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.     

The Ultrastructure of the Daughter Sporocyst Tegument of Cercaria vaullegeardi Pelseneer (Digenea, Hemiuridae)

The body wall of the daughter sporocyst of Cercaria vaullegeardi Pelseneer, 1906 is unusual for a species without a birth pore in consisting of an outer anucleated, microvillous syncytial tegument and a cellular subtegument which lacks secretory cells. In contrast, most other known daughter sporocysts without birth pores have a nucleated region above the microvillous region of the tegument. The significance and functional aspects of this structure are discussed.     

Morphology and biology of cystophorous cercariae from the Bering sea]

Three new species of cystophorous cercariae, Cercaria appendiculata Pelseneer, 1906, C. octocauda Tschubrik, 1952 and C. saccocaudata Tschubrik, 1966, are described from the gastropod Tectonatica clausa (Broderip et Sowerby). C. saccocaudata is a larva of trematodes of the genus Lecithaster. The development of parthenites of this species carries out within one summer season. Parthenites of C. appendiculata and C. octocauda are capable to survive unfavourable winter conditions and produce cercariae in the next summer. The above three species were found to eject cercariae through the ejaculatory tube which is an important adaptation of chemiurids to the infection of the second intermediate hosts.     

Aerobic glucose metabolism in the digestive gland of Littorina saxatilis rudis (Maton) and in the daughter sporocysts of Microphallus similis (J?g.).

Experiments, some in vitro and some in vivo, with glucose-U-14C, acetate-U-14C, succinate-1,4-14C, pyruvate-U-14C and citrate-1,5-14C indicate that the digestive gland of Littorina saxatilis rudis and the daughter sporocysts of Microphallus similis aerobically catabolise glucose via an EMP pathway, a TCA cycle, phosphoenolpyruvate carboxylation and malate decarboxylation. The host and parasite have similar transamination and synthetic reactions and alanine as a major carbohydrate excretory product. Oxidative metabolism appears to be less efficient in the parasite than in the host.     

Helminth fauna of the yellow-legged gull Larus cachinnans in Galicia, north-west Spain

Thirty-six helminth species were found in 324 gulls examined during June 1994 to February 1996 from different localities of Galicia: 25 trematodes (Brachylaima sp., Brachylecithum microtesticulatum, Cardiocephaloides longicollis, Cryptocotyle lingua, Cryptocotyle concavum, Diplostomum spathaceum, Echinostephilla virgula, Galactosomum phalacrocoracis, Gigantobilharzia acotylea, Gymnophallus deliciosus, Gynaecotyla longiintestinata, Himasthla elongata, Himasthla quissetensis, Knipowitschiatrema nicolai, Levinseniella (Levinseniella) propinqua, Maritrema gratiosum, Maritrema linguilla, Microphallus primas, Microphallus similis, Ornithobilharzia canaliculata, Parorchis acanthus, Phagicola minuta, Psilostomum brevicolle, Renicola sp. and Stephanoprora denticulata), four cestodes (Alcataenia micracantha, Microsomacanthus ductilis, Tetrabothrius (Oriana) erostris and Wardium cirrosa), six nematodes (Anisakis simplex, Contracaecum rudolphii, Cosmocephalus obvelatus), Eucoleus contortus, Paracuaria adunca and Tetrameres (Tetrameres) skrjabini) and one acanthocephalan (Arhythmorhynchus longicollis). Tetrabothrius erostris was the most prevalent species (79.6%), followed by C. obvelatus (47.8%), C. lingua (37.4%), G deliciosus (30.9%), G. longiintestinata (22.8%), P. adunca (21.9%), B. microtesticulatum (17.6%), E. contortus (14.5%) and M. similis (9.3%). Microphallus similis was the dominant species, with a Berger-Parker index (BP) of 0.32, followed by T. erostris (BP=0.10). All species presented an aggregated dispersion except G. acotylea and G. phalacrocoracis, which showed a random dispersion. Species that seem to have the greatest predilection for specific sites along the intestine are: C. longicollis and A. micracantha (first third), Brachylaima sp., M. similis and G. longiintestinata (last third) and A. longicollis (second half). Eight species are known to be pathogenic to commercially important fish or molluscan species and several are pathogenic to humans.     

Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland

This study analyzed the influence of several abiotic and biotic variables on the distribution of digenetic trematode infections in a mudsnail, Hydrobia ventrosa, population inhabiting 12 ponds on the Melabakkar salt marsh in Iceland, the northwestern limits of the geographical distribution. Nine trematode species were found to infect the snail population, which included Microphallus pirum, Microphallus breviatus, Microphallus claviformis, Maritrema subdolum (Microphallidae), Cercaria Notocotylidae sp. 11 Deblock, 1980, C. Notocotylidae sp. 12 Deblock, 1980, C. Notocotylidae sp. 13 Deblock, 1980 (Notocotylidae), Cryptocotyle concavum (Heterophyidae), and Psilostomum brevicolle (Psilostomatidae). Correlations between biotic variables (snail density in the ponds and vegetation cover), abiotic variables (distance of each pond from the sea, pond elevation above chart datum, size, average depth, salinity, and some characters of the littoral zone and sediments), and trematode infections were analyzed. These variables indirectly affected the trematode infections because some determined how attractive the ponds were for the final hosts, which were various species of marine and shore birds. We propose that their habitat use and defecating habits are the main determinants of the trematode distribution in the area.     

Variations in the number of metacercariae in the daughter sporocysts of Microphallus pygmaeus (Trematoda: Microphallidae)

The daughter sporocystes of Microphallus pygmaeus from the snails of Littorina saxatilis and L. obtusata were investigated. The average quantity of metacercariae in sporocysts is influenced by host species, its syze and by the season. There are differences in the average number of larvae from parthenites of L. saxatilis, collected in the Barents and White seas.     

Effect of parasites on host adaptation to abiotic environmental factors: host-parasite relationship of trematode parthenites--mollusc system

This laboratory study examined the survival of extreme environmental conditions by the White Sea periwinkle Littorina saxatilis. Molluscs from localities with high and low prevalence of Microphallus piriformes, which is a representative of the "pygmaeus" group of digeneans (Microphallidae), were compared. These parasites have not a stage of free-living cercariae in their life cycle. Metacercariae mature inside the sporocysts parasitizing the molluscan host. No negative influence of infection was found on resistance of molluscs to prolonged desiccation and extremes of air and water temperature. On the contrary, significant lower mortality of high infected snails was observed in some experiments. Exposure to fresh water was the only treatment that caused more intensive mortality of high infected snails in comparison with low infected one. The results of the experiments were discussed taking into consideration the available data on mechanisms of molluscan resistance and features in the relationships of "pygmaeus" group sporocysts with the organism of molluscan host. It was emphasized that the wide spread opinion regarding the only negative influence of trematode infection on the resistance of infected molluscs should be revised.     

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.     

Influence of host age and sex on the helminth fauna of the yellow-legged gull (Larus michahellis) in Galicia (northwestern Spain)

We studied the influence of host age and sex on the helminth fauna of 324 Larus michahellis captured in different locations in the region of Galicia (northwestern Spain). Gulls were grouped into prefledglings, first-year immature birds, second- and third-year immature birds, and adults. Second-year, third-year, and adult birds were grouped by sex. Thirty-six helminth species were recorded. Total species richness and mean infracommunity species richness were both significantly lower for pre-fledglings than for the other age groups. Prevalence increased significantly with age for Brachylecithum microtesticulatum, probably reflecting changing feeding habits. Likewise, 8 species (Cardiocephaloides longicollis, Microphallus similis, Maritrema gratiosum, Gynaecotyla longiintestinata, Brachylecithum microtesticulatum, Himasthla elongata, Parorchis acanthus, and Renicola sp.) were absent or had very low prevalence in prefledglings. At least 5 of these 8 species are transmitted to gulls through ingestion of molluscs or crustaceans, which suggests that these types of prey are seldom fed to prefledglings. In Gymnophallus deliciosus, G. longiintestinata, and Cosmocephalus obvelatus, mean intensity, and in the latter case prevalence, declined with age, suggesting that protective immunity against these species increase with age. Only G. deliciosus, Microphallus similis, and G. longiintestinata presented significant differences between the sexes.     

Modification of the structure of penial glands in males of the intertidal molluscs Littorina saxatilis and L. obtusata under the influence of the infestation by trematode parthenites

Sporocycts of the "pygmaeus" microphallides (Microphallus piriformes) are localized in hepatopancreas and gonads of Littorina molluscs causing total parasitic castration. A histological study of penial glands in Littorina saxatilis and L. obtusata males infested with trematodes M. piriformes has been made. Copulatory organs of noninfested molluscs, molluscs after recent contamination (with not completely formed daughter sporocysts), and molluscs containing mature metacercariae inside daughter sporocysts were examined. Based on the data obtained, probable dynamics of the histological structure of infested glandular apparatus was established. It was shown, that the trematode infestation have an influence on the muscular and secretory parts of penial glands. The wall of the penial gland muscular capsule becomes more fine in infested L. saxatilis. On the contrary, this wall is vastly thicker in infested L. obtusata, as compared with noninfested individuals. Glandular cells of the molluscs' penial glands decreases the amount of granular secret in both species. In L. obtusata the number of secretory cells is shown to be reduced up to their total disappearance. The above pathological changes probably prevent normal function of penial glands.     

Redescriptions of two echinostomes from freshwater fishes,with comments on Singhia Yamaguti, 1958 and Caballerotrema Prudhoe, 1960 (Digenea: Echinostomatidae)

The type-species of Singhia and Caballerotrema (Digenea: Echinostomatidae), parasites of freshwater fishes which have previously been assigned to the subfamily Singhiinae Yamaguti, 1958, are redescribed. One of the specimens of the type-series of Caballerotrema brasiliense Prudhoe, 1960 was identified as C. aruanense Thatcher, 1980. C. arapaimense Thatcher, 1980 is considered a species inquirenda. Himasthla piscicola Stunkard, 1960 is transferred to Caballerotrema as C. piscicola n. comb. The generic diagnoses of Singhia and Caballerotrema are redefined and Singhia is re-allocated to the Echinostomatinae Looss, 1899, the Singhiinae becoming a synonym of the latter.     

New records of alien monogeneans from Lepomis gibbosus and Silurus glanis in Italy

The first geographical records of five alien monogeneans for Italy is reported. Four species have been detected from Lepomis gibbosus (Linnaeus, 1758): Actinocleidus recurvatus Mizelle et Donahue, 1944, Actinocleidus oculatus (Mueller, 1934), Urocleidus similis (Mueller, 1936) and Urocleidus dispar (Mueller, 1936); one species from Silurus glanis Linnaeus, 1758: Thaparocleidus vistulensis (Siwak, 1932) n. comb.     

Host partitioning by parasites in an intertidal crustacean community

Patterns of host use by parasites throughout a guild community of intermediate hosts can depend on several biological and ecological factors, including physiology, morphology, immunology, and behavior. We looked at parasite transmission in the intertidal crustacean community of Lower Portobello Bay, Dunedin, New Zealand, with the intent of: (1) mapping the flow of parasites throughout the major crustacean species, (2) identifying hosts that play the most important transmission role for each parasite, and (3) assessing the impact of parasitism on host populations. The most prevalent parasites found in 14 species of crustaceans (635 specimens) examined were the trematodes Maritrema novaezealandensis and Microphallus sp., the acanthocephalans Profilicollis spp., the nematode Ascarophis sp., and an acuariid nematode. Decapods were compatible hosts for M. novaezealandensis, while other crustaceans demonstrated lower host suitability as shown by high levels of melanized and immature parasite stages. Carapace thickness, gill morphology, and breathing style may contribute to the differential infection success of M. novaezealandensis and Microphallus sp. in the decapod species. Parasite-induced host mortality appears likely with M. novaezealandensis in the crabs Austrohelice crassa, Halicarcinus varius, Hemigrapsus sexdentatus, and Macrophthalmus hirtipes, and also with Microphallus sp. in A. crassa. Overall, the different parasite species make different use of available crustacean intermediate hosts and possibly contribute to intertidal community structure.     

Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis

There is a gap in our understanding of the relative and interactive effects of different parasite species on the same host population. Here we examine the effects of the acanthocephalan Acanthocephalus galaxii, an unidentified cyclophyllidean cestode, and the trematodes Coitocaecum parvum and Microphallus sp. on several fitness components of the amphipod Paracalliope fluviatilis, using a combination of infection surveys and both survival and behavioural trials. In addition to significant relationships between specific parasites and measures of amphipod survival, maturity, mating success and behaviour, interactions between parasite species with respect to amphipod photophilia were also significant. While infection by either A. galaxii or C. parvum was associated with increased photophilia, such increases were negated by co-infection with Microphallus sp. We hypothesize that this is due to the more subtle manipulative effect of A. galaxii and C. parvum being impaired by Microphallus sp. We conclude that the low frequency at which such double infections occur in our sampled population means that such interactions are unlikely to be important beyond the scale of the host individual. Whether or not this is generally true, implying that parasitological models and theory based on single parasite species studies do generally hold, requires cross-species meta-analytical studies.     

A comparative ultrastructural study of in vivo and in vitro derived adults of Microphallus similis

Davtes C. 1980. A comparative ultrastructural study of in vivo and in vitro derived adults of Microphallus similis. International Journal for Parasitology10: 217–266. The ultrastructure of in vitro cultured adults of Microphallus similis was examined by TEM and SEM and compared to that of metacercariae and in vivo grown adults. In cultured flukes the most conspicuous abnormalities were observed in secretory cells, especially those of the tegument, digestive caecum, forebody glands and vitellaria. In the tegumental cells and the forebody gland cells, the secretory granules appeared to lose some of their contents within the cell bodies suggesting that there may be some defect in the transport and/or packaging of secretory granules in vitro. In the vitellaria of cultured flukes some of the granules lost their characteristic appearance, becoming ragged in outline and very electrondense. The premature tanning of the vitelline secretions within the vitellaria is correlated with abnormal egg production in vitro. The caecal cells of cultured flukes differed from those of the metacercaria and the normal adult in several important respects which suggested that their function was probably impaired.     

Evolutionary relationships within 'pygmaeus' group microphallids using genetic analysis and scanning electron microscopy

There are four species of 'pygmaeus' microphallids, namely Microphallus pygmaeus, M. piriformes, M. pseudopygmaeus and M. triangulatus (Trematoda: Microphallidae) which are parasites of marine birds and their sporocysts give rise to transmissible metacercariae inside littoral gastropods (mostly littorines). Universally primed polymerase chain reaction (UP-PCR) showed no apparent pattern between genetic diversity of the metacercariae as estimated by genomic banding profiles and their geographic region or molluscan host species. At the same time UP-PCR product cross-hybridization showed that M. pseudopygmaeus and M. triangulatus are genetically very similar, indicating that these taxa represent one species complex. In contrast, M. pygmaeus and M. piriformes are genetically well separated from each other and also from the pseudopygmaeus-triangulatus complex. Scanning electron microscopy of ventral spines, and analyses of spine angles and the number of teeth per spine, showed that all species differed significantly from one another. It was concluded that M. piriformes represents the original western member of the 'pygmaeus' group. Microphallus pygmaeus probably diverged from M. piriformes as it progressively specialized for sea duck final hosts. Microphallus pseudopygmaeus and M. triangulatus diverged from each other and the piriformes-pygmaeus ancestral line relatively recently. Microphallus pseudopygmaeus specialized for adoption of a wide range of gastropod host species and M. triangulatus developed morpho-functional specialization associated with final host exploitation.     

Microphallus koreana n. sp. (Trematoda: Microphallidae) transmitted by a marine crab, Macrophthalmus dilatatus

Microphallus species occur primarily as intestinal parasites of birds and mammals, and metacercariae of a new species belonging to this genus have been discovered from the crab, Macrophthalmus dilatatus, in the Republic of Korea. The metacercaria of this fluke was round with 2 thick walls, and the excysted one had mature genital organs. The adult flukes recovered from experimentally infected chicks had numerous intrauterine eggs, well-developed pars prostatica, widely bifurcating ceca, and prominent uterine bulge. After observing internal structures, it was concluded that this species is different from any other known Microphallus spp. Based on the morphology of metacercariae and adult flukes, we describe this specimen as a new species, Microphallus koreana n. sp.     

Impact of trematode parasitism on the fauna of a North Sea tidal flat

The impact of larval trematodes on the fauna of a North Sea tidal flat is considered at the individual and at the population level, depicting the digenean parasites of the common periwinkle,Littorina littorea, and their life cycles, as an example. On the German North Sea coast,L. littorea is first intermediate host for 6 larval trematodes representing 6 digenean families —Cryptocotyle lingua (Heterophyidae),Himasthla elongata (Echinostomatidae),Renicola roscovita (Renicolidae),Microphallus pygmaeus (Microphallidae),Podocotyle atomon (Opecoelidae) andCercaria lebouri (Notocotylidae). All exceptP. atomon utilize shore birds as final hosts; adultP. atomon parasitize in the intestine of teleosts, mainly pleuronectid flatfish. Second intermediate hosts ofC. lingua are various species of fish; the cercariae ofH. elongata encyst in molluscs and polychaetes, those ofR. roscovita in molluscs;M. pygmaeus has an abbreviated life cycle;C. lebouri encysts free on solid surfaces; and the fish trematodeP. atomon utilizes benthic crustaceans, mainly amphipods, as second intermediate hosts. On the tidal flats of the Königshafen (Sylt), up to 77% of the periwinkles have been found to be infested by larval trematodes. Maximum infestations in individual samples were 23% forC. lingua, 47% forH. elongata and 44% forR. roscovita. The digeneans cause complete parasitic castration of their carriers and hence exclude a considerable proportion of the snails from the breeding population. Infestation reduces the longevity of affected hosts, and size-related, trematode-induced differential mortality causes changes in the normal size-frequency distribution of individual snail-age classes. Young flatfishPleuronectes platessa from the Königshafen are 100% infested with metacercariae ofC. lingua. Heavy infestation of the gills causes obstruction of blood vessels and respiratory impairment; metacercariae in the eyes and optic nerves cause visual and neurological disturbances. A single metacercaria is sufficient to kill a larval fish.Mytilus edulis andCardium (Cerastoderma) edule are 100% infested with metacercariae ofH. elongata. Heavy infestation impairs the byssus-thread production in mussels and affects the burrowing ability of cockles. Longevity and resistance to environmental — particularly thermal — stress are reduced in bivalves infested withH. elongata andR. roscovita. There is evidence that, in the study area, population size and age composition of the molluscs discussed are (indirectly) controlled by trematode parasites employing sea birds as final hosts, rather than directly by the predatory activities of these birds.