor 2014, Weis et al 2014) that has been linked to poor condition and lower survival in crows (Taff and Townsend 2017). Although other parasites have been described in the Davis crow population, we did not evaluate them because they were either low in prevalence (e.g., poxviral dermatitis; Wheeler et al 2014) or they had no detectable negative health consequences on their hosts (e.g., other haemosporidian parasites; Townsend et al 2018a) and therefore were less likely to exert evolutionary pressure on host genetic diversity and composition (Ferrer et al 2014). Crows are well suited to this study because they inbreed regularly in some populations (Townsend et al 2009a(Townsend et al , 2010a, and because low heterozygosity in crows has been associated with elevated disease probability (Townsend et al 2009a), suppressed immune response (Townsend et al 2010b), and lower survival (Townsend et al 2009a(Townsend et al , 2010a).…”