Parasite Co-Infections and Their Impact on Survival of Indigenous Cattle

Thumbi, Samuel M.; Bronsvoort, Barend M. deC.; Poole, Elizabeth J.; Kiara, Henry K.; Toye, Philip G.; Mbole-Kariuki, Mary; Conradie, Ilana; Jennings, Amy; Handel, Ian; Coetzer, Jacobus A.W.; Steyl, Johan Christian Abraham; Hanotte, Olivier; Woolhouse, Mark E. J.

doi:10.1371/journal.pone.0076324

Cited by 57 publications

(71 citation statements)

References 30 publications

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“…Impacts of parasites on their hosts are usually studied in simple one parasite — one host species context. However, multispecies infections are not uncommon (Alizon, de Roode, & Michalakis, ; Hughes & Boomsma, ; Lagrue & Poulin, ; Lange, Reuter, Ebert, Muylaert, & Decaestecker, ; Pedersen & Fenton, ; Thumbi et al., ). Furthermore, although each infection event is often independent, the presence of multiple parasite species within a host may have synergistic or antagonistic effects compared to the presence of one parasite alone (Alizon et al., ; Lagrue & Poulin, ; Lange et al., ).…”

Section: Introductionmentioning

confidence: 99%

Differential impacts of shared parasites on fitness components among competing hosts

Friesen

Poulin

Lagrue

2017

Ecology and Evolution

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Effects of parasites on individual hosts can eventually translate to impacts on host communities. In particular, parasitism can differentially affect host fitness among sympatric and interacting host species. We examined whether the impact of shared parasites varied among host species within the same community. Specifically, we looked at the impacts of the acanthocephalan Acanthocephalus galaxii, the trematodes Coitocaecum parvum and Maritrema poulini, and the nematode Hedruris spinigera, on three host species: the amphipods, Paracalliope fluviatilis and Paracorophium excavatum, and the isopod, Austridotea annectens. We assessed parasite infection levels in the three host species and tested for effects on host survival, behavior, probability of pairing, and fecundity. Maritrema poulini and C. parvum were most abundant in P. excavatum but had no effect on its survival, whereas they negatively affected the survival of P. fluviatilis, the other amphipod. Female amphipods carrying young had higher M. poulini and C. parvum abundance than those without, yet the number of young carried was not linked to parasite abundance. Behavior of the isopod A. annectens was affected by M. poulini infection; more heavily infected individuals were more active. Paracorophium excavatum moved longer distances when abundance of C. parvum was lower, yet no relationship existed with respect to infection by both M. poulini and C. parvum. The differential effects of parasites on amphipods and isopods may lead to community‐wide effects. Understanding the consequences of parasitic infection and differences among host species is key to gaining greater insight into the role of parasite mediation in ecosystem dynamics.

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Section: Introductionmentioning

confidence: 99%

Differential impacts of shared parasites on fitness components among competing hosts

Friesen

Poulin

Lagrue

2017

Ecology and Evolution

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“…Since parasites can bring about distinct changes to host hematology, body condition and immune investment (Budischak et al., 2012, van Wyk et al., 2014), it follows that even disparate parasites can boost (Monteiro et al., 2007b, Knowles, 2011, Thumbi et al., 2014) or suppress one another (Moreno et al., 2013) via their influences on host immune function (Cox, 2001, Ulrich and Schmid-Hempel, 2012). Although the logistics and economics of collecting long-term, individual-based infection data are challenging, these data are critical to study the effects of age, social structure, life history, time, seasonal variation, and co-infection on disease dynamics (Clutton-Brock and Sheldon, 2010).…”

Section: Introductionmentioning

confidence: 99%

Temporal and demographic blood parasite dynamics in two free-ranging neotropical primates

Erkenswick

Watsa

Gozalo

et al. 2017

International Journal for Parasitology: Parasites and Wildlife

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Parasite-host relationships are influenced by several factors intrinsic to hosts, such as social standing, group membership, sex, and age. However, in wild populations, temporal variation in parasite distributions and concomitant infections can alter these patterns. We used microscropy and molecular methods to screen for naturally occurring haemoparasitic infections in two Neotropical primate host populations, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, in the lowland tropical rainforests of southeastern Peru. Repeat sampling was conducted from known individuals over a three-year period to test for parasite-host and parasite-parasite associations. Three parasites were detected in L. weddelli including Trypanosoma minasense, Mansonella mariae, and Dipetalonema spp., while S. imperator only hosted the latter two. Temporal variation in prevalence was observed in T. minasense and Dipetalonema spp., confirming the necessity of a multi-year study to evaluate parasite-host relationships in this system. Although callitrichids display a distinct reproductive dominance hierarchy, characterized by single breeding females that typically mate polyandrously and can suppress the reproduction of subdominant females, logistic models did not identify sex or breeding status as determining factors in the presence of these parasites. However, age class had a positive effect on infection with M. mariae and T. minasense, and adults demonstrated higher parasite species richness than juveniles or sub-adults across both species. Body weight had a positive effect on the presence of Dipetalonema spp. The inclusion of co-infection variables in statistical models of parasite presence/absence data improved model fit for two of three parasites. This study verifies the importance and need for broad spectrum and long-term screening of parasite assemblages of natural host populations.

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“…Observations on one parasite may imply greater or lower risks or intensities of infection with other parasites, including zoonotic parasites. In addition, the results emphasize that parasite-specific interventions, or even rodent control, will have implications for a range of parasites and may influence patterns of zoonotic species maintenance: potentially either adding value to the control program or counteracting it if other parasites, such as life-threatening leptospires, are released from competition (Lello et al 2004, Telfer et al 2010, Thumbi et al 2014, as is also the case with human coinfection (Lello et al 2013, Griffiths et al 2014).…”

Section: Discussionmentioning

confidence: 93%

Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum

et al. 2019

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We examine coinfection between helminth species and the bacterium Leptospira interrogans in a natural population of the Norway rat, Rattus norvegicus. We ask whether coinfection can influence the probability and intensity of infection of these enzootic and zoonotic parasites in urban rats, which may affect the loads of parasites excreted into the environment. Rodent sampling was carried out during two seasons in 2014 in a Brazilian urban slum. We sampled rats’ feces, kidney imprints, and urine to identify and quantify helminth eggs/larvae and infection by L. interrogans. Eleven species/groups of helminths and L. interrogans were identified among 299 captured rats. Simple correlation tests and generalized linear models were performed to identify general patterns of coinfection and potential direction of effects, respectively, after controlling for consolidated environmental and host biotic variables. Significant associations were illustrated in an interaction network. Focusing on parasites with the potential to cause zoonoses among humans, we observed that coinfection between L. interrogans and the nematode Angiostrongylus cantonensis was significantly more frequent than expected. Reduced prevalence of A. cantonensis was found in the presence of Nippostrongylus brasiliensis, and N. brasiliensis intensities (eggs per gram of feces) were increased with greater intensities of both L. interrogans and Strongyloides sp., the latter of which was, in turn, found to increase the intensities of A. cantonensis. A higher probability of finding L. interrogans was associated with infection by Strongyloides sp. Our study provides a novel perspective on evaluating helminth coinfection profiles in populations of naturally infected urban rats, moving beyond previous studies which have been limited to descriptions of co‐occurrence. Noticeably, infection risk was dependent on coinfection and this should be accounted for when targeting the control of zoonotic pathogens in natural populations.

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Parasite Co-Infections and Their Impact on Survival of Indigenous Cattle

Cited by 57 publications

References 30 publications

Differential impacts of shared parasites on fitness components among competing hosts

Differential impacts of shared parasites on fitness components among competing hosts

Temporal and demographic blood parasite dynamics in two free-ranging neotropical primates

Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum

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