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...

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Main Authors: Susana Carolina Martins Ferreira, Heribert Hofer, Luis Madeira de Carvalho, Marion L. East
Format: Article
Language:English
Published: Wiley 2019-08-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.5431
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spelling doaj-f53cc9758cca40ccbfc437de1bd317512021-03-02T05:01:59ZengWileyEcology and Evolution2045-77582019-08-019158783879910.1002/ece3.5431Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection loadSusana Carolina Martins Ferreira0Heribert Hofer1Luis Madeira de Carvalho2Marion L. East3Department of Ecological Dynamics Leibniz Institute for Zoo and Wildlife Research Berlin GermanyDepartment of Ecological Dynamics Leibniz Institute for Zoo and Wildlife Research Berlin GermanyCentre for Interdisciplinary Research in Animal Health (CIISA), Faculdade de Medicina Veterinaria Universidade de Lisboa Lisbon PortugalDepartment of Ecological Dynamics Leibniz Institute for Zoo and Wildlife Research Berlin GermanyAbstract 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.https://doi.org/10.1002/ece3.5431fitnessgastrointestinal parasitesjuvenile survivalresistanceSerengeti ecosystemspotted hyena
collection DOAJ
language English
format Article
sources DOAJ
author Susana Carolina Martins Ferreira
Heribert Hofer
Luis Madeira de Carvalho
Marion L. East
spellingShingle Susana Carolina Martins Ferreira
Heribert Hofer
Luis Madeira de Carvalho
Marion L. East
Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load
Ecology and Evolution
fitness
gastrointestinal parasites
juvenile survival
resistance
Serengeti ecosystem
spotted hyena
author_facet Susana Carolina Martins Ferreira
Heribert Hofer
Luis Madeira de Carvalho
Marion L. East
author_sort Susana Carolina Martins Ferreira
title Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load
title_short Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load
title_full Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load
title_fullStr Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load
title_full_unstemmed Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load
title_sort parasite infections in a social carnivore: evidence of their fitness consequences and factors modulating infection load
publisher Wiley
series Ecology and Evolution
issn 2045-7758
publishDate 2019-08-01
description 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.
topic fitness
gastrointestinal parasites
juvenile survival
resistance
Serengeti ecosystem
spotted hyena
url https://doi.org/10.1002/ece3.5431
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