Modification of Hosts' Behavior by a Parasite: Field Evidence for Adaptive Manipulation

Abstract

Parasites relying on trophic transmission to complete their life cycles often induce modifications of their host's behavior in ways that may increase their susceptibility to predation by final hosts. These modifications have often been interpreted as parasite adaptations, but very few studies have demonstrated that host manipulation has fitness benefits for the parasite. The aim of the present study was to address the adaptive significance of parasite manipulation by coupling observations of behavioral manipulation to estimates of trophic transmission to the definitive host in the natural environment. We show that the acanthocephalan parasite Pomphorhynchus laevis manipulates the drifting behavior of one of its intermediate hosts, the amphipod Gammarus pulex, but not of a sympatric host, the introduced amphipod Gammarus roeseli. We found a 26.3-28.3 times higher proportion of infected G. pulex in the stomach content of one of the definitive hosts of P. laevis, the bullhead Cottus gobio, than in the benthos. No such trend was observed for G. roeseli. The bell-shaped curve of mean parasite abundance (MPA) relative to host size observed in G. pulex also supported an increased predation mortality of P. laevis-infected individuals compared to uninfected amphipods. Again, no such pattern was observed in G. roeseli. Furthermore, our results indicate that the modifications induced by P. laevis are specific to the definitive host and do not increase the risk of predation by inappropriate hosts, here the adult edible frog Rana esculenta. Overall, our study is original in that it establishes, under field conditions, a direct link between parasitic manipulation and increased transmission to the definitive host, and more importantly, identifies the specificity of the manipulation both in the intermediate host species and toward the definitive host.

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

“…Making the host more suitable for competing parasites, attracting non-vectors to an infested plant that outcompete the vector, or increasing predation rates in the absence of the predator who serves as the definitive host, are all scenarios can select against the evolution of a manipulation effect. In this context, a particularly elegant approach used naturally co-existing and taxonomically related species of intermediate hosts, among which only one host can reasonably be assumed to have co-evolved with the parasite: increased transmission rates after host phenotypic alterations were observed for the native, but not the invasive intermediate host of a native parasite, an observation that represents a strong argument in favor of an adaptive manipulation (Lagrue et al, 2007). In general, a promising strategy to identify manipulators as well as the underlying mechanisms would compare the interactions of parasites that have undergone a recent host shift to the interactions among their ancestors and the original host.…”

Acanthocephalan parasites: help or burden in gammarid amphipods exposed to cadmium?

“…Among the numerous complex life cycle parasites, acanthocephalans are known to alter the phenotype of their intermediate hosts in a way that make it more prone to predation and thus, favour its transmission to the final vertebrate host (Kennedy 2006;Lagrue et al 2007). If behavioural changes induced by the parasite have been intensively studied (Cézilly et al 2000;Bauer et al 2005;Médoc et al 2006), the modifications of host antitoxic responses has become a topic of interest in a context of rising pollution in freshwater ecosystems.…”

Serum Biochemistry, Serology, and Parasitology of Boreal Caribou (Rangifer Tarandus Caribou ) in the Northwest Territories, Canada

“…Industrial development and large-scale anthropogenic disturbances in boreal caribou habitat have been implicated in range and population declines via increased hunting, habitat fragmentation and loss, and linear barriers to movement such as roads (Weclaw and Hudson, 2004;Vors et al, 2007). Viral, bacterial, and parasitic diseases can also affect the boreal caribou population by increasing susceptibility to predation, hunting, and accidents, as well as by causing direct mortality (Lagrue et al, 2007;Miller et al, 2008). Little is known about the prevalence of disease agents in boreal caribou, although there is considerable concern regarding the possible introduction and effect of diseases, such as chronic wasting disease, and parasites, including Parelaphostrongylus tenuis.…”