Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity

Larval helminths often share intermediate hosts with other individuals of the same or different species. Competition for resources and/or conflicts over transmission routes are likely to influence both the association patterns between species and the life history strategies of each individual. Parasites sharing common intermediate hosts may have evolved ways to avoid or associate with other species depending on their definitive host. If not, individual parasites could develop alternative life history strategies in response to association with particular species. Three sympatric species of helminths exploit the amphipod Paracalliope fluviatilis as an intermediate host in New Zealand: the acanthocephalan Acanthocephalus galaxii, the trematode Microphallus sp. and the progenetic trematode Coitocaecum parvum. Adult A. galaxii and C. parvum are both fish parasites whereas Microphallus sp. infects birds. We found no association, either positive or negative, among the three parasite species. The effects of intra- and interspecific interactions were also measured in the trematode C. parvum. Both intra- and interspecific competition seemed to affect both the life history strategy and the size and fecundity of C. parvum. Firstly, the proportion of progenesis was higher in metacercariae sharing their host with Microphallus sp., the bird parasite, than in any other situation. Second, the intensity of intraspecific competition apparently constrained the ability of metacercariae to adopt progenesis and limited both the growth and egg production of progenetic individuals. These results show that the life history strategy adopted by a parasite may be influenced by other parasites sharing the same host.     

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.     

Morphological observations of Echinochasmus japonicus cercariae and the in vitro maintenance of its life cycle from cercariae to adults

The cercaria morphology of Echinochasmus japonicus was investigated using light and scanning electron microscopy. Cercariae, liberated from naturally infected snails (Parafossarulus manchouricus), had ovoid bodies and diminutive tails. The cercaria tegument was covered with minute spines. Four type II sensory papillae were observed on the dorsal side of the oral sucker, and type I papillae were distributed on the dorsal tegument surfaces. When cercariae were kept in the same bath as the freshwater fish, Pseudorasbora parva, which were free from trematode infections, parasites encysted only in the gills of fishes at day 4 postinfection (PI). The outermost metacercaria wall was fully formed in host tissues at day 7 PI. Adult worms were recovered from the intestines of rats, chicks, and ducks 28 days after experimental exposure to metacercariae. The head crown of the adult was armed with 24 collar spines, which were interrupted dorsal to the oral sucker, and the species was identified as E. japonicus.     

Migration, site selection, and development of Ornithodiplostomum sp. metacercariae (Digenea: Strigeoidea) in fathead minnows (Pimephales promelas)

The metacercarial stage of trematodes is typically considered an encysted, developmentally quiescent, resting stage. Yet the metacercariae of some species of strigeoid trematode undergo extravagant development within specific tissues of their second intermediate host. Our understanding of patterns of migration, site selection and development of these types of metacercariae is known for only a few species. In this study, we characterize the invasion and development of Ornithodiplostomum sp. metacercariae in their second intermediate host, the fathead minnow, Pimephales promelas. Diplostomules completed their migration into the abdominal cavity between 15 min and 48 h p.i. Most diplostomules migrated along muscular and connective tissue then penetrated the peritoneal lining of the abdominal cavity en route to the liver or pancreas. Alternatively, some diplostomules migrated within the host’s circulatory system, including the heart and arteries of the hepatic portal system. Metacercarial development in the liver and pancreas involved distinct growth, encystment and consolidation phases. Metacercarial volume increased 15-fold between 48 h and 4 weeks p.i., presumably due to absorptive and/or ingestive feeding activities within host tissues. By 2 weeks p.i., metacercariae were enveloped within a cyst wall and they were found loosely attached to the surfaces of internal tissues or unattached within the body cavity. These results emphasize the complex nature of metacercarial migration and growth and demonstrate that their growth and encystment phases occur within different habitats within their intermediate hosts.     

Carbohydrate Mimicry of the Parasite in the <Emphasis Type="Italic">Himasthla elongata</Emphasis> (Trematoda: Echinostomatidae)—<Emphasis Type="Italic">Littorina littorea</Emphasis> (Mollusca: Prosobranchia) System

Using labeled lectins, a comparative study of the surface of tegument of Himasthla elongata at different stages of development cycle (daughter rediae, cercariae, and metacercariae) and glycocalyx of plasma membranes of hemocytes of molluscs Littorina littorea and Mytilus edulis that are the first and second intermediate hosts of this trematode species, respectively, has been carried out. It is found that in the course of the development cycle of the parasite there occurs a change of the set of terminal sacharides of the glycocalyx of the H. elongata tegument surface as well as differences are revealed in the pattern of binding of three out of five tested lectins with hemocytes of blue mussel and periwinkle. At the same time, the presence of similar carbohydrate determinants on the surface of hemocytes of L. littorea and daughter rediae of H. elongata is shown. The established similarity in composition of glycocalyx of hemocytes of the mollusc and the trematode parthenitae is, most likely, a result of coevolution of the parasite and the host and is of the adaptive nature. Use of the mechanism of the carbohydrate mimicry by parthenitae of this species allows them to avoid attacking by effector cells of the internal defense system of the mollusc-host.__________Translated from Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, Vol. 41, No. 2, 2005, pp. 114–118.Original Russian Text Copyright © 2005 by Iakovleva, Gorbushin.     

From first to second and back to first intermediate host: the unusual transmission route of Curtuteria australis (Digenea: Echinostomatidae)

The trematode Curtuteria australis uses the whelk Cominella glandiformis as first intermediate host and the cockle Austrovenus stutchburyi as second intermediate host before maturing in shorebirds. The whelk also happen to be an important predator of cockles on intertidal mudflats. In this study we show that whelks can act as temporary paratenic hosts for the trematode. A single whelk feeding on 1 cockle can ingest large numbers of metacercariae, which remain within the whelk for 1-3 days before passing out in feces. The viability of these metacercariae assessed as the percentage capable of successfully excysting under conditions simulating those inside a bird's digestive tract, is lower after passage through a whelk (48%) than before (59%). Still, given that shorebird definitive hosts prey on whelks as well as cockles, survival inside the whelk allows C. australis to complete its life cycle: overall, though, whelk predation is likely to be an important sink for the trematode population. To our knowledge, this is the first report of a trematode using a snail as both first intermediate host and paratenic host, offering an alternative transmission route for the parasite as a result of the unusual trophic relationships of its hosts.     

Spatial variation in parasite-induced mortality in an amphipod: shore height versus exposure history

Characterizing the causes of spatial and temporal variation in parasite-induced mortality under natural conditions is crucial to better understanding the factors driving host population dynamics. Our goal was to quantify this variation in the amphipod Paracalliope novizealandiae, a second intermediate host of the trematode, Maritrema novaezealandensis. If infection and development of trematode metacercariae are benign, we expected mature metacercariae to accumulate within amphipods inhabiting high infestation areas. In field samples, intensity levels of mature metacercariae decreased linearly when amphipods harbored >5 immature metacercariae. This finding is consistent with the hypothesis that the parasite can be detrimental at high intensities of infection. Short-term field experiments showed that host survival also declines with the intensity of new infections and drops below 80% when early stage metacercariae reach 10 amphipod^?1. However, parasite effects varied over space and time. High-shore amphipods suffered an increased risk of infection in the summer and a lower likelihood of survival: there was a 10–30% decrease in survivorship for any given infection intensity at high- versus low-shore locations. We also tested for differences in the susceptibility of naive and exposed populations using transplant experiments, and found that naive amphipods acquired greater parasite loads (on average, 4.7 vs. 2.8 metacercariae amphipod^?1). Because survival decreases rapidly with infection intensity of both early- and late-stage metacercariae, naive populations would suffer considerably if the parasite were to increase its range. Our results indicate that trematode infections cause high mortality in amphipods during summer months under natural conditions, and emphasize that the effects of parasitism vary at local spatial scales and with exposure history.     

Infection by Paragonimus miyazakii cercariae of their crab hosts, Geothelphusa dehaani, by percutaneous penetration

Identification of the transmission routes of the trematode parasite Paragonimus miyazakii into different intermediate hosts would help to explain the natural distribution of the parasite. The behavior of P. miyazakii cercariae released from snails into water and in the presence of a living host or a whole crab leg was observed by stereoscopic or light microscopy at various times after exposure started. On encountering a crab leg or cheliped, the cercariae became entangled with the host via mucoid strands arising from the cercariae. Within 3 hr, most cercariae were attached to the host; cuticular penetration took between 5 and 6 hr, after which cercariae were found in the cavity of the leg. Crabs examined 102-149 days after exposure to the cercariae contained fully developed metacercariae. The metacercariae were fed to 2 rats, and the rats were killed 83 or 111 days later. Some of the metacercariae had reached maturity in the rats. That the cercariae were not ingested by the crabs but penetrated the crabs percutaneously (through hard as well as soft tissue) means that transmission can occur even in areas in which crabs and the host snails do not coexist, as they would if the usual route were oral (when the crabs ate infected snails).     

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.     

Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda)

Because resistance to parasites usually has a cost for host species, it is theoretically expected that, in case of multi-infection, host immune responses should vary according to the levels of parasite pathogenicity. The crustacean gammarid Gammarus aequicauda is the second intermediate host of 4 trematode species. Three of these parasites always encyst in the abdomen of gammarids and have no particular effect on the host. However, 1 of these species is sometimes able to encyst in the cerebroid ganglia of the gammarid and strongly alter its behavior in a way that increases its predation risk by aquatic birds, the definitive hosts. In accordance with the hypothesis that the level of parasite pathogenicity influences the likelihood and the degree of host reaction, cases of melanization in our gammarid collection almost exclusively concern the cerebral metacercariae. Our results also indicate that this melanization is able to cancel the behavioral alterations induced by the parasite, suggesting that the cause of the manipulation is not the physical presence of metacercariae in the brain.     

Developmental and functional ultrastructure of Ornithodiplostomum ptychocheilus diplostomula (Trematoda: Strigeoidea) during invasion of the brain of the fish intermediate host, Pimephales promelas

We examined tegumental development of the diplostomulum of Ornithodiplostomum ptychocheilus, with respect to structural transformations that have functional relevance to the invasion, migration, and site establishment processes in the brain of the fish second-intermediate host, Pimephales promelas. Using a combination of brightfield, scanning electron microscopy (SEM), transmission electron microscopy (TEM), and confocal microscopy (CM), we demonstrated that the diplostomula become established in the outer region of the optic lobes within 24-48 hr of penetration and continue to grow and transform over a period of 4-14 days. During this period, the J-shaped body consists of 2 distinct regions: (1) a highly motile prosoma with distinctive tegumental spines and (2) an opisthosoma, the tegument of which is elaborated into a dense uniform layer of long, thin microvilli. The prosoma is alternately invaginated into and everted from the opisthosoma, thus constituting a protrusible proboscis. By day 14 postinfection (PI), the body has lost this bipartite structure and has taken on the uniformly flattened form characteristic of metacercariae. The transitory complex structure of the diplostomula appears to be well suited to burrowing through host tissues (primarily by action of the prosoma), followed by rapid dissociation of host tissue and nutrient accumulation (primarily by action of the opisthosoma) in preparation for metacercaria encystment.     

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.     

Increased abundance of snails and trematode parasites of <Emphasis Type="Italic">Fundulus heteroclitus</Emphasis> (L.) in restored New Jersey wetlands

The Hackensack Meadowlands District is a large heavily degraded, brackish marsh system in the urbanized northeastern region of New Jersey, USA. Six study sites were used, three of which were restored (Mill Creek, Skeetkill Creek and Vince Lombardi), and three others were unrestored (Richard DeKorte Park, Cedar Creek and Kingsland Creek). Highly significant differences were found with respect to snail abundance and gill parasite abundance. In the three restored sites, significantly more Littoridinops tenuipes were found, and Fundulus heteroclitus had significantly more digenean trematode metacercariae gill infections than at unrestored sites. As habitat quality improves following restoration, the number of suitable digenean trematode parasite hosts multiplies as substrate for benthic invertebrates (first intermediate host) increases and usage by other species, such as Fundulus spp. (second intermediate host), is encouraged, which then attracts more wading birds (definitive host). Though the restoration process enhances trophic complexity, including primary consumers (gastropods), secondary consumers (fish) and tertiary consumers (wading birds), and ultimately parasite diversity, restoration also helps facilitate parasite life cycles.     

Developmental and Phylogenetic Characteristics of Stellantchasmus falcatus (Trematoda: Heterophyidae) from Thailand

This study aimed to investigate the infection status, worm development, and phylogenetic characteristics of the intestinal trematode, Stellantchasmus falcatus. The metacercariae of S. falcatus were detected only in the half-beak (Dermogenus pusillus) out of the 4 fish species examined. Their prevalence was 90.0%, and the intensity of infection was 919 metacercariae on average. Worms were recovered from 33 (97.1%) of 34 chicks that were experimentally infected with 200 S. falcatus metacercariae each, and the average recovery rate was 43.0%. The body size and inner organs of S. falcatus quickly increased in the experimental chicks over days 1-2 post-infection (PI). In addition, ITS2 sequence data of this parasite were analyzed to examine the phylogenetic relationships with other trematodes using the UPGMA method. The results indicated that the ITS2 sequence data recorded from trematodes in the family Heterophyidae appeared to be monophyletic. This study concluded that D. pusillus serves as a compatible second intermediate host of S. falcatus in Thailand and that S. falcatus can develop rapidly in the experimental chicks. Data collected from this study can help to close the gap in knowledge regarding the epidemiology, biology, and phylogenetic characteristics of S. falcatus in Thailand.     

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.     

Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas)

Intensity-dependent development of Ornithodiplostomum ptychocheilus metacercariae was studied in fathead minnows (Pimephales promelas) exposed to 0, 20, or 120 cercariae. Subsamples of hosts were necropsied at 2-wk intervals to monitor parasite recruitment, growth, and time to encystment. The complex development of metacercariae within the cranium of minnows involved growth, encystment, and consolidation phases, each of which were affected by intensity. At the end of the growth phase, metacercariae from low-dose fish were 20% longer than those from high-dose fish and the latter took 2-4 wk longer to encyst. At the end of the postencystment consolidation phase (6-8 wk postinfection), the size of metacercariae decreased by approximately 50%. The rate of consolidation was slower in high-dose fish. Our results show that time, intensity, and temperature affect development of O. ptychocheilus. Because metacercariae development and differentiation are linked to infectivity, events occurring in intermediate hosts can potentially impact the structure and size of trematode suprapopulations.     

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.     

The combined influence of trematode parasites and predatory salamanders on wood frog (<Emphasis Type="Italic">Rana sylvatica</Emphasis>) tadpoles

Predators can have important impacts on host–parasite dynamics. For many directly transmitted parasites, predators can reduce transmission by removing the most heavily infected individuals from the population. Less is known about how predators might influence parasite dynamics in systems where the parasite relies on vectors or multiple host species to complete their life cycles. Digenetic trematodes are parasitic flatworms with complex life cycles typically involving three host species. They are common parasites in freshwater systems containing aquatic snails, which serve as obligate first intermediate hosts, and multiple trematode species use amphibians as second intermediate hosts. We experimentally examined the impact of predatory salamanders (Ambystoma jeffersonianum) and trematode parasites (Echinostoma trivolvis and Ribeiroia ondatrae) on short-term survival of wood frog tadpoles (Rana sylvatica) in 150-L outdoor pools. Two trematode species were used in experiments because field surveys indicated the presence of both species at our primary study site. Parasites and predators both significantly reduced tadpole survival in outdoor pools; after 6 days, tadpole survival was reduced from 100% in control pools to a mean of 46% in pools containing just parasites and a mean of 49% in pools containing just predators. In pools containing both infected snails and predators, tadpole survival was further reduced to a mean of 5%, a clear risk-enhancement or synergism. These dramatic results suggest that predators may alter transmission dynamics of trematodes in natural systems, and that a complete understanding of host–parasite interactions requires studying these interactions within the ecological framework of community interactions.     

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.