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.     

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.     

Molecular link of different stages of the trematode host of Neorickettsia risticii to Acanthatrium oregonense

Neorickettsia risticii , the obligatory intracellular bacterium that causes Potomac horse fever, has been detected in various developmental stages of digenetic trematodes in the environment. Neorickettsia risticii -infected gravid trematodes were identified as Acanthatrium oregonense , based on morphologic keys. However, whether immature trematodes harbouring N. risticii are also A. oregonense was unknown. The objective of this study was to infer the life cycle of N. risticii -positive trematode hosts and transstadial transmission of the bacterium by molecularly characterizing the relationship among adult and immature stages of trematodes confirmed infected with N. risticii . Sequences of 18S ribosomal RNA genes up to 1922 bp in size were obtained from infected adult gravid trematodes, sporocysts and cercariae, and metacercariae. The sequences from the different immature stages of trematode are closely related to those of adult trematodes, some with 100% sequence identity; thus, they likely are life stages of A. oregonense . Comparisons with known 18S ribosomal RNA gene sequences of other digenetic trematodes indicated that all tested stages of the N. risticii -positive trematodes belong to the family Lecithodendriidae, supporting the morphological identification.     

The life history of Sanguinicola klamathensis

The life history of the trematode blood fluke, $\text{Sanguinicola klamathensis}$ was studied using experimentally infected cutthroat trout ($\text{Salmo clarki}$) and by examining wild salmonid populations. This study was carried out at the Hagerman National Fish Hatchery, Idaho, during 1971–1973. Ova, miracidia, sporocysts, cercariae, immature flukes, and adult flukes were measured, described, and photographed. A life cycle for the blood fluke is presented.     

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.     

Invaders of an invader - Trematodes in Potamopyrgus antipodarum in Poland

The subject of the following study was the natural and experimental invasion of trematode larvae in Potamopyrgus antipodarum from Bory Tucholskie National Park (Poland). Only one out of the 14,908 dissected specimens had oval sporocysts and mature cercariae of fish fluke, which belongs to the Sanguinicolidae family. It is the first recorded case in the European population of P. antipodarum living in inland water. The experimental study showed the possibility of native metacercariae (Echinostoma revolutum, Echinoparyphium aconiatum and Hypoderaeum conoideum) settlement in those immigrant snail species; however, exposure to parasites resulted in an increase in snail mortality. The three out of six used cercariae species were able to transform into metacercariae in P. antipodarum as in the second intermediate host, but the exposure to parasitic larvae of four of the used species resulted in an increase in snails’ mortality. It may suggest that not only metacercariae settlement but also the attack of cercariae (Rubenstrema opisthovitellinum at a temperature of 22 °C) affected the low survival of experimental snails in comparison to control animals. The subject of discussion presented in this paper is also the hypothesis on probable effect of the interaction between P. antipodarum and native snail species (as a source of invasive larvae of parasites) living in the same habitat.     

Activity of detoxifying and antioxidant enzymes in the pond snail <Emphasis Type="Italic">Lymnaea stagnalis</Emphasis> (Gastropoda: Pulmonata) during invasion by trematode cercariae

A comparative analysis of changes of detoxifying and antioxidant enzyme activities was carried out in the body homogenate of the pond snail Lymnaea stagnalis. Molluscs with the shell size of 4–6 mm infested with cercariae of one (Echinopharipjium aconiatum, E. recurvatum or Moliniella anceps) or two (E. aconiatum + M. anceps or E. aconiatum + E. recurvatum or M. anceps + E. recurvatum) trematode species. It has been reveled that activities of detoxifying and antitoxidant enzymes in the mollusc Lymnaea stagnalis body change at invasion with trematodes and that the character of the changes depends on the stage of development of the trematodes in the host body, the variant of infestation (monoinvasion or mixed infestation), and the species of the parasite. The first 2 h after penetration of the trematode cercariae into the mollusc tissues is accompanied by an increase of activities of the detoxifying and antioxidant enzymes. During the long coexistence of metacercariae in the host body (no less than for 13 days), activities of non-specific esterases and glutathione-S-transferase decrease, while the superoxide dismutase activity increases.     

The life cycle of Gyliauchen volubilis Nagaty, 1956 (Digenea: Gyliauchenidae) from the Red Sea

Although nothing is known about gyliauchenid life cycles, molecular phylogenetic studies have placed the Gyliauchenidae Fukui, 1929 close to the Lepocreadiidae Odhner, 1905. The gyliauchenid Gyliauchen volubilis Nagaty, 1956 was found in the intestine of its type-host, Siganus rivulatus, a siganid fish permanently resident in a lagoon within the mangrove swamps on the Egyptian coast of the Gulf of Aqaba. Larval forms of this trematode (mother sporocysts, rediae and cercariae) were found in the gonads and digestive gland of Clypeomorus clypeomorus (Gastropoda: Cerithiidae), a common snail in the same lagoon. So, this life cycle of G. volubilis was elucidated under natural conditions: eggs are directly ingested by the snail; mother sporocysts and rediae reach their maturity 3-6 and 11-13 weeks post-infection; rediae contain 23-29 developing cercariae; fully developed cercariae are gymnocephalus, without penetration glands, emerge from the snail during the night 16-18 weeks post-infection and rapidly encyst on aquatic vegetation (no second intermediate host); encysted metacercariae are not progenetic; 4-day-old metacercariae encysted on filamentous algae fed to S. rivulatus developed into fully mature worms 6-8 weeks post-infection. The cycle was completed in about 26 weeks and followed one of the three known patterns of lepocreadiid life cycles, and except for the gymnocephalus cercariae, the other larval stages are very similar to those of lepocreadiids. Generally, the life cycle of G. volubilis implicitly supports the phylogenetic relationship of Gyliauchenidae and Lepocreadiidae inferred from molecular phylogenetic studies.     

Asexual reproduction in Pygospio elegans claparède (Annelida, Polychaeta) in relation to parasitism by Lepocreadium setiferoides (Miller and Northup) (Platyhelminthes, Trematoda)

Life-history theory predicts that parasitized hosts should alter their investment in reproduction in ways that maximize host reproductive success. I examined the timing of asexual reproduction (fragmentation and regeneration) in the polychaete annelid Pygospio elegans experimentally exposed to cercariae of the trematode Lepocreadium setiferoides. Consistent with adaptive host response, polychaetes that became infected by metacercariae of trematodes fragmented sooner than unexposed controls. Parasites were not directly associated with fission in that exposed polychaetes that did not become infected also fragmented earlier than controls. For specimens of P. elegans that were not exposed to trematodes, new fragments that contained original heads were larger than those that contained original tails, whereas original head and tail fragments did not differ in size for infected polychaetes. In infected specimens, metacercariae were equally represented in original head and tail fragments and were more likely to be found in whichever fragment was larger. Despite early reproduction, parasitism was still costly because populations of P. elegans exposed to parasites were smaller than controls when measured 8 weeks later and because exposure to cercariae reduced survivorship of newly divided polychaetes. Taken together, my results suggest that early fragmentation is a host response to minimize costs associated with parasitism.     

A brachylaimid trematode from marsupial mice with observations on its life cycle

A species of digenetic trematode, Brachylaime antechini (Family Brachylaimidae), is described from adult worms recovered from the intestine and rectum of two species of marsupial mice, Antechinus stuartii(10 of 56 infected) and Antechinus swainsonii (2 of 5 infected). On experimental evidence unencysted metacercariae from the kidney of a terrestrial gastropod, Strangesta capillacea, are considered to be larval stages of Brachylaime antechini. Miracidia, sporocysts and cercariae have not been recovered, but circumstantial evidence suggests that Strangesta capillacea fulfils the role of first intermediate host. Brachylaime antechini most closely resembles Brachylaime chiapensis, a parasite of deer mice in Mexico.     

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.     

Metacercarial dispersion and intracellular parasitism in a strigeid trematode

Combes C. and Nassi H. 1977. Metacercarial dispersion and intracellular parasitism in a strigeid trematode. International Journal for Parasitology7: 501–503. The life cycle of Apatemon graciliformis Szidat, 1928 (Trematoda, Strigeidae), a parasite of Biorrphalaria glabrata in Guadeloupe, involves a novel mode of transmission, experimentally demonstrated, between the second intermediate host and the definitive host. The furcocercariae penetrate gravid females of the ovoviviparous fish, Poecilia reticulata, and develop into metacercariae in vitelline vesicles of the embryos where they encyst a short time before parturition. The young guppies are born infected with 1–3 metacercariae. It is considered that young infected fish are more prone to predation by the definitive host, thereby increasing the probability of the cycle being completed. Domestic ducks have been experimentally infected with these metacercariae. If cercariae penetrate non-gravid P. reticulata, they enter the oocytes; this represents a phase of intracellular parasitism.     

The life-cycle of Helicometra gibsoni n. sp. (Digenea: Opecoelidae)

The life-cycle of Helicometra gibsoni n. sp., an opecoelid trematode of marine fishes, is elucidated and the life-history stages are described. Natural infections with the cercariae, which are typically opecoelid in many respects but characterised by having very long, extensile tails, were found in the intertidal snail Anachis terpsichore collected from the Lawson's Bay Coast, Bay of Bengal. Metacercariae were found in the thoracic muscles of the shooting shrimp Alphaeus malabaricus as prominent, reddish-brown, oval cysts. Laboratory experiments demonstrated that 14 days are required for the development of cercaria into the infective metacercarial stage in shrimps. Natural infections with the adult fluke were found in Scorpaenopsis cirrhosus. Therapon jarbua served as an experimental host. Fourteen-day-old metacercariae fed to T. jarbua developed into egg-producing adults in 40–43 days. Intra-specific variations noted in the flukes obtained from natural and experimental infections are presented. H. fasciata of Madhavi (1975) is regarded as a synonym of H. gibsoni.     

Molecular identification of larval bucephalids, Prosorhynchoides ozakii and Parabucephalopsis parasiluri , infecting the golden mussel, Limnoperna fortunei , by PCR-RFLP

A polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) technique was developed for the molecular identification of 2 introduced bucephalid trematodes, Prosorhynchoides ozakii and Parabucephalopsis parasiluri . The method was applied for sporocysts and cercariae obtained from the golden mussel Limnoperna fortunei collected in the Uji River, Japan. The PCR-RFLP method showed that L. fortunei is the intermediate host of both trematode species. The present study thus recognizes the risk of L. fortunei , an invasive molluscan species, as a potential host for pathogenic trematodes.     

Crepidula fornicata is not a first intermediate host for trematodes: who is?

Trematode larvae must generally invade a molluscan intermediate host, usually a gastropod, before they can reach reproductive maturity in another definitive host. The research literature to date has focused almost exclusively on the documented specificity between particular trematode species and particular molluscan hosts; little attention has been paid to gastropod species that do not appear to serve as hosts. We sampled Rhode Island and Massachusetts populations of the marine gastropod Crepidula fornicata to determine whether this widespread species serves as a first intermediate host for trematodes. We also sampled from the same habitat populations of Littorina littorea and Ilyanassa obsoleta, gastropods known to serve as first intermediate hosts for several trematode species. All individuals were examined by dissection for the presence of sporocysts, rediae, or developing cercariae. Although 4-28% of L. littorea (N=112) and I. obsoleta (N=84) were infected by larvae of at least one trematode species, no individuals of C. fornicata sampled from the same locations were so infected (N=136). A survey of the Biological Abstracts computer database indicates that snails in only about 10% of marine gastropod families are known to serve as first intermediate hosts for trematodes. We suggest that more attention be paid to marine gastropods that appear not to be infected by trematode miracidia. Such species may productively serve as new models for understanding trematode host specificity and gastropod resistance to infection.     

The distribution and incidence of larval trematodes in the freshwater fauna of the Wentloog level, South Wales

The Wentloog level, in South Wales, is a low-lying coastal plain dissected by a network of drainage channels. The latter contain a rich aquatic invertebrate fauna which harbour a wide range of larval digenetic trematodes. Few of the host species examined were not infected with larval trematodes. Miracidia together with their associated sporocysts, rediae and cercariae were more host specific than metacercariae but many of the miracidia which developed in pulmonate molluscs could do so in more than one genus. Metacercarial host specificity is less rigid, and usually species are only restricted to members of one phylum although several were found which could develop in two or more phyla. Most larval stages showed some host preference when they occurred in several host species and this was attributed to ecological or physiological factors or to mechanical barriers. Seasonal variation of infection rate occurs in all larval stages: infection with developing cercariae showed peaks during June and August, but metacercarial infection rates varied according to the host. In molluscs there may be two peaks of infection with metacercariae (as in the cercarial stages), but for many arthropods infections show a gradual increase through the year. The factors mainly responsible for these seasonal changes are considered to be the life-cycle of the intermediate hosts and the environmental temperature, the latter acting on the rate of development of the trematodes. Rainfall, and patterns of egg production of adult trematodes in the definitive hosts are also important.     

Relationship between Snail Population Density and Infection Status of Snails and Fish with Zoonotic Trematodes in Vietnamese Carp Nurseries

Background

Fish-borne zoonotic trematodes (FZT) are a food safety and health concern in Vietnam. Humans and other final hosts acquire these parasites from eating raw or under-cooked fish with FZT metacercariae. Fish raised in ponds are exposed to cercariae shed by snail hosts that are common in fish farm ponds. Previous risk assessment on FZT transmission in the Red River Delta of Vietnam identified carp nursery ponds as major sites of transmission. In this study, we analyzed the association between snail population density and heterophyid trematode infection in snails with the rate of FZT transmission to juvenile fish raised in carp nurseries.

Methodology/Principal Findings

Snail population density and prevalence of trematode (Heterophyidae) infections were determined in 48 carp nurseries producing Rohu juveniles, (Labeo rohita) in the Red River Delta area. Fish samples were examined at 3, 6 and 9 weeks after the juvenile fish were introduced into the ponds. There was a significant positive correlation between prevalence of FZT metacercariae in juvenile fish and density of infected snails. Thus, the odds of infection in juvenile fish were 4.36 and 11.32 times higher for ponds with medium and high density of snails, respectively, compared to ponds where no infected snails were found. Further, the intensity of fish FZT infections increased with the density of infected snails. Interestingly, however, some ponds with no or few infected snails were collected also had high prevalence and intensity of FZT in juvenile fish. This may be due to immigration of cercariae into the pond from external water sources.

Conclusions/Significance

The total number and density of potential host snails and density of host snails infected with heterophyid trematodes in the aquaculture pond is a useful predictor for infections in juvenile fish, although infection levels in juvenile fish can occur despite low density or absence infected snails. This suggests that intervention programs to control FZT infection of fish should include not only intra-pond snail control, but also include water sources of allochthonous cercariae, i.e. canals supplying water to ponds as well as snail habitats outside the pond such as rice fields and surrounding ponds.     

Gymnophallid digenean Parvatrema duboisi uses Manila clam as the first and second intermediate host

To identify the metacercariae of a gymnophallid trematode in the Manila clam Ruditapes philippinarum from the Ariake Sea, experimental infection and molecular analysis were conducted. Based on the morphology of adult worms obtained from experimentally infected mice, the parasite was identified as Parvatrema duboisi. Comparison of internal transcribed spacer (ITS) region of ribosomal DNA (rDNA) sequences for metacercariae and sporocysts from Manila clams and adult worms collected from wild wigeon Anas penelope showed minor differences ranging from 0 to 0.8%. These data strongly suggest that in the Ariake Sea, the parasite has a lifecycle using the Manila clam as the first and second intermediate hosts and wigeon as the definitive host.     

An empirical model of the optimal timing of reproduction for female amphipods infected by trematodes

Life-history theory predicts that hosts should reproduce when first infected by parasites if hosts are capable and if parasites have a lower cost on current than on future reproduction of hosts. We constructed an empirical model to explore fitness of females of the intertidal amphipod Corophium volutator that reproduced soon versus long after infection by the trematode Gynaecotyla adunca. For uninfected females, the optimal time to reproduce was at their maximum body length. However, for females infected by low or high intensities of trematode metacercariae, reproductive potential (realized fecundity) was highest for females that mated immediately after becoming infected. Even after removing a high cost of delaying reproduction for infected amphipods (high likelihood of depredation by sandpipers, which are final hosts of G. adunca), realized fecundity remained highest if reproduction occurred immediately following infection by trematodes. Results from our model support the view that early reproduction of female amphipods following infection by G. adunca is an adaptive life-history response to parasitism.     

Occurrence of a diploid type and a new first intermediate host of a human lung fluke, Paragonimus westermani, in Korea

The biology, chromosome number, and karyotype of a lung fluke, Paragonimus westermani (Kerbert, 1878) collected in Haenam, Haenam-gun Chollanam-do, Korea were analyzed. We compared the size of metacercariae from Haenam with those taken from a crayfish collected at Youngam, Youngam-gun, Chollanam-do, Korea. The mean length of P. westermani metacercariae from Haenam was 300.3 microm and that from Youngam was 362.0 microm. Adult worms were recovered from the lungs of experimentally infected dogs. The mean egg sizes obtained from adult flukes were 72.1 x 46.8 microm from Haenam and 93.5 x 54.2 microm from Youngam. Semisulcospira tegulata collected in the Youngam area were found to be infected with cercariae of P. westermani, one of the snail-borne human lung fluke trematodes in Korea. Of 4218 snails studied, 5 (0.12%) harbored P. westrermani larvae. This is the first report of S. tegulata serving as the initial intermediate host of P. westermani. The chromosome numbers of P. westermani from Haenam and Youngam were 2n = 22 and 3n = 33. The diploid type of P. westermani has not been previously reported in Korea.