Aspidogastrid and Digenetic Trematode Single and Double Infections in the Gastropod, Elimia Livescens, from the Upper Cuyahoga River

Home , Aspidogaster conchicola, Aspidogastrea, Elimia livescens

Proc. Helminthol. Soc. Wash. 54(2), 1987, pp. 200-203

Aspidogastrid and Digenetic Trematode Single and Double Infections in the Gastropod, Elimia livescens, from the Upper Cuyahoga River

MARTIN K. HUEHNER Biology Department, Hiram College, Hiram, Ohio 44234

ABSTRACT: Elimia livescens were collected from the Upper Cuyahoga River, Ohio, from July 1978 to December 1983. Aspidogaster conchicola, plagiorchid, heterophyid, opecoelid, strigeid, and philophthalmid single and double infections occurred in 844 snails. Larger snails (> 16 mm) had significantly greater prevalence of digenean infections. Aspidogaster conchicola was significantly more prevalent and intense during colder months of No- vember through April and in snails with digenean parthenitae. The number of gravid A. conchicola showed the same distribution. This and previous studies of experimental aspidogastrid and digenean infections in E. livescens suggest that concurrent digenean infections may be beneficial to the establishment and development of A. conchicola. KEY WORDS: Trematoda, Digenea, Aspidogastrea, Aspidogaster conchicola, Elimia livescens, polyspecific infections, parasite seasonally, cercaria, snails, Ohio.

Gastropods are very frequently parasitized by quently squashed between microscope slides to search asexual reproductive stages of digenetic trema- for smaller worms by compound microscopy. Aspi- todes, but several operculate snail species are dogastrids were isolated, heat-fixed under minimal coverslip pressure, examined for the presence of eggs, also known to serve as definitive or intermediate measured with an ocular micrometer, and later stained hosts for various aspidogastrid trematodes with acetocarmine for whole mounts. Digenean infec- (Rohde, 1972, 1975; Hendrix et al., 1985). Rohde tions, identified by type and cercariae, were treated as and Sandland (1973) reported the aspidogastrid above. Chi-square 2x2 contingency tables and 2-tailed values of Chi-square were used to evaluate statistical Lobatostoma manteri to occur more frequently significance of data. in an Australian prosobranch snail infected with digenean parthenitae and this is the sole record Results of naturally occurring aspidogastrid-digenean Of a total of 1,887 E. livescens examined, 844 double infections to date. Using Elimia livescens were found to contain either single or double as hosts, Huehner (1975) experimentally dem- trematode infections. Snails with single infec- onstrated that Aspidogaster conchicola could es- tions consisted of 652 plagiorchid (xiphidiocer- tablish itself and successfully develop in snails cous cercariae; 2 sizes possibly representing 2 with preexisting plagiorchid, opecoelid, and species), 58 A. conchicola, 58 heterophyid (pleu- strigeid infections, and that these infections could rolophocercous cercariae; probably Apophallus occur in nature. The present study reports sea- sp.), 11 strigeid (pharyngeate furcocercous cer- sonality of such infections in E. livescens from cariae), and 1 each of an opecoelid (microcercous the Upper Cuyahoga River, where A. conchicola cercariae) and a philophthalmid (gymnocepha- also parasitizes the snail Cipangopaludina chi- lous cercariae quickly producing lightbulb-shaped nensis and several unionid mussel species. cysts). Aspidogaster conchicola occurred in con- junction with digeneans to produce 62 double Materials and Methods infections (48 plagiorchid, 12 heterophyid, 1 Elimia livescens were collected by hand or dip net strigeid, and 1 opecoelid). Only a single strictly from a 25-m section of the Cuyahoga River 0.3 km digenean double infection (plagiorchid and strig- upstream from the Ohio State Route 82 bridge (Man- eid) was observed. The remaining 1,043 snails tua, Ohio) on 7 August 1978, 24 May 1981, and 31 were uninfected. August and 14 December 1982, and on the first day of each month during 1983. Snails were maintained in Snails examined ranged in spire height from 8 aerated river water at 10°C and examined not more to 24 mm, with an average of 15.4 mm and a than 7 days after collection. Each snail was measured median of 15.8 mm. Size of collected snails did for spire height and anesthetized with menthol prior not vary significantly with season (x2 = 21.3 for to dissecting out the viscera, which were teased apart on a glass microscope slide. The tissues were first 16 df; P > 0.05), but infection prevalence varied searched, by dissecting microscopy, for larger A. con- with snail size. Frequency of trematode infec- chicola and digenean parthenitae, and were subse- tions of all kinds was 79% for snails al and above

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Table 1. Shell spire height and trematode infections Table 2. Prevalence and intensity of A. conchicola in of Elimia livescens. E. livescens snails with concurrent digenean infections.

No. snails infected/ Infection prevalence and intensity* uninfected spire height Aspido- Aspido- gastrid Chi-square Chi-square gastrid + mm mm X2 P alone digenean X2 P All infections* 177/483 560/667 131.7 <0.001 Prevalence Plagiorchid 134/526 566/661 122.7 <0.001 All digenean 58/1,101 62/786 5.3 <0.05 Heterophyid 13/647 57/1,170 8.6 <0.01 Plagiorchid 58/1,101 48/700 2.0 <0.2 Aspidogastrid 38/622 82/1,145 0.6 >0.05 Heterophyid 58/1,101 12/70 16.5 <0.001 All double infections 1 1/649 52/1,175 8.8 <0.01 Intensity All digenean 62/1,101 90/786 17.7 <0.001 * Includes groups (opecoelid, etc.) not individually listed. Plagiorchid 62/1,101 72/700 11.5 <0.001 Plagiorchid, heterophyid, and aspidogastrid numbers include Heterophyid 62/1,101 16/70 24.1 <0.001 double infections. Gravid A. conchicola intensity All digenean 9/1,101 26/786 15.0 <0.001 and 21% below the rounded median of 16 mm Plagiorchid 9/1,101 19/700 9.7 «3.01 Heterophyid 9/1,101 6/70 28.6 <0.001 spire height (Table 1). Plagiorchid infections ac- counted for the majority of this distribution, * Prevalence = number of infected snails out of total snails whereas heterophyids and all double infections in each group; intensity = number of A. conchicola found in were of lesser significance. No host size prefer- each group of snails. ence was noted for A. conchicola. Aspidogaster conchicola displayed significant ing a distribution that was almost inversely mir- changes in infection prevalence and intensity be- rored by that of A. conchicola. Although heter- tween otherwise uninfected snails and those with ophyid prevalence showed no significant concurrent digenean infections (Table 2). Al- seasonality, aspidogastrid/heterophyid and pla- though A. conchicola prevalence was not signif- giorchid/aspidogastrid double infections were icantly greater in 2 of the groups (all digenean more common in cold months (Table 3). Inten- pooled and plagiorchid), intensity of infection sity of A. conchicola infections also varied with was. Intensity ranged from 1 to 2 worms in single season (Table 3), being greater in cold than warm infections, from 1 to 12 worms in snails with months for all single and double infections. In- concurrent plagiorchid infections, and from 1 to terestingly, A. conchicola showed the least sea- 2 worms in snails with concurrent heterophyid sonality of intensity alone and the greatest sea- infections. Fifty-eight percent of A. conchicola sonality in plagiorchid-infected snails that were found came from the 786 (41.7%) snails with least abundant during cold months. The number digenean parthenitae, while the remaining 1,101 of gravid A. conchicola was also significantly snails (58.3%) contained only 42%. Not only was greater in cold months. the greater portion of the A. conchicola popula- tion found in those snails with digenean infec- Discussion tions, but this group also carried the greatest The strong correlation between larger E. li- number of gravid worms (nearly triple that of vescens and their increased probability of dige- single A. conchicola infections). netic trematode infection is difficult to explain. Significant seasonal differences in infection Cheng (1971) showed that digenean infections prevalence were noted by comparing infection sometimes caused snails to grow exceptionally frequency of snails collected during warm months large shells by modifying their calcium metab- (8/78, 8/82, and 5/83-10/83) to that of snails olism. Although this phenomenon may occur in collected in cold months (11/82, 1/83-4/83, and the host-parasite systems presently studied, it is 11/83-12/83). With the exception of hetero- of uncertain consequence to E. livescens, which phyids, infection prevalence showed significant has an estimated life in the field of up to 4 yr seasonality (Table 3). Plagiorchids reached a (Dazo, 1965). During such a lifespan, several in- maximum in July 1983 (102/128 snails) and a fections could be gained and lost. The present minimum in March 1983 (16/125 snails), show- observations could simply result from older,

Table 3. Seasonality of infection prevalence and intensity in E. livescens.

Infection prevalence and intensity* Chi-square Warm monthsf Cold months

Prevalence Aspidogastrid 51/993 69/894 5.3 <0.05 Plagiorchid 472/993 228/894 97.8 < 0.001 Heterophyid 39/993 31/894 2.8 <0.1 Aspidogastrid/plagiorchid 25/472 23/228 4.6 <0.05 Aspidogastrid/heterophyid 3/39 9/31 5.5 <0.05 Aspidogastrid/all digenean 28/518 34/268 12.9 <0.001 Intensity Aspidogastrid/all snails 56/993 96/894 14.0 <0.001 Gravid aspidogastrid/all snails 11/993 24/894 6.2 <0.02 Aspidogastrid/all digenean 32/518 58/268 31.8 <0.001 Aspidogastrid alone 27/521 53/666 3.1 <0.1 Aspidogastrid/plagiorchid 29/472 43/228 21.1 <0.001 Aspidogastrid/heterophyid 4/39 18/31 9.5 <0.01

* Prevalence = number of infected snails out of total snails in each group; intensity = number of A. conchicola found in each group of snails, t May-October. larger snails gaining greater exposure to trema- snails with only A conchicola present (see Hueh- tode transmission stages because they may eat ner and Etges, 1977 for A. conchicola develop- or move more. ment studies). The presence of plagiorchid spo- Rohde and Sandland (1973) reported a signif- rocysts had no significant effect on aspidogastrid icant tendency for the aspidogastrid, Lobato- growth, but a triple infection (opecoelid/plagior- stoma manteri, to occur more frequently in snails chid/aspidogastrid) produced significantly (P < with digenean infections and suggested that re- 0.01) larger A conchicola. These results suggest duced resistance to a second infection may be that some digeneans may produce beneficial ef- responsible. Present findings demonstrate more fects on concurrent aspidogastrid infections and strongly that digenean infection significantly in- that they were not harmful in any instance. These creases the probability of aspidogastrid infection findings are consistent with the present report of or vice versa. The mechanism that produces this greater A. conchicola prevalence, intensity, and relationship is not known but could be either frequency of gravid worms in snails with dige- physiological (reduced resistance) or behavioral nean infections. (i.e., increased feeding or exposure to eggs or Infection seasonally reported here for A. con- miracidia). chicola is opposite that reported for L. manteri The presently observed high frequency and (Rohde and Sandland, 1973). Increased preva- thereby apparently low antagonism between as- lence, intensity, and frequency of gravid A. con- pidogastrid and digenean double infections may chicola during cold months has no explanation be explained by the different microhabitats they at this time although cycles other than seasonal occupy within the snail host. Aspidogaster con- ones may be involved. Steinberg (1931) reported chicola is coelozoic within digestive diverticulae that A. conchicola from the unionid Pseudoan- and digeneans are histozoic in either hepatopan- odonta anatina produced eggs from mid-May to creas hemolymph spaces or the gonads. No direct October, and infection prevalence did not fluc- contact between parasites is therefore possible as tuate during the year. Such seasonality was not long as excessive damage does not occur. By ex- evident in the present study. It is possible that perimentally infecting digenean-bearing snails the E. livescens infrapopulation of A. conchicola with A. conchicola, Huehner (1975) found that in the Cuyahoga River is not representative of E. livescens with strigeid infections produced sig- its suprapopulation in other hosts from this and nificantly larger (P < 0.01) worms and that ma- other localities. turity was reached 60 days earlier than in control While profound complexities cloud our un-

Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 54, NUMBER 2, JULY 1987 • 203 derstanding of host-parasite ecology, the inter- trids (Trematoda) and their hosts in North Amer- actions between polyspecific infections and their ica. Proceedings of the Helminthological Society of Washington 52:289-296. hosts are even further veiled from scrutiny. Pre- Huehner, M. K. 1975. Studies on the biology of As- vious studies of intramolluscan intertrematode pidogaster conchicola von Baer, 1827, Cotylaspis interactions (Joe et al., 1965; Lim and Heyne- insignis Leidy, 1858, and Cotylogasteroid.es bar- man, 1972) have focused on digenean parthen- rowi Huehner and Etges, 1972. Doctoral Disser- itae in either direct or indirect antagonism. The tation, University of Cincinnati, Cincinnati, Ohio. , and F. J. Etges. 1977. The life cycle and present report is based on an obviously more development of Aspidogaster conchicola in the indirect relationship between trematodes in sep- snails, Viviparus malleatus and Goniobasis lives- arate microhabitats of the same host and some- cens. Journal of Parasitology 63(4):669-674. times the same host organ. This novel system Joe, L. K., P. F. Basch, and T. Umathevy. 1965. An- tagonism between two species of larval trematodes offers numerous opportunities for further inves- in the same snail. Nature (London) 206:422-423. tigation. Lim, H., and D. Heyneman. 1972. Intramolluscan intertrematode antagonism: a review of factors in- Acknowledgments fluencing the host-parasite system and its possible Thanks go to Dennis J. Taylor and the re- role in biological control. Recent Advances in Par- asitology 10:191-268. viewers for their helpful comments on improving Rohde, K. 1972. The Aspidogastrea, especially Mul- this manuscript. ticotyle purvisi Dawes, 1941. Recent Advances in Parasitology 10:76-152. Literature Cited . 1975. Early development and pathogenesis of Lobatostoma manteri Rodhe (Trematoda: As- Cheng, T. C. 1971. Enhanced growth as a manifes- pidogastrea). International Journal of Parasitology tation of parasitism and shell deposition in par- 5:597-607. asitized molluscs. Pages 103-137 in T. C. Cheng, -, and R. Sandland. 1973. Host-parasite rela- ed. Aspects of the Biology of Symbiosis. Univer- tions in Lobatostoma manteri Rohde (Trematoda: sity Park Press, Baltimore, Maryland. Aspidogastrea). Zeitschrift fur Parasitenkunde 42: Dazo, B. C. 1965. The morphology and natural his- 115-136. tory of Pleurocera acuta and Goniobasis livcscens Steinberg, D. 1931. Die Geschlechtsorgane von As- (Gastropoda: Cerithiacea: Pleuroceridae). Mala- pidogaster conchicola Baer und ihr Jahreszyklus. cologia 3:1-80. Zoologischer Anzeiger 94:153-170. Hendrix, S. S., M. F. Vidrine, and R. H. Hartenstine. 1985. A list of records of freshwater aspidogas-

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