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Speciation in the Coral-Boring Bivalve Lithophaga Purpurea: Evidence from Ecological, Biochemical and SEM Analysis

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Speciation in the Coral-Boring Bivalve Lithophaga Purpurea: Evidence from Ecological, Biochemical and SEM Analysis MARINE ECOLOGY PROGRESS SERIES Published November 4 Mar. Ecol. Prog. Ser. Speciation in the coral-boring bivalve Lithophaga purpurea: evidence from ecological, biochemical and SEM analysis ' Department of Zoology, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel Department of Life Sciences, Bar Ilan University, Ramat Gan 52900, Israel ABSTRACT The bonng mytil~d L~thophagapurpurea densely inhabits the scleractinian corals Cyphastrea chalc~d~cum(Forskal 1775) and Montlpora erythraea Marenzeler, 1907 In the Gulf of Ellat, Red Sea Profound differences in reproductive seasons postlarval shell morphology and isozyme poly- morphism exlst between the bivalve populatlons inhabihng the 2 coral specles wh~chshare the same reef environments Two distlnct reproductive seasons were identified in the blvalves L purpurea inhabiting A4 erythraea reproduce in summer while those In C chalcjd~cumreproduce in late fall or early winter SEM observations revealed distlnct postlarval shell morphologies of bivalves inhabiting the 2 coral hosts Postlarvae from C chalc~dcumare chalactenzed by tooth-like structures on their dissoconch, as opposed to the smooth dissoconch surface of postlarvae from M erythraea In addition, there is a significant difference (p<0 001) In prodissoconch height between the 2 bivalve populations Results obtained from isozyme electrophores~sshowed d~stinctpatterns of aminopeptidase (LAP) and esterase polymorphism, indicating genehc differences between the 2 populahons These data strongly support the hypothesis that L purpurea inhabiting the 2 coral hosts are indeed 2 d~stlnctspecles Species specificity between corals and their symbionts may therefore be more predominant than prev~ouslybeheved INTRODUCTION Boring organisms play an important role in regulat- ing the growth of coral reefs (MacCeachy & Stearn A common definition of the term species is included 1976). Bivalves belonging to the subfamily Litho- in the 'biological species concept' as 'groups of actually phaginae (Mytilidae: Bivalvia) are responsible for the or potentially interbreeding natural populations, which erosion and eventual destruction of a wide range of are reproductively isolated from other groups' (Mayr calcareous substrates (Morton 1983). Members of the 1963).Speciation may, at times, be affected by physical genus Lithophaga bore in a variety of live coral hosts in boundaries (as in allopatric speciation) and/or repro- the Gulf of Eilat, Red Sea (Loya 1981, Brickner 1985, ductive boundaries (as in sympatric speciation). Thus, Winter 1985).The common corals Montipora erythraea a new species may slowly evolve due to some physical and Cyphastrea chalcidicum were found to be infested or physiological boundaries which keep 2 or more by purple colored bivalves identified by K. Kleemann groups from genetically mixing (Tauber & Tauber as Lithophaga purpurea Kleemann. Lithophaginae are 1989). In order to understand important ecological taxonomically categorized by various physical charac- phenomena, such as species specific interactions teristics such as coloration, shell size and structure and between different organisms, systematic accuracy to soft body morphology (Wilson 1979, Kleemann 1980, the species level is imperative. In the present study, we Morton & Scott 1980). Due to the strong resemblance examine 2 bivalve populations which are currently between species of live-coral boring Lithophaga, defined as 1 species, but are found within 2 different morphological techniques alone provide a rather coral hosts. subjective method of taxonomy (see McLaughlin et al. 1982). L. purpurea is a good example of these taxo- 'Addressee for correspondence nomic difficulties. Kleemann (1980) claims that Litho- @ Inter-Research 1993 140 Mar. Ecol. Prog. Ser. phaga lima reported by Gohar & Soliman (1963) boring during 1982-1983 from the reef at the H. Steinitz Marine in Montipora spp, and Cyphastrea spp. in the Red Sea Biology Laboratory in the Gulf of Eilat. Three to five is, in fact, L. purpurea. His definition of this species Lithophaga purpurea-infested coral colonies of each from the Great Barrier Reef is based on the mor- species were collected at 3 to 6 m depth. The corals were phology and texture of the valves (Kleemann 1980). broken apart using a hammer and chisel in order to Coral host specificity of live-coral boring Lithophaga release intact bivalves. The entire mussel population was spp. ranges from single host borers to wide spectrum extracted from each coral and measured for length, width borers (Morton 1983). These bivalves are sessile and height (see Morton & Scott 1980). Dimensions throughout their adult life span. Fertilization occurs in measured were used to construct allometric relationships. the water column (Culliney 1971, Scott 1988). The The reproductive condition of the mussels was deter- planktonic larvae of Lithophaga spp. select a settle- mined according to the reproductive index (RI) defined ment substrate and metamorphose irreversibly on it by Seed (1969).Smears of the bivalves' mantle were ex- (Scott 1988, Mokady et al. 1993). Thus, it is this stage in amined microscopically for the appearance of gonadal the bivalves' Life history which is responsible for the tissue. The gonadal index (GI) was determined using observed host specificity (Mokady et al. 1991, 1992). the method of Seed & Brown (1977).Monthly samples of Once settled and metamorphosed, the adult boring 5 to 10 bivalves were used for histological preparations. bivalve may be subjected to morphogenic effects of its Mussels were fixed in 4% formaldehyde in filtered habitat. For this reason, Goodsell et al. (1992) sug- seawater, rinsed in fresh water after 24 h and preserved gested that closer examination (SEM) of larvae and in 70 % ethanol. Following removal of the valves, 10 pm early postlarvae of lamellibranch species might pro- thick serial histological sections were taken, stained vide a means of early identification and help resolve by hematoxylin and eosin, and examined by light taxonomic ambiguities. microscopy. Recently, Morrow et al. (1992) used allozyme elec- The reproductive cycle of the corals was studied by trophoresis to distinguish between 2 populations of measurement of oocyte diameter in histological sec- dorid nudibranchs of the genus Doto which feed on tions (see Shlesinger 1985). Preparation of the sections 2 different hydroid species in the same environment. followed Rinkevich & Loya (1979). The genetic divergence found by Morrow et al. (1992) Early postlarval stages of Lithophaga purpurea were in the nudibranch Doto coronata resulted in the collected from the surface of the corals Montipora definition of the 2 new species Doto sarsiae and Doto erythraea and Cyphastrea chalcidicum, and removed hydrallmaniae. We believe that in addition to mor- using a fine needle and a pasteur pipette. The young phology, other research tools, including SEM exarnina- bivalves were examined under a dissecting micro- tion, ecological observations, and biochemical charac- scope, and the height of the prodissoconch and the teristics (i.e. protein electrophoresis; see Koehn & length of the total shell were measured for 25 indi- Mitton 1972), may help resolve taxonomic ambiguities viduals of each population. The height of the larval between bivalve populations inhabiting corals. shell, defined as the greatest distance from the tip of The corals Montipora erythraea and Cyphastrea the umbo to the ventral margin, was used to compare chalcidicum belong to different families (Acroporidae between the bivalve populations. and Faviidae respectively) and are different in growth Shells of postlarvae of Lithophaga purpurea were form, surface topography and other features. These examined by a Joel JSM-840 SEM. Specimens were differences may act as a driving force for speciation of dehydrated in a series of alcohols and coated by Gold- cryptobionts such as boring bivalves (see Wilson 1979). Palladium. In the current study we apply biochemical and SEM Fifteen adult bivalves were extracted from 4 to 5 methods combined with ecological observations to try coral colonies of each host coral (either Montipora and resolve the taxonomic question of whether the erythraea or Cyphastrea chalcidcum) by gently break- Lithophaga purpurea populations found in Monti- ing the coral. Mussels were immediately stored at pora erythraea and Cyphastrea chalcidicum are actu- -70°C. To extract proteins, soft tissues were scraped ally 1 species. This may shed a new Light on our under- and homogenized in 15% sucrose, 0.1% mercapto- standing of species distributions and species specific ethanol and 0.5% triton X-100 in saline. Samples interactions within the coral reef. were run on vertical polyacrylamide gel (7 to 9%) in borate buffer (pH = 8.2). Gels were stained for a-esterase and arninopeptidase-l (leucine amino MATERIALS AND METHODS peptidase, LAP) using methods slightly modified from Shaw & Prasad (1970). Monthly samples of the massive corals Cyphastrea Statistical analyses were carried out according to chalcidicum and Montipora erythraea were collected Sokal & Rotill (1969). Br~ckneret al.. Speciation of L~thophagapurpurea 141 RESULTS M. erythraea were significantly greater than these dimensions for bivalves from C. chalcidicurn (p< 0.001 The 2 Lithophaga purpurea populations show very for all 3 dimensions). Maximal length of bivalves from similar allometric relationships (Fig. 1).The data pre- C. chalcidicum and M. erythraea was 15 and 33.5 mm sented in Fig. 1 represent the allometric
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