Sleeping site ecology, but not sex, affect ecto- and hemoparasite risk, in sympatric, arboreal primates (Avahi occidentalis and Lepilemur edwardsi)

Abstract

BackgroundA central question in evolutionary parasitology is to what extent ecology impacts patterns of parasitism in wild host populations. In this study, we aim to disentangle factors influencing the risk of parasite exposure by exploring the impact of sleeping site ecology on infection with ectoparasites and vector-borne hemoparasites in two sympatric primates endemic to Madagascar. Both species live in the same dry deciduous forest of northwestern Madagascar and cope with the same climatic constraints, they are arboreal, nocturnal, cat-sized and pair-living but differ prominently in sleeping site ecology. The Western woolly lemur (Avahi occidentalis) sleeps on open branches and frequently changes sleeping sites, whereas the Milne-Edward’s sportive lemur (Lepilemur edwardsi) uses tree holes, displaying strong sleeping site fidelity. Sleeping in tree holes should confer protection from mosquito-borne hemoparasites, but should enhance the risk for ectoparasite infestation with mites and nest-adapted ticks. Sex may affect parasite risk in both species comparably, with males bearing a higher risk than females due to an immunosuppressive effect of higher testosterone levels in males or to sex-specific behavior. To explore these hypotheses, ectoparasites and blood samples were collected from 22 individuals of A. occidentalis and 26 individuals of L. edwardsi during the dry and rainy season.Results L. edwardsi, but not A. occidentalis, harbored ectoparasites, namely ticks (Haemaphysalis lemuris [Ixodidae], Ornithodoros sp. [Argasidae]) and mites (Aetholaelaps trilyssa, [Laelapidae]), suggesting that sleeping in tree holes promotes infestation with ectoparasites. Interestingly, ectoparasites were found solely in the hot, rainy season with a prevalence of 75% (N = 16 animals). Blood smears were screened for the presence and infection intensity of hemoparasites. Microfilariae were detected in both species. Morphological characteristics suggested that each lemur species harbored two different filarial species. Prevalence of microfilarial infection was significantly lower in L. edwardsi than in A. occidentalis. No significant difference in infection intensity between the two host species, and no effect of season, daytime of sampling or sex on prevalence or infection intensity was found. In neither host species, parasite infection showed an influence on body weight as an indicator for body condition.ConclusionsOur findings support that sleeping site ecology affects ectoparasite infestation in nocturnal, arboreal mammalian hosts in the tropics, whereas there is no significant effect of host sex. The influence of sleeping site ecology to vector-borne hemoparasite risk is less pronounced. The observed parasite infections did not affect body condition and thus may be of minor importance for shaping reproductive fitness. Findings provide first evidence for the specific relevance of sleeping site ecology on parasitism in arboreal and social mammals. Further, our results increase the sparse knowledge on ecological drivers of prim...

Ectoparasite communities of small-bodied Malagasy primates: seasonal and socioecological influences on tick, mite and lice infestation of Microcebus murinus and M. ravelobensis in northwestern Madagascar

“…“microcebi” with respect to the proposed life-cycle model for H. lemuris [ 71 ] by adding mouse lemurs as potential hosts also for adult ticks in the rainy season. Detection of adult haemaphysaline ticks on Lepilemur edwardsi [ 72 ] in the rainy season supports the predicted univoltine life-cycle and implies a vector potential for disease transmission between endemic lemur species.…”

Differences in infection patterns of vector-borne blood-stage parasites of sympatric Malagasy primate species (Microcebus murinus, M. ravelobensis)

“…previously described in Malagasy lemurs.SpeciesHost speciesAdult ♂Microfilaria Dipetalenoma petteri (Chabaud and Choquet, 1955) Lepilemur ruficaudatus (in captivity)not describedLength: 285 μm Paulianfilaria puliani (Chabaud et al, 1961) Propithecus verreauxi Length: 23–29 mm, Width: 300 μm, Nerve ring: 285 μm from the anterior end, Tail: 165 μm, without lateral alae, 7 pericloacal papillae, 2 pairs of papillae at the posterior third of the tail, 1 pair of papillae at the terminus, Spiculae length: left 375 μm, right 125 μmLength: 230 μm Courduriella courdurieri (Chabaud et al, 1961) Indri indri Length: 21 mm, Width: 125 μm, Nerve ring: 135 μm from the anterior end, Tail: 70 μm, small ventro-lateral caudal alae, Pericloacal papillae small: 1 anterior to the cloaca, 5 pairs around lateral and posterior borders of the cloaca, 1 pair of papillae at the posterior third of the tail, Spiculae length: left 360 μm, right 95 μmLength: 128–140 μm Protofilaria furcata (Chandler, 1929) Varecia rubra (in captivity), Hapalemur griseus Length: 13–15 mm, Width: 150–175 μm, Nerve ring: 270 μm from the anterior end, Tail: 95–100 μm, Pericloacal papillae small and difficult to discern, Spiculae length: left 98 μm, right 78 μmLength: 250–277 μm Lemurfilaria lemuris (this study)/Onchocercidae sp. (Hokan et al, 2017) Microcebus murinus , Lepilemur edwardsi Length: 36.48 mm, Width: 478 μm, Nerve ring: 382 μm from the anterior end, Tail: 443.5 μm, Caudal papillae not clearly recognizable, Spicluae length: not clearly distinguishableLength:177–226 μm…”

“…no. KY586137, Hokan et al, 2017). In a phylogenetic analysis, the two sequences generated in this study unambiguously nested within a clade of Onchocercidae spp.…”

“…no. : KY586137), that was sampled at the same study site (Hokan et al, 2017). This high sequence identity again indicates that both belong to the same filarial nematode species, suggesting low host specificity and pathogen transmission across genus boundaries.…”

“…Infections with Babesia spp., Plasmodium spp., trypanosomes and filarial nematodes have been described in several, mostly larger-bodied, Malagasy lemur hosts (Uilenberg et al, 1972; Irwin and Raharison, 2009; Springer et al, 2015; Larsen et al, 2016; Hokan et al, 2017). This is the first systematic investigation of blood-stage parasites in two sympatric small-bodied lemur species, the Golden-brown Mouse Lemur ( Microcebus ravelobensis ) and the Grey Mouse Lemur ( M. murinus ), in consideration of potential factors that may contribute to heterogeneity of infection.…”