Habitat and host specificity of trematode metacercariae in fiddler crabs from mangrove habitats in Florida

Fiddler crabs (Uca spp.) are common inhabitants of temperate and tropical coastal communities throughout the world, often occupying specific microenvironments within mangrove and salt marsh habitats. As second intermediate hosts for trematodes, we investigated patterns of host distribution and parasitism for 3 species of sympatric fiddler crabs in mangrove habitats adjacent to the Indian River Lagoon, Florida. Fiddler crab distribution varied among species, with Uca speciosa dominating the low and mid intertidal regions of mangrove banks. This species also exhibited higher prevalence and abundance of Probolocoryphe lanceolata metacercariae compared with Uca rapax, which is relatively more abundant in the high intertidal zone. We conducted a field experiment to test whether U. speciosa was more heavily parasitized by P. lanceolata as a result of its habitat distribution by raising U. speciosa and U. rapax under identical environmental conditions. After exposure to shedding cercariae under the same field conditions, all individuals of U. speciosa became parasitized by P. lanceolata, whereas no U. rapax were parasitized, suggesting that differences in parasitism were driven by host selection.     

Photo- and geo-orientation by Echinostome cercariae results in habitat selection.

The effect of light and gravity on orientation was studied in cercariae of 4 echinostome species: Pseudechinoparyphium echinatum, Echinostoma revolutum, Hypoderaeum conoideum, and Isthmiophora melis. The cercariae were placed into vertical and horizontal cuvettes, illuminated with 2 different light intensities from various directions, and their distribution recorded for 6 hr Each species showed its individual pattern of horizontal photo-orientation and geo-orientation, with distinct changes during the time after emerging. The geo-orientation was controlled differently in each species by the intensity and the direction of light radiation. The different orientation patterns suggest functions such as leaving the habitats of the host-snails emitting the cercariae, dispersal, and frequenting the microhabitats of potential hosts. The high diversity of orientation patterns among the species that originated from the same first intermediate host Lymnaea stagnalis in the same ponds and that invade similar host spectra suggests adaptations to different ecological conditions.     

Proximate control of diel vertical migration in Phyllosoma larvae of the Caribbean spiny lobster Panulirus argus

Phyllosoma larvae of the spiny lobster Panulirus argus undergo diel vertical migration (DVM), in which they are at depth during the day and nearer the surface at night. This study determined the visual spectral sensitivity of Stage I larvae and investigated whether light plays a proximate role in DVM as an exogenous cue and as an entrainment cue for an endogenous rhythm in vertical migration. Under constant conditions, larvae have a circadian rhythm (24.5-h period) in vertical swimming that resulted in a twilight DVM pattern. The behavioral response spectrum and electroretinogram recording indicated two photoreceptor spectral classes with maxima at 360 and 486 nm. When stimulated in an apparatus that simulated the underwater angular light distribution, dark-adapted larvae showed only positive phototaxis, with a threshold intensity of 1.8 × 10(13) photons m(-2) s(-1) (3.0 × 10(-5) μmoles photons m(-2) s(-1)). They have an avoidance response to predator shadows in which they descend upon sudden decreases in light intensity of more than 69%. When stimulated with relative rates of decrease in light intensity as occur at sunset they ascended, whereas they descended upon relative rates of light intensity increase as occur at sunrise. Thus, the DVM pattern is controlled by both an endogenous circadian rhythm in swimming and behavioral responses to light at sunrise and sunset.     

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.     

The effect of light and darkness on the production of cercariae of Schistosoma haematobium from Bulinus globosus

The cercariae of Schistosoma haematobium showed a diurnal periodicity of emergence from Bulinus globosus in a twelve hour light/dark cycle. Peak emission occurred at 11.00 hrs with a smaller peak at 20.00 hrs, following the start of the period of darkness. In continuous illumination this second peak was not seen, indicating that only the morning peak is circadian in origin. The evening peak occurs in response to dark treatment and can be produced by periods of darkness ranging from eight seconds to one hour. The longer the period of dark treatment the longer the rise in output is maintained on return to light conditions. Subjection of snails to periods of dark treatment during the normal light period caused a reduction in the evening peak with the largest effect seen following the longest period of darkness. An increased output of cercariae was seen following fifteen minutes exposure to a range of light intensities, the largest increase occurring at 10,000 and 7000 lux and complete darkness. The rapidity of this reaction to variations in light intensity suggests that the cercariae of S. haematobium are showing emergence in response to shadows.     

The daily cercarial emission rhythm of Schistosoma margrebowiei with particular reference to dark period stimuli

The cercariae of Schistosoma margrebowiei showed two peaks of emergence from Bulinus natalensis in a 12 h light/dark cycle. Peak emission occurred at 0700 h (one hour after the onset of light) and at 1900 h (one hour after the onset of darkness). Both peaks were of equal magnitude and were maintained during constant illumination indicating that the rhythm is innate. Delaying or advancing the timing of the dark period did not affect the timing of these two peaks. Following a five minute dark treatment elevation in cercarial output resulted irrespective of when the treatment was applied. Subjecting snails to various intensities of light only resulted in an elevation in output when a sudden change in intensity from 0 to 360 Lux or the reverse was applied. No response was seen to a gradual change in light intensity although the parasite could detect a change in light from 1 to 0 Lux. These responses appear to optimize the chances of host parasite contact.     

Host location and selection cues in a generalist tachinid parasitoid

Tachinid flies are diverse and ecologically important insect parasitoids. However, the means by which tachinid species locate and select hosts are poorly known. Many tachinids exhibit unusually wide host ranges and they also possess well-developed visual systems. These characteristics suggest that tachinids differ from parasitic wasps in their reliance on various sensory modes and types of cues. A series of behavioral assays using the generalist tachinid Exorista mella Walker (Diptera: Tachinidae) were conducted to examine what types of cues this parasitoid uses to locate and accept hosts, and how the cues used may reflect its ecological relationships with hosts. Female E. mella responded strongly to host motion in assays using both live hosts and host corpses, and this cue is shown to be an important elicitor of attack behavior. Females also responded to volatile chemicals associated with damaged food plants of their host in an olfactometer. Flies responded only weakly to direct visual contact with stationary hosts and odors directly associated with hosts. The behavior of female E. mella changed with experience such that more experienced flies recognized and attacked hosts more readily than did inexperienced flies. The use of general olfactory and visual cues by E. mella may be an effective strategy by this polyphagous parasitoid to locate a broad range of potential hosts.     

Behavioral responses of Poecilia vivipara (Osteichthyies: Cyprinodontiformes) to experimental infections of Acanthocollaritrema umbilicatum (Digenea: Cryptogonimidae)

The swimming behavior of Poecilia vivipara was evaluated using an image analysis system comparing laboratory-reared uninfected fish before and after experimental infection with different intensities of cercariae of the trematode Acanthocollaritrema umbilicatum. Two experiments were performed, each with 30 fish which were individually exposed to 30 and 50 cercariae, respectively, shed from experimentally infected molluscs, Heleobia australis. Before and after (17–27 days) infection, the behavior of each fish was monitored in terms of Distance travelled, Ambulatory time, Stereotypic time, Resting time and Average speed. At the end of the experiments, the fish were dissected to count the number of metacercariae recovered. In the experiment with 30 cercariae, fish with 2–10 metacercariae did not exhibit any significant differences in their swimming activity, but those with 11–22 metacercariae had a significantly enhanced Stereotypic time and a reduced Time Resting. In the experiment with 50 cercariae, fish with 5–22 metacercariae had an enhanced Distance travelled and a reduced Average speed; highly significant differences occurred with regard to all behavioral parameters when considering the subgroup 23–36 metacercariae: Distance travelled, Stereotypic time, Resting time, Ambulatory time and Average speed. The swimming behavior of P. vivipara changed influenced by an intensity-dependence on metacercariae of A. umbilicatum, supporting the prediction that parasites are able to alter the behavior of their hosts.     

How females of the rotifer Asplanchna brightwelli swim in darkness and light: an automated tracking study

This work explores the effect of darkness on the swimming behaviour of females of the rotifer Asplanchna brightwelli. Females were filmed in flat dishes alternately in white light (WL, 5000 µW cm^–2) and in infra-red light (IR, 155 µW cm^–2), each female for a total of eight successive periods of fifteen minutes per period. An automated tracking system was used to describe the swimming path of each female: twenty five x and y coordinates of the center of gravity of the animal per second, in a discrete space of 512 × 512 pixels. Indices characterizing the swimming performances of the females were then calculated: linear speed, angular speed and other angular parameters of the tracks. A Principal Component Analysis of swimming characteristics discriminated between WL tracks and IR tracks. Females swam slower and turned more in darkness than in light. These results show that beside a positive phototactic response, there is a photokinesis which increases the dispersion of animals in the light.     

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).     

Age and serotonin effects on locomotion in marine trematode cercariae

The effect of serotonin solutions on the locomotor activity of cercariae with different swimming patterns, Cryptocotyle lingua and Himasthla elongate, was investigated during their lifespan using motion track analysis and a frame-by-frame count of behavioral elements. Serotonin caused a noticeable alteration of several locomotion parameters in both species studied, while the activity per se decreased significantly with age. In intermittently swimming C. lingua cercariae, serotonin induced an increase in the frequency of active swimming phases (spurts) without significant changes in the duration and velocity of the spurts themselves. In continuously swimming H. elongata cercariae, serotonin increased the number of stops during the first hour after the emission from the host mollusk under a constant average swimming velocity. Immunocytochemical visualization of serotonin revealed a decline in its level with age (time after emission) and different dynamics of this process in neurons located in the tail and body of C. lingua cercariae. The data are interpreted in the light of the modulatory role of serotonin known for other animals.     

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.     

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.     

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.     

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.     

Effect of light intensity on Opisthorchis viverrini cercarial shedding levels from Bithynia snails--a preliminary study

Opisthorchis viverrini requires Bithynia snails as the first intermediate host and cyprinid fish as the second intermediate host. Very low natural infection rates have been reported in Bithynia snails, but very high rates have been found in cyprinid fish in the same endemic region. This study investigated the effect of light intensity, the most important stimulus, on the quantity of O. viverrini cercariae shed from naturally infected Bithynia (Digoniostoma) siamensis goniomphalos snails. Snails were evaluated for cercariae output every hour after exposure to various light intensities for a total period of 7 h. The same infected snail was tested under different intensities of light: in the dark, and at 1000, 3000 and 5000 lx. The data showed that under exposure to 1000 and 3000 lx of light, the average percentage and number of cercariae released were higher than that exposed to 5000 lx during the first 2 h of the experiment. In contrast, under higher illumination (5000 lx) a longer time (6 h) was required to stimulate the peak emergence of cercariae. Darkness was not able to induce O. viverrini cercariae emergence. Among the three intensities of light, exposure at 1000 lx induced the highest average number of released cercariae per snail and the highest percentage of cercarial emergence within the first 2 h (125, 54.86%), followed by exposure at 3000 lx (69, 25.58%) and 5000 lx (12, 7.78%). The results suggest that the light intensity of 1000 lx for 2 h would be optimal for O. viverrini cercarial shedding from naturally infected B. (D.) siamensis goniomphalos snails.     

How do ectoparasitic nycteribiids locate their bat hosts?

Nycteribiids (Diptera: Nycteribiidae) are specific haematophagous ectoparasites of bats, which spend nearly all their adult lives on hosts. However, females have to leave bats to deposit their larva on the walls of the roosts, where they later emerge as adult flies. Nycteribiids had thus to evolve efficient sensorial mechanisms to locate hosts from a distance. We studied the sensory cues involved in this process, experimentally testing the role of specific host odours, and general cues such as carbon dioxide, body heat, and vibrations. As models we used two nycteribiids (Penicillidia conspicua and Penicillidia dufourii) and their primary bat hosts (Miniopterus schreibersii and Myotis myotis, respectively). Carbon dioxide was the most effective cue activating and orientating the responses of nycteribiids, followed by body heat and body odours. They also responded to vibration, but did not orientate to its source. In addition, sensory cues combined (carbon dioxide and body heat) were more effective in orientating nycteribiids than either cue delivered alone. Results suggest that nycteribids have some capacity to distinguish specific hosts from a distance, probably through their specific body odours. However, the strong reliance of nycteribiids on cues combined indicates that they follow these to orientate to nearby multispecies bat clusters, where the chances of finding their primary hosts are high. The combination of sensory cues seems therefore an effective strategy used by nycteribiids to locate bat hosts at a distance.     

The effects of host distributional patterns on parasite transmission: Aedes aegypti larvae and Plagiorchis noblei Cercariae

The effects of distributional patterns of the host on the acquisition of Plagiorchis noblei cercariae by Aedes aegypti larvae were determined. Mosquito larvae that were allowed to disperse were more susceptible to infection than confined larvae. Because these mosquito larvae are known to aggregate in light and disperse in darkness, they are more likely to acquire P. noblei infections at night. The timing of cercarial emergence in relation to the distributional patterns of the mosquito host is discussed.