Effects of ultraviolet radiation on the transmission process of an intertidal trematode parasite

The transmission of parasites takes place under exposure to a range of fluctuating environmental factors, one being the changing levels of solar ultraviolet radiation (UVR). Here, we investigated the effects of ecologically relevant levels of UVR on the transmission of the intertidal trematode Maritrema novaezealandensis from its first intermediate snail host (Zeacumantus subcarinatus) to its second intermediate amphipod host (Paracalliope novizealandiae). We assessed the output of parasite transmission stages (cercariae) from infected snail hosts, the survival and infectivity of cercariae, the susceptibility of amphipod hosts to infection (laboratory experiments) and the survival of infected and uninfected amphipod hosts (outdoor experiment) when exposed to photo-synthetically active radiation only (PAR, 400-700 nm; no UV), PAR+UVA (320-700 nm) or PAR+UVA+UVB (280-700 nm). Survival of cercariae and susceptibility of amphipods to infection were the only two steps significantly affected by UVR. Survival of cercariae decreased strongly in a dose-dependent manner, while susceptibility of amphipods increased after exposure to UVR for a prolonged period. Exposure to UVR thus negatively affects both the parasite and its amphipod host, and should therefore be considered an influential component in parasite transmission and host-parasite interactions in intertidal ecosystems.     

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 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.     

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.     

Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario

Agricultural activity and landscape features have previously been associated with diversity and prevalence of trematode species in amphibian second intermediate hosts. In this study, the density, diversity, and size of snail first intermediate hosts, and the diversity and prevalence of their trematode species, were assessed in 2 types of ponds, i.e., those adjacent to cornfields and those from the same region in southwestern Ontario that were adjacent to nonagricultural settings. Species of trematodes included, but were not restricted to, those that are known parasites of larval and adult frogs. We also assessed landscape factors likely to influence use by definitive hosts. Presence of the herbicide atrazine in ponds was measured to check that ponds adjacent to agriculture had potential to be affected by agricultural runoff. Both snail size and the proportion of snails releasing cercariae were greater in nonagricultural ponds, contrasting with a previous finding of lower trematode infection in tadpoles from nonagricultural ponds. Percentage of forest cover was associated with prevalence of certain trematode species, but not with estimates of combined prevalence. Absence of relations of trematode prevalence to measures of road density also contrasted with previous studies. We interpret our results in light of how agricultural activity might influence trematode viability, snail growth, and use by wildlife definitive hosts, independently of landscape factors.     

Life cycles of the trematode species Azygia hwangtsiytii and A. robusta (Azygiidae) in Primorsky Territory

As a result of experimental and faunistic investigations it is established that the development of the trematode species Azygia hwangtsiytii Tsin, 1933 in Primorsky Territory is realized in the first intermediate host, snail Cipangopaludina ussuriensis, and in second hosts, fishes Perccottus glehni and Channa argus warpachowskii, which can serve as transit, as well as final hosts. For Azygia robusta Odhner, 1911 terms of the development in the first intermediate host, snail Anisus centrifugus are established.     

Local diversity reduces infection risk across multiple freshwater host‐parasite associations

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Effects of trematode double infection on the shell size and distribution of snail hosts

Infection with larval trematodes sometimes alters the phenotypes of their snail hosts. While some trematode species have distinct effects on host phenotypes, it is still unclear how snail phenotypes are altered when they are parasitized with multiple trematode species. Here, we report that double infection with trematode species averages the effects of parasitic alteration on host phenotype. We found that snail hosts Batillaria attramentaria (Batillariidae) infected with Cercaria batillariae (Heterophyidae) have abnormally large shells and distribute in lower areas of the intertidal zone. Snails with another dominant trematode species, the renicolid cercaria I (Renicolidae), have slightly larger shells and distribute in upper areas of the intertidal zone. A number of double infections with both trematodes was observed in this study. Snails infected with both trematode species exhibited an intermediate size and inhabited a depth between those of snails solely infected with either trematode species, suggesting that the two trematodes simultaneously affected the snail phenotypes. Because altered host phenotypes are frequently beneficial to parasites, two trematode species may compete for successful transmission through alteration of host phenotypes.     

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.     

Trematodes associated with mangrove habitat in Puerto Rican salt marshes

Batillaria minima is a common snail in the coastal estuaries of Puerto Rico. This snail is host to a variety of trematodes, the most common being Cercaria caribbea XXXI, a microphallid species that uses crabs as second intermediate hosts. The prevalence of infection was higher (7.1%) near mangroves than on mudflats away from mangroves (1.4%). Similarly, there was a significant positive association between the proportion of a site covered with mangroves and the prevalence of the microphallid. The association between mangroves and higher trematode prevalence is most likely because birds use mangroves as perch sites and this results in local transmission to snails.     

Alternative reproductive strategies in the progenetic trematode Coitocaecum parvum: comparison of selfing and mating worms

The progenetic opecoelid trematode Coitocaecum parvum can reproduce either precociously by selfing in its second intermediate amphipod host or by mating in its normal definitive fish host. In this study, we describe and compare the infection parameters and some life history traits of both egg-producing worms and non-egg producing worms in both their second intermediate and definitive hosts. We showed that 58% of worms start to produce eggs while still in the amphipod. The relative abundance of progenetic worms increased with amphipod size, and egg-producing worms achieved greater size in amphipods than in fish. These 2 findings support the reproductive insurance hypothesis. No difference in size was revealed between eggs produced in the amphipods and those produced in the fish. Although more information is needed to thoroughly assess the respective costs and benefits of selfing and mating in this species, our conclusion is that adopting progenesis may have few, if any, long-term negative consequences for the parasite.     

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.     

Trematodes in snails near raccoon latrines suggest a final host role for this mammal in California salt marshes

Of the 18 trematode species that use the horn snail, Cerithidea californica, as a first intermediate host, 6 have the potential to use raccoons as a final host. The presence of raccoon latrines in Carpinteria Salt Marsh, California, allowed us to investigate associations between raccoons and trematodes in snails. Two trematode species, Probolocoryphe uca and Stictodora hancocki, occurred at higher prevalences in snails near raccoon latrines than in snails away from latrines, suggesting that raccoons may serve as final hosts for these species. Fecal remains indicated that raccoons fed on shore crabs, the second intermediate host for P. uca, and fish, the second intermediate host for S. hancocki. The increase in raccoon populations in the suburban areas surrounding west coast salt marshes could increase their importance as final hosts for trematodes in this system.     

Intermediate host availability masks the strength of experimentally-derived colonisation patterns in echinostome trematodes

A fundamental goal of parasite evolutionary ecology is to elucidate patterns of host use and determine the underlying mechanisms of parasite colonisation. In order to distinguish the relative contributions of host encounter rates and host compatibility to infection outcomes, we compared host use in both field and experimental laboratory settings. Two years of bi-weekly snail sampling at a freshwater pond demonstrated fluctuating availability among three potential second intermediate snail host species and suggested that two trematode species (Echinostoma revolutum and Echinoparyphium sp.) did not colonise the three potential snail host species, Lymnaea elodes, Physa gyrina and Helisoma trivolvis, differentially. However, a series of experimental infections demonstrated that both parasites colonised H. trivolvis more so than the other two host species. Thus, more echinostome parasites utilised snail hosts that cannot serve as their first intermediate host. In experimental infections, host size and vagility were not strong determinants of infection. By utilising field and laboratory approaches, we were able to compare the strength of host compatibility under controlled conditions with patterns of infection in nature. Based on the results from these studies, it appears that host encounter is the primary mechanism dictating infection outcomes in the field.     

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.     

Parasite-induced alteration of diurnal rhythms in a freshwater snail

The trematode Microphallus sp. alters the behavior of its snail intermediate host, Potamopyrgus antipodarum, in ways that seem to increase transmission to its final host, e.g., waterfowl, and decrease the probability of being eaten by other predators, e.g., fish. The parasite seems to cause the snail to move from the top to the bottom of rocks at about 0900 hr. Waterfowl feed predominantly before 0900 hr, and fish feed predominantly after 0900 hr. In the present study, we tested the hypothesis that Microphallus sp.-infected snails exhibit a change in behavior at around 0900 hr by examining their response to light and vertical orientation before and after 0900 hr. Results demonstrated that uninfected snails generally move toward light, oriented downward, and move a greater distance in the light compared with the dark at all times of day. Microphallus sp.-infected snails behaved differently from uninfected snails in the early morning but similarly to uninfected snails in the late morning with regard to downward orientation and distance moved in response to light. Snails infected with parasites other than Microphallus sp. behaved similarly to uninfected snails during both time periods. These results suggest that Microphallus sp. manipulates the behavior of Potamopyrgus sp. by altering rates of movement in response to light and vertical orientation in a manner consistent with the hypothesized 0900-hr shift.     

Trematode communities in snails can indicate impact and recovery from hurricanes in a tropical coastal lagoon

In September 2002, Hurricane Isidore devastated the Yucatán Peninsula, Mexico. To understand its effects on the parasites of aquatic organisms, we analyzed long-term monthly population data of the horn snail Cerithidea pliculosa and its trematode communities in Celestún, Yucatán, Mexico before and after the hurricane (February 2001 to December 2009). Five trematode species occurred in the snail population: Mesostephanus appendiculatoides, Euhaplorchis californiensis, two species of the genus Renicola and one Heterophyidae gen. sp. Because these parasites use snails as first intermediate hosts, fishes as second intermediate hosts and birds as final hosts, their presence in snails depends on food webs. No snails were present at the sampled sites for 6 months after the hurricane. After snails recolonised the site, no trematodes were found in snails until 14 months after the hurricane. It took several years for snail and trematode populations to recover. Our results suggest that the increase in the occurrence of hurricanes predicted due to climate change can impact upon parasites with complex life cycles. However, both the snail populations and their parasite communities eventually reached numbers of individuals and species similar to those before the hurricane. Thus, the trematode parasites of snails can be useful indicators of coastal lagoon ecosystem degradation and recovery.     

洞庭湖外睾吸虫新种及其生活史

本文报告洞庭湖区鲶鱼肠道寄生的洞庭湖外睾吸虫Exorchis dongtinghuensis sp.nov(新种)及其全程生活史,其第一中间宿主为湖北钉螺Oncomelania hupensis;第二中间宿主为鲤鱼、鲫鱼和金鱼;终宿主为鲶鱼Parasilurus asotus。作者对各期宿主作了人工感染试验和现场自然感染调查。对其发育过程作了观察比较。