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

ABSTRACT: Host immune defenses are important components of host-parasite interactions that affect the outcome of infection and may have fitness consequences for hosts when increased allocation of resources to immune responses undermines other essential life processes. Research on host-parasite interactions in large free-ranging wild mammals is currently hampered by a lack of verified noninvasive assays. We successfully adapted existing assays to measure innate and adaptive immune responses produced by the gastrointestinal mucosa in spotted hyena (Crocuta crocuta) feces, including enzyme-linked immunosorbent assays (ELISAs), to quantify fecal immunoglobulins (total IgA, total IgG) and total fecal O-linked oligosaccharides (mucin). We investigated the effect of infection load by an energetically costly hookworm (Ancylostoma), parasite richness, host age, sex, year of sampling, and clan membership on immune responses and asked whether high investment in immune responses during early life affects longevity in individually known spotted hyenas in the Serengeti National Park, Tanzania. Fecal concentrations of IgA, IgG, and mucin increased with Ancylostoma egg load and were higher in juveniles than in adults. Females had higher mucin concentrations than males. Juvenile females had higher IgG concentrations than juvenile males, whereas adult females had lower IgG concentrations than adult males. High IgA concentrations during the first year of life were linked to reduced longevity after controlling for age at sampling and Ancylostoma egg load. Our study demonstrates that the use of noninvasive methods can increase knowledge on the complex relationship between gastrointestinal parasites and host local immune responses in wild large mammals and reveal fitness-relevant effects of these responses.

SUBMITTER: Ferreira SCM

PROVIDER: S-EPMC8216923 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:Gastrointestinal parasite (GIP) infections control has an important role to play in increasing livestock production from a limited natural resource base and to improve animal health and welfare. This study aimed to collect indigenous knowledge and identify wild plants locally used by goat smallholders of three territories of Haut-Katanga province for treating signs of gastrointestinal parasitism. Ethnoveterinary surveys were conducted by semi-structured interviews and a bibliographic screening of the biological activities relating to cited plants was carried out. Our interviews showed that ethnosemantic diagnoses of GIP diseases are based on signs. Eighty-seven informants reported that 27 plant species from 15 families, dominated by Fabaceae (29.6%) and Lamiaceae (18.5%) were commonly used in their goats treatment. Among these plants, five species with palmately compound leaves were considerably more used. From those, we noted a substitution of Vitex congolensis De Wild. and T. Durand (Lamiaceae) by Oldfieldia dactylophylla (Welw. Ex Oliv.) J. Leonard (Picrodendraceae) and of Vitex mombassae Vatke by Vitex madiensis Oliv. Subsp. Milanjiensis (Britten) F. White. Roots (46.9%), leaves (28.0%) and seeds (12.5%) were the most frequently used plant organs, and maceration is applied for most of the medicinal preparations (62.2%). Recipes were administered by oral route, for GIP 1) prevention (33.3%), by macerating the ground plant material in drinking water for 2 weeks at the start of each season (dry and rainy); and 2) treatment (66.7%). According to the literature, some of these plants have few or no studies investigating their anthelmintic activity. The cited plants are worth investigating further as they could constitute an effective alternative strategy in maintaining animal productivity. Studies on the biological activity of these plants can also provide indications of promising leads for extracts that could be developed into commercial standardized medications.

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

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