Associations Between Two Trematode Parasites, an Ectosymbiotic Annelid, and Thiara (Tarebia) Granifera (Gastropoda) in Jamaica

J. Parasitol., 97(5), 2011, pp. 000–000 F American Society of Parasitologists 2011

ASSOCIATIONS BETWEEN TWO TREMATODE PARASITES, AN ECTOSYMBIOTIC ANNELID, AND THIARA (TAREBIA) GRANIFERA (GASTROPODA) IN JAMAICA Stacey A. McKoy, Eric J. Hyslop, and Ralph D. Robinson Department of Life Sciences, The University of the West Indies, Mona, Kingston 7, Jamaica. e-mail: [email protected]

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ABSTRACT: This work describes associations of Thiara (Tarebia) granifera, its larval trematode community, and Chaetogaster limnaei limnaei at a freshwater reservoir in Jamaica. Larvae of 2 trematodes were present, i.e., a notocotylid (15.3%) and Philophthalmus sp. (1.3%), in 3,575 T. granifera examined. The prevalence of both infections increased with snail shell length (H 5 56, P , 0.01, H 5 23.1, P , 0.01, respectively). Only 3.0% (n 5 595) of infected snails possessed reproductive stages, compared with 90.3% (n 5 2,980) of uninfected snails (x2 5 2,059.8, df 5 1, P , 0.001); both trematodes negatively impacted snail reproduction. Chaetogaster l. limnaei occurred within the mantle cavity of T. granifera with a prevalence of 2.3% (n 5 3,575); intensity ranged from 1 to 6 annelids. Notocotylid larvae occurred in 32.5% (n 5 83) of snails also harboring C. l. limnaei, compared with 14.9% (n 5 3,492) of snails lacking the annelid (x2 5 18.127; P , 0.001). Chaetogaster l. limnaei appears not to influence the recruitment of egg-transmitted, notocotylid infections to snails. Ingestion of emergent cercariae by the annelid was observed; this may impact transmission of the parasite. The article presents the first report of a notocotylid and C. l. limnaei in T. granifera, and of Philophthalmus sp. in Jamaica.

et al., 2005). However, no practical application of this association appears to have materialized (Rodgers et al., 2005). On the other hand, several reports have implicated T. granifera in displacement of snails on several Caribbean islands. Perez et al. (2001) reported local geographic displacement of Biomphalaria glabrata from the Dominican Republic; B. glabrata is a major intermediate host of Schistosoma mansoni in the region. Butler et al. (1980) in Puerto Rico, Prentice (1983) in St. Lucia, and Perera de Puga et al. (1994) in Cuba provided similar observations. Further investigations in the Dominican Republic suggest avoidance of T. granifera by B. glabrata is possibly based on chemical release by T. granifera, or by physical contact with a large number of individuals of T. granifera (Perez et al., 2001). Although there exists no overt evidence of influence of the rise of T. granifera on the freshwater fauna in Martinique (Pointier et al., 1998), concern, however, was expressed by Jacobson (1975) regarding the possible detrimental effects of T. granifera on species of the native Hemisinus (Thiaridae) in Cuba. In the present study, associations among T. granifera, its parasitic trematode larvae, and epizootic C. l. limnaei were investigated at a manmade reservoir in Jamaica.

Thiara (Tarebia) granifera Lamarck 1822 is a freshwater snail that was introduced to Jamaica in the late 1980s or early 1990s (Hyslop, 2003). The snail is now common in rivers, lakes, and man-made reservoirs throughout the island. Elsewhere in the Caribbean, T. granifera has been reported from Puerto Rico, Vieques, Dominican Republic, Grenada, Venezuela, Haiti, Antigua, Guadeloupe, Martinique, and Costa Rica (for review, see Sodeman, 1992). Thiara granifera is a parthenogenetic species; snails mature within 122 days, at which time juveniles as small as 2 mm are released from the cephalic brood pouch (Chantois et al., 1980; Prentice, 1983). The shell length of an adult varies from 6 to 40 mm, with an average length of 25 mm (Abbott, 1952; Chantois et al., 1980). The parasitological significance of T. granifera stems from observations that, depending on geographical location, the snails serve as first intermediate hosts for several species of trematodes that are known to parasitize birds, fish-eating mammals, and, occasionally, humans (Sodeman, 1991). At least 8 species of Chaetogaster Baer 1827 (Oligochaeta: Naididae) are distributed in nonfrigid zones globally. These annelids mainly occur on plants or pebbles in stagnant or slowflowing fresh or brackish water. They feed on algae or zooplankton, but sand grains and other undigestible materials are also found in the intestine (Streit,1977). Chaetogaster limnaei Baer 1827 differs from other species in the genus in that it forms ecological associations with gastropods, and other aquatic organisms. One subspecies, Chaetogaster limnaei vaghini Gruffydd 1965, is parasitic in freshwater snails, and mainly feeds on renal tissue (Buse, 1974), whereas another subspecies, C. l. limnaei Baer 1827, lives as a motile commensal in the mantle cavity or outer surfaces of freshwater snails and mussels (Esch and Fernandez, 1994). Chaetogaster l. limnaei feeds on materials foraged by their hosts, and on parasitic microorganisms that include trematode larvae otherwise associated with the internal tissues of the mollusk (Buse, 1974; Fernandez et al., 1991; Rodgers et al., 2005; Fried et al., 2008). The observed predatory behavior of C. l. limnaei on trematode larvae has led to discussions of its potential as a biological control agent that effectively reduces the likelihood of establishment of infections in susceptible snails (Michelson, 1964; Berg, 1973; Sankhurathri and Holmes, 1976; Fernandez et al., 1991; Callisto

MATERIALS AND METHODS Mona Reservoir (18u009N, 76u459W) is located on the eastern rim of Kingston, Jamaica. The reservoir has an area of 32,375 m2 and a maximum depth of about 11 m. Thiara granifera is the most common macroinvertebrate at the reservoir; the vertebrate fauna includes mainly teleost fishes, e.g., mosquitofish (Gambusia affinis), tilapia (Oreochromis spp.), and mountain mullet (Agonostomus monticola), as well as birds such as snowy egrets (Egretta thula), blue herons (Egretta caerulea), pied-billed grebes (Podilymbus podiceps), and brown pelicans (Pelecanus occidentalis). Monthly collections of T. granifera were conducted for 18 mo (April 1998–September 1999) at 4 locations around Mona Reservoir. Fifty snails from each location (200 in all) were measured from apex to aperture to the nearest 0.05 mm for all months (except May 1998, when, owing to inclement weather, 175 snails were collected), and placed in 2-mm size classes. A total of 3,575 snails was analyzed. Snails were cracked open, and the bodies depressed between microscope slides according to the method of Crews and Esch (1986). The prevalence of each type of trematode larva, and the prevalence and intensity of C. l. limnaei were recorded. Cercariae were identified with the use of taxonomic keys by Schell (1970). Observations of the color and formation of the body of each snail, and the occurrence of reproductive stages (eggs, embryos, juveniles) within the brood pouch were also made: For the purposes of this study, snails containing reproductive stages within their brood pouch were characterized as fecund. All statistical analyses were performed with the use of StatisticaH 6.0; parametric and nonparametric analyses were employed in analyses where indicated (Zar, 1999).

Received 26 March 2011; revised 5 May 2011; accepted 11 May 2011. DOI: 10.1645/GE-2494.1 0

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FIGURE 1. Mean shell length of Thiara granifera plotted against the prevalence of larvae of a notocotylid and Philophthalmus sp. for the period April 1998–September 1999 at Mona Reservoir, Jamaica. Vertical lines represent standard errors of the means.

RESULTS Of the 3,575 T. granifera collected at Mona Reservoir, most were distributed within the size range 14–16 mm (Fig. 1). The mean shell length of snails varied significantly during the sampling period (F 5 71.6, P , 0.01): the smallest snails were collected in August 1998 and June 1999 (12.48 ± 0.18 mm and 14.1 ± 0.17 mm, respectively), whereas the largest snails occurred in September and October 1998 (18.22 ± 0.19 mm and 18.12 ± 0.17 mm), respectively. Thiara granifera serves as intermediate host for larvae of 2 species of trematodes at the reservoir. One of the trematodes was monostomate, and belonged to the Notocotylidae; the other was Philophthalmus sp. (Philophthalmidae). The overall prevalence of infection with the notocotylid and Philophthalmus sp. in T. granifera was 15.3% and 1.3% (n 5 3,575), respectively. The 2 types of trematode larvae did not coexist within the snails sampled in the study. The notocotylid larvae occurred in snails in all the monthly samples and, although their prevalence appeared to peak in September of both 1998 and 1999 (Fig. 1), this was not statistically significant (F 5 1.73; P 5 0.06). Similarly, there was no significant difference in prevalence of Philophthalmus sp. larvae in snails during the 18-m sampling period. The prevalence of notocotylid infections increased with monthly mean shell length (R2 5 0.158, P , 0.0001): Prevalence was low (5.5%, n 5 200) in August 1998 when snails with the smallest mean length were collected, whereas the highest prevalence (39%, n 5 200) of notocotylids was recorded in September 1998 when large snails were in abundance. The prevalence of infection with Philophthalmus sp. was generally low throughout the 18-mo sampling period (Fig. 1). In the months of November 1998, and January and February 1999 relatively large-sized snails were present (17.26 ± 0.19 mm, 15.37 ± 0.14 mm and 15.54 ± 0.14 mm, respectively); during these months, prevalence of Philophthalmus sp. .3% (n 5 200). However, the association was not statistically significant. In comparison, however, the prevalence of both notocotylid and Philophthalmus sp. infection increased significantly with the 2-mm shell size class (H 5 56.0 and 23.1, respectively; P , 0.01) (Fig. 2).

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FIGURE 2. Prevalence of larvae of a notocotylid and Philophthalmus sp. within 2-mm shell-length classes of Thiara granifera at Mona Reservoir, Jamaica. The number of snails in each size class is indicated in parentheses.

Of 3,575 snails examined, 75.8% were fecund. However, only 3.0% (n 5 595) of the total number of trematode-infected snails were fecund, compared with 90.3% (n 5 2,980) of uninfected snails (x2 5 2,059.8, df 5 1, P , 0.001) (Table I). Sixteen (2.9%) of the 547 notocotylid-infected and 2 (4.2%) of the 48 Philophthalmus-infected snails were fecund. Snails infected with either trematode displayed limp bodies and uncoiled digestive glands, compared with fecund, nonparasitized snails, which were characterized by firm bodies, darkbrown, coiled digestive glands, and distinct branched ovaries. The digestive glands of notocotylid-infected snails were green in color and laden with rediae and cecariae measuring ,300 mm in length. In comparison, snails infected with Philophthalmus sp. displayed mottled, white and brown patches comprising the digestive gland. The white areas signified the presence of larval stages (rediae and cercariae measuring ,500 mm); brown areas represented the remains of the digestive gland. Rediae and cercariae of either trematode occurred initially within the digestive gland of the snails, but spread to the ovary in cases of heavy infections. Chaetogaster l. limnaei was found within the mantle cavity and on the outer body of T. granifera. The overall prevalence of C. l. limnaei in T. granifera at Mona Reservoir was 2.3% (n 5 3,575); infection intensity ranged from 1 to 6 annelids. No adverse physical effects of C. l. limnaei were observed in the tissues of nontrematode-parasitized snails. Notocotylid larvae occurred in 32.5% (n 5 83) of snails also harboring C. l. limnaei, compared with 14.9% (n 5 3,492) of snails lacking the annelid (x2 5 18.127; P , 0.001) (Table II). Notocotylid cercariae were observed within the transparent intestine of C. l. limnaei, and also in histological sections. In comparison, only 1 (1.7%) of the 56 snails harboring C. l. limnaei alone was infected with Philophthalmus sp., whereas 47 (1.6%) of 2,972 snails that had neither C. l. limnaei nor notocotylids were infected with Philophthalmus sp. No evidence of predation of the parasite larvae by C. l. limnaei was observed in the single infected snail collected. DISCUSSION The natural distribution of T. granifera includes India, Sri Lanka, southern Japan, the Philippines, French Polynesia, and

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TABLE I. Contingency table showing the frequency of fecundity and the occurrence of trematode larvae in Thiara granifera at Mona Reservoir, Jamaica.

TABLE II. Contingency table showing the frequency of occurrence of notocotylid larvae and Chaetogaster limnaei limnaei in Thiara granifera at Mona Reservoir, Jamaica.

Fecund Trematode larvae Present Absent Total

0

Notocotylid larvae

Yes

No

Total

Chaetogaster l. limnaei

Yes

No

Total

18 2,693 2,711

577 287 864

595 2,980 3,575

Present Absent Total

27 520 547

56 2,972 3,028

83 3,492 3,575

study, notocotylid infection resulted from ingesting eggs found in bird stools, whereas snails harboring Philophthalmus sp. larvae become infected by means of penetrating miracidia. The viability of trematode eggs over longer periods (Esch et al., 2001), in contrast to miracidia, which survive only 24–72 hr (Esch and Fernandez, 1994) is also a likely contributing factor for the high prevalence of notocotylids at the reservoir. Thiarids tend to reproduce largely in summer/warmer months (Chantois et al., 1980; Dudgeon, 1986), which may explain the high frequency of smaller-size snails in the summer months (August 1998 and June 1999) compared with cooler months (September and October 1998), which had, on average, the largest snails. Correspondingly, lower notocotylid prevalence was observed in August 1998 and June 1999 when snails were younger (,12 mm), and may be less likely to have been exposed to infective stages than older snails that were numerous in September and October 1998. Grazing activities also increase in older snails, thereby increasing chances of ingesting trematode eggs (Curtis and Hurd, 1983; Fernandez and Esch, 1991; Kuris and Lafferty, 1994; McCurdy et al., 2000). Further, miracidia are generally attracted to larger-size snails, as they are more active and more of the exposed body could be targeted by miracidia (Lim and Heyneman, 1972), which may explain any tendency of Philophthalmus sp. to occur more frequently in larger snails. According to Sorensen and Minchella (2001), trematodes with rediae cause severe mechanical damage to host tissue when compared with parasites possessing just sporocyst stages. In the present study, rediae of both trematodes appeared to be responsible for the destruction of the digestive gland and, eventually, the ovary of T. granifera, with approximately 3% of total infected snails possessing eggs, embryos, or juveniles in the brood pouch, compared with 90% of uninfected snails. Because the ovary appears not to be targeted by the early stages of infection by either parasite, some snails are probably still able to reproduce (as observed in 3% of total infected snails); however, once the ovary is destroyed, reproduction is inhibited (Hurd, 2001). The ecological impact of such parasitic castration, though potentially significant (see Lafferty and Kuris, 2009) remains to be investigated in T. granifera. Early work by James (1965) on the prosobranch Littorina saxatilis tenebrosa indicated the digestive gland of healthy (uninfected) snails to be dark brown. However, the presence of trematode larvae resulted in changes in coloration and destruction of the visceral hump comprising the digestive gland and gonad. In the present study, the physical appearance of the digestive gland of T. granifera was a reliable indicator of trematode infection. The coiled and dark brown appearance of digestive gland of uninfected snails indicates that it is rich in nutrients (glycogen) required for growth and reproduction of the snail (Fretter and

Hawaii (Abbott, 1952). The snail was introduced into Florida, probably from Hawaii, in the 1940s (Rader, 1994), and has since spread through the islands of the Caribbean (Pointier et al., 1998). Having arrived in Jamaica about 20 yr ago, the T. granifera snail is common in many freshwater water systems, but appears to be excluded from areas of high elevation (.1,000 m above sea level) or salinity (.0.5 ppt) (Hyslop, 2003). Thiara granifera is well established as an intermediate host for several species of trematodes, particularly heterophyids and philophthalmids (Murray and Haines, 1969; Nollen and Murray, 1978; Sodeman, 1991). Despite of reports to the contrary, the snail is apparently not a host of the human lung fluke Paragonimus westermani or, apparently, of Metagonimus yokogawai (see Sodeman, 1992). On the other hand, the present study appears to be the first record of a notocotylid occurring in T. granifera, although a new notocotylid cercaria, Cercaria viskhapatnamensis III sp. nov., was reported from the hepatopancreas of congeneric T. tuberculata collected in India (Dhanumkumari et al., 1992). We also report for the first time the occurrence of Philophthalmus sp. in Jamaica. Waders such as herons are known definitive hosts of the notocotylids (Skirnisson et al., 2004), and waterfowl, among others, harbor philophthalmids (Murray, 1964, Nollen and Murray, 1978). Potential sources of infection at Mona Reservoir are snowy egrets, blue herons, pied-billed grebes, and brown pelicans, all of which are common, year-round residents in Jamaica (Goodbody and Goodbody, 1994, 1998; Raffaele et al., 1998; Haynes-Sutton et al., 2009). The 2 species of trematode larvae observed in the study did not coexist within any of the snails sampled. Although it is possible that this observation may result from the relatively low prevalence (1.3%; n 5 3,575) of Philophthalmus sp. at the reservoir, double infection of trematode larvae in snails is usually infrequent (Sousa, 1983; Kuris and Lafferty, 1994; Lafferty et al., 1994). A possibility also exists that some form of interaction occurs between the parasite larvae that results in competitive exclusion within the snail host (see Kuris and Lafferty, 1994; Lafferty and Kuris, 2009). According to Esch et al. (2001), in natural settings, trematode prevalence in snails usually ranges from 5 to 10%, with a few exceptions as high as 60%. In addition, parasites with long latent periods in snails (time from infection to cercariae release) are likely to generate low prevalence (Anderson and May, 1979): The comparatively long latent period (exceeding 3 mo) that is typical of philophthalmids (Alicata, 1962; Ismail and Arif, 1993; Nollen and Kanev, 1995) may help to explain the low prevalence of Philophthalmus sp. at Mona Reservoir. Further, parasite prevalence appears to be related to the nature of the infective stage, whether egg or miracidium (Fernandez and Esch, 1991; Williams and Esch, 1991; Snyder and Esch, 1993). Thiara granifera is a detritus feeder (Sodeman, 1992). In the present

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Sankhurathri and Holmes (1976) have indicated that cercariae with lengths of up to 500 mm are readily consumed by C. l. limnaei compared with much larger cercariae such as those of Echinostoma trivolis that may reach 900 mm. The role, if any, of C. l. limnaei in controlling recruitment of miracidia of Philophthalmus sp. by T. granifera can be neither confirmed nor disproved by our data set, and awaits further study. Notocotylid trematode infections are not zoonotic. However, human cases of philophthalmosis have been previously reported in Yugoslavia, Sri Lanka, Thailand, Mexico, and the United States (Rajapakse et al., 2009), where the adult parasite was identified as Philophthalmus lacrimosus, Philophthalmus palpebrarum, or uncertain species. No cases of human philophthalmosis have been reported in Jamaica.

Graham, 1994). However, the presence of trematode larvae results in loss of nutrients (Cheng and Snyder, 1962), hence the discoloration and limp structure of infected T. granifera. Chaetogaster limnaei has been recorded as an ectosymbiont in several genera of freshwater snails, e.g., Lymnaea, Physa, Planorbis, Biomphalaria, and Melanoides on several continents (Buse, 1974; Esch and Fernandez, 1994; Callisto et al., 2005), but the present study appears to represent the first report of the annelid occurring in association with T. granifera. Studies by Fernandez et al. (1991) indicated that C. l. limnaei was more likely to occur in snails (Helisoma anceps) shedding cercariae (Halipegus occidualis) than nonshedding snails, and that the cercariae served as a food resource for C. l. limnaei. Similarly, Fried et al. (2008) observed digestion and absorption of cercariae infecting Helisoma trivolis in the gut of C. limnaei, and confirmed cercaria larvae as a nutrient source. Hence, the presence of notocotylid cercariae in the gut of C. l. limnaei at Mona Reservoir suggests the larvae serve as a food source for the annelid, possibly affecting recruitment to the subsequent host. In the present study, however, notocotylid larvae were twice as likely (32.5%, n 5 83) to occur in snails also harboring C. l. limnaei, compared with snails that did not possess the annelid (14.9%, n 5 3492). In marked contrast, Rodgers et al. (2005) reported a significantly higher prevalence (70%) of Schistosoma mansoni in Biomphalaria glabrata that were devoid of C. l. limnaei, compared with 34% of those that were colonized by the annelid, whereas several other studies (Michelson, 1964; Sankhurathri and Holmes, 1976; Ibrahim, 2007) confirmed the potential protective action of C. l. limnaei against trematode infection in snails. Clearly, the impact of C. l. limnaei on the success of parasite recruitment by the snail host is dependent on the mode of transmission of the infective stage, whether by penetrating miracidia or ingestion of embryonated eggs by the snail. Observations by Sankhurathri and Holmes (1976) suggest the feeding pattern of C. l. limnaei (whereby the annelid constantly protrudes its anterior portion into the water combined with the darting and expansion of its mouth) prevents or obstructs miracidia that penetrate the snail host (Physa gyrina) directly. However, this feeding behavior would not affect recruitment of notocotylids, as snails become infected by eating parasite eggs. For example, C. l. limnaei was not effective in controlling infection by Notocotylus urbanensis in P. gyrina, compared with Echinoparyphium recurvatum, which possesses externally invading miracidia (Sankhurathri and Holmes, 1976), nor did C. l. limnaei protect H. anceps against H. occidualis as snails also become infected by ingesting eggs in stool (Williams and Esch, 1991; Zelmer and Esch, 1998). Histological studies by Murrills et al. (1988) revealed that following ingestion of eggs of Notocotylus attenuatus the opercular cord injects the sporocyst through the gut wall of the snail host (Lymnaea peregra). Hence, although C. l. limnaei does not impact the recruitment of notocotylid larvae in T. granifera at Mona Reservoir, ingestion of emergent cercariae by the annelid as a food source may have some influence further transmission of the parasite. In the present study, only 1 snail harbored both Philophthalmus sp. and C. l. limnaei, and there was no evidence of predation on cercariae. Notwithstanding the larger size of philophthalmid cercariae (,500 mm) compared with notocotylid cercariae (,300 mm), size alone is unlikely to deter C. l. limnaei from consuming them. Studies by Fernandez et al. (1991) and

ABBOTT, R. T. 1952. A study of an intermediate snail host (Thiara granifera) of the oriental lung fluke (Paragonimus). Proceedings of the United States National Museum 102: 71–115. ALICATA, J. E. 1962. Life cycle and developmental stages of Philophthalmus gralli in the intermediate and final hosts. Journal of Parasitology 48: 47–54. ANDERSON, R. M., AND R. M. MAY. 1979. Prevalence of schistosome infections within molluscan populations: Observed patterns and theoretical predictions. Parasitology 79: 63–94. BERG, C. O. 1973. Biological control of snail–borne diseases: A review. Experimental Parasitology 33: 318–330. BUSE, A. 1974. The relationship of Chaetogaster limnaei (Oligochaeta: Naididae) with a variety of gastropod species. Journal of Animal Ecology 43: 821–837. BUTLER, J. M., F. F. FERGUSON, J. R. PALMER, AND W. R. JOBIN. 1980. Displacement of a colony of Biomphalaria glabrata by an invading population of Tarebia granifera in a small stream in Puerto Rico. Caribbean Journal of Science 16: 73–79. CALLISTO, M., P. MORENO, J. F. GONCALVES, W. R. FERREIRA, AND C. L. Z. GOMES. 2005. Malacological assessment and natural infestation of Biomphalaria straminea (Dunker, 1848) by Schistosoma mansoni (Sambon, 1907) and Chaetogaster limnaei (K. Von Baer, 1827) in an urban eutrophic watershed. Brazilian Journal of Biology 65: 1–13. CHANTOIS, B. N., J. M. BUTLER, F. F. FERGUSON, AND W. R. JOBIN. 1980. Bionomics of Tarebia granifera (Gastropoda: Thiaridae) in Puerto Rico, an Asiatic vector of Paragonimus westermani. Caribbean Journal of Science 16: 81–90. CHENG, T. C., AND R. W. SNYDER. 1962. Studies on host–parasite relationships between larval trematodes and their hosts. I. A review. II. The utilization of the hosts glycogen by the intramolluscan larvae of Glypthelmins pennsylvaniensis Cheng, and associated phenomena. Transactions of the American Microscopical Society 81: 209–228. CREWS, A. E., AND G. W. ESCH. 1986. Seasonal dynamics of Halipegus occidualis (Trematoda: Hemiuridae) in Helisoma anceps and its impact on fecundity of the snail host. Journal of Parasitology 72: 646–651. CURTIS, L. A., AND L. E. HURD. 1983. Age, sex and parasites: Spatial heterogeneity in a sandflat population of Ilyanassa obsoleta. Ecology 64: 819–828. DHANUMKUMARI, C., K. H. RAO, AND K. SHYAMASUNDARI. 1992. Cercaria visakhapatnamensis 3 sp. nov. (Trematoda: Heterophyidae) from a thiarid gastropod Thiara tuberculata (Mu¨ller) from Visakhapatnam, India. Indian Journal of Helminthology 43: 119–123.

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ACKNOWLEDGMENTS The authors would like to thank The National Water Commission of Jamaica. Special thanks are due to Mr. A. Benjamin (Operations Manager), Mr. W. Davis (Supervisor, Mona Water Treatment Plant), and Ms. S. Fennell and Ms. S. Guy for facilitating access to Mona Reservoir. The work was undertaken while 1 of us (S.A.M.) was a research student at the University of the West Indies, Jamaica.

LITERATURE CITED

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THE JOURNAL OF PARASITOLOGY, VOL. 97, NO. 5, OCTOBER 2011

Authors Queries Journal: The Journal of Parasitology Paper: para-97-05-18 Title: ASSOCIATIONS BETWEEN TWO TREMATODE PARASITES, AN ECTOSYMBIOTIC ANNELID, AND THIARA (TAREBIA) GRANIFERA (GASTROPODA) IN JAMAICA Dear Author During the preparation of your manuscript for publication, the questions listed below have arisen. Please attend to these matters and return this form with your proof. Many thanks for your assistance

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