Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load

Abstract

There are substantial individual differences in parasite composition and infection load in wildlife populations. Few studies have investigated the factors shaping this heterogeneity in large wild mammals or the impact of parasite infections on Darwinian fitness, particularly in juveniles. A host's parasite composition and infection load can be shaped by factors that determine contact with infective parasite stages and those that determine the host's resistance to infection, such as abiotic and social environmental factors, and age. Host–parasite interactions and synergies between coinfecting parasites may also be important. We test predictions derived from these different processes to investigate factors shaping infection loads (fecal egg/oocyte load) of two energetically costly gastrointestinal parasites: the hookworm Ancylostoma and the intracellular Cystoisospora , in juvenile spotted hyenas ( Crocuta crocuta ) in the Serengeti National Park, in Tanzania. We also assess whether parasite infections curtail survival to adulthood and longevity. Ancylostoma and Cystoisospora infection loads declined as the number of adult clan members increased, a result consistent with an encounter‐reduction effect whereby adults reduced encounters between juveniles and infective larvae, but were not affected by the number of juveniles in a clan. Infection loads decreased with age, possibly because active immune responses to infection improved with age. Differences in parasite load between clans possibly indicate variation in abiotic environmental factors between clan den sites. The survival of juveniles (<365 days old) to adulthood decreased with Ancylostoma load, increased with age, and was modulated by maternal social status. High‐ranking individuals with low Ancylostoma loads had a higher survivorship during the first 4 years of life than high‐ranking individuals with high Ancylostoma loads. These findings suggest that high infection loads with energetically costly parasites such as hookworms during early life can have negative fitness consequences.

Carnivore Detection at the Domestic/Wildlife Interface within Mpumalanga Province, South Africa

“…Therefore, smaller carnivores with shorter lifespans might be more important epidemiologically. Small felids including African wildcat, serval, and caracal are therefore expected to have a higher impact on environmental contamination with Toxoplasma gondii oocysts compared to lions, leopards, and cheetahs [ 3 , 81 , 82 ]…”

Noninvasively measured immune responses reflect current parasite infections in a wild carnivore and are linked to longevity

“…Finally, we investigated the link between each immune measure and individual longevity. For this purpose, we only included juveniles sampled before they reached 12 months of age (Ferreira et al, 2019).…”

Effects of life history stage and climatic conditions on fecal egg counts in plains zebras (Equus quagga) in the Serengeti National Park

“…Even so, previous studies revealed substantial variation between individuals in terms of their burden of infection with various parasite taxa, the diversity of co-infecting parasite taxa, and how these measures change over time (Irvine et al 2000;Behnke et al 2005;Irvine 2006;Ferreira et al 2019). Individuals differ in their exposure to parasite infective stages, in their ability to mount immune responses to control or clear infections due to factors such as climatic conditions, age, and diet (Cattadori et al 2005;Behnke et al 2005;Råberg et al 2009;Turner and Getz 2010;Hayward et al 2011;Ferreira et al 2019).…”

“…There is also a current lack of non-invasive (fecal) assays for wild mammalian species to measure relevant immunological responses to gastrointestinal parasite infections and how these responses are changed by prevailing conditions such as season, nutrition, and physiological stress throughout an individual’s lifespan (Lee 2006 ; Martin et al 2008 ; Ardia et al 2011 ). Even so, previous studies revealed substantial variation between individuals in terms of their burden of infection with various parasite taxa, the diversity of co-infecting parasite taxa, and how these measures change over time (Irvine et al 2000 ; Behnke et al 2005 ; Irvine 2006 ; Ferreira et al 2019 ). Individuals differ in their exposure to parasite infective stages, in their ability to mount immune responses to control or clear infections due to factors such as climatic conditions, age, and diet (Cattadori et al 2005 ; Behnke et al 2005 ; Råberg et al 2009 ; Turner and Getz 2010 ; Hayward et al 2011 ; Ferreira et al 2019 ).…”