The role of competition – colonization tradeoffs and spatial heterogeneity in promoting trematode coexistence

Mordecai, Erin A.; Jaramillo, Alejandra G.; Ashford, Jacob E.; Hechinger, Ryan F.; Lafferty, Kevin D.

doi:10.1890/15-0753.1

Cited by 21 publications

(23 citation statements)

References 66 publications

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“…After experimental setup, we dissected the extra sentinel snails ( n = 129), and found non‐patent infections in 12.4% of snails (consistent with previous results; Mordecai et al. ). Therefore, after experimental initiation, we allowed ~1 month for non‐patent infections to become patent, collected all experimental snails on 18 August, and screened them as before on 21, 25, and 28 August, removing snails that shed.…”

Section: Methodssupporting

confidence: 87%

Host density increases parasite recruitment but decreases host risk in a snail–trematode system

Buck

Hechinger

Wood

et al. 2017

Ecology

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Most species aggregate in local patches. High host density in patches increases contact rate between hosts and parasites, increasing parasite transmission success. At the same time, for environmentally transmitted parasites, high host density can decrease infection risk to individual hosts, because infective stages are divided among all hosts in a patch, leading to safety in numbers. We tested these predictions using the California horn snail, Cerithideopsis californica (=Cerithidea californica), which is the first intermediate host for at least 19 digenean trematode species in California estuaries. Snails become infected by ingesting trematode eggs or through penetration by free-swimming miracidia that hatch from trematode eggs deposited with final-host (bird or mammal) feces. This complex life cycle decouples infective-stage production from transmission, raising the possibility of an inverse relationship between host density and infection risk at local scales. In a field survey, higher snail density was associated with increased trematode (infected snail) density, but decreased trematode prevalence, consistent with either safety in numbers, parasitic castration, or both. To determine the extent to which safety in numbers drove the negative snail-density-trematode-prevalence association, we manipulated uninfected snail density in 83 cages at eight sites within Carpinteria Salt Marsh (California, USA). At each site, we quantified snail density and used data on final-host (bird and raccoon) distributions to control for between-site variation in infective-stage supply. After three months, overall trematode infections per cage increased with snail biomass density. For egg-transmitted trematodes, per-snail infection risk decreased with snail biomass density in the cage and surrounding area, whereas per-snail infection risk did not decrease for miracidium-transmitted trematodes. Furthermore, both trematode recruitment and infection risk increased with infective-stage input, but this was significant only for miracidium-transmitted species. A model parameterized with our experimental results and snail densities from 524 field transects estimated that safety in numbers, when combined with patchy host density, halved per capita infection risk in this snail population. We conclude that, depending on transmission mode, host density can enhance parasite recruitment and reduce per capita infection risk.

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Section: Methodssupporting

confidence: 87%

Host density increases parasite recruitment but decreases host risk in a snail–trematode system

Buck

Hechinger

Wood

et al. 2017

Ecology

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“…This pattern is in line with results obtained by Mordecai et al. () in a similar trematode guild where the incidence of infection is negatively correlated with position in the dominance hierarchy at levels sufficient to promote coexistence of subordinates.…”

Section: Discussionsupporting

confidence: 92%

“…By contrast, subordinate species might invest more in reproduction within the snail (as an adaptive response for those species with a greater chance of being killed by dominants) and have longer‐lived eggs (as an adaptive response to increase arrival and survival; Mordecai et al. ).…”

Section: Introductionmentioning

confidence: 99%

A strong colonizer rules the trematode guild in an intertidal snail host

Alda

Bonel

Cazzaniga

et al. 2019

Ecology

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We examined the extent to which supply‐side, niche, and competition theories and concepts help explain a trematode community in which one species comprises 87% of the trematode individuals, and the remaining 15 species each have <3%. We collected and dissected the common and wide‐ranging snail host Heleobia australis over four seasons from three distinct habitats from the intertidal area of the Bahía Blanca estuary, Argentina. Inside a snail, trematodes interact with each other with outcomes that depend on facilitation, competition, and preemption, suggesting that dominant species should be common. The abundant trematode species, Microphallus simillimus, is a weak competitor, but has life‐history traits and strategies associated with higher colonization ability that could increase its probability of invading the host first, allowing it to preempt the rare species. Rather than segregate by habitat, trematode species aggregated in pans during the summer where dominant trematode species often excluded subordinate ones. Despite losses to competition, and a lack of niche partitioning, M. simillimus ruled this species‐rich trematode guild through strong recruitment and (potentially) preemption. Therefore, extremely skewed species abundance distributions, like this one, can derive from extremely skewed colonization abilities.

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“…Furthermore, biotic factors can strongly influence local species distributions (Jablonski, ), and some studies have shown macroecological signals of such species interactions (Gotelli, Graves, & Rahbek, ). Further research may integrate biotic factors including species interactions such as competition (Mordecai, Jaramillo, Ashford, Hechinger, & Lafferty, ), specialization (Fjeldså & Lovett, ), population and community dynamics (Locey & Lennon, ; Ralston, DeLuca, Feldman, & King, ), distributional shifts (Knowles & Massatti, ) and niche differentiation (Brown et al, ). A key question is whether and how such factors contribute to the origins and maintenance of species endemism in some areas and not in others that share similar environmental characteristics.…”

Section: Discussionmentioning

confidence: 99%

The origins and maintenance of global species endemism

Zuloaga

Currie

Kerr

2018

Global Ecol Biogeogr

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Aim We test macroecological hypotheses (H1: long‐term climate stability; H2: climate seasonality; H3: climate distinctiveness or rarity; and, H4: spatial heterogeneity in contemporary climate, topography or habitat) proposed to explain broad‐scale patterns of total species endemism. Location Continental areas worldwide and zoogeographical realms. Methods Using species distribution maps for mammals and amphibians, we calculated five metrics of species endemism, based on inverse and median range size, and range size cut‐offs. We performed multi‐model averaging. We tested the accuracy of fitted models using cross‐validation, comparing observed versus predicted values of endemism among zoogeographical realms. Results Model averaging showed that species endemism for amphibians and mammals was statistically related to all set of predictors (H1, H2, H4 and richness), except for climate distinctiveness (H3). Effect sizes for spatial heterogeneity were larger and more consistent among zoogeographical realms than the effect sizes of climate stability. The effect of species richness on species endemism varies widely and depends on the metric of endemism and taxonomic group used in the analysis. Cross‐validation across all zoogeographical realms showed that predictions of endemism systematically fail for both taxa. In most cases, low to moderate endemism is predicted reasonably well. However, areas with high numbers of endemic species are systematically under‐predicted. Main conclusions Our results are not consistent with any of the processes hypothesized to create and maintain global patterns of endemism. Although we found statistically significant relationships, they failed the stronger test of a causal relationship: accurate prediction in independent data. The inconsistent effect of richness in our models suggests that patterns of endemism are not driven by the same variables as total richness. Patterns of endemism have no consistent relationships with climatic stability among zoogeographical realms, so suggestions that endemism reflect climatic stability are likely due to collinearity with other factors, especially spatial heterogeneity.

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The role of competition – colonization tradeoffs and spatial heterogeneity in promoting trematode coexistence

Cited by 21 publications

References 66 publications

Host density increases parasite recruitment but decreases host risk in a snail–trematode system

Host density increases parasite recruitment but decreases host risk in a snail–trematode system

A strong colonizer rules the trematode guild in an intertidal snail host

The origins and maintenance of global species endemism

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