Broadening the ecology of fear: non-lethal effects arise from diverse responses to predation and parasitism.

Research on the 'ecology of fear' posits that defensive prey responses to avoid predation can cause non-lethal effects across ecological scales. Parasites also elicit defensive responses in hosts with associated non-lethal effects, which raises the longstanding, yet unresolved question of how non-lethal effects of parasites compare with those of predators. We developed a framework for systematically answering this question for all types of predator-prey and host-parasite systems. Our framework reveals likely differences in non-lethal effects not only between predators and parasites, but also between different types of predators and parasites. Trait responses should be strongest towards predators, parasitoids and parasitic castrators, but more numerous and perhaps more frequent for parasites than for predators. In a case study of larval amphibians, whose trait responses to both predators and parasites have been relatively well studied, existing data indicate that individuals generally respond more strongly and proactively to short-term predation risks than to parasitism. Apart from studies using amphibians, there have been few direct comparisons of responses to predation and parasitism, and none have incorporated responses to micropredators, parasitoids or parasitic castrators, or examined their long-term consequences. Addressing these and other data gaps highlighted by our framework can advance the field towards understanding how non-lethal effects impact prey/host population dynamics and shape food webs that contain multiple predator and parasite species.

Euhaplorchis californiensis Cercariae Exhibit Positive Phototaxis and Negative Geotaxis.

Parasites often use external cues to identify and move toward environments where they are likely to encounter suitable hosts. The trematode parasite Euhaplorchis californiensis produces cercariae that emerge from California horn snails ( Cerithideopsis californica [= Cerithidea californica]) to infect California killifish ( Fundulus parvipinnis) as second intermediate hosts. Based upon work on a congeneric Euhaplorchis species from Florida, and based on the ecology of its killifish host, we hypothesized that E. californiensis cercariae in southern California estuaries are positively phototactic and negatively geotactic, using both sunlight and gravity to guide their movement to the upper water column. To distinguish positive phototaxis from negative geotaxis, we first quantified E. californiensis movement in response to light along a horizontal plane and determined they were positively phototactic. In a second experiment, we quantified E. californiensis movement along a vertical plane in response to an overhead light, a light from below, or no light. We found that E. californiensis exhibit negative geotaxis in the absence of light, but will swim in the direction of gravity to move toward a light source from below. Thus, E. californiensis are both positively phototactic and negatively geotactic, but cercariae prioritize phototactic cues. These results suggest that E. californiensis cercariae aggregate in the open water, indicating that the pelagic zone represents an area of high infection risk for California killifish hosts.

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

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.

No One Saw This Coming: Endoparasitic Mites Behind the Eyes of a Double-Crested Cormorant.

We found hundreds of mites behind the eyes of a Double-crested Cormorant, Phalacrocorax auritus (Suliformes: Phalacrocoracidae). The mites were Neottialges evansi (Acari: Hypoderatidae), representing the first report of this parasite in P. auritus from western North America. Deutonymphs of N. evansi are endoparasites, typically reported infecting fat deposits over the pectoral muscles, axillary areas, and vent of cormorants. Here mites infected only orbital tissues, a new infection site for hypoderatid mites. We suggest a lack of reports of this infection site could be explained by limited scrutiny of orbits, and deutonymphs mites infecting orbits may be more common than expected.

Digenean metacercariae of fishes from the lagoon flats of Palmyra Atoll, Eastern Indo-Pacific.

Although many studies on the taxonomy of digenean trematodes of marine fishes have been completed in the Eastern Indo-Pacific (EIP) marine ecoregion, only a few have considered metacercarial stages. Here, the results are presented of a taxonomic survey of the digenean metacercariae of fishes from Palmyra Atoll, a remote and relatively pristine US National Wildlife Refuge located 1680 km SSW of Hawaii. Up to 425 individual fish were collected, comprising 42 fish species, from the sand flats bordering the lagoon of the atoll. Quantitative parasitological examinations of each fish were performed. Morphological descriptions of the encountered digenean metacercariae are provided, together with their prevalence, mean intensities, host and tissue-use. Up to 33,964 individuals were recovered representing 19 digenean metacercaria species from eight families. The species composition of digeneans in lagoon fishes at Palmyra Atoll is a subset of what has previously been reported for the EIP. Further, the large diversity and abundance of metacercariae reported in this study highlight the utility of including this group in future ecological research in the EIP marine ecoregion.

Ecology of the brain trematode Euhaplorchis californiensis and its host, the California killifish ( Fundulus parvipinnis ).

We describe the distribution and abundance of the brain-encysting trematode Euhaplorchis californiensis and its second intermediate host, the California killifish (Fundulus parvipinnis), in 3 estuaries in southern California and Baja California. We quantified the density of fish and metacercariae at 13-14 sites per estuary and dissected 375 killifish. Density (numbers and biomass) was examined at 3 spatial scales, i.e., small replicate sites, habitats, and entire estuaries. At those same scales, factors that might influence metacercaria prevalence, abundance, and aggregation in host individuals and populations were also examined. Metacercaria prevalence was 94-100% among the estuaries. Most fish were infected with 100s to 1,000s of E. californiensis metacercariae, with mean abundance generally increasing with host size. Although body condition of fish did not vary among sites or estuaries, the abundance of metacercariae varied significantly among sites, habitats, estuaries, and substantially with host size and gender. Metacercariae were modestly aggregated in killifish (k > 1), with aggregation decreasing in larger hosts. Across the 3 estuaries, the total populations of killifish ranged from 9,000-12,000 individuals/ha and from 7-43 kg/ha. The component populations of E. californiensis metacercariae ranged from 78-200 million individuals/ha and from 0.1-0.3 kg/ha. Biomass of E. californiensis metacercariae constituted 0.5-1.7% of the killifish biomass in the estuaries. Our findings, in conjunction with previously documented effects of E. californiensis, suggest a strong influence of this parasite on the size, distribution, biomass, and abundance of its killifish host.

Trematodes associated with mangrove habitat in Puerto Rican salt marshes.

Batillaria minima is a common snail in the coastal estuaries of Puerto Rico. This snail is host to a variety of trematodes, the most common being Cercaria caribbea XXXI, a microphallid species that uses crabs as second intermediate hosts. The prevalence of infection was higher (7.1%) near mangroves than on mudflats away from mangroves (1.4%). Similarly, there was a significant positive association between the proportion of a site covered with mangroves and the prevalence of the microphallid. The association between mangroves and higher trematode prevalence is most likely because birds use mangroves as perch sites and this results in local transmission to snails.