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Research Articles NAT Research articles NAT. HIST. BULL. SIAM SOC. 56(1): 25-53, 2008 TROPHIC POLYMORPHISM IN THE MALAYSIAN FISH NEOLISSOCHILUS SOROIDES AND OTHER OLD WORLD BARBS (TELEOSTEI, CYPRINIDAE) Tyson R. Roberts' andM. Z. Khaironizam2 ABSTRACT Population samples of the cyprinid species Neolissochilus soroides from upper Sungai Gombak (a small, high-gradient tributary of the Sungai Kelang near Kuala Lumpur in the middle of peninsular Malaysia), exhibit marked variation of oral morphology involving the lips, horny jaw sheaths, and presence or absence of a mentum (a fleshy median lobe between the lower lips). There are specimens with moderately developed lips and horny jaw sheaths without notable specializations; others with lower horny jaw sheaths thickened and with a trenchant keratinized (dark brown) cutting edge and a thin lower lip; and still others with more or less thickened upper and lower lips and a posteriorly-directed ventromedian process or mentum on the lower lip and weakly developed lower horny jaw sheath (pale or yellowish). Development of the mentum, when present, ranges from barely perceptible to so broad, thick and long as the most highly developed mentum in species of the cyprinid genus Tor. The variation is interpreted here as intraspecific polymorphism. Recognition of polymorphism involving the mouth parts of Neolissochilus soroides contributes to a better understanding of the systematics of nominal Neolissochilus species in the Malay Peninsula including N. tweediei (HERRE & MYERS 1937) and N. hendersoni (HERRE 1940). Trophic morphs of N. soroides represent non-sexual varieties with the potential to evolve into new species and genera. Trophic polymorphism closely comparable to that of N. soroides also occurs in at least one population of N. hendersoni on Penang Island. This species, thought to be endemic to Penang but present also on Langkawi Island and on the mainland of the Malay Peninsula in Kedah, differs consistently in having fewer scales in the lateral series but otherwise is closely similar to N. soroides. Malaysian and Indonesian populations of the species Tor tambra exhibit polymorphism of the lips and mental lobe comparable to that observed in the "normal" and "Tor" type morphs of N. soroides but apparently members of these populations do not develop a horny cutting edge on the lower horny jaw sheath as in the "Acrossocheilus or Lissochilus morph" of N. soroides. Trophic polymorphism similar to that reported here in N. soroides and N. hendersoni occurs in Tor grypus in the Tigrus-Eurphrates basin, in the South African species currently referred to as Barbus or Labeobarbus brucii, and in many other Old World barbin cyprinids not documented here. Intraspecific variation comparable to that found in Neolissochilus and Tor also occurs in some isolated populations of the cyprinid subfamily Schizothoracinae (HORA, 1934). This suggests that such trophic polymorphism evolved before the divergence of Barbinae- Schizothoracinae and that it played an important role in the schizothoracin adaptive radiation. Trophic polymorphism apparently represents an ancient evolutionary heritage of the "barbels" or barbin cyprinids. It evidently has played an important role in the speciation, adaptive radiation, and evolution of distinctive genera in this large fish group. This implies that in these fishes, while geographic or ecological isolation is probably necessary for speciation to occur, evolutionary divergence leading to speciation and formation of genera can occur within populations or in other words sympatrically. 1 Research Associate, Smithsonian Tropical Research Institute; [email protected] 2 Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia Received 25 July 2007; accepted 30 December 2007. 25 26 TYSON R. ROBERTS AND M. Z. KHAIRONIZAM Key words: Ostariophysi, Cypriniformes, intraspecific trophic polymorphism, lips, horny jaw sheaths, mentum, Neolissochilus soroides, Acrossocheilus hexagonolepis, Neolissochilus hendersoni, Neolissochilus tweediei, Tor tambra, Tor grypus, Barbus brucii, Labeobarbus brucii, Schizothoracinae, Malaysia, Indonesia, South Africa, Near East, Euphrates-Tigris INTRODUCTION The objectives of this paper are to 1) document the occurrence of pronounced intraspecific trophic polymorphism in the Southeast Asian cyprinid species Neolissochilus soroides (DUNCKER, 1904), based mainly upon intensively studied samples from Sungai Gombak in central Malaysia; 2) provide biological information relevant to this example; 3) point out a number of similar examples of intraspecific trophic polymorphism in other Old World Cyprinidae; and 4) indicate the significance of such polymorphism in the systematics and evolutionary biology of Cyprinidae. The trophic polymorphism described here was recently recognized by the first author in a sample of Neolissochilus soroides obtained by researchers from the School of Biology of the Universiti Sains Malaysia in Penang from Sungai Kenyir, a high gradient stream in the Terengganu basin of eastern Peninsular Malaysia, in 1997. That sample, however, comprises relatively few specimens and does not show the full range of variation in trophic structures occurring in this species. The site is relatively remote and has not been revisited for additional sampling of its Neolissochilus. Here we report on N. soroides samples with numerous specimens exhibiting similar trophic polymorphism collected mainly in 2005-2006 near the University of Malaya Field Study Center in Ulu Gombak, Selangor. Only 40 minutes' drive from Kuala Lumpur, the site is being utilized for the second author's doctoral study on N. soroides. The first author visited there in December 2006. In order to follow the ensuing account, it is necessary to appreciate the distinction between cyprinid lips and horny jaw sheaths. Neolissochilus, like all cyprinids at all stages of their life history, have no true teeth on the oral jaws. Cyprinidae do possess true teeth, but they are restricted to the pharyngeal jaws in their throat. The toothless bones of the upper and lower oral jaws of Neolissochilus and other cyprinids are covered by two discrete skin structures, the lips and the horny jaw sheaths. The latter directly cover the jaw bones where they come into contact with food items. Generally the lips and horny jaw sheaths are separated from each other by well defined furrows. The jaw bones do not extend into the lips. The superficial layer of the skin of the lips and horny jaw sheaths is often (perhaps invariably) keratinized. The superficial layer of keratinized epidermal cells often gives rise to a variety of specialized structures including ridges or plicae, papillae, unculi (unicellular projections, often hook- shaped), and sharpened cutting edges. Collectively these substitute for the teeth of other bony fishes and contribute to the stunning adaptive radiation of feeding structures of the cyprinoid fishes (including the trophic morphs of Neolissochilus). The mental lobe, sometimes referred to as "mental barbel" or "mentum", is a soft, fleshy median structure located between the lower lips on the ventral surface of the lower jaw. It occurs in the Old World cyprinid subfamilies Schizothoracinae and Barbinae. In Barbinae it is best known in the Asian species of the Tor and in various African species usually referred to the genus Barbus but which may more properly belong in Tor. It also occurs in Folifer. TROPHIC POLYMORPHISM IN NEOLISSOCHILUS SOROIDES 27 It is reported here in Neolissochilus for the first time. The mentum characteristically occurs only in species or intraspecific trophic morphs in which the lips are more or less thickened or hypertrophied. Its superficial appearance and thickness generally is comparable to that of the lips. Like the lips it is well supplied with taste buds. Although often referred to as a "mental lobe", the mentum is really a flap. It appears to be a smooth rounded lobe because the margins of the flap fold above the structure when the mouth is closed to form a smooth cylindrical lobe with a rounded tip. Presumably the lobe expands into a flap when the mouth is fully opened in live fish when they are feeding but observations are lacking to confirm this. Trophic polymorphism comparable to or even more complex than that reported here occurs in many other cyprinids, particularly in the Old World subfamily Barbinae. A number of examples are mentioned in the discussion section of this paper. The genetic basis of this intraspecific variation is perhaps the most important unstudied aspect of the phenomenon. This will require cross-breeding and out-crossing among the various morphs within particular species. So far as we are know such experiments have not been conducted. Since several species are widely utilized in aquaculture, the techniques for artificial spawning and rearing of Cyprinidae are well-known. Although it presently occurs only as a wild fish, N. soroides is a popular food fish in Malaysia, and is an excellent candidate for aquaculture, as are some other species with trophic polymorphism. In instances of intraspecific polymorphism one would usually expect to find that the early stages up to a certain size are morphologically indistinguishable. This appears to be so in the Sungai Gombak population ofN. soroides. All fish observed under 40 mm in standard length have mouth parts similar to the "normal" or Neolissochilus-like morph. The smallest specimen with Acrossocheilus-like mouth parts is 40.5 mm, and the smallest with Tbr-like
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