Using Larval Trematodes That Parasitize Snails to Evaluate a Saltmarsh Restoration Project

Huspeni, Todd C.; Lafferty, Kevin D.

doi:10.1890/01-5346

Cited by 135 publications

(128 citation statements)

References 44 publications

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“…There could be general ecological scenarios in which positive diversity-disease relationships might arise. For example, during succession or restoration, host species must establish in a community before their parasites can invade (26). More broadly, theoretical models suggest that the effect of biodiversity on disease depends on the traits of hosts, parasites, and additional species (27,28).…”

Section: Resultsmentioning

confidence: 99%

Biodiversity inhibits parasites: Broad evidence for the dilution effect

Civitello

Cohen

Fatima

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

587

542

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Infectious diseases of humans, wildlife, and domesticated species are increasing worldwide, driving the need to understand the mechanisms that shape outbreaks. Simultaneously, human activities are drastically reducing biodiversity. These concurrent patterns have prompted repeated suggestions that biodiversity and disease are linked. For example, the dilution effect hypothesis posits that these patterns are causally related; diverse host communities inhibit the spread of parasites via several mechanisms, such as by regulating populations of susceptible hosts or interfering with parasite transmission. However, the generality of the dilution effect hypothesis remains controversial, especially for zoonotic diseases of humans. Here we provide broad evidence that host diversity inhibits parasite abundance using a metaanalysis of 202 effect sizes on 61 parasite species. The magnitude of these effects was independent of host density, study design, and type and specialization of parasites, indicating that dilution was robust across all ecological contexts examined. However, the magnitude of dilution was more closely related to the frequency, rather than density, of focal host species. Importantly, observational studies overwhelmingly documented dilution effects, and there was also significant evidence for dilution effects of zoonotic parasites of humans. Thus, dilution effects occur commonly in nature, and they may modulate human disease risk. A second analysis identified similar effects of diversity in plant-herbivore systems. Thus, although there can be exceptions, our results indicate that biodiversity generally decreases parasitism and herbivory. Consequently, anthropogenic declines in biodiversity could increase human and wildlife diseases and decrease crop and forest production.H uman activities are dramatically reducing biodiversity (1), and the frequency and severity of infectious disease outbreaks in human, wildlife, and domesticated species are increasing (2-5). These concurrent patterns have prompted suggestions that biodiversity and the spread of diseases may be causally linked. For example, the dilution effect hypothesis proposes that diverse host communities inhibit the abundance of parasites through several mechanisms, such as regulating populations of susceptible hosts or interfering with the transmission process (6-8). Thus, diverse communities may inhibit the proliferation of parasites, thereby promoting the stability of ecological communities and ecosystem services (e.g., nutrient cycling, carbon sequestration, and natural product production) (9).Understanding the generality of these dilution effects is crucial for projections of future disease outbreaks, which can threaten human health, species conservation, and ecosystem services (3, 9). If biodiversity generally inhibits parasites, then human-driven biodiversity loss could exacerbate disease risk for humans and wildlife. Biodiversity conservation might then limit the abundance of many parasites of wildlife and humans (10-12). However, if parasites a...

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Section: Resultsmentioning

confidence: 99%

Biodiversity inhibits parasites: Broad evidence for the dilution effect

Civitello

Cohen

Fatima

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

587

542

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“…For this reason, parasites may be excellent indicators of food web structure (3,10,(37)(38)(39). A strong relationship exists between the diversity of bird species that serve as final hosts and trematode diversity (as measured in snails) among sites within the Carpinteria Salt Marsh food web (40).…”

Section: Discussionmentioning

confidence: 99%

Parasites dominate food web links

Lafferty

Dobson

Kuris³

2006

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

712

627

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Parasitism is the most common animal lifestyle, yet food webs rarely include parasites. The few earlier studies have indicated that including parasites leads to obvious increases in species richness, number of links, and food chain length. A less obvious result was that adding parasites slightly reduced connectance, a key metric considered to affect food web stability. However, reported reductions in connectance after the addition of parasites resulted from an inappropriate calculation. Two alternative corrective approaches applied to four published studies yield an opposite result: parasites increase connectance, sometimes dramatically. In addition, we find that parasites can greatly affect other food web statistics, such as nestedness (asymmetry of interactions), chain length, and linkage density. Furthermore, whereas most food webs find that top trophic levels are least vulnerable to natural enemies, the inclusion of parasites revealed that mid-trophic levels, not low trophic levels, suffered the highest vulnerability to natural enemies. These results show that food webs are very incomplete without parasites. Most notably, recognition of parasite links may have important consequences for ecosystem stability because they can increase connectance and nestedness.connectance ͉ parasitism ͉ trophic ͉ predation ͉ trematode F ood webs trace the flow of energy through an ecosystem. In revealing how consumer-resource interactions lead to trophic cascades, apparent competition, and diversity-stability relationships, food webs provide a unifying theme for ecology (1). Ironically, the most common consumer strategy, parasitism (2), is usually left out of food webs because parasites are often more difficult to quantify by standard ecological methods (3). To fit the resulting parasite-free food webs, prominent theoretical concepts, such as the cascade (4) and niche (5) models, generally assume that consumers eat species smaller than themselves, suggesting that new theoretical models may be needed to accommodate parasites, which eat species larger than themselves. Before taking this step, however, it is expedient to consider how, if at all, parasites affect food webs.Insect parasitoids are the only type of parasite commonly included in food webs. This is because parasitoids are large relative to host size, are easy to sample, and can affect insect population dynamics. However, insights gained from adding parasitoids to food webs may not extend to other infectious agents that have very different life histories (6). In comparison with highly host-specific parasitoids, individual life stages of typical parasites (an adult tapeworm in a dog's gut) can have a broad host range (7). Furthermore, many typical parasites have complex multiple-host life cycles that are embedded in food webs (3). Calls for considering typical parasites in food webs (3,(8)(9)(10) have gained few responses. The initial efforts have shown little effect of including parasites in food webs beyond obvious increases in species richness, number of links, trophi...

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“…HELMINTHOLOGIA, 51, 4: 301 -308, 2014 Microhabitat differences surrounding a pond affects the distribution of trematode parasites among a pulmonate snail community (Esch & Fernandez, 1994;Sapp & Esch, 1994;Detwiler & Minchella, 2009). Changing microhabitat may not only affect the distribution of aquatic snails, but may also indirectly affect the encounter rate of the gastropods with the definitive hosts (Huspeni & Lafferty, 2004;Lafferty & Kuris, 2005;Urban, 2006;Hechinger et al, 2007;Marcogliese & Pietrock, 2011). Consequently, the frequency of snails encountering eggs or miracidia of trematode parasites that infect them may be altered.…”

Section: Introductionmentioning

confidence: 99%

“…Microhabitat differences relating to the surrounding vegetation, particularly open versus wooded habitat, were suspected to impact the trematode infection patterns in the snail community. In particular, the habitat preference of the definitive hosts can have an impact on trematode infection in the snail population (Smith, 2001;Huspeni et al, 2004;Hechinger & Lafferty, 2005;Urban, 2006). Differences in the microhabitat preferences of autogenic host species, e.g., Rana spp.…”

Section: Introductionmentioning

confidence: 99%

Microhabitat differences surrounding a pond affects the distribution of trematode parasites among a pulmonate snail community

Zimmermann¹,

Luth

Esch

2014

Helminthologia

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Anthropogenic disturbance associated with clear-cutting and changing the environmental landscape can lead to distinct microhabitat structure surrounding aquatic habitats. The transmission dynamics of trematode parasites in their snail first intermediate hosts were examined to determine if these alterations affect trematode parasite distribution. This was accomplished by examining 2,771 pulmonate snails belonging to two species (Physa gyrina and Lymnaea columella) over a three month period in a pond surrounded by distinct microhabitats as a result of anthropogenic changes to the environmental landscape. Trematode parasite distribution in the snail first intermediate hosts was largely tied to the microhabitat preference of their vertebrate definitive hosts. Autogenic species were found further away from the center of the open microhabitat and allogenic parasites were closer to the centralized point, most likely as a result of habitat preference by their frog and waterfowl definitive hosts, respectively. Additionally, there was increased parasitism in the molluscan hosts at the edges of the wooded environments due to habitat overlap of autogenic and allogenic species hosts, indicating that microhabitat structure can have profound effects on parasite distribution.

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Using Larval Trematodes That Parasitize Snails to Evaluate a Saltmarsh Restoration Project

Cited by 135 publications

References 44 publications

Biodiversity inhibits parasites: Broad evidence for the dilution effect

Biodiversity inhibits parasites: Broad evidence for the dilution effect

Parasites dominate food web links

Microhabitat differences surrounding a pond affects the distribution of trematode parasites among a pulmonate snail community

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