The life-cycle, ecology and host specificity of the freshwater leech Alboglossiphonia polypompholyx (Glossiphoniidae) in Egypt

Hydrobiologia 222: 173-178, 1991. C 1991 Kluwer Academic Publishers. Printed in Belgium. 173 The life-cycle, ecology and host specificity of the freshwater leech Alboglossiphonia polypompholyx (Glossiphoniidae) in Egypt N.A. El-Shimy & Ronald W. Davies Department of Zoology, Faculty of Science, University of Assiut, Assiut, Egypt; Aquatic Ecology Research Group, Division of Ecology, Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4 Received 5 July 1990; in revised form 18 December 1990; accepted 21 December 1990 Key words: life cycle, A. polypompholyx, leech, reproduction, host, Egypt Abstract Alboglossiphonia polypompholyx spends most of its life cycle endoparasitic in the mantle cavity of the snail Bulinus truncatus - possibly its only host. Adult A. polypompholyx leaves the snail about one month before the commencement of egg-laying. Hatching occurred after about 15 d and after brooding on the venter of the parent for 7-10 d, the young briefly become free-living before entering the mantle cavity of B. truncatus. Within the mantle cavity, A. polypompholyx feeds and grows for 16-20 weeks before leaving the snail as adults. In the field and in laboratory experiments, adult leeches left the snails in August/September and January with cocoons produced in October/November and February/March, respectively. Free-living adult leeches do not feed and die 1-2 months after the cessation of brooding. Introduction Few studies have been conducted on the ecology and life cycles of freshwater leeches of Egypt, although El-Shimy (1987) and Hussein et al. (1988) published some preliminary data on Helobdella conifera (Moore, 1933), Batracob- delloides tricarinata (Blanchard, 1897) and Barbronia assiuti Hussein & El-Shimy, 1982. The apparently endemic species Alboglossiphonia poly- pompholyx, described from Egypt (Oosthuizen et al., 1988), is recorded but nothing is known of its ecology. Based on field collection and labora- tory experiments, this paper describes the life- cycle of A. polypompholyx and its feeding ecology. As most small species of Glossiphoniidae are habitually malacophagous, some feeding almost exclusively on aquatic snails, and Alboglossiphonia heteroclita (L.) forms different associations with molluscs (Wilkialis, 1964; Gruffydd, 1965; Hatto, 1968), the prey/hosts of A. polypompholyx were first looked for within this phylum. The abundant species of Mollusca at sites containing A. poly- pompholyx were examined for leeches and in a series of laboratory experiments prey/host prefer- ence and specificity determined. Material and methods Leech collections were made from 25 sites dis- tributed all over Egypt (Fig. 1), although Alboglossiphonia polypompholyx was recorded from only 12 sites (Table 1). The sites at Asyl{ 174 Fig. 1. Map of Egypt showing collecting sites. and Shtg were sampled monthly, but others were only visited seasonally (spring, summer, autumn, winter), from June 1987 to February 1988 and September 1988 to May 1989. Over the June 1987-May 1989 period, field water tempera- ture ranged between 18-24 C, pH 7.5-8.5, dis- solved oxygen 65-100% and conductivity 27-45 x 10-5 - . At each site a 30 min hand collection of leeches was made from each solid substrate type (rocks, stones, etc.) including vegetation (primarily Eichhornia crassipes). The vegetation was exam- Table 1. Sites from which Alboglossiphonia polypompholyx were collected. m - sampled monthly, s - sampled seasonally (spring, summer, autumn, winter). Site Location Sampling al-Mahmidya canal near Damanhir 31 12' N/30° 28' E s TalhA canal in TalhA City 31° 02' N/31° 22' E s al-Simbellawein canal in 30° 43' N/31° 28' E s al-Simbellawein City Mit Heby§ canal TantA 30° 41' N/31° 02' E s Nile at al-Giza City 30 02' N/31° 13' E s al-Sont canal (AsyCt) 27 11' N/31° 11' E m al-Raiesia canal (Asyfit) 27° U11' N/31 11' E m Tema irrigation canal (SUh8A) 26° 55' N/31° 26' E m TehIt irrigation canal (SUhag) 26° 46' N/31° 30' E m Sihlg City 26°40' N/31° 35' E m Nile (QinS) 26 ° 10' N/32° 42' E s Nile (Luxor) 25 42' N/32 40'E s ined leaf by leaf with a hand lens ( x 2.5 magnifica- tion). The common leeches of Egypt (Barbronia assiuti, Helobdella conifera and Batrocobdelloides tricarinata) were collected from all substrate types including the vegetation but A. polypompholyx was never collected from plants. The numbers of A. polypompholyx collected each month from the Asyt and Shdg sites are shown in Table 2. Table 2. Number of Alboglossiphonia polypompholyx collected each month from the Asyfit and Sfihg sites, with number carrying eggs in parentheses. Sites Asyit Sfihag Months al-Sont al-Raiea Tema Tahta Slhag city 1987 0 0 0 0 0 June 0 0 0 0 0 July 0 0 0 0 0 August 5 0 2 3 0 September 22 (9) 3 0 5 (0) 1 October 0 0 0 0 0 November 0 0 0 0 0 December 1988 January 52 15 12 40 5 February 12 (8) 7 (7) 0 17 (13) 2 September 2 0 0 3 0 October 9 (3) 2 (2) 1 2 (2) 1 November 1 0 0 2 0 December 0 1 0 0 1 1989 January 170 95 55 42 186 February 37 (11) 41 (19) 12 (5) 15 (14) 5 (5) March 19 (8) 8 0 12 3 April 0 0 0 0 0 May 0 0 0 0 0 175 One hundred specimens of each of the six com- mon snail species (Biomphalaria alexandrina, Bulinus truncatus, Lymnaea cailliaudi, Gyraulus mareoticus, Physa acuta and Theodoxus niloticus) in the Asyflt and Shdi sites were collected monthly from September 1987 through February 1988 and from September 1988 through March 1989. The shell of each snail was carefully removed and the soft parts examined for leeches under magnification ( x 20). Four snail species were selected for experi- mental studies: Bulinus truncatus, Biomphalaria alexandrina (the two Egyptian bilharzia-carrying snails), Physa acuta and Theodoxus niloticus. To determine which species are hosts of A. polypompholyx, 100 specimens of each of the six snail species were collected from Silha in January and maintained (20 per 2 1 glass jar) in the laboratory at 20 C in aerated water for 8 weeks. Daily observations were made and the numbers of A. polypompholyx appearing from each snail species recorded. To determine if adult A. polypompholyx leave host snails on a seasonal basis, 200 B. truncatus from SThadg were collected each month from Sep- tember 1987 through March 1988 and examined daily for the presence of A. polypompholyx (Table 3). The preferred snail host of A. polypompholyx was determined by placing a mature leech brooding 25 young on its venter into a 2 1 glass jar containing 40 snails (10 each of B. truncatus, B. alexandrina, P. acuta and T. niloticus). After 1 week, when all the young had left the parent leech, all the snails were dissected and examined for the presence of young leeches. In addition, 10 speci- mens of each of the four snail species were maintained in separate 2 1 glass jars. A mature A. polypompholyx brooding 18-25 young was placed into each jar and daily records made for 4 weeks of the numbers of young remaining on the parent leech and free living. At the end of the experiment all the snails were dissected and exam- ined for leeches. To study the life cycle of the A. polypompholyx in the laboratory, 35 mature leeches collected after they had left the snail host in January were put into a glass jar with 20 B. truncatus. Daily obser- vations were made on the process of egg laying, cocoon production, egg hatching time, and brooding. Results Adult Alboglossiphonia polypompholyx (7-13 mm) in the field were collected from the undersides of stones, rocks, bottles and other solid objects. Of the six snail species collected in the field, A. polypompholyx was found in the mantle cavity of 56% of Bulinus truncatus but were never recorded in any of the other snail species. Adult A. polypompholyx living endoparasitic in the mantle cavity of B. truncatus left the host snail about 4 weeks before the start of reproduction (September and January) with leeches carrying Table 3. Number of Alboglossiphonia polypompholyx leaving groups of 200 Bulinus truncatus collected monthly (September- March) from Shg. Months 1987 1988 September October November December January February March Days 1-7 8 12 0 0 0 10 0 8-15 20 5 0 0 17 3 0 16-23 20 1 0 0 13 2 0 24-30 8 0 0 0 3 0 0 Total 56 18 0 0 33 15 0 176 Fig. 2. Alboglossiphonia polypompholyx showing A) embryos and B) young on the parent's venter. cocoons appearing in the field in October/ November and February/March (Table 2). Young A. polypompholyx were never recorded free-living in the field. The specificity of the snail host species were confirmed in the laboratory. After 8 weeks, 33 adult A. polypompholyx had left the 100 B. trun- catus and were observed free living in the jars. No leeches appeared in the jars containing Biomphalaria alexandrina, Physa acuta or Theodoxus niloticus and none were found in these snail species when dissected. Adult A. polypompholyx left the host snails on a seasonal basis (Table 3) with free living leeches appearing in September/October and January/ February but none appearing in November, December of March. Given the choice of four snail species as poten- tial hosts, young A. polypompholyx entered speci- mens of B. truncatus only. Within 7 d all the young leeches had left the parent. This was confirmed by opening the snails and finding young leeches in the mantle cavity. The majority (8) of the snails contained only one leech, two snails contained two leeches and 13 leeches had apparently died. When B. alexandrina, T. niloticus or P. acuta were available as potential hosts, the brooding young A. polypompholyx remained on the parent leech for 10-12 d and after they left it remained free living in the jars until they died after 3-4 weeks. The absence of young A. polypompholyx from B. alexandrina, T. niloticus and P. acuta was con- firmed at the end of the experiment by dissection. In the laboratory, the life cycle of 35 adult 177 A. polypompholyx which had recently left B. trun- catus was studied by maintaining them at 20 °C with 20 B. truncatus. Before egg-laying, which commenced within 4 weeks from when the leech left the snail, the ovisacs could be seen filled with mature eggs, especially in the region of the female gonopore. The adult leech attached itself to a solid substrate with both suckers, flattening its body against the substrate, rising and constricting very slowly. This process continued for 1-2 d during which time the eggs were laid and arranged in one layer attached to the ventral body surface of the parent. Between 30-50 eggs (mean diameter 0.28 mm) covered by a thin transparent cocoon membrane, approximately filling the posterior two thirds of the body venter, were produced by each leech. Thirty-three percent of the leeches laid eggs in February/March. After brooding, the adults did not fed, even though B. truncatus were pres- ent, and died within 4-8 weeks. Egg hatching commenced about 15 d after lay- ing. The embryos became attached to the parent's venter by an ectodermal process behind the ante- rior sucker. After about 7 d the posterior sucker was fully developed and used for attachment instead of the ectodermal process which dis- appeared. The young (0.6-0.8 mm) left the parent 7-10 d after hatching and entered the snail host. This was confirmed by dissecting the snails and the discovery of young leeches in the mantle cavity. The young leeches grew to maturity in the mantle cavity and left the snails after 16-20 weeks to reproduce. Although feeding in the mantle cavity could not be observed directly, the growth of the A. poly- pompholyx from 0.6-0.8 mm to 7-13 mm and the presence of fluid within the crop of the leech indi- cates feeding occurred. Discussion The life-cycle of Alboglossiphoniapolypompholyx is simple with adults leaving the host snail Bulinus truncatus in September and January about one month before the start of egg production in October/November or February/March. After hatching and then brooded by the parents for 7-10 d, the young leave the parent, become free- living and enter the mantle cavity of the host snail where they remain for up to 16-20 weeks before leaving the host as adults prior to reproducing. As A. polypompholyx spends the largest part of its life-cycle within the mantle cavity of the host where it feeds on the body fluids of the host without killing it, the mode of life is, therefore, parasitic rather than predatory. While the major- ity of glossiphoniids are predators, devouring the body fluids and killing the prey, several studies on glossiphoniids have demonstrated a parasite-host association with molluscs (Bennike, 1943; Wilkialis, 1964; Gruffydd, 1965; Hatto, 1968; Sarah, 1971; Klemm, 1973, 1975, 1976). Some species have host preference for specific molluscs when available, but A. polypompholyx is unique in being the only glossiphoniid so far recorded feeding on and living in only one species (B. truncatus). Young A. polypompholyx leave the parent leech sooner in the presence of B. truncatus than in the presence of alternate snail species (Biomphalaria alexandrina, Physa acuta, Theodoxus niloticus) suggesting that B. truncatus in some way stimu- lates the cessation of brooding. Mann (1962) con- cluded that the availability of suitable hosts is the most important factor affecting the distribution and abundance of sanguivorous leeches. Unless alternate hosts are discovered, the distribution of A. polypompholyx must be directly correlated with the distribution of B. truncatus. Unlike other haementeriin glossiphoniids in Egypt, A. polypompholyx is semelparous, repro- ducing once and then dying and is thus similar to another African haementeriin Marsupiobdella africana (Van der Lande & Tinsley, 1976) and the duck leeches Theromyzon cooperei (Oosthuizen & Fourie, 1985), T. rude and T. tessulatum (Wilkialis & Davies, 1980). 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