Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts

Sato, Tadanobu; Egusa, Tomohiro; Fukushima, Keitaro; Oda, Takayuki; Ohte, Nobuhito; Tokuchi, Naoko; Watanabe, Katsutoshi; Kanaiwa, Minoru; Murakami, Isaya; Lafferty, Kevin D.

doi:10.1111/j.1461-0248.2012.01798.x

Cited by 121 publications

(103 citation statements)

References 54 publications

(116 reference statements)

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“…Phenotypic alterations brought about by parasites in their hosts can have several consequences for ecosystems, e.g. by releasing the prey community from predation pressure (Sato et al, 2012) or by affecting the availability of trophic resources to plant and animal communities (Hernandez and Sukhdeo, 2008;Boze et al, 2012). However, although the influence of PIPAs on ecosystem functioning is widely acknowledged (Thomas et al, 1997;Hatcher et al, 2012), we do not know to what extent the ecological impact of a parasite is related to the number of phenotypic alterations it brings about in its host.…”

Section: Introductionmentioning

confidence: 88%

Multidimensionality in parasite-induced phenotypic alterations: ultimateversusproximate aspects

Cézilly

Favrat

Perrot‐Minnot

2013

Journal of Experimental Biology

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SummaryIn most cases, parasites alter more than one dimension in their host phenotype. Although multidimensionality in parasite-induced phenotypic alterations (PIPAs) seems to be the rule, it has started to be addressed only recently. Here, we critically review some of the problems associated with the definition, quantification and interpretation of multidimensionality in PIPAs. In particular, we confront ultimate and proximate accounts, and evaluate their own limitations. We end up by introducing several suggestions for the development of future research, including some practical guidelines for the quantitative analysis of multidimensionality in PIPAs.

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Section: Introductionmentioning

confidence: 88%

Multidimensionality in parasite-induced phenotypic alterations: ultimateversusproximate aspects

Cézilly

Favrat

Perrot‐Minnot

2013

Journal of Experimental Biology

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“…While most previous work on this system and for aquatic parasites generally has involved laboratory, mesocosm or cage studies (Kiesecker 2002, Schotthoefer et al 2003, ecosystem-scale experiments play an important role in ecology by testing the validity of findings reported from more artificial settings or correlative studies (Tilman 1989, Carpenter et al 1995, 2011, Schindler 1998, Vredenburg 2004, Sato et al 2012. By using a BACI design in an experimentally divided lake, we found that the addition of ;500 Ribeiroia infected snails, which represented a small fraction of the overall snail biomass but a significant increase in parasite cercarial release, resulted in a seven-fold increase in observed infection abundance among larval and metamorphic P. regilla.…”

Section: Discussionmentioning

confidence: 99%

“…The experiment at Hog Lake, which represents one of the few studies to manipulate aquatic parasites at an ecosystem scale (see also Nassi et al 1979, Sato et al 2012, showed that large-scale manipulations of trematode populations are feasible. The study also demonstrated that the relationship between Ribeiroia infection and host pathology varied in strength as a function of study venue (field surveys, lab experiments, and field enclosure cages).…”

Section: Discussionmentioning

confidence: 99%

Using an ecosystem‐level manipulation to understand host‐parasite interactions and how they vary with study venue

2012

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Abstract. We investigated interactions between the virulent trematode Ribeiroia ondatrae, which has been linked to amphibian malformations across the United States, and its amphibian host (Pseudacris regilla) using a hierarchical approach involving multi-year regional field surveys, replicated pond enclosures, and an unreplicated ecosystem manipulation of parasite infection. Results of this multi-tiered approach provide strong evidence of the causal linkage between infection and malformations while offering additional insights about the influence of experimental venue on effect size. Among years and across 18 wetlands in northern California, Ribeiroia infection was a strong predictor of malformation frequency, which ranged from 0 to 77% at all sites (n ¼ 6,511). Correspondingly, the addition of .500 Ribeiroia infected snails to an experimentally divided wetland using a three-year Before After Control Impact (BACI) design caused sharp increases in Ribeiroia infection and severe malformations in P. regilla during the manipulation year (but not pre-or post-manipulation). These results were complemented by the findings from a replicated (n ¼ 16) enclosure/exclosure study conducted on both sides of the divided wetland (Hog Lake), which showed increased infection and malformations only among larvae within cages that allowed parasite entry and only on the manipulated side. No differences in mortality were observed among animals as a function of cage type. A comparison of the slope between observed infection and malformations as a function of venue (previous laboratory work and the two spatial scales of this study (cages and whole-pond)) indicated that small-scale experiments exhibit stronger effects relative to results from larger spatial extents. Multi-year sampling also indicated that malformed frogs were unlikely to return as breeding adults, highlighting the potential for population-level impacts associated with high Ribeiroia infections. Taken together, these results provide support for the causal relationship between Ribeiroia infection and amphibian malformations under realistic conditions while simultaneously emphasizing the influence of study venue on the strength of this relationship.

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“…Ecosystem-level effects of invasive predators may extend beyond the habitat where they reside if native prey moves between ecosystems (Baxter et al 2004, Epanchin et al 2010, Sato et al 2012. Affected ecosystems may extend beyond areas adjacent to invaded ecosystems and be hundreds of kilometers away depending on the behavior of the animals that connect them (Reiners and Driese 2004), such as salmon (Holtgrieve and Schindler 2011).…”

Section: Introductionmentioning

confidence: 99%

Introduced lake trout alter nitrogen cycling beyond Yellowstone Lake

2015

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Citation: Tronstad, L. M., R. O. Hall Jr., and T. M. Koel. 2015. Introduced lake trout alter nitrogen cycling beyond Yellowstone Lake. Ecosphere 6(11):224. http://dx.doi.org/10.1890/ES14-00544.1Abstract. Introduced predators can have large effects on the ecosystem in which they were introduced, but how much these effects extend to other ecosystems beyond the invaded one is less known. We compared how lake trout (Salvelinus namaycush) affected nutrient cycling in an invaded and adjacent ecosystem in Yellowstone National Park, Wyoming, USA. Introduced lake trout in Yellowstone Lake caused the native Yellowstone cutthroat trout (Oncoryhynchus clarkii bouvieri ) population to decline. Native cutthroat trout are a dominant animal in the lake and may alter nutrient cycling in both Yellowstone Lake where they reside and in tributary streams used for spawning. We estimated changes in nutrient transport and nutrient uptake in both Yellowstone Lake and Clear Creek, a spawning stream, before and after the invasion of lake trout. Annual area-specific excretion fluxes from cutthroat trout were nine times higher in Clear Creek compared to Yellowstone Lake when cutthroat trout were abundant. However, fluxes within the lake and stream were similar after cutthroat trout declined. In Yellowstone Lake, zooplankton excretion supplied 86% of ammonium (NH 4 þ ) that was taken up, but cutthroat trout only supplied ,0.3% after the introduction of lake trout. Conversely, NH 4 þ excreted by cutthroat trout was likely a major flux in ClearCreek, because NH 4 þ fluxes from cutthroat trout exceeded watershed export of NH 4 þ in years when .3000 cutthroat trout spawned. Furthermore, NH 4 þ excretion fluxes from spawning cutthroat trout in ClearCreek supplied up to 6.1% of the NH 4 þ demanded by microbes after the introduction of lake trout.However, based on modeled past NH 4 þ uptake, we estimated that up to 60% of NH 4 þ excreted by spawning cutthroat trout may have been taken up by stream microbes when cutthroat trout were abundant. Therefore, transported NH 4 þ from spawning cutthroat trout was likely an integral part of N cycling in tributary streams in the past. By comparing the effects of declining cutthroat trout on two ecosystems, we show that lake trout had a larger effect on N cycling within an adjacent stream ecosystem than the invaded lake ecosystem itself, because the migratory behavior of cutthroat trout concentrated them in spawning streams increasing their effect.

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Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts

Cited by 121 publications

References 54 publications

Multidimensionality in parasite-induced phenotypic alterations: ultimateversusproximate aspects

Multidimensionality in parasite-induced phenotypic alterations: ultimateversusproximate aspects

Using an ecosystem‐level manipulation to understand host‐parasite interactions and how they vary with study venue

Introduced lake trout alter nitrogen cycling beyond Yellowstone Lake

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