Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions .... or pure randomness?

Abstract

SUMMARYExperimental data establish that interactions exist between species of intestinal helminths during concurrent infections in rodents, the strongest effects being mediated through the host's immune responses. Detecting immune-mediated relationships in wild rodent populations has been fraught with problems and published data do not support a major role for interactions in structuring helminth communities. Helminths in wild rodents show predictable patterns of seasonal, host age-dependent and spatial variation in species richness and in abundance of core species. When these are controlled for, patterns of co-infection compatible with synergistic interactions can be demonstrated. At least one of these, the positive relationship betweenHeligmosomoides polygyrusand species richness of other helminths has been demonstrated in three totally independent data-sets. Collectively, they explain only a small percentage of the variance/deviance in abundance data and at this level are unlikely to play a major role in structuring helminth communities, although they may be important in the more heavily infected wood mice. Current worm burdens underestimate the possibility that earlier interactions through the immune system have taken place, and therefore interactions may have a greater role to play than is immediately evident from current worm burdens. Longitudinal studies are proposed to resolve this issue.

Pathogen Diversity and Hidden Regimes of Apparent Competition

“…A system containing more competing species will generally suffer from smaller sample sizes (the number of hosts carrying each kind of parasite), hindering quantitative inference. This may partly explain why studies reporting correlations have involved fewer species (Behnke 2008; Lello et al 2004). Pathogen association studies in general can be limited by the presence of hidden confounding factors, such as shared risks for pathogen acquisition, and spurious associations generated by the system’s nonlinear dynamics (Behnke et al 2005; Fenton et al 2010; Karvonen et al 2009; Lello et al 2008).…”

“…Detecting this tradeoff only from correlations in natural carriage might be extremely difficult and potentially misleading (Fenton et al 2010; Holt 1984; Holt and Lawton 1993). Experiments in animal models, longitudinal coinfection studies augmented by immunological data, and interventions such as vaccines that target specific pathogens or strains could help to identify and, critically, quantify the strengths of direct and indirect effects (Behnke 2008; Bradley and Jackson 2008; Telfer et al 2010). …”

Helminth species richness in wild wood mice,Apodemus sylvaticus, is enhanced by the presence of the intestinal nematodeHeligmosomoides polygyrus

“…In some hosts, notably birds that harbour species-rich helminth communities, the evidence is indisputable, but in others such as fish and wild rodents characterized by relatively depauperate helminth communities, evidence in support of a role for interactions in structuring communities has been elusive (reviewed Behnke et al 2001). This contrasts markedly with laboratory studies where interactions between helminths have been clearly demonstrated and mostly assigned to interactions mediated through the immune response of the host (Behnke et al 2001 ;Behnke, 2008). The search for evidence of interactions among wild-caught hosts, has been hampered by a number of difficulties ; for example, the statistical analyses required to dissect out the evidence for interactions is complex (Haukisalmi and Henttonen, 1998 ;Howard et al 2001 ;Bottomley et al 2005), and there is a lack of support for any specific interaction between particular parasites being a consistent enough feature wherever both species of parasites co-occur with the host.…”

Variation in the helminth community structure ofThrichomys pachyurus(Rodentia: Echimyidae) in two sub-regions of the Brazilian Pantanal: the effects of land use and seasonality

“…Moreover, climatic factors are known to influence the development of free-living stages of parasites and can affect survival, transmission and host infection (Haukisalmi & Henttonen, 1990;Behnke, 2008).…”