Competition and mutualism among the gut helminths of a mammalian host

Lello, Joanne; Boag, B.; Fenton, Andy; Stevenson, Ian R.; Hudson, Peter J.

doi:10.1038/nature02490

Cited by 274 publications

(317 citation statements)

References 25 publications

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“…The high seasonal variability of the immune response points to the significant costs of mounting it, and has clear implications for the evolutionary ecology of host-parasite interactions. Other parasites will be affected by, and contribute to, the hosts' immune status in varying ways (Lello et al 2004;Cattadori et al 2007a,b). This study provides some new insights into parasite-host dynamics and for our studies sets the scene for future experimental investigations of the interaction of T. retortaeformis with the community of parasites in rabbits.…”

Section: Discussionmentioning

confidence: 99%

Seasonality, cohort-dependence and the development of immunity in a natural host–nematode system

et al. 2007

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Acquired immunity is known to be a key modulator of the dynamics of many helminth parasites in domestic and human host populations, but its relative importance in natural populations is more controversial. A detailed long-term dataset on the gastrointestinal nematode Trichostrongylus retortaeformis in a wild population of European rabbits (Oryctolagus cuniculus) shows clear evidence of seasonal acquired immunity in the age-structured infection profiles. By fitting a hierarchy of demographic infectionimmunity models to the observed age-structured infection patterns, we are able to quantify the importance of different components (seasonality, immunity and host age structure) of the parasite dynamics. We find strong evidence that the hosts' immunocompetence waxes and wanes with the seasons, but also contains a lifelong cohort factor, possibly acting through a maternal effect dependent on the host's month of birth. These observations have important and broad implications for the ecology of parasite infection in seasonal natural herbivore systems.

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Section: Discussionmentioning

confidence: 99%

Seasonality, cohort-dependence and the development of immunity in a natural host–nematode system

et al. 2007

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“…In addition, or alternatively, to this main effect, it is possible that concurrent parasite infection exerts a synergistic effect. Although not easy to detect (Behnke et al 2005) such interactions have recently been documented for protozoa (Bajer et al 2002) and helminths (Lello et al 2004) in wild mammal populations. That is, infection with one species enhances proliferation of another species.…”

Section: Associations Between Protozoan Speciesmentioning

confidence: 99%

Epidemiology of parasitic protozoan infections in Soay sheep (Ovis ariesL.) on St Kilda

et al. 2006

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The feral Soay sheep (Ovis aries L.) population on Hirta, St Kilda, is host to a diverse component parasite community, but previous parasitological studies of the population have only focussed on the metazoan species. This paper reports the first epidemiological study of the protozoan species comprising Cryptosporidium parvum, Giardia duodenalis and 11 species of Eimeria in Soay sheep across 3 years of varying host population density. Prevalence and intensity of almost all species of protozoa significantly decreased with host age, with the exception of E. granulosa, which increased in prevalence with host age. The prevalence of C. parvum appeared to vary positively with host population density but that of G. duodenalis did not vary significantly with density. Most species of Eimeria showed a distinct lag in infection level following the host population crash of 2002, taking up to 2 years to decrease. Mixed Eimeria species intensity and diversity were highest in 2002, a year of low host density. Parasite diversity decreased with host age and was higher in males. There were 5 positive pair-wise associations between protozoa species in terms of prevalence. The results of this study highlight the potential for protozoal infection to shape the evolution of parasite resistance in wild host populations harbouring diverse parasite species.

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“…In earlier work we were able to detect evidence of a network of interspecific parasite interactions among the gut helminth community of the wild rabbit (Oryctolagus cuniculus) [4]. However, in all the statistical analyses of these helminths, month emerged as a strongly significant term [4].…”

Section: Introductionmentioning

confidence: 99%

“…However, in all the statistical analyses of these helminths, month emerged as a strongly significant term [4]. Therefore, the interplay between seasonal dynamics and the interspecific pathogen interactions may be important.…”

Section: Introductionmentioning

confidence: 99%

“…predator-prey relationships [1], hostpathogen relationships [2], resource competition [3]) have the capacity to alter the population dynamics of the interacting species. Further, there is growing interest in the dynamical consequences that co-infecting pathogen species have on each other [4]. Such interspecific pathogen interactions can crucially alter pathogen dynamics, host health and the success of control strategies [5].…”

Section: Introductionmentioning

confidence: 99%

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Pathogen Interactions, Population Cycles, and Phase Shifts

Lello¹,

Norman²,

Boag³

et al. 2008

The American Naturalist

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Interspecific pathogen interactions can profoundly affect pathogen population dynamics and the efficacy of control strategies. However, many pathogens exhibit cyclic abundance patterns (e.g. seasonality) and temporal asynchrony between interacting pathogens has the potential to reduce the impact of those interactions. Here we use an extension of our previously published model to investigate the effects of cyclic abundance patterns on pathogen interaction. We demonstrate that for interactions mediated through host immunity, immune memory can maintain the impact of an interaction even when the effector pathogen abundance is low or the pathogen is absent. Paradoxically, immune memory can result in pathogens interacting more strongly when temporally out of phase.We find that interactions between species can not only alter pathogen abundance but can also result in changes to the temporal pattern of the affected species. We further demonstrate that this phenomenon may be observed in a natural host / pathogen data set.Given that there is both a continuing debate as to the relevance of pathogen interactions in natural systems and increasing concern regarding treatment of coinfections of veterinary and medical importance, both the discovery of this measurable shift in cycle in the empirical data and the mechanism by which we identified the shift are important. Finally, as the model structure used here is analogous to simple predator-prey system models we also consider the consequences of these findings in the context of that system.

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Competition and mutualism among the gut helminths of a mammalian host

Cited by 274 publications

References 25 publications

Seasonality, cohort-dependence and the development of immunity in a natural host–nematode system

Seasonality, cohort-dependence and the development of immunity in a natural host–nematode system

Epidemiology of parasitic protozoan infections in Soay sheep (Ovis ariesL.) on St Kilda

Pathogen Interactions, Population Cycles, and Phase Shifts

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