A gastropod scavenger serving as paratenic host for larval helminth communities in shore crabs

The whelk Cominella glandiformis is an important predator-scavenger of New Zealand intertidal ecosystems; a few whelks can quickly eat all the soft tissues of recently dead crabs. In this study, we demonstrate that whelks can also ingest and act as paratenic hosts for at least 4 helminth species that use crabs as intermediate hosts: metacercariae of the trematode Maritrema sp. and of another unidentified trematode, larval acuariid nematodes, and cystacanths of the acanthocephalans Profilicollis spp. Large whelks ingest disproportionately more helminth larvae than small whelks, but the survival of parasites during their short stay in the whelks is not affected by whelk size. The majority of metacercariae and nematodes are passed out in whelk feces within 3 days of ingestion, whereas the few cystacanths found did not leave whelks until after that time; no parasite was left in whelks 5 days postingestion. Survival of all 4 helminth species was generally very high, though it decreased day by day in 2 species. Given that the avian definitive hosts of all 4 helminths also eat whelks, our results indicate that alternative transmission pathways exist and that parasites can take routes through food webs that are too often ignored.     

Parasite Induced Summer Mortality in the Cockle Cerastoderma edule by the Trematode Gymnophallus choledochus

In late summer 2004, a conspicuous cockle (Cerastoderma edule) mortality event was observed on a tidal flat in the northern Wadden Sea (North Sea, Germany) with many fresh valves and still living cockles lying on the sediment surface. To investigate whether trematode parasites utilizing the cockle as first or second intermediate host were involved in this mortality, buried and surfaced cockles were sampled and analyzed, and a laboratory experiment conducted. The field survey showed no statistical difference in intensity of parasites encysted in the foot of cockles. Three species of Himasthla utilizing the cockle as second intermediate host and known to impair the cockle’s burrowing ability were found in buried cockles with 148.4±111.1 metacercariae/foot and in surfaced cockles with 164.2±84.4. There was also no difference in infection levels of parasites utilizing the cockles as second intermediate host in other cockle tissues between buried and surfaced cockles. In contrast, surfaced cockles showed a ten times higher prevalence (71.0%) than buried cockles (7.4%) of the trematode Gymnophallus choledochus – a parasite utilizing the cockle as first (and second) intermediate host – filling almost the entire body cavity and eliminating gonad structures. In an aquarium experiment of 14 days, all cockles found buried on the tidal flat survived compared to only 23.3% found on the surface. This suggests G. choledochus to be a castrating agent and a serious mortality factor in adult cockle populations.     

Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi

Metacercariae of the trematode Curtuteria australis (Echinostomatidae) accumulate in the foot of the New Zealand cockle Austrovenus stutchburyi, severely impairing the cockle's ability to burrow under the sediments. This results in increased predation by birds on cockles, and thus enhanced transmission rates of the parasite to its bird definitive hosts. This host manipulation by the trematode is costly: fish regularly crop the tip of the foot of cockles stranded on the sediment surface, killing any metacercariae they ingest. A second, previously undetected trematode species (characterized by 23 collar spines) co-existing with C. australis, has been found in the foot of cockles in the Otago Harbour, South Island, New Zealand. The relative abundance of the two species varies among localities, with the identity of the numerically dominant species also changing from one locality to the next. Both C. australis and the new species have a strong preference for encysting in the tip of the cockle's foot, where their impact on the burrowing ability of the host is greatest, and where they both face the risk of cropping by fish. Results indicate that these two species are ecological equivalents, and their combined numbers determine how the cockle population is affected.     

Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare

Parasites with complex life cycles, relying on trophic transmission to a definitive host, very often induce changes in the behaviour or appearance of their intermediate hosts. Because this usually makes the intermediate host vulnerable to predation by the definitive host, it is generally assumed that the parasite's transmission rate is increased, and that the modification of the host is, therefore, of great adaptive significance to the parasite. However, in the ecological "real world" other predators unsuitable as hosts may just as well take advantage of the facilitation process and significantly erode the benefit of host manipulation. Here we show that the intertidal New Zealand cockle (Austrovenus stutchburyi), manipulated by its echinostome trematode (Curtuteria australis) to rest on the sediment surface fully exposed to predation from the avian definitive host, is also subject to sublethal predation from a benthic feeding fish (Notolabrus celidotus, Labridae). The fish is targeting only the cockle-foot, in which the parasite preferentially encysts, reducing the infection intensity of manipulated cockles to levels comparable with those in non-manipulated, buried cockles. Based on the frequency and intensity of the foot cropping and predation rates on surfaced cockles by avian hosts, it is estimated that 2.5% of the parasite population in manipulated cockles is transmitted successfully whereas 17.1% is lost to fish. We argue that the adaptive significance of manipulation in the present system depends critically on the feeding behaviour of the definitive host. If cockles constitute the majority of prey items, there will be selection against manipulation. If manipulated cockles are taken as an easily accessible supplement to a diet composed mostly of other prey organisms, behavioural manipulation of the cockle host appears a high risk, high profit transmission strategy. Both these feeding behaviours of birds are known to occur in the field.     

Parasite‐induced surfacing in the cockle Austrovenus stuchburyi: adaptation or not?

Parasite manipulation of host behaviour is a compelling example of the extended phenotype. However, in many cases, such manipulation may be incorrectly assumed. Previous work has demonstrated that Austrovenus stuchburyi cockles stranded on mud-flat surfaces due to an inability to re-burrow both contain significantly more metacercariae of the trematode Curtuteria australis and are predated by the definitive host of this parasite at a faster rate than burrowed cockles. These results have been interpreted as strong evidence for a manipulation of cockle behaviour by the trematode to facilitate transmission to the definitive host. The model presented here, however, indicates that the selective advantage to the parasite of the altered host behaviour is currently of a negligible level at our study site that is highly unlikely to have been realized as an adaptation over evolutionary time. Hence, there are no grounds on which the more parsimonious explanation, that the altered host behaviour observed is simply an incidental side-effect of infection, can be rejected. We thus maintain that for any change in the behaviour of infected hosts to be confirmed as potentially a parasite trait that has evolved in response to selection, the adaptive benefit taking into account the entire parasite life cycle may need to be considered.     

Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp

The complex life cycle of digenean trematodes with alternating stages of asexual multiplication and sexual reproduction can generate interesting within-host population genetic patterns. Metacercarial stages found in the second intermediate host are generally accumulated from the environment. Highly mobile second intermediate hosts can sample a broad range of cercarial genotypes and accumulate genetically diverse packets of metacercariae, but it is unclear whether the same would occur in systems where the second intermediate host is relatively immobile and cercarial dispersal is the sole mechanism that can maintain genetic homogeneity at the population level. Here, using polymorphic microsatellite markers, we addressed this issue by genotyping metacercariae of the trematode Gymnophallus sp. from the New Zealand cockle Austrovenus stutchburyi. Despite the relatively sessile nature of the second intermediate host of Gymnophallus, very high genotypic diversity of metacercariae was found within cockles, with only two cockles harbouring multiple copies of a single clonal lineage. There was no evidence of population structuring at the scale of our study, suggesting the existence of a well-mixed population. Our results indicate that (i) even relatively sessile second intermediate hosts can accumulate a high diversity of genotypes and (ii) the dispersal ability of cercariae, whether passive or not, is much greater than expected for such small and short-lived organisms. The results also support the role of the second intermediate host as an accumulator of genetic diversity in the trematode life cycle.     

Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve

Spatial heterogeneities in the abundance of free-living organisms as well as in infection levels of their parasites are a common phenomenon, but knowledge on parasitism in invertebrate intermediate hosts in this respect is scarce. We investigated the spatial pattern of four dominant trematode species which utilize a common intertidal bivalve, the cockle Cerastoderma edule, as second intermediate host in their life cycles. Sampling of cockles from the same cohort at 15 sites in the northern Wadden Sea (North Sea) over a distance of 50 km revealed a conspicuous spatial heterogeneity in infection levels in all four species over the total sample as well as among and within sampling sites. Whereas multiple regression analyses indicated the density of first intermediate upstream hosts to be the strongest determinant of infection levels in cockles, the situation within sites was more complex with no single strong predictor variable. However, host size was positively and host density negatively correlated with infection levels and there was an indication of differential susceptibility of cockle hosts. Small-scale differences in physical properties of the habitat in the form of residual water at low tide resulted in increased infection levels of cockles which we experimentally transferred into pools. A complex interplay of these factors may be responsible for within-site heterogeneities. At larger spatial scales, these factors may be overridden by the strong effect of upstream hosts. In contrast to first intermediate trematode hosts, there was no indication for inter-specific interactions. In other terms, the recruitment of trematodes in second intermediate hosts seems to be largely controlled by pre-settlement processes both among and within host populations.     

Inertia of parasite infection versus host biomass fluctuation

Infection by parasites with complex life cycles such as trematodes depends on many environmental factors which may result in a time-lag between host biomass fluctuations and parasite density in hosts. A cockle (marine bivalve, second intermediate host) population and its associated parasite community were monitored over 15 years. A time-shift correlation analysis suggests that trematode abundance in cockles responds to cockle biomass after a long delay (8 year time-lag). Thus, these parasites can sustainably support a deficit of their intermediate host.     

Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae)

Marine bivalves harbour a diversity of trematode parasites affecting population and community dynamics of their hosts. Although ecologically and economically important, factors influencing transmission between first (snail) and second (bivalve) intermediate hosts have rarely been studied in marine systems. In laboratory experiments, the effect of temperature (10, 15, 20, 25 degrees C) was investigated on (1) emergence from snails, (2) survival outside hosts and (3) infectivity in second intermediate hosts of cercariae of the trematode Renicola roscovita (Digenea: Renicolidae), a major parasite in North Sea bivalves. Emergence of cercariae peaked at 20 degrees C (2609 +/- 478 cercariae snail(-1) 120 h(-1)) and was considerably lower at 10 degrees C (80 +/- 79), 15 degrees C (747 +/- 384) and 25 degrees C (1141 +/- 334). Survival time decreased with increasing temperature, resulting in 50% mortality of the cercariae after 32.8 +/- 0.6 h (10 degrees C), 26.8 +/- 0.8 h (15 degrees C), 20.2 +/- 0.5 h (20 degrees C) and 16.6 +/- 0.3 h (25 degrees C ). Infectivity of R. roscovita cercariae in cockles Cerastoderma edule increased with increasing temperature and was highest at 25 degrees C (42.6 +/- 3.9%). However, mesocosm experiments with infected snails and cockle hosts in small aquaria, integrating cercarial emergence, survival and infectivity, showed highest infection of cockles at 20 degrees C (415 +/- 115 metacercariae host(-1)), indicating 20 degrees C to be the optimum temperature for transmission of this species. A field experiment showed metacercariae of R. roscovita to appear in C. edule with rising water temperature in April; highest infection rates were in August, when the water temperature reached 20 degrees C. Since another trematode species (Himasthla elongata; Digenea: Echinostomatidae) occurring at the experimental site showed a similar temporal pattern, trematode transmission to second intermediate bivalve hosts may peak during especially warm (> or = 20 degrees C) summers in the variable climate regime of the North Sea.     

Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects

Parasitism has long been emphasised as an important process structuring animal communities. However, empirical evidence documenting the impact of parasites in other than simple laboratory settings is lacking. Here we examine the trait-mediated indirect effects of echinostome trematodes on a New Zealand soft bottom intertidal community of macroinvertebrates. Curtuteria australis and a second related but undescribed trematode both utilise the cockle Austrovenus stutchburyi as second intermediate host in which the parasites infect the foot tissue. Heavily infected cockles are therefore more sessile than lightly infected individuals, and, unable to bury, often rest on the sediment surface. We utilised these behavioural changes in two long term field experiments, respectively manipulating the parasite load of buried cockle (i.e. bioturbation), and the density of surfaced cockles (i.e. surface structures and seabed hydrodynamics). Both high parasite loads in buried cockles and the presence of surfaced cockles increased species richness and generally also the density of certain species and of major systematic and functional groups of benthic macroinvertebrates. Species diversity (alpha) peaked under intermediate densities of surfaced cockles. Our results demonstrate that parasites, solely through their impact on the behaviour of a single community member, can be significant determinants of animal community structure and function.     

Diversity of trematode genetic clones within amphipods and the timing of same-clone infections

The genetic diversity of trematodes within second intermediate hosts has important implications for the evolution of trematode populations as these hosts are utilized after the parasites reproduce asexually within first intermediate hosts and before sexual reproduction within definitive hosts. We characterised the genetic clonal diversity of the marine trematode Maritrema novaezealandensis within amphipod (Paracalliope novizealandiae) second intermediate hosts using four to six microsatellite loci to determine if multiple copies of identical trematode clones existed within naturally infected amphipods. To determine the relative timing of infections by identical clones within hosts, trematode metacercariae were assigned to six developmental stages and the stages of identical clones were compared. The genotypes of 306 trematodes were determined from 44 amphipods each containing more than one trematode. Six pairs of identical trematode clones were recovered in total (representing five amphipods: 11% of amphipods with greater than one trematode) and all pairs of clones belonged to the same developmental stage. This suggests that identical clone infections are effectively synchronous. A general decrease in the number of metacercariae recovered, prevalence, and mean intensity of infection for each subsequent developmental stage coupled with large numbers of metacercariae (>9) only being recovered from recent infections, supports the occurrence of post-infection amphipod mortality and/or within-host trematode mortality. Taken together, our results indicate that natural infections are characterised by high genetic diversity, but that amphipods also periodically encounter "batches" of genetically identical clones, potentially setting the stage for interactions within and between clonal groups inside the host.     

Ten polymorphic microsatellite loci for the trematode Curtuteria australis (Echinostomatidae)

Ten polymorphic loci were isolated and characterised from the intertidal New Zealand trematode Curtuteria australis. This common parasite manipulates the burrowing behaviour of its abundant bivalve host Austrovenus stutchburyi, with cascading impacts on the biodiversity of intertidal communities. Observed heterozygosities of the 10 loci ranged from 0.500 to 0.905, and three to 14 alleles were detected in 24 trematode metacercariae. These loci are currently being used to investigate the molecular ecology of this species within its intermediate hosts.     

Intra-host competition between co-infecting digeneans within a bivalve second intermediate host: Dominance by priority-effect or taking advantage of others?

We experimentally investigated the interactions between two parasites known to manipulate their host's phenotype, the trematodes Acanthoparyphium sp. and Curtuteria australis, which infect the cockle Austrovenus stutchburyi. The larval stages of both species encyst within the tissue of the bivalve's muscular foot, with a preference for the tip of the foot. As more individuals accumulate at that site, they impair the burrowing behaviour of cockles and increase the probability of the parasites' transmission to a bird definitive host. However, individuals at the foot tip are also vulnerable to non-host predators in the form of foot-cropping fish which selectively bite off the foot tip of exposed cockles. Parasites encysted at the foot base are safe from such predators although they do not contribute to altering host behaviour, but nevertheless benefit from host manipulation as all parasites within the cockle are transmitted if it is ingested by a bird. Experimental infection revealed that Acanthoparyphium sp. and C. australis have different encystment patterns within the host, with proportionally fewer Acanthoparyphium metacercariae encysting at the foot tip than C. australis. This indicates that Acanthoparyphium may benefit indirectly from C. australis and incur a lower risk of non-host predation. However, in co-infections, not only did C. australis have higher infectivity than Acanthoparyphium, it also severely affected the latter's infection success. The asymmetrical strategies and interactions between the two species suggest that the advantages obtained from exploiting the host manipulation efforts of another parasite might be offset by traits such as reduced competitiveness in co-infections.     

Spatial covariation between infection levels and intermediate host densities in two trematode species

Both theoretical arguments and empirical evidence suggest that parasite transmission depends on host density. In helminths with complex life cycles, however, it is not clear which host, if any, is the most important. Here, the relationships between the abundance of metacercariae in second intermediate hosts, and the local density of both the first and second intermediate hosts of two trematode species, are investigated. Samples of the snail Potamopyrgus antipodarum, the amphipod Paracalliope fluviatilis and the isopod Austridotea annectens were collected from ten stations in a New Zealand lake. In the trematode Coitocaecum parvum, neither the density of the snail first intermediate host nor that of the amphipod second intermediate host correlated with infection levels in amphipods. In contrast, in the trematode Microphallus, infection levels in isopod second intermediate hosts were positively associated with isopod density and negatively associated with the density of snail first intermediate hosts. These relationships are explained by a negative correlation between snail and isopod densities, mediated in part by their different use of macrophyte beds in the lake. Overall, the results suggest that, at least for Microphallus, local infection levels depend on local intermediate host densities.     

The mud flat anemone-cockle association: mutualism in the intertidal zone?

The intertidal cockle Austrovenus stutchburyi exists in a symbiotic relationship with the mud flat anemone Anthopleura aureoradiata, the latter using the shell of buried cockles as the only available hard substrate for attachment. The cockles are also host to a detrimental larval trematode Curtuteria australis that invades the bivalves through the filtration current, and here we demonstrate that the anemones significantly depress the rate by which cockles accumulate parasites in the field. Along the tidal gradient, the relative parasite load of cockles was lowest where anemones were most abundant, and the area occupied by anemones per square meter sediment surface explained 30% of the spatial variation in infection intensity. At a smaller spatial scale, parasite loads were significantly lower (34%) in cockles from patches with than without anemones at the same tidal height. A field experiment manipulating the density of anemones showed that the rate of parasite accumulation in cockles decreased with increasing anemone density, and that the generally positive relationship between infection intensity and cockle size tended to disappear in the presence of anemones. The results suggest that the anemone-cockle symbiosis is a non-obligate mutualistic relationship in which the former is provided with a suitable substrate for attachment whereas the latter obtains protection against parasitic infections.     

First record and description of metacercariae of Curtuteria arguinae n. sp. (Digenea: Echinostomatidae), parasite of cockles Cerastoderma edule (Mollusca: Bivalvia) in Arcachon Bay, France

A new Himasthlinae species, Curtuteria arguinae, is described as metacercariae from the cockle Cerastoderma edule (L.), collected at Banc d'Arguin (southwestern France). These metacercariae encysted preferentially in the mantle and also in the foot of cockles. Encysted and chemically excysted metacercariae were studied by light microscopy and scanning electron microscopy, respectively. Excysted metacercariae were elongated and curved ventrally. They bore a 33-spine circumoral collar. Sensory papillae were arranged around the oral sucker and also symmetrically along the ventral surface body, from the collar to the acetabulum. The dorsal and ventral tegument surfaces were densely packed with similar pointed spines. The posterior end of the body was without any spines. Among the Curtuteria species described previously, only Curtuteria haematopodis Smogorjewskaja and Iskova, 1966 had the same number of circumoral collar spines. A 6-yr field survey showed that the cockle population at Banc d'Arguin was subjected to a summer infection of C. arguinae. Curtuteria arguinae phenology of infection is characterized by interannual variability and seasonality (beginning in July-August and maximum in autumn). The first intermediate and final hosts remain unknown.     

Annotated key to the trematode species infecting Batillaria attramentaria (Prosobranchia: Batillariidae) as first intermediate host

In eastern Asia and western North America at least nine morphologically distinguishable species of digenean trematode infect the mud snail, Batillaria attramentaria (Sowerby 1855) (=B. cumingi (Crosse 1862)), as first intermediate host. Further, molecular and morphological evidence indicates that several of these trematode species comprise complexes of cryptic species. I present an identification key to these nine trematode morphospecies (including four newly reported species). Additionally, I provide an annotated list, which includes further diagnostic information on the larval stages (cercariae, parthenitae, and metacercariae), information on second intermediate host use, links to the previous relevant reports of trematodes infecting B. attramentaria and notes on other aspects of the species' biology.     

Redescription and life cycle of the monorchiid Postmonorcheides maclovini Szidat, 1950 (Digenea) from the Southwestern Atlantic Ocean: Morphological and molecular data

The adult monorchiid, Postmonorcheides maclovini Szidat, 1950, digenean parasite of the Patagonian blennie Eleginops maclovinus (Cuvier) (Eleginopidae) from Puerto Deseado (47° 45′ S, 65° 55′ W), Argentina, was characterized and its life cycle elucidated. P. maclovinus is the only species of the genus Postmonorcheides, proposed by Szidat (1950) from Tierra del Fuego province (~ 54° S), Argentina. This digenean uses the Patagonian blennie as definitive host, and the intertidal bivalve Lasaea adansoni (Gmelin) (Lasaeidae) as both first and second intermediate hosts (metacercariae encyst inside sporocysts), being the first record of this clam as intermediate host of trematode parasites. The cercaria may, in addition to encysting in the sporocyst, emerge and presumably infect other intermediate hosts. This is the second report of a monorchiid species with metacercariae encysting inside the sporocyst. Adults were found parasitizing the fish stomach, pyloric caeca and intestine with a prevalence of 100%; sporocysts with cercariae and/or metacercariae were found parasitizing the gonad of the bivalve with a prevalence of 2.78%. The cercariae possess a well-developed tail and eye-spots are absent. The ITS1 sequence from the adult digeneans found in the Patagonian blennie, identified as P. maclovini, was found to be identical to the ITS1 sequences obtained both from sporocysts containing cercariae and encysted metacercariae found in L. adansoni.     

Life history and life cycles: production and behavior of trematode cercariae in relation to host exploitation and next-host characteristics

Life history trade-offs affect trematode parasites reproducing inside their 1st intermediate hosts. Within the constraint of the effect on host survival, parasite production of cercariae is subject to a size-numbers trade-off. Within each cercaria, resources must be partitioned between host-seeking and subsequent developmental functions. Three species of microphallid trematodes with the same 1st intermediate host (the gastropod Littorina saxatilis) were investigated. Maritrema arenaria periodically released many small cercariae. Microphallus similis released fewer, 15% larger, cercariae without periodicity. Microphallus similis cercariae were strong swimmers, moving toward the dark and downward in turbulent water, whereas Ma. arenaria cercariae remained suspended. Maritrema arenaria cercariae, although smaller in body and tail size, were produced at an average daily volume nearly twice that of M. similis. These differences are interpreted as transmission adaptations related to mobility and predictability of the 2nd intermediate host. Microphallus similis, with a mobile and less predictable crab host, adopted a 'bethedging' prolonged production of fewer cercariae by less intensive host exploitation, each cercaria having a high allocation to host-seeking behavior. Maritrema arenaria, with predictable sessile barnacle hosts, produced less mobile but potentially longer-lived cercariae in larger numbers. Microphallus piriformes metacercariae remain in the gastropod host. The number of M. piriformes metacercariae increased in larger hosts. The 3 species differed in the number of sporocysts and (meta)cercariae per sporocyst within the gastropod but not in the within-host volume of parasites. Variation in host exploitation and life history appeared adaptive for transmission to the next host.