The Hydrobia ulvae-Maritrema subdolum association: cercarial emergence controlled by host activity

The release of Maritrema subdolum cercariae (Digenea: Microphallidae) from the marine mud snail Hydrobia ulvae is significantly affected by temperature, salinity, light and exudates from the second intermediate amphipod host. Based on (i) previously published data on temperature-salinity dependent H. ulvae activity, (ii) new experimental data on H. ulvae activity in light and darkness as well as in the presence and absence of host exudates, and (iii) the cercarial emergence rate from free moving snails and snails prevented from crawling, the present analysis indicates that emergence of M. subdolum larvae is regulated mainly by host activity as the ultimate factor for release. The adaptive significance of such an emergence strategy is emphasized.     

Laboratory Studies of Parasite Transmission Aspects between Hydrobia spp. (Gastropoda) and Corophium volutator (Amphipoda)

Aspects of parasite transmission between Hydrobia spp. and Corophium volutator, first and second intermediate host of digenetic trematodes, were investigated under laboratory conditions. H. ventrosa is used as an intermediate host by several trematode species. Under laboratory conditions the most frequently observed emergence from H. ventrosa was of cercariae of Maritrema subdolum. The number of cercariae shed per day varied considerably. It was observed that 30 cercariae on average and up to 450 cercariae at maximum can emerge from a single H. ventrosa per day. Cercarial production continued until the death of the snails. The life-span of cercariae of the species M. subdolum decreased as the water temperature increased. It can be concluded that under natural conditions the cercariae, after emerging, have a maximum period of 1 day in which to seek out their second intermediate host C. volutator. Almost all specimens of C. volutator exposed to cercariae of the species M. subdolum died within the test period of 6 days. High average cercarial densities caused short life-spans (<50 h), while at lower densities longer survival times were possible. For cercariae of other Trematoda species, we were unable to find any equally clear evidence of a reduction in the survival rate of C. volutator within the test period. Mortality of C volutator, and other effects of infestation, as observed in our experiment, can be assumed to be a result of the penetration process of the cercariae but they also can be attributed to the mesocercariae.     

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.     

Climate influences parasite-mediated competitive release

Parasitism is believed to play an important role in maintaining species diversity, for instance by facilitating coexistence between competing host species. However, the possibility that environmental factors may govern the outcome of parasite-mediated competition has rarely been considered. The closely related amphipods Corophium volutator and Corophium arenarium both serve as second intermediate host for detrimental trematodes. Corophium volutator is the superior competitor of the two, but also suffers from higher mortality when exposed to infective trematode stages. Here, we report parasite-mediated competitive release of C. arenarium in an intertidal habitat, in part triggered by unusually high temperatures linked to the North Atlantic climate oscillation (NAO). The elevated temperatures accelerated the transmission of cercariae from sympatric first intermediate hosts (mud snails) to amphipods, causing a local collapse of the parasite-sensitive C. volutator population and concordant increase in the abundance of the competitively inferior C. arenarium.     

Studies on Austrobilharzia terrigalensis (Trematoda: Schistosomatidae) in the Swan Estuary, Western Australia: observations on the biology of the cercaria

The emergence of Austrobilharzia terrigalensis cercariae from the snail Velacumantus australis decreased with decreasing salinity and temperature. This was most marked between 23 and 25 and between 24 and 19°C. Very few cercariae were shed below 23 regardless of temperature. The decrease in cercarial emergence was associated with the decreasing metabolic activity of the intermediate host. The emergence pattern of A. terrigalensis cercariae from V. australis was diurnal. There was a major peak between 08h00 and 10h00 and a minor second one between 16h00 and 18h00. No cercariae were shed between 22h00 and 04h00. Cercariae survived in sea water (35) for up to 48h, with a half-life of 30h. There was evidence that the prevalence of A. terrigalensis infection in the intermediate host population in the Swan estuary was higher during the summer than during the winter. The production of cercariae in the sporocyst also appeared to be a seasonal phenomenon. Mature cercariae were rare in sporocysts examined during the winter months (May–October) and absent altogether from those examined in September.     

The effects of temperature on the distribution and establishment of Echinoparyphium recurvatum metacercariae in Lymnaea peregra

The establishment and distribution of Echinoparyphium recurvatum metacercariae in the second intermediate host, Lymnaea peregra, were investigated at a temperature range of 5-29 degrees C. Preliminary studies on the survival and infectivity of E. recurvatum cercariae showed that both parameters were temperature dependent. No cercarial transmission occurred at 5 or 10 degrees C. Nevertheless, the transmission efficiency (1/H0) indicated that transmission was temperature independent in the temperature range 17-25 degrees C and was much lower than in previous studies using this host-parasite system. These differences were attributed to low cercarial densities used in this study. The effect of temperature on encystment site choice (mantle cavity, kidney, pericardium) by metacercariae showed that the mantle cavity was the prime site of encystment, followed by the pericardium and the kidney. Temperatures at the lower and upper ranges (14 and 29 degrees C), however, caused a significant reduction in encystment in the mantle cavity but not in the pericardium or kidney. The importance of cercarial densities, the physiological mechanisms influencing metacercarial distribution and their implications for parasite transmission to the definitive host are discussed.     

Vertical distribution of trematode cercariae Cryptocotyle concavum (Heterophyidae) and Maritrema subdolum (Microphallidae) in the water column

The effect of gravity and light on vertical distribution of Cryptocotyle concavum (Heterophyidae) and Maritrema subdolum (Microphallidae) cercariae in the water column was experimentally studied. Maximal larvae concentration was found in zones where the highest probability of contact with potential host is considered.     

Patterns and processes of larval emergence in an estuarine parasite system

Trematode parasites in intertidal estuaries experience constantly varying conditions, with the presence or absence of water potentially limiting larval transport between hosts. Given the short life spans (< or =24 h) of cercariae, emergence timing should be optimized to enhance the probability of successful transmission. In the present study, field measurements and laboratory experiments identified processes that regulate the emergence of cercariae from their first intermediate snail hosts in an intertidal marsh. Larvae emerged over species-specific temperature ranges, exclusively during daylight hours, and only when snails were submerged. The three factors operate over different temporal scales: temperature monthly, light diurnally (24-h period), and water depth tidally (12-h period). Each stimulus creates a necessary condition for the next, forming a hierarchy of environmental cues. Emergence as the tide floods would favor transport within the estuary, and light may trigger direct (downward or upward) swimming toward host habitats. Abbreviated dispersal would retain asexually reproduced cercariae within the marsh, and local mixing would diversify the gene pool of larvae encysting on subsequent hosts. In contrast to the timing of cercarial release, emergence duration was under endogenous control. Duration of emergence decreased from sunrise to sunset, perhaps in response to the diminishing lighted interval as the day progresses. Circadian rhythms that control cercarial emergence of freshwater species (including schistosomes) are often set by the activity patterns of subsequent hosts. In this estuary, however, the synchronizing agent is the tides. Together, exogenous and endogenous factors control emergence of trematode cercariae, mitigating the vagaries of an intertidal environment.     

Patterns of swimming of cercariae in some trematode species

Swimming activity of cercariae in the trematode species Cryptocotyle lingua, Himasthla elongata, Maritrema subdolum, and Cercaria parvicaudata (Renicola sp.) is studied using video microfilming. The larvae of C. lingua demonstrate a typical intermittent swimming with regularly alternating periods of active movement and passive floating. The duration of both periods during the first 30 min of cercaria's life retains equal, and later the passive period becomes longer. In 15 h the duration of the active period is 0.5-1 s and the passive one--20-30 s. The cercariae of H. elongata during the first 10-15 min of their free life make short stops (1-2 s) in every 10-15 s of swimming. Later these stops become rare and their duration reduces to 0.5-1 s. The cercariae of M. subdolum and C. parvicaudata are continuous swimmers, having left the molluscan host they move persistently. If stops take place they are very rare (one case in 5-15 min) and very short (0.5-1 s). The movements of cercariae body and their tail during swimming are similar in all species studied. The proximal part of the tail undulates in lateral plane, and the middle and distal parts of this organ in the top view circumscribe a figure of eight. In the side view the middle and distal parts of the tail being rotate form a figure like a screw. The cercariae move along the screw axis. The linear swimming rate in the beginning of cercariae's life is 4.8 mm/s for C. lingua, 2.4 mm/s for H. elongata, and 0.35 mm/s for M. subdolum and C. parvicaudata. By the aging the cercariae swimming rate decreases down to the full cease of swimming activity, and the larvae sediment onto the bottom. The age dynamics of swimming rate is different in cercariae of different species and is determined by the morphological functional features of the larvae.     

Infection dynamics of Centrocestus armatus cercariae (Digenea: Heterophyidae) to second intermediate fish hosts

The infection dynamics of Centrocestus armatus cercariae with respect to second intermediate fish hosts were investigated using cercariae collected from naturally infected Semisulcospira libertina. Cercariae survival and infectivity were recorded at 2-hr intervals. Survival remained constant but decreased abruptly at 30 hr of age. An age-dependent model presented the best-fit curve for the survival data (r2 0.936), implying that cercariae tended to allocate resources equally among themselves and then died once those resources were depleted. Cercariae infectivity remained constant over the first 10 hr of life and then declined; an age-dependent model also provided a better fit (r2 = 0.956). The transmission rate of C. armatus cercariae to the fish host was relatively low near the time of emergence from the snail host but peaked at 85% after 1 hr and then maintained a plateau period until 5 hr of exposure to fish. The pattern of transmission was also investigated initially at varying densities of cercariae and then by maintaining a constant cercariae density but varying the total number. Results revealed that the pattern of transmission was frequency-dependent.     

Respiration and motor activity of cercariae of three trematode species from the intertidal mollusc Littorina littorea L (Gastropoda) from the White sea

The age dynamics in oxygen consumption of the cercariae Himasthla elongata, Cryptocotyle lingua and Cercaria parvicaudata (Renicola sp.) was studied using modified Winkler's method. It was detected that under stable temperature and water salinity conditions the rate of oxygen uptake depends directly on cercariae size. The highest intensity of energetic metabolism was recorded in the first few hours of cercariae life when their movement activity was maximal. The following reduction of oxygen consumption passed unequally in three cercariae species studied. Large, long-lived H. elongata cercariae after relatively short period of active swimming turn to crawling on the bottom. The rate of oxygen uptake in such cercariae was two times less than in free-swimming ones and remained approximately invariable up to the cercariae death. The smaller sized, short-lived Renicola sp. cercariae swim actively in the water and during this time the level of their energetic metabolism remains more or less stable. It decreased drastically after cercariae sinking to the bottom, after that they perished very soon. Also relatively small C. lingua cercariae alternate the active and passive phases of swimming. Thanks to that they consume the energetic resources economically and prolong their longevity. During free-swimming period the rate of oxygen uptake of C. lingua cercariae remains more or less stable. As in the case of Renicola sp. cercariae, it decreased drastically after the cercariae sinking to the bottom. Apparently such cercariae lose their ability to infect the second intermediate host (fish).     

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 role of light and gravity in the experimental transmission of Echinostoma caproni (Digenea: Echinostomatidae) cercariae to the second intermediate host, Biomphalaria glabrata (Gastropoda: Pulmonata)

Trematode cercariae inhabit predictable environments and respond to trigger cues with genetically fixed releaser responses when foraging for the upstream host. The effect of light and gravity on the transmission of Echinostoma caproni cercariae to Biomphalaria glabrata was investigated experimentally. Transmission chambers were constructed of clear polyvinyl chloride pipe. Snails were constrained within the chamber to prevent movement, while permitting the cercariae to swim freely. A trial consisted of 2 infected B. glabrata shedding E. caproni cercariae placed at the center of the chamber, with 5 uninfected B. glabrata placed 10 cm on either side (or above and below) of the shedding snails as sentinels. There was no significant difference in the prevalence of infection sentinel snails in either experiment (light vs. dark or top vs. bottom); however, mean intensity was significantly higher in sentinel snails in the dark portion of the chamber (42.5 vs. 10.4; P = 0.001) and the top of the transmission chamber (66.1 vs. 38.0; P = 0.0003). There was a high correlation between the number of metacercariae collected from sentinel snails and the total number of infective units (metacercariae + unsuccessful cercariae): r = 0.992 (light vs. dark) and r = 0.957 (top vs. bottom), respectively, at cercariae densities estimated from 22 to 3,304/L. The results suggest that cercariae of E. caproni exhibit negative photo- and geotaxis in searching for a second intermediate host. Stereotypical releaser responses to environmental trigger cues (light and gravity) allow E. caproni cercariae to exploit flexible strategies for completing the life cycle consistent with the broad range second intermediate and definitive hosts used by E. caproni cercariae and adults, respectively.     

Toxic effects of cadmium and zinc on the transmission of Echinoparyphium recurvatum cercariae

The toxicity of cadmium, zinc and Cd/Zn mixtures to the transmission of Echinoparyphium recurvatum (Digenea: Echinostomatidae) cercariae into the snail second intermediate hosts was investigated at concentrations ranging from 100 microg l-1 to 10 000 microg l-1 in both soft and hard water. A differential response in the infectivity of metal-exposed cercariae into Lymnaea peregra and Physa fontinalis was demonstrated which was dependent on the snail species being infected. Exposure of L. peregra, P. fontinalis, and L. stagnalis to heavy metals caused a differing susceptibility to E. recurvatum cercariae depending on the snail species being exposed. The mechanism and effects of metal toxicity, together with the importance of the parasite/host strain on cercarial transmission are discussed.     

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).     

Internal movement of estuarine digenetic trematodes through their intermediate snail host Cerithidea californica

The ability of free-swimming larval parasites to control emergence from their hosts can be critical in increasing the chances of successful infection transmission. For a group of estuarine trematodes, emergence of cercariae from their snail hosts is known to match favorable temperature, tidal activity, and light intensity. How the larvae time this behavior is not well understood, but the pathway that the larvae take through their host may play a role. Through video and histological analysis, we were able to identify the snail's anus as the emergence point and the peri-intestinal sinus dorsal to the intestines as the route by which they reach that point. By moving through this open sinus, the larvae have an energetically efficient pathway to reach their emergence point while minimizing damage to the host. Most importantly, it allows control over emergence to be maintained by the parasite, not the host, thus increasing the chances of the larva successfully reaching its intended destination.     

Comparative photobehavior of marine cercariae with differing secondary host preferences

Light may serve as an important exogenous cue for parasitic larvae that have multi-host lifecycles and need to locate specific microhabitats, thereby increasing the probability of encountering their next host. We studied light as an initiating and orienting cue for swimming in two species of marine cercariae (Trematoda), Euhaplorchis sp. and Probolocoryphe lanceolata, which initially parasitize the same species of benthic snail, but then utilize different second intermediate hosts located in pelagic and benthic habitats, respectively. When tested in a laboratory simulation of underwater angular light distribution, dark-adapted Euhaplorchis cercariae swam slowly in darkness but ascended quickly toward downwelling light at quantal intensities over 4.0 × 10(15) photons m(-2) s(-1). They oriented toward a directional light source in a horizontal trough, confirming that light plays both an initiating and an orienting role in phototactic behavior that results in ascent in the water column to locate a fish host. In contrast, Probolocoryphe lanceolata cercariae exhibited haphazard vertical swimming in darkness, with downward swimming upon exposure to angular light at lower quantal intensities (>4.0 × 10(14) photons m(-2) s(-1)) than initiated swimming in Euhaplorchis. However, P. lanceolata cercariae did not swim in response to a directional light source, suggesting that while light initiated descent behavior, its orientation was controlled by another factor. These differences in photobehavior support the idea that trematode cercariae use light in selecting for microhabitats frequented by potential hosts: an adaptive benefit that optimizes their contact and transmission to the next host.     

The pattern of gill perfusion in two species of Corophium (Crustacea: Amphipoda) and its relation to environmental salinity

Total surface area of the ion-permeable lamellar gills of Corophium volutator and Corophium curvispinum is 0·81 mm²mg^-1 and 0·78 mm²mg^-1 (wet weight), respectively. In both species, haemolymph flow (as visualized by haemocyte movements) is rapid through the peripheral canal and central luminal lacunae of each gill, general flow being from posterior to anterior margin of the gill. There appears to be countercurrent flow of haemolymph and ventilatory current water over the gill integument, which may facilitate dissolved-gas exchange.
Rate of haemolymph flow (perfusion) through the gills of the euryhaline C. volutator is markedly reduced immediately following transfer to a considerably hyperosmotic salinity ( e.g. 15% S.W. to 85% S.W. transfer). No reduction in the rate of gill perfusion occurs following transfer of C. volutator to hypoosmotic salinity. The freshwater C. curvispinum does not tolerate hyperosmotic salinity transfers, but does exhibit a similar immediate gill perfusion restriction. The onset of gill perfusion restriction is dependent on a change in the magnitude of the ionic ([NaCl]), not the osmotic, gradient across the integument. In C. volutator only, normal rate of gill perfusion is eventually restored (within 24 hours of transfer), but can be immediately restored if the animal is transferred back to the acclimation salinity.
In C. volutator , branchial perfusion pattern is postulated to be regulated in relation to environmental salinity by a mechanism operating under neural control. The possible significance of gill perfusion restriction to C. volutator as a short-term adaptive osmoregulatory response is considered. Perfusion restriction in the gills of C. curvispinum is considered to be a relic of a recent estuarine ancestry.     

Opportunity or catastrophe? effect of sea salt on host-parasite survival and reproduction

Seawater intrusion associated with decreasing groundwater levels and rising seawater levels may affect freshwater species and their parasites. While brackish water certainly impacts freshwater systems globally, its impact on disease transmission is largely unknown. This study examined the effect of artificial seawater on host-parasite interactions using a freshwater snail host, Biomphalaria alexandrina, and the human trematode parasite Schistosoma mansoni. To evaluate the impact of increasing salinity on disease transmission four variables were analyzed: snail survival, snail reproduction, infection prevalence, and the survival of the parasite infective stage (cercariae). We found a decrease in snail survival, snail egg mass production, and snail infection prevalence as salinity increases. However, cercarial survival peaked at an intermediate salinity value. Our results suggest that seawater intrusion into freshwaters has the potential to decrease schistosome transmission to humans.