Potential for Emergence of Foodborne Trematodiases Transmitted by an Introduced Snail (Melanoides tuberculata) in California and Elsewhere in the United States.

We document that 3 human-infectious trematodes and their introduced first intermediate host snail (Melanoides tuberculata) are widespread throughout southern California. We surveyed 41 fishing localities, 19 of which harbored snails infected with zoonotic trematodes. Two of the parasites, Haplorchis pumilio and Centrocestus formosanus, are fishborne intestinal trematodes recognized as being important human pathogens in other areas of the world; the third, Philophthalmus gralli, can infect the human eye. An additional 5 species detected infecting M. tuberculata are likely of little direct threat to people; however, they may be recently introduced to the Americas, highlighting the risk that additional pathogenic trematodes transmitted by the snail in its native range could be introduced to the United States. The current, possible human-infection risk in California clarifies the need to consider the introduced snail and its parasites from a public health perspective anywhere in the United States the snail has been introduced.

We report that 3 human-infecting trematodes and their introduced intermediate host snail are widespread in southern California freshwater fishing localities. Eating undercooked or underfrozen fish is the way people get infected by 2 of the parasite species, which are recognized as important human pathogens in other areas of the world. We also found 5 non­human-infectious trematodes carried by the snail that may be cointroduced, highlighting the possibility that other dangerous pathogens transmitted by the snail where it is native could arrive later or already be present in the United States. The common presence of the human-infecting fishborne trematodes at fishing localities, the widespread popularity of eating uncooked fish (eg, as sashimi, sushi, poke, or ceviche), and the potential for additional human-infecting trematodes to also be introduced, all justify consideration of the introduced snail and its parasites from a public health perspective in California and other areas in the United States where the parasites or the host snail have already been reported.

Lynnia grapsolytica n. gen, n. sp. (Ciliophora: Apostomatida: Colliniidae), a Deadly Blood Parasite of Crabs with a Novel Pseudocytopharynx.

We describe a new genus and species of blood-dwelling apostome ciliate, Lynnia grapsolytica n. gen., n. sp. (Apostomatida: Colliniidae). A distinct kinety "hook" pattern on the tomite's posterior ventral face, coupled with its marine habitat and use of a decapod host, readily distinguishes this ciliate from all known colliniids. We detected the parasite in ~12% of Pachygrapsus crassipes (Brachyura: Grapsidae) crabs in a California estuary and confirmed its presence at a Baja California rocky intertidal site. As existing methods failed to adequately stain this ciliate, we developed a new miniaturized silver carbonate impregnation staining method that produced excellent somatic and nuclear stains in all five observed cell types. A possibly unique trait is the active invagination of the tropho-tomont's anterior to form a temporary "pseudocytopharynx," likely used for feeding. Histological examination revealed that the ciliate invaded and damaged skeletal muscle, the heart, connective tissues, and gonads. Survivorship analysis indicated that infected crabs experienced 2.6 times greater daily mortality than uninfected crabs. Laboratory and field experimental infection attempts failed, suggesting a complex life cycle with outside-host development. Phylogenetic analysis at the 18S and COI loci confirmed the ciliate's placement in the Colliniidae. We emend the diagnosis of Family Colliniidae.

Social trematode parasites increase standing army size in areas of greater invasion threat.

Organisms or societies are resource limited, causing important trade-offs between reproduction and defence. Given such trade-offs, optimal allocation theory predicts that, for animal societies with a soldier caste, allocation to soldiers should reflect local external threats. Although both threat intensity and soldier allocation can vary widely in nature, we currently lack strong evidence that spatial variation in threat can drive the corresponding variation in soldier allocation. The diverse guild of trematode parasites of the California horn snail provides a useful system to address this problem. Several of these species form colonies in their hosts with a reproductive division of labour including a soldier caste. Soldiers are non-reproductive and specialized in defence, attacking and killing invading parasites. We quantified invasion threat and soldier allocation for 168 trematode colonies belonging to six species at 26 sites spread among 10 estuaries in temperate and tropical regions. Spatial variation in invasion threat was matched as predicted by the relative number of soldiers for multiple parasite species. Soldier allocation correlated with invasion threat at fine spatial scales, suggesting that allocation is at least partly inducible. These results may represent the first clear documentation of a spatial correlation between allocation to any type of caste and a biotic selective agent.

Metabolic theory of ecology successfully predicts distinct scaling of ectoparasite load on hosts.

The impacts of parasites on hosts and the role that parasites play in ecosystems must be underlain by the load of parasites in individual hosts. To help explain and predict parasite load across a broad range of species, quantitative theory has been developed based on fundamental relationships between organism size, temperature and metabolic rate. Here, we elaborate on an aspect of that 'scaling theory for parasitism', and test a previously unexplored prediction, using new data for total ectoparasite load from 263 wild birds of 42 species. We reveal that, despite the expected substantial variation in parasite load among individual hosts, (i) the theory successfully predicts the distinct increase of ectoparasite load with host body size, indicating the importance of geometric scaling constraints on access to host resources, (ii) ectoparasite load appears ultimately limited by access-not to host space-but to host energy, and (iii) there is a currency-dependent shift in taxonomic dominance of parasite load on larger birds. Hence, these results reveal a seemingly new macroecological pattern, underscore the utility of energy flux as a currency for parasitism and highlight the promise of using scaling theory to provide baseline expectations for parasite load for a diversity of host species.

Parasite and host biomass and reproductive output in barnacle populations in the rocky intertidal zone.

The rocky intertidal zone has a long history of ecological study with barnacles frequently serving as a model system to explore foundational theories. Parasites are often ignored in community ecology studies, and this particularly holds for true for the rocky intertidal zone. We explore the role of the isopod parasite, Hemioniscus balani, on its host, the acorn barnacle, Chthamalus fissus. We use the currencies of biomass and reproduction measured at the individual level, then applied to the population level, to evaluate the importance of this parasite to barnacle populations. We found H. balani can comprise substantial biomass in 'apparent' barnacle populations, sometimes even equaling barnacle biomass. Additionally, parasite reproduction sometimes matched barnacle reproduction. Thus, parasites divert substantial energy flow from the barnacle population and to near-shore communities in the form of parasite larvae. Parasites appeared to decrease barnacle reproduction per area. Potentially, this parasite may control barnacle populations, depending on the extent to which heavily infected barnacle populations contribute to barnacle populations at larger scales. These findings regarding the importance of a particular parasite for host population dynamics in this well studied ecosystem call for the integration of disease dynamics into community ecological studies of the rocky intertidal zone.

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

Competition - colonization tradeoffs occur in many systems, and theory predicts that they can strongly promote species coexistence. However, there is little empirical evidence that observed competition - colonization tradeoffs are strong enough to maintain diversity in natural systems. This is due in part to a mismatch between theoretical assumptions and biological reality in some systems. We tested whether a competition - colonization tradeoff explains how a diverse trematode guild coexists in California horn snail populations, a system that meets the requisite criteria for the tradeoff to promote coexistence. A field experiment showed that subordinate trematode species tended to have higher colonization rates than dominant species. This tradeoff promoted coexistence in parameterized models but did not fully explain trematode diversity and abundance, suggesting a role of additional diversity maintenance mechanisms. Spatial heterogeneity is an alternative way to promote coexistence if it isolates competing species. We used scale transition theory to expand the competition - colonization tradeoff model to include spatial variation. The parameterized model showed that spatial variation in trematode prevalence did not isolate most species sufficiently to explain the overall high diversity, but could benefit some rare species. Together, the results suggest that several mechanisms combine to maintain diversity, even when a competition - colonization tradeoff occurs.

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

Competition - colonization tradeoffs occur in many systems, and theory predicts that they can strongly promote species coexistence. However, there is little empirical evidence that observed competition- colonization tradeoffs are strong enough to maintain diversity in natural systems. This is due in part to a mismatch between theoretical assumptions and biological reality in some systems. We tested whether a competition - colonization tradeoff explains how a diverse trematode guild coexists in California horn snail populations, a system that meets the requisite criteria for the tradeoff to promote coexistence. A field experiment showed that subordinate trematode species tended to have higher colonization rates than dominant species. This tradeoff promoted coexistence in parameterized models but did not fully explain trematode diversity and abundance, suggesting a role of additional diversity maintenance mechanisms. Spatial heterogeneity is an alternative way to promote coexistence if it isolates competing species. We used scale transition theory to expand the competition - colonization tradeoff model to include spatial variation. The parameterized model showed that spatial variation in trematode prevalence did not isolate most species sufficiently to explain the overall high diversity, but could benefit some rare species. Together, the results suggest that several mechanisms combine to maintain diversity, even when a competition - colonization tradeoff occurs.

Parasites affect food web structure primarily through increased diversity and complexity.

Comparative research on food web structure has revealed generalities in trophic organization, produced simple models, and allowed assessment of robustness to species loss. These studies have mostly focused on free-living species. Recent research has suggested that inclusion of parasites alters structure. We assess whether such changes in network structure result from unique roles and traits of parasites or from changes to diversity and complexity. We analyzed seven highly resolved food webs that include metazoan parasite data. Our analyses show that adding parasites usually increases link density and connectance (simple measures of complexity), particularly when including concomitant links (links from predators to parasites of their prey). However, we clarify prior claims that parasites "dominate" food web links. Although parasites can be involved in a majority of links, in most cases classic predation links outnumber classic parasitism links. Regarding network structure, observed changes in degree distributions, 14 commonly studied metrics, and link probabilities are consistent with scale-dependent changes in structure associated with changes in diversity and complexity. Parasite and free-living species thus have similar effects on these aspects of structure. However, two changes point to unique roles of parasites. First, adding parasites and concomitant links strongly alters the frequency of most motifs of interactions among three taxa, reflecting parasites' roles as resources for predators of their hosts, driven by trophic intimacy with their hosts. Second, compared to free-living consumers, many parasites' feeding niches appear broader and less contiguous, which may reflect complex life cycles and small body sizes. This study provides new insights about generic versus unique impacts of parasites on food web structure, extends the generality of food web theory, gives a more rigorous framework for assessing the impact of any species on trophic organization, identifies limitations of current food web models, and provides direction for future structural and dynamical models.

Parasite species richness and intensity of interspecific interactions increase with latitude in two wide-ranging hosts.

Although the latitudinal diversity gradient is a well-known and general pattern, the mechanisms structuring it remain elusive. Two key issues limit differentiating these. First, habitat type usually varies with latitude, precluding a standardized evaluation of species richness. Second, broad-scale and local factors hypothesized to shape diversity patterns covary with one another, making it difficult to tease apart independent effects. Examining communities of parasites in widely distributed hosts can eliminate some of these confounding factors. We quantified diversity and interspecific interactions for trematode parasites infecting two similar snail species across 27 degrees of latitude from 43 locations in tropical and temperate oceans. Counter to typical patterns, we found that species richness, levels of parasitism, and intensity of intraguild predation increased with latitude. Because speciation rates are precluded from driving diversity gradients in this particular system, the reversed gradients are likely due to local ecological factors, specifically, increased productivity and stability. We highlight how this system may serve as a useful tool to provide insight into what processes drive diversity gradients in general.

Ecosystem energetic implications of parasite and free-living biomass in three estuaries.

Parasites can have strong impacts but are thought to contribute little biomass to ecosystems. We quantified the biomass of free-living and parasitic species in three estuaries on the Pacific coast of California and Baja California. Here we show that parasites have substantial biomass in these ecosystems. We found that parasite biomass exceeded that of top predators. The biomass of trematodes was particularly high, being comparable to that of the abundant birds, fishes, burrowing shrimps and polychaetes. Trophically transmitted parasites and parasitic castrators subsumed more biomass than did other parasitic functional groups. The extended phenotype biomass controlled by parasitic castrators sometimes exceeded that of their uninfected hosts. The annual production of free-swimming trematode transmission stages was greater than the combined biomass of all quantified parasites and was also greater than bird biomass. This biomass and productivity of parasites implies a profound role for infectious processes in these estuaries.

Two 'new' renicolid trematodes (Trematoda: Digenea: Renicolidae) from the California horn snail, Cerithidea californica (Haldeman, 1840) (Gastropoda: Potamididae).

This manuscript describes the daughter parthenitae (sporocysts) and cercariae of two species of renicolid xiphidiocercaria that infect the California horn snail, Cerithidea californica, which serves as first intermediate host for a diverse and ecologically important guild of digenean trematode parasitic castrators. The two species described here have previously been considered to be a single morphospecies in ecological and evolutionary research. We provide provisional species names to respect that digenean alpha taxonomy is currently focused on sexual (adult) stages, while simultaneously respecting the spirit and utility of formal nomenclature in providing unambiguously unique, species-level names that also clarify to the extent possible species' taxonomic affiliations. The first species, Renicola sp. "polychaetophila" is most readily distinguishable from previously described renicolid xiphidiocercariae by a combination of (1) having a penetration gland duct arrangement of 2[(1+3+1)+1], (2) having one pair of penetration glands positioned anteriorly to the main gland cluster, (3) lacking tegmental spines, and (4) infecting Cerithidea californica. The second species, Renicola sp. "martini", is most readily distinguishable from other renicolid xiphidiocercariae that also have tegmental spines by a combination of (1) having a simple, bullet-shaped oral stylet sclerotized for 50-80% of its length, (2) having a cystogenous-gland field with an anterior-most extent about half way between the oral and ventral suckers, and (3) in infecting Cerithidea californica. Phylogenetic analyses using DNA (COI and ITS1) sequence data support that these two trematodes represent distinct species of Renicola. We also (1) provide an emended diagnosis for renicolid cercariae, (2) highlight a few morphological characters that may be useful for future taxonomic work involving renicolid xiphidiocercariae, and (3) suggest that future descriptive work involving trematode parthenitae include more information pertaining to the group of parthenitae as a whole.

A metabolic and body-size scaling framework for parasite within-host abundance, biomass, and energy flux.

Energetics may provide a useful currency for studying the ecology of parasite assemblages within individual hosts. Parasite assemblages may also provide powerful models to study general principles of ecological energetics. Yet there has been little ecological research on parasite-host energetics, probably due to methodological difficulties. However, the scaling relationships of individual metabolic rate with body or cell size and temperature may permit us to tackle the energetics of parasite assemblages in hosts. This article offers the foundations and initial testing of a metabolic theory of ecology (MTE) framework for parasites in hosts. I first provide equations to estimate energetic flux through observed parasite assemblages. I then develop metabolic scaling theory for parasite abundance, energetics, and biomass in individual hosts. In contrast to previous efforts, the theory factors in both host and parasite metabolic scaling, how parasites use host space, and whether energy or space dictates carrying capacity. Empirical tests indicate that host energetic flux can set parasite carrying capacity, which decreases as predicted considering the scaling of host and parasite metabolic rates. The theory and results also highlight that the phenomenon of "energetic equivalence" is not an assumption of MTE but a possible outcome contingent on how species partition resources. Hence, applying MTE to parasites can lend mechanistic, quantitative, predictive insight into the nature of parasitism and can inform general ecological theory.

Let's restart formally naming 'larval' trematodes.

Arguably the most unique biological features of trematode parasites involve their clonal parthenitae and cercariae. These life stages are biologically fascinating, medically and scientifically important, and often studied for years, lacking knowledge of their corresponding sexual adult stages. But sexual adults are the focus of trematode species-level taxonomy, partially explaining the relative neglect of documenting the diversity of parthenitae and cercariae and why researchers who do describe them give them only provisional names. Provisional names are unregulated, unstable, often ambiguous, and, I argue, often unnecessary. I suggest that we recommence formally naming parthenitae and cercariae using an improved naming scheme. The scheme should permit us to reap the benefits of formal nomenclature and thereby enhance research involving these diverse and important parasites.

Social evolution: Diverse divisions of labor in trematode parasites.

Some animal societies solve problems, like foraging or defense, by cooperatively dividing labor. A new discovery highlights that trematodes are unique in forming different societies at multiple parts of their complex life cycle with distinct divisions of labor to solve different problems.

EXPERIMENTAL INFECTIONS WITH EUHAPLORCHIS CALIFORNIENSIS AND A SMALL CYATHOCOTYLID INCREASE CONSPICUOUS BEHAVIORS IN CALIFORNIA KILLIFISH (FUNDULUS PARVIPINNIS).

Some parasites manipulate their host's phenotype to enhance predation rates by the next host in the parasite's life cycle. Our understanding of this parasite-increased trophic transmission is often stymied by study-design challenges. A recurring difficulty has been obtaining uninfected hosts with a coevolutionary history with the parasites, and conducting experimental infections that mimic natural processes. In 1996, Lafferty and Morris provided what has become a classic example of parasite-increased trophic transmission; they reported a positive association between the intensity of a brain-infecting trematode (Euhaplorchis californiensis) in naturally infected California killifish (Fundulus parvipinnis) and the frequency of conspicuous behaviors, which was thought to explain the documented 10-30× increase in predation by the final host birds. Here, we address the primary gap in that study by using experimental infections to assess the causality of E. californiensis infection for increased conspicuous behaviors in F. parvipinnis. We hatched and reared uninfected F. parvipinnis from a population co-occurring with E. californiensis, and infected them 1-2 times/week over half their life span with E. californiensis and a small cyathocotylid trematode (SMCY) that targets the host's muscle tissue. At 3 time points throughout the hosts' lives, we quantified several conspicuous behaviors: contorting, darting, scratching, surfacing, and vertical positioning relative to the water's surface. Euhaplorchis californiensis and SMCY infection caused 1.8- and 2.5-fold overall increases in conspicuous behaviors, respectively. Each parasite was also associated with increases in specific conspicuous behaviors, particularly 1.9- and 1.4-fold more darting. These experimental findings help solidify E. californiensis-F. parvipinnis as a classic example of behavioral manipulation. Yet our findings for E. californiensis infection-induced behavioral change were less consistent and strong than those previously documented. We discuss potential explanations for this discrepancy, particularly the idea that behavioral manipulation may be most apparent when fish are actively attacked by predators. Our findings concerning the other studied trematode species, SMCY, highlight that trophically transmitted parasites infecting various host tissues are known to be associated with conspicuous behaviors, reinforcing calls for research examining how communities of trophically transmitted parasites influence host behavior.

Flying shells: historical dispersal of marine snails across Central America.

The geological rise of the Central American Isthmus separated the Pacific and the Atlantic oceans about 3 Ma, creating a formidable barrier to dispersal for marine species. However, similar to Simpson's proposal that terrestrial species can 'win sweepstakes routes'-whereby highly improbable dispersal events result in colonization across geographical barriers-marine species may also breach land barriers given enough time. To test this hypothesis, we asked whether intertidal marine snails have crossed Central America to successfully establish in new ocean basins. We used a mitochondrial DNA genetic comparison of sister snails (Cerithideopsis spp.) separated by the rise of the Isthmus. Genetic variation in these snails revealed evidence of at least two successful dispersal events between the Pacific and the Atlantic after the final closure of the Isthmus. A combination of ancestral area analyses and molecular dating techniques indicated that dispersal from the Pacific to the Atlantic occurred about 750 000 years ago and that dispersal in the opposite direction occurred about 72 000 years ago. The geographical distribution of haplotypes and published field evidence further suggest that migratory shorebirds transported the snails across Central America at the Isthmus of Tehuantepec in southern Mexico. Migratory birds could disperse other intertidal invertebrates this way, suggesting the Central American Isthmus may not be as impassable for marine species as previously assumed.

Social organization in a flatworm: trematode parasites form soldier and reproductive castes.

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of 'parthenitae' within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the 'recognition of self' and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.

Colloquium paper: homage to Linnaeus: how many parasites? How many hosts?

Estimates of the total number of species that inhabit the Earth have increased significantly since Linnaeus's initial catalog of 20,000 species. The best recent estimates suggest that there are approximately 6 million species. More emphasis has been placed on counts of free-living species than on parasitic species. We rectify this by quantifying the numbers and proportion of parasitic species. We estimate that there are between 75,000 and 300,000 helminth species parasitizing the vertebrates. We have no credible way of estimating how many parasitic protozoa, fungi, bacteria, and viruses exist. We estimate that between 3% and 5% of parasitic helminths are threatened with extinction in the next 50 to 100 years. Because patterns of parasite diversity do not clearly map onto patterns of host diversity, we can make very little prediction about geographical patterns of threat to parasites. If the threats reflect those experienced by avian hosts, then we expect climate change to be a major threat to the relatively small proportion of parasite diversity that lives in the polar and temperate regions, whereas habitat destruction will be the major threat to tropical parasite diversity. Recent studies of food webs suggest that approximately 75% of the links in food webs involve a parasitic species; these links are vital for regulation of host abundance and potentially for reducing the impact of toxic pollutants. This implies that parasite extinctions may have unforeseen costs that impact the health and abundance of a large number of free-living species.

Mortality affects adaptive allocation to growth and reproduction: field evidence from a guild of body snatchers.

BACKGROUND: The probability of being killed by external factors (extrinsic mortality) should influence how individuals allocate limited resources to the competing processes of growth and reproduction. Increased extrinsic mortality should select for decreased allocation to growth and for increased reproductive effort. This study presents perhaps the first clear cross-species test of this hypothesis, capitalizing on the unique properties offered by a diverse guild of parasitic castrators (body snatchers). I quantify growth, reproductive effort, and expected extrinsic mortality for several species that, despite being different species, use the same species' phenotype for growth and survival. These are eight trematode parasitic castrators-the individuals of which infect and take over the bodies of the same host species-and their uninfected host, the California horn snail. RESULTS: As predicted, across species, growth decreased with increased extrinsic mortality, while reproductive effort increased with increased extrinsic mortality. The trematode parasitic castrator species (operating stolen host bodies) that were more likely to be killed by dominant species allocated less to growth and relatively more to current reproduction than did species with greater life expectancies. Both genders of uninfected snails fit into the patterns observed for the parasitic castrator species, allocating as much to growth and to current reproduction as expected given their probability of reproductive death (castration by trematode parasites). Additionally, species differences appeared to represent species-specific adaptations, not general plastic responses to local mortality risk. CONCLUSIONS: Broadly, this research illustrates that parasitic castrator guilds can allow unique comparative tests discerning the forces promoting adaptive evolution. The specific findings of this study support the hypothesis that extrinsic mortality influences species differences in growth and reproduction.