Brooding in Corbicula madagascariensis (Bivalvia, Corbiculidae)

Brooding in Corbiculidae • M. Glaubrecht et al.diploid, diocious with uniflagellate sperm), was found in anearlier study (Hurukawa & Mizumoto 1953) to be nonbroodingwith its larvae being nonswimming, transforming intobenthic juveniles immediately after leaving the egg capsulesat a size of 0.18 mm (see Table 2). This has resulted in somespeculation as to the lake’s fauna being a marine relic (seeHarada & Nishino 1995: 404, and references therein). Similarspeculations have long been upheld in the case of the thalassoidmalacofauna of Lake Tanganyika in East Africa (seereview in Glaubrecht 1996). The lacustrine C. sandai beingoviparous is noteworthy insofar as many limnic organismsincluding molluscs, in particular from so-called ‘ancient’lakes, are known to exhibit viviparity even when closelyrelated nonlacustrine forms are oviparous, but most rarelyvice versa. Therefore, it would be interesting to establish,based on the study of extensive series, whether sandai isindeed nonbrooding, in order to exclude the theoreticalpossibility that the originally studied material for whateverreason lacked larvae and marsupial gills, a point also raisedearlier by Morton (1979).Hitherto, prolonged incubation of large embryos withwell-developed shells, here termed euviviparity (see Table 2),was thought to not only characterize native South Americancorbiculids, but also believed to be an important feature forelevating the rank and placing them in a seperate genusNeocorbicula Fischer, 1887 (Parodiz & Hennings 1965). Thelatter genus not only differs substantially in shell morphologybut also in characteristics of branchial incubation of embryos,which is carried out in different ways (Ituarte 1994). Generally,Corbicula (with the exception of C. japonica) incubateembryos in large numbers (> 10 000) within the water tubesof the two inner demibranchs (endobranchous) which areunmodified; late veligers or pediveligers (c. 200–240 µm indiameter) are released after a short incubation period (e.g.Britton & Morton 1979). In contrast, Neocorbicula developsbrood pouches by cellular proliferation of the interlamellarjunction epithelium of the inner demibranchs, with a singleembryo within each pouch and a total of about 20–30 (maximum45) embryos of different cohorts; the offspring arereleased as fully developed juveniles with sizes of c. 1.1 mm,with some remaining within the pouch until their shells havereached 4–5 mm in length (Ituarte 1994). However, detailedstudies as to the existence of specialized tissue with a nutritivefunction, as done for sphaeriids (e.g. Hetzel 1993), and thusproviding direct evidence for matrotrophy, are lacking notonly for Neocorbicula but also for other corbiculids.Modes of incubationRecently, in Indonesian corbiculids, particularly in populationsfrom Sulawesi and Sumatra (which possess uniflagellatespermatozoa, thus being meiotic, i.e. nonclonal), a greaterdiversity of brooding characteristics was documented thanwitnessed previously for the rest of the collective Old Worldrange of Corbicula (Glaubrecht et al. 2003; Korniushin &Glaubrecht 2003). All Corbicula species endemic to Sulawesiand C. moltkiana from Sumatra were found to be endobranchous,i.e. to incubate their young in their inner demibranchsat least until the stage of juveniles with straight-hinged shells(D-shaped), thus being ovoviviparous.In contrast, two other strategies were found among theendemic Sulawesi taxa that were hitherto unknown in anyother congeners. Corbicula possoensis Sarasin & Sarasin, 1898from Lake Poso, which was found as adelphotaxon to thecementing (i.e. sessile) C. anomioides (see details in Rintelen& Glaubrecht 2006) from the same lake, exhibits tetragenousbrooding (i.e. incubation in both demibranchs). However, asin most other Corbicula species, it incubates relatively small,straight-hinged juveniles, whereas in another species fromSulawesi, viz. C. linduensis Bollinger, 1914, prolonged incubationwithin the maternal gill was found, with juvenile shellsreaching up to 1.3 mm in length and with well-developedhinges. In addition, this latter euviviparous taxon is reportedto have sequential brooding, releasing umbonal larvae ofabout 1.5 mm (Korniushin & Glaubrecht 2003; Glaubrechtet al. 2003). While in all other corbiculid studies so far broodingis synchronous, the only other known exception to this wasfound in Neocorbicula limosa, where incubation is also sequential(Ituarte 1994).Thus, next to Neocorbicula in South America, onlyC. linduensis from Sulawesi is truly representive of a euviviparouscorbiculid from Southeast Asia. The evidence providedhere, even when indirect, now adds C. madagascariensis fromMadagascar. The position and size of the shelled juvenilesfound in the adult body of the latter taxon are comparable tothose encountered only in the former. The size variationwithin the juveniles further suggests that the brood originatesfrom more than one preceding spawning event. Consequently,we anticipate here that the type of brooding inC. madagascariensis also follows a sequential mode as found inC. linduensis. Following a similar argument put forward forsphaeriids by Cooley & Ó Foighil (2000), this can be hypothesizedas a derived condition in both cases among corbiculids,while synchronous brooding is the plesiomorphic feature.In contrast, other African corbiculids such as C. fluminalis,ranging from North Africa and the Middle East to CentralAsia, have ovoviviparous brooding with short-termed incubationof many larvae in gills (Korniushin 2004). They wereboth found to incubate a large number of small larvae ofsimilar size of around 0.2 mm (with the largest larvae 217 µm),lying densely packed within (and filling almost all the available)interlamellar spaces of the ctenidium. These larvae wereD-shaped, weakly calcified and fragile, the hinge edge straightand no hinge structures seen, and of varying sizes. Thisfinding of a distinct reproductive mode serves as further650 Zoologica Scripta, 35, 6, November 2006, pp641–654 • © 2006 The Authors. Journal compilation © 2006 The Norwegian Academy of Science and Letters