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Journal ArticleDOI

Photocycle-dependent emergence by cercariae of Halipegus occidualis from Helisoma anceps, with special reference to cercarial emergence patterns as adaptations for transmission.

01 Dec 1990-Journal of Parasitology (American Society of Parasitologists)-Vol. 76, Iss: 6, pp 790-795
TL;DR: Nocturnal emergence by cercariae was confirmed, and alternate hypotheses were developed to explain periodic emergence byC.
Abstract: Emergence by cercariae of Halipegus occidualis (Hemiuridae) from naturally infected Helisoma anceps (Pulmonata) was evaluated with respect to change in temperature and light. Total cercarial emergence per snail per day increased with temperature in 2 experiments: at constant temperatures of 16, 22, and 28 C, and at temperatures varying within the range 15-30 C. The number of cercariae emerging per snail per day varied extensively among snails and from day to day for individual snails. The proportion of cercariae that emerged during darkness in each 24-hr period on a 12-hr light: 12-hr dark photocycle was consistent for each snail over 3 photocycles, but it varied among snails: a mean of 73% of cercariae emerged during darkness at 16 C, 84% at 22 C, and 89% at C. The ecological consequences of nocturnal emergence by sessile, long-lived cercariae, such as those of H. occidualis, are discussed with reference to 3 hypotheses: synchronization with activity of the next host, enhancement of dispersal, and reduction of mortality. Daily cycles of emergence by cercariae from molluscan hosts are reported widely (Rees, 1948; Macy et al., 1960; Asch, 1972; Betterton, 1979; Th6ron, 1985, 1989; Lewis et al., 1989). These cycles of emergence correspond to daily changes in ambient light or temperature and often correlate with activity cycles of the next host (Ginetsinskaya, 1968; Cable, 1972; Betterton, 1979; Th6ron, 1984, 1985; Lewis et al., 1989). An absence of daily cycles has been reported for cercariae that encyst in the external medium following emergence (Kendall and McCullough, 1951; Ginetsinskaya, 1968). Several authors (Ginetsinskaya, 1968; Cable, 1972; Th6ron, 1984) interpreted these types of contrasting observations as evidence that daily cycles of emergence evolved as adaptations for transmission, by enhancing the ability of active, short-lived cercariae to find hosts rapidly. However, not all digeneans produce such cercariae. Cercariae of Halipegus occidualis are nonmotile and long-lived (Shostak and Esch, 1990) and they are ingested by their microcrustacean second intermediate hosts. Macy et al. (1960), in a limited study, reported that cercariae of H. occidualis tend to emerge from Helisoma subcrenatum during late afternoon and night. This observation seems contrary to the usual hypothesis to explain periodicity of cercarial emergence Received 9 April 1990; revised 12 June 1990; accepted 14 June 1990. * Present address: Department of Zoology, University of Alberta, Edmonton, Alberta, Canada T6G 2E9. (i.e., a necessity to find hosts rapidly). The present study evaluated the emergence of cercariae ofH. occidualis from Helisoma anceps, primarily with respect to photocycle but also with respect to the modifying influence of temperature. Nocturnal emergence by cercariae was confirmed, and alternate hypotheses were developed to explain periodic emergence by cercariae. MATERIALS AND METHODS Helisoma anceps was collected from Charlie's Pond, an impoundment in the piedmont area of North Carolina (described in Crews and Esch [ 1986]), in October 1987 and maintained at 20-24 C under natural lighting in a 50-L aquarium containing pond water and vegetation. Lettuce was provided. After 1-2 mo snails were screened individually for infection with H. occidualis, following the methods of Goater et al. (1989). One experiment evaluated the effect of temperature. At 1030 hr on day 0, 7 naturally infected snails (shell diameter: 9.0-11.3 mm) in individual 55-mm-diameter dishes, containing 30 ml filtered pond water and a 1-cm2 piece of lettuce, were placed in a controlled environment chamber at 22 ? 1 C. A 12-hr light: 12hr dark photocycle (light commencing 0500 hr) was established in the chamber using a 25-watt incandescent light bulb suspended 25 cm above the dishes. Based on the study by Asch (1972), it was assumed that body temperatures of H. occidualis changed negligibly when illuminated. At 1030 hr daily until day 24, each snail was transferred to a new dish containing fresh water and lettuce and cercariae in the old dishes were counted (total counts if 500 cercariae). The temperature was changed by 5 C every 3-4 days (Fig. 1). Snails were killed on day 24, and sporocysts and rediae were counted. A second experiment evaluated the effect of light. At 0700 hr on day 0, 24 infected snails (shell diameter:

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Journal ArticleDOI
TL;DR: The results suggest that the small increases in air and water temperature forecast by many climate models will not only influence the geographical distribution of some diseases, but may also promote the proliferation of their infective stages in many ecosystems.
Abstract: Global warming can affect the world's biota and the functioning of ecosystems in many indirect ways. Recent evidence indicates that climate change can alter the geographical distribution of parasitic diseases, with potentially drastic consequences for their hosts. It is also possible that warmer conditions could promote the transmission of parasites and raise their local abundance. Here I have compiled experimental data on the effect of temperature on the emergence of infective stages (cercariae) of trematode parasites from their snail intermediate hosts. Temperature-mediated changes in cercarial output varied widely among trematode species, from small reductions to 200-fold increases in response to a 10 degrees C rise in temperature, with a geometric mean suggesting an almost 8-fold increase. Overall, the observed temperature-mediated increases in cercarial output are much more substantial than those expected from basic physiological processes, for which 2- to 3-fold increases are normally seen. Some of the most extreme increases in cercarial output may be artefacts of the methods used in the original studies; however, exclusion of these extreme values has little impact on the preceding conclusion. Across both species values and phylogenetically independent contrasts, neither the magnitude of the initial cercarial output nor the shell size of the snail host correlated with the relative increase in cercarial production mediated by rising temperature. In contrast, the latitude from which the snail-trematode association originated correlated negatively with temperature-mediated increases in cercarial production: within the 20 degrees to 55 degrees latitude range, trematodes from lower latitudes showed more pronounced temperature-driven increases in cercarial output than those from higher latitudes. These results suggest that the small increases in air and water temperature forecast by many climate models will not only influence the geographical distribution of some diseases, but may also promote the proliferation of their infective stages in many ecosystems.

389 citations


Cites background from "Photocycle-dependent emergence by c..."

  • ...…also directly influenced by temperature: within the range of temperatures in which host and parasite can live, an increase in temperature is almost invariably coupled with an increase in cercarial output (e.g., Shostak and Esch, 1990; Lo and Lee, 1996; Umadevi and Madhavi, 1997; Mouritsen, 2002)....

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Journal ArticleDOI
TL;DR: The present review shows that trematodes, similarly as other helminths presenting larval stages living freely in the environment and/or larval Stage parasitic in invertebrates easily affected by climate change as arthropods and molluscs as intermediate hosts, may be largely more susceptible to climate change impact than those helminthiases in whose life cycle such phases are absent or reduced to a minimum.

327 citations

BookDOI
01 Jan 2003

247 citations


Cites background from "Photocycle-dependent emergence by c..."

  • ...This aspect was investigated in the long-lived cercariae of Halipegus occidualis (Shostak and Esch, 1990)....

    [...]

  • ...It has been suggested (Shostak and Esch, 1990) that here we are concerned with an adaptation that lowers the risk of the emitted cercariae being eaten by the commensal oligochaetes Chaetogaster limnaei, which search for their prey by sight....

    [...]

Journal ArticleDOI
TL;DR: Cercariae, like miracidia, are non-parasitic larval stages implicated in the life cycle of all trematodes for the host-to-host parasite transmission.
Abstract: Cercariae, like miracidia, are non-parasitic larval stages implicated in the life cycle of all trematodes for the host-to-host parasite transmission. Almost all cercariae are free-living in the external environment. With a few exceptions (cercariae of Halipegus occidualis (Halipegidae) can live several months, Shostak & Esch, 1990a), cercariae have a short active life during which they do not feed, living on accumulated reserves. Most cercariae encyst as metacercariae in second intermediate hosts which are prey of the definitive host; in certain species, the interruption of the active life is achieved by an encystment in the external environment (or a simple immobile waiting strategy in a few species). In some two-host life cycles, the cercariae develop into adults after penetration (this is the case for various species causing human schistosomiasis). Some cercariae do not leave the mollusc which must then be ingested by the definitive host.

180 citations

References
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Journal ArticleDOI
20 Mar 1987-Science
TL;DR: Estuarine snails Ilyanassa obsoleta bearing larvae of the trematode Gynaecotyla adunca behave singularly in comparison with conspecifics lacking this parasite, and the modified (induced) snail behavior is apparently a parasite adaptation facilitating cercarial transmission to these crustaceans.
Abstract: Estuarine snails Ilyanassa obsoleta bearing larvae of the trematode Gynaecotyla adunca behave singularly in comparison with conspecifics lacking this parasite. Following high tides, and especially at night, infected snails were found stranded high on beaches and sandbars. Semiterrestrial crustaceans living well up on the shore serve as the next host, and the modified (induced) snail behavior is apparently a parasite adaptation facilitating cercarial transmission to these crustaceans. The altered behavior is unusual because of its apparent enhancement of host-to-host transmission by cercariae rather than predation, the process commonly recognized as being enhanced by parasitic modification of host behavior.

107 citations

Journal ArticleDOI
TL;DR: A comparative analysis of the cercarial shedding of 2 Schistosoma mansoni populations originating from the same endemic area (Guadeloupe) allows us to distinguish an early (peak emergence at 1100 hr) and a late (peak at 1600 hr) shedding patterns of cercariae.
Abstract: A comparative analysis of the cercarial shedding of 2 Schistosoma mansoni populations originat- ing from the same endemic area (Guadeloupe) allows us to distinguish an early (peak emergence at 1100 hr) and a late (peak at 1600 hr) shedding patterns of cercariae. This intraspecific variation in the chronobiology of S. mansoni cercariae may be related to the ecology in the transmission site. The early shedding pattern char- acterizes schistosome populations originated from urbanized foci where man plays the main role in the parasite transmission; the late shedding pattern characterizes schistosome populations originated from sylvatic focus where a rat (R. rattus) is the main host. The late shedding of cercariae is considered as an adaptation favoring transmission to a murine host whose behavior is preferentially crepuscular. All studies concerned with the cercarial shed-

102 citations

Journal ArticleDOI
TL;DR: It is concluded that the occurrence of HP- and LP-infections indicates differences in reproductive capacity of the parasite.
Abstract: The effects of exposure of juvenileLymnaea stagnalis to one, two or, four miracidia ofTrichobilharzia ocellata on the following parameters were studied: infection rate, length of prepatent period, production of cercariae, growth and ovipository activity of the snails, and the weights of their accessory sex organs. An infection rate of 100% was established with all miracidial doses. Mortality of the snails was low in all experimental groups. In cercarial production high-(HP) and low-productive (LP) infections could be distinguished. An increase in miracidial dose at exposure results in an increase in the number of snails with HP-infections and decreases the length of the prepatent period of these infections. Snails with HP-infections grow faster than controls after day 14 post-exposure and show giant growth, while the accessory sex organs remain very small. The snails show hardly any ovipository activity. In all snails with HP-infections these effects are observed independent of the miracidial dose at exposure. Snails with LP-infections demonstrate no signs of gigantism, their accessory sex organs are almost identical to those of controls, and the snails show ovipository activity. It is concluded that the occurrence of HP- and LP-infections indicates differences in reproductive capacity of the parasite. HP-infections can only develop when the parasites can adjust the host to their requirements at an early stage of the infection.

87 citations

Journal ArticleDOI
TL;DR: Experience showed that emergence occurred in the light or in darkness while changes in the hydrogen-ion concentration of the water containing the snails had no effect on emergence, and there was some evidence that an increase of carbondioxide in the water slowed but did not inhibit emergence but depletion of oxygen had no apparent effect.
Abstract: 1. Observations on Fasciola hepatica in Limnaea truncatula under laboratory conditions showed that the cercariae did not emerge at temperatures below 9°C. Above 9°C. emergence proceeded indiscriminately up to the limit of experimental observation (26°C). 2. Experience showed that emergence occurred in the light or in darkness while changes in the hydrogen-ion concentration of the water containing the snails (within the range 5.5 to 8.5) had no effect on emergence. There was some evidence that an increase of carbondioxide in the water slowed but did not inhibit emergence but depletion of oxygen had no apparent effect. 3. In the laboratory, emergence could be induced by removing snails from dry habitats and immersing them in water or by removing snails from watery habitats and placing them in fresh water. We were unable to determine the exact physical.or chemical factors acting as a stimulus under such conditions.

81 citations

Journal ArticleDOI
W. Pflüger1
TL;DR: Long-term alternations between two temperature levels resulted in prepatent periods corresponding exactly to the proportional time-temperature products, however, slight accelerations of up to 7% and more could be observed when the prepatency began in a period of high temperature.
Abstract: Laboratory experiments have permitted the quantification of the developmental times (prepatent periods) ofSchistosoma mansoni in the snail over the whole possible range of constant temperatures. The basis relationship is satisfactorily described by a hyperbola of the formulay=268/(x−14.2),y being the minimum time from miracidial infection to cercariae shedding (in days)x the mean temperature, and 14.2 the theoretical temperature threshold (in °C). Cercariae production takes place within the limits of +16°C and 35°C, the number of cercariae being low and the mortality of snails high at the extreme values.

59 citations