Photocycle-Dependent Emergence by Cercariae of Halipegus occidualis from Helisoma anceps, with Special Reference to Cercarial Emergence Patterns as Adaptations for Transmission

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: