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.

Models with environmental drivers offer a plausible mechanism for the rapid spread of infectious disease outbreaks in marine organisms.

The first signs of sea star wasting disease (SSWD) epidemic occurred in just few months in 2013 along the entire North American Pacific coast. Disease dynamics did not manifest as the typical travelling wave of reaction-diffusion epidemiological model, suggesting that other environmental factors might have played some role. To help explore how external factors might trigger disease, we built a coupled oceanographic-epidemiological model and contrasted three hypotheses on the influence of temperature on disease transmission and pathogenicity. Models that linked mortality to sea surface temperature gave patterns more consistent with observed data on sea star wasting disease, which suggests that environmental stress could explain why some marine diseases seem to spread so fast and have region-wide impacts on host populations.

Facultative Parasitism by the Bivalve Kurtiella pedroana in the Mole Crab Emerita analoga.

Evolutionary transitions to parasitism are rare. In this study, we documented a potential step toward parasitism in the commensal clam Kurtiella pedroana (Bivalvia: Galeommatoidea). Galeommatoideans are known commensals of various invertebrates, including crustaceans. Emerita analoga (Decapoda: Hippidae) is an abundant intertidal mole crab inhabiting Pacific coast beaches in North and South America. Mole crabs collected from Monterey Bay, California, were measured and examined externally and internally for associated molluscs. Out of the 520 mole crabs, 37 large female individuals harbored 49 clams (prevalence of 7.11% and mean intensity of 1.3). Forty-one ectocommensal clams were attached by their byssal threads to the inside of the gill chambers or to the lateroventral surfaces. However, our key finding was 8 clams that lacked byssal threads and were living in the hemocoel of 6 crabs. These internal clams were smaller than the ectocommensals. Because these internal clams lacked access to their normal food, we hypothesize they might have fed on hemolymph as would a parasite. Clam larvae have no obvious exit from the hemocoel, implying that endoparasitism is a dead-end for K. pedroana. Regardless, facultative parasitism in a free-living or an ectocommensal is uncommon and suggests a pathway to parasitism.

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.

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.

Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects.

Decadal-scale observations of marine reserves suggest that indirect effects on taxa that occur through cascading trophic interactions take longer to develop than direct effects on target species. Combining and analyzing a unique set of long-term time series of ecologic data in and out of fisheries closures from disparate regions, we found that the time to initial detection of direct effects on target species (±SE) was 5.13 ± 1.9 years, whereas initial detection of indirect effects on other taxa, which were often trait mediated, took significantly longer (13.1 ± 2.0 years). Most target species showed initial direct effects, but their trajectories over time were highly variable. Many target species continued to increase, some leveled off, and others decreased. Decreases were due to natural fluctuations, fishing impacts from outside reserves, or indirect effects from target species at higher trophic levels. The average duration of stable periods for direct effects was 6.2 ± 1.2 years, even in studies of more than 15 years. For indirect effects, stable periods averaged 9.1 ± 1.6 years, although this was not significantly different from direct effects. Populations of directly targeted species were more stable in reserves than in fished areas, suggesting increased ecologic resilience. This is an important benefit of marine reserves with respect to their function as a tool for conservation and restoration.

Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis.

California killifish (Fundulus parvipinnis) infected with the brain-encysting trematode Euhaplorchis californiensis display conspicuous swimming behaviours rendering them more susceptible to predation by avian final hosts. Heavily infected killifish grow and reproduce normally, despite having thousands of cysts inside their braincases. This suggests that E. californiensis affects only specific locomotory behaviours. We hypothesised that changes in the serotonin and dopamine metabolism, essential for controlling locomotion and arousal may underlie this behaviour modification. We employed micropunch dissection and HPLC to analyse monoamine and monoamine metabolite concentrations in the brain regions of uninfected and experimentally infected fish. The parasites exerted density-dependent changes in monoaminergic activity distinct from those exhibited by fish subjected to stress. Specifically, E. californiensis inhibited a normally occurring, stress-induced elevation of serotonergic metabolism in the raphae nuclei. This effect was particularly evident in the experimentally infected fish, whose low-density infections were concentrated on the brainstem. Furthermore, high E. californiensis density was associated with increased dopaminergic activity in the hypothalamus and decreased serotonergic activity in the hippocampus. In conclusion, the altered monoaminergic metabolism may explain behavioural differences leading to increased predation of the infected killifish by their final host predators.

Small estuarine fishes feed on large trematode cercariae: lab and field investigations.

In aquatic ecosystems, dense populations of snails can shed millions of digenean trematode cercariae every day. These short-lived, free-living larvae are rich in energy and present a potential resource for consumers. We investigated whether estuarine fishes eat cercariae shed by trematodes of the estuarine snail Cerithidea californica. In aquaria we presented cercariae from 10 native trematode species to 6 species of native estuarine fishes. Many of these fishes readily engorged on cercariae. To determine if fishes ate cercariae in the field, we collected the most common fish species, Fundulus parvipinnis (California killifish), from shallow water on rising tides when snails shed cercariae. Of 61 killifish, 3 had recognizable cercariae in their gut. Because cercariae are common in this estuary, they could be frequent sources of energy for small fishes. In turn, predation on cercariae by fishes (and other predators) could also reduce the transmission success of trematodes.

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.

Trematodes in snails near raccoon latrines suggest a final host role for this mammal in California salt marshes.

Of the 18 trematode species that use the horn snail, Cerithidea californica, as a first intermediate host, 6 have the potential to use raccoons as a final host. The presence of raccoon latrines in Carpinteria Salt Marsh, California, allowed us to investigate associations between raccoons and trematodes in snails. Two trematode species, Probolocoryphe uca and Stictodora hancocki, occurred at higher prevalences in snails near raccoon latrines than in snails away from latrines, suggesting that raccoons may serve as final hosts for these species. Fecal remains indicated that raccoons fed on shore crabs, the second intermediate host for P. uca, and fish, the second intermediate host for S. hancocki. The increase in raccoon populations in the suburban areas surrounding west coast salt marshes could increase their importance as final hosts for trematodes in this system.

Parasites in the thoracic ganglion of Pachygrapsus marmoratus (Brachyura: Grapsidae) from the coast of Portugal.

We examined 149 marbled shore crabs, Pachygrapsus marmoratus, from the coast of Portugal for parasites. In particular, we focused our effort on the crab thoracic ganglion. The thoracic ganglion is the largest concentration of nervous tissue in a crab and thus, parasites associated with this organ are well situated to influence host behavior. We found metacercariae of two microphallid trematode species in the thoracic ganglion. We also found a microsporan and an apicomplexan associated with the thoracic ganglion. Other parasites not associated with the thoracic ganglion included gregarine trophozoites which were present in the digestive diverticulae in some of the crabs and the entoniscid isopod, Grapsion cavolini. Metacercariae of one of the trematodes (probably Microphallus pachygrapsi (Deblock and Prevot)), may influence the mortality of its host.

Parasites and marine invasions.

Introduced marine species are a major environmental and economic problem. The rate of these biological invasions has substantially increased in recent years due to the globalization of the world's economies. The damage caused by invasive species is often a result of the higher densities and larger sizes they attain compared to where they are native. A prominent hypothesis explaining the success of introduced species is that they are relatively free of the effects of natural enemies. Most notably, they may encounter fewer parasites in their introduced range compared to their native range. Parasites are ubiquitous and pervasive in marine systems, yet their role in marine invasions is relatively unexplored. Although data on parasites of marine organisms exist, the extent to which parasites can mediate marine invasions, or the extent to which invasive parasites and pathogens are responsible for infecting or potentially decimating native marine species have not been examined. In this review, we present a theoretical framework to model invasion success and examine the evidence for a relationship between parasite presence and the success of introduced marine species. For this, we compare the prevalence and species richness of parasites in several introduced populations of marine species with populations where they are native. We also discuss the potential impacts of introduced marine parasites on native ecosystems.

The evolution of trophic transmission.

Parasite increased trophic transmission (PITT) is one of the more fascinating tales of parasite evolution. The implications of this go beyond cocktail party anecdotes and science fiction plots as the phenomenon is pervasive and likely to be ecologically and evolutionarily important. Although the subject has already received substantial review, Kevin Lafferty here focuses on evolutionary aspects that have not been fully explored, specifically: (1) How strong should PITT be? (2) How might sexual selection and limb autotomy facilitate PITT? (3) How might infrapopulation regulation in final hosts be important in determining avoidance of infected prey? And (4) what happens when more than one species of parasite is in the same intermediate host?

Parasitology meets ecology on its own terms: Margolis et al. revisited.

We consider 27 population and community terms used frequently by parasitologists when describing the ecology of parasites. We provide suggestions for various terms in an attempt to foster consistent use and to make terms used in parasite ecology easier to interpret for those who study free-living organisms. We suggest strongly that authors, whether they agree or disagree with us, provide complete and unambiguous definitions for all parameters of their studies.

Environmental parasitology: What can parasites tell us about human impacts on the environment?

There are a variety of ways that environmental changes affect parasites, suggesting that information on parasites can indicate anthropogenic impacts. Parasitism may increase if the impact reduces host resistance or increases the density of intermediate or definitive hosts. Parasitism may decrease if definitive or intermediate host density declines or parasites suffer higher mortality directly (eg. from toxic effects on parasites) or indirectly (infected hosts suffer differentially high mortality). Although these scenarios are opposing, they can provide a rich set of predictions once we understand the true associations between each parasite and impact. In this review, Kevin Lafferty discusses how parasite ecologists have used and can use parasites to assess environmental quality.

Infestation of an introduced host, the European green crab, Carcinus maenas, by a symbiotic nemertean egg predator, Carcinonemertes epialti.

The recent introduction of the European green crab, Carcinus maenas, to the west coast of the U.S. has provided an opportunity for host transfer of the symbiotic nemertean egg predator, Carcinonemertes epialti, from its native shore crab host, Hemigrapsus oregonensis to the exotic C. maenas. Two surveys of C. maenas in Bodega Harbor, California, revealed that, in March 1995 prevalence of C. epialti on C. maenas was significantly lower than on H. oregonensis (11% versus 74%), but in November 1995 there was no significant difference between the 2 species (79% versus 98%). Only juvenile C. epialti were recovered from C. maenas in March 1995. However, in November 1995, ovigerous C. maenas were harboring actively feeding adult worms. Prevalence in both crab species significantly differed from March to November. Laboratory studies revealed that C. epialti fed and reproduced on eggs of C. maenas. The feeding rate of C. epialti on C. maenas eggs (2.5 eggs/trial) was not significantly different from that on H. oregonensis eggs (3.6 eggs/trial). Our findings suggest that this nemertean may have less host specificity than was previously thought. If C. epialti causes brood mortality of C. maenas in nature, it could potentially impact populations of this exotic crab.