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The form, function andphylogenetic significance of thevomero-palatine organ in cyprinidfishesGordon McGregor Reid aa Conservation (Natural History) , Merseyside CountyMuseums , William Brown Street, Liverpool, L3 8EN, EnglandPublished online: 17 Feb 2007.

To cite this article: Gordon McGregor Reid (1982) The form, function and phylogeneticsignificance of the vomero-palatine organ in cyprinid fishes, Journal of Natural History, 16:4,497-510, DOI: 10.1080/00222938200770401

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JOVRNAL OF NATVRAL HISTORY, 1982, 16:497--510

The form, function and phylogenetic significance of the vomero-palat ine organ in cyprinid fishes

GORDON McGREGOR REID

Conservation (Natural History), Merseyside County Museums, William Brown Street, Liverpool L3 8EN, England.

Introduct ion Situated on the buccopharyngeal roof in some, but not all, cyprinid fish is a

double row of fleshy transverse folds of extraordinary appearance. These folds, together with associated structures, are referred to as a vomero-palatine organ. The first published description (albeit brief) and figure of this organ is by Steindachner (1870, 562, pl. 7, fig. 1 a). Steindachner found a vomero-palatine organ in Labeo coubie (a Nilotic and West African species) but since then this structure has been often noted in other African and Asian cyprinids (Boulenger 1907, 161; Majumdar 1952, fig. lb ; Majumdar and Saxena 1961, fig. 2; Girgis 1952 a, fig. 1, 1952 b, fig. I; Matthes 1963, pl. IIa; Sinha 1979, fig. 1). Although this curious organ has been known for over a century its function remains obscure and so, too, its phylogenetic significance. This situation persists, perhaps because authors have not considered the systematic distribution of the organ and have studied its histology in isolation from its comparative anatomy. Also, the ecology of the fishes which have the organ has been largely ignored in the literature (apart from the work of Matthes 1963).

In this paper, the vomero-palatine organ is considered from the point of view of its comparative and functional anatomy, with due attention being paid to the ecology of 'organ-bearing' fishes. From this analysis, hypotheses are advanced on the function and phylogenetic importance of the vomero-palatine organ.

Mater ia l s and m e t h o d s Material examined: The British Museum (Natural History) register numbers of

figuredi dissected specimens are given in the text. The present study forms a part of an unpublished thesis on the comparative anatomy and systematics of tropical-old- world cyprinids, for which a large number of representative genera and species were studied. A complete catalogue of examined radiographs, skeletal material, alizarin specimens and spirit specimens is given in this thesis (Reid 1978, 685-703). A copy of this catalogue is also available from the author, on request.

Histology: Numerous published studies adequately detail the histology of the cyprinid buccopharynx (see table 1). However, in order to confirm existing descriptions, sixty histological sections were cut through the buccopharynx of Labeo nilotieus specimens (B.M.N.H. registered slides--Tray 2: 16219-16318; Tray 3: 16319-16338; Tray 4: 16339-16358). Formalin fixed specimens were, by standard techniques, embedded in wax, serially sectioned at 12 pm and stained. A range of stains were used to accentuate different histological features: Masson's Trichrome; PAS Haemalum; Heidenhain's Azan; Mallory's PTAH; Haemalum and Eosin; Feulgen's Reagent.

(X}22 2!133/82/1604 0497 S04"{~) (~'! |982 Taylor & Francis Ltd

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Table 1. An approximate synonymy of terms used in describing the buccopharyngeal roof.

This text Other Authors

(1) vomero-palatine organ (sensu stricto)

(2) vomero -palatine organ (sensu lato): longitudinal ridges and membraneous folds lateral lamellae

raised border of pharynx

(3) dorsal pharyngeal cushion

doppelreihe von hautingen querfalten, Steindachner, 1870; groups of large papillae, Boulenger, 1907: 161; comb-shaped plates, Majumdar, 1952, fig. I b; comb plate region, Majumdar & Saxena, 1961, fig. 2; lamellar organ of palate, Girgis, 1952a, fig. 1, 1952b, fig. 1; vomero-palatine organ, Matthes, 1963, pl. 2a; region of the comb-shaped plate, Sinha, 1979, fig. I.

lateral ridge region, Majumdar. 1952; longitudinal ridges and membraneous folds, Majumdar and Saxena, 1961; lamellar folds, Matthes, 1963: region of the outer fold, Sinha, 1979. lateral ridge region, Majumdar, 1952; Majumdar & Saxena, 1961; lamellar projections, Matthes, 1963; giant papillae, Sinha, 1979.

border of pharynx, Girgis, 1952 b; tubercular protuber- ances, Majumdar and Saxena, 1961, fig. 2; posterior ridge, Matthes, 1963, pl. 2 c; minute papillae, Sinha, 1979.

'Valatours tongue' (from Valatour, 1861); posterior region of the palate, Majumdar, 1952, fig. 2; Majumdar and Saxena, 1961, fig. 2; pharyngeal pad, Girgis, 1952 a, fig. 1, 1952b, fig. 1; Matthes, 1963, pl. 2c; palatal organ, Jara, 1957, 1963; Okada and Kubota, 1956; palatine organ, King, 1975, figs 2, 3; palate, Doffer and Bellon, 1951/52; middle and side of the posterior region, Sinha, 1979.

Taxonomic nomenclature: For convenience of description an abbreviated nomen- clature has been adopted:

This text Labeo = Labeo-like cyprinids =

Garra

Garra-like cypffnids

Tylogn~Uhus

Formal nomenclature Labeo Cuvier, 1817: type species L. niloticus (Forsskhl, 1775). Labiobarbus van Hasselt, 1823 [not Labeobarbus Riippell, 1836]. Cirrhinus (Cuvier) Oken, 1817. Osteochilus Gfinther, 1868.

= Garra Hamilton, 1822: type species. Cyprinus larata Ham., 1822.

= Crossocheilus van Hasselt, 1823. Paracrossocheilus Popta, 1904. Epalzeorhynchos Bleeker, 1851. Mekongina Fowler, 1937. Typhlogarra Trewavas, 1955. Iranocypris Bruun and Kaiser, 1943. Semilabeo Peters, 1880. Labeo bicolor species-group ( i .e .L. bicolor Smith, I931; L. munensis Smith, 1934; L. frenatus Fowler, 1934; L. erythrura Fowler, 1937).

= Tylognathus Heckel, 1843 sensu Bleeker, 1868: type species Varicorhinus diplostomus Heekel, 1843 [not Tyloqnathus sen~u Giinther, 1868].

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Vomero-palatine organ in cyprinids 499

Barbus = Barbus Cuvier and Cloquet, 1816: type species Barbus barbus L.

Barbus-like cyprinids = Capoeta Cuvier and Valenciennes, 1842. Varicorhinus Rfippell, 1836. Prolabeo Norman, 1932. Prolabeops Shultz, 1941. Oreodaimon Greenwood & Jubb, 1967.

Anatomical nomenclature: Majumdar and Saxena (1961) classify the bucco- pharyngeal roof of Labeo dero into several zones. I have adopted a modified, abbreviated form of this classification. An approximate synonymy of terms used in describing the buccopharyngeal roof is given in table 1. All other anatomical nomenclature follows current usage. The scale line on each text figure represents 0"5 c a .

Abbreviations used in the figures ct.d Central depression, buccopharyngeal roof 1.1m Lateral lamella lm Lamella lt.r Lateral ridge mb.f Membraneous fold mx.v. Maxillary valve ph.c Pharyngeal cushion ph.p Pharyngeal pad of basioccipital bone r.b.ph Raised border to pharynx vm.p Vermiform papillae

O b s e r v a t i o n s Comparative anatomy (1) Vomero-palatine organ (sensu stricto) (fig. 1): This organ lies in a navicular depression of buccal tissue covering the ventral surface of the vomer bone (anteriorly), the parasphenoid bone (posteriorly) and the metapterygoid bones

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(laterally). This region of the buccopharynx is innervated by fine anastomoses of the facial (VII), glossopharyngeal (IX) and vagus (X) nerves (see also Casati 1923, Edwards 1930, Krawarik and Sfiss, 1936, Dorier and Bellon 1951/52, Ping et al. 1959, Kappers et al., 1960). The elements of the organ vary both ontogenetically and within and between species, but in adults it is essentially formed from a paired longitudinal series of overlapping transverse fleshy folds or lamellae. Each lamella has an unciform tip and a bluntly serrated posterior margin which freely depends from the roof of the mouth into the buccal cavity. The anterior and posterior lamella are generally small or rudimentary in comparison with the others. Steindachner (1870, 562) has compared the overall disposition of lamellae to the form of the cephalic disc in the Shark Sucker (Echeneis) and I consider this to be a fair analogy.

In most species there are as many as 7 (_+2) perfectly formed lamellar pairs (figs. 2 a, 3 a, 5 a, 6 a, 7 b). Epalzeorhynchos (fig. 6 b) and members of the Labeo bicolor species-group have an extremely large number of lamellae (ca 26). In Tylognathus, however, the lamellar pairs normally are fewer (4 or 5) and the individual lamellae larger and fleshier (fig. 3 b). Garra (and ?Semilabeo) have, at least in early ontogeny, the generalized number oflamellar pairs ii.e. up to 7_+ 2) but in adults the organ may be regressed. In adult Garra the regression may be extreme, almost to the point of absence. Regression also takes place in some species of African Labeo (e.g. in members of the L. forskalii species-group, especially in L. sorex). There is little difficulty in distinguishing between cases where the vomero-palatine organ is truly absent (e.g. in Barbu8 and Barbus-like cyprinids) and cases where it is present but extremely regressed. In Barbus and Barbus-like cyprinids the tissue of the buccopharyngeal roof is, in adults and juveniles, developed as a series of fine longitudinal rugae (see e.g. Matthes 1963, plates 6b and 10). In contrast, the regresssed vomero-palatine organ is evident as a 'disturbed' ovoid patch of feeble, more or less transverse corrugations (fig. 5 b).

The particular arrangement and form oflamellae varies between taxa. In Labeo victorianus, for example, (fig. 4b) the lamellae have a characteristic exfoliate appearance, whereas in L. rohita and Cirrhinus jullieni they appear spiky (figs 2 b, 7 a). In Labeo seeberi the lamellae are globose and 'scattered' while in Osteochilus hasselti they are swollen and transversely arranged (figs 4 a, 6 a). Histologically, the lamellae are rich in mucous cells while taste buds are relatively few in number (personal observations). Sinha (1979, 366) finds in Cirrhinus mrigala tha t mucous cells are abundant at the base of each lamella but rare at the tip. By surface-scanning electron microscopy (SEM) pores are visible at the base of each lamella and these are probably the apices of mucous cells, while a honeycomb pattern marks the free lameUar margins where taste buds occur (Sinha 1979, fig. 20). A few muscle fibres run into the lamellar submucosa (personal observations and Majumdar 1952, fig. 3; Majumdar and Saxena 1961, fig. 3; Girgis 1952 b, figs 5 and 6; Matthes 1963, pl. 5 a). (2) Vomero-palatine organ (sensu lato) (fig. 1): In the region underlying the ventral surface of the palatine bones, the antero-lateral aspects of the tissue lining the buccal cavity are formed as a pair of longitudinal ridges. These ridges may be developed anteriorly as membranous folds and are seen particularly well in Tylognathus (fig. 3 b). In Labeo, in Labeo-like cyprinids, and in Tylognathus, lateral lamellae (lying outside the central depression) may be associated with each longitudinal ridge (figs 3 b, 7 b). Histologically, the epithelium of the longitudinal ridge resembles that of the lamellae but the submucosa contains many striated muscle fibres (Majumdar and Saxena 1961, fig. 4).

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Vomero-palatine organ in cyprinids 503

The posterior lip of the central depression (which contains the lamellae) forms a raised border between the buccal cavity and the pharynx, but this is not well developed in the mid-line. The raised border is, on each side, formed as a Y-shaped peak, with the tail of the 'Y' pointing anteriorly. In Labeo fi~rgoriatus the raised border is especially pronounced (fig. 3 a). Histologically, the epithelium covering the raised border is similar to that of the lateral ridges but taste buds are more numerous (Majumdar and Saxena 1961, fig. 4).

The vomero-palatine organ and adjacent structures become fully formed probably within 3 months of hatching in most cases, e.g. early post-larval Labeo gonius of ca 5 mm SL have 5 paired lamellar rudiments and L. niloticus of ca 9 mm SL have up to 8 paired rudiments. The entire organ is perfectly formed in L. niloticus of 23 mm Sir--the serrated edges to the lamellae being distinct. L.forskalii of 14 mm SL (ca 40 days post-hatching) have three transverse pairs oflamellar rudiments. These rudiments are quite distinct at 31 mm SL (ca 64 days post-hatching) but in specimens of 56 mm SL they are regressed. This regressed state is the definitive condition in this species. (3) Dorsalpharyngeal cushion (fig. 1): The tissue covering the roof of the pharynx has the overall appearance of a bi-lobed fleshy cushion. This cushion underlies the ventral surfaces of: the prootic bones (antero-laterally), the basioccipital bone (medially) and the exoccipital bones (postero-laterally). The anterior pharynx has numerous papillae 'scattered' over it; these may be globose or vermiform (ca 0"5- 1 mm long). These papillae, the tips of which are directed posteriorly, grade into (merge with) the smaller, more numerous, globose papillae of the posterior pharynx.

Histologically, papillar epithelium is poor in mucous cells and rich in taste buds compared with elsewhere on the buccopharyngeal roof (Girgis 1952 b, 337-338, fig. 8; Majumdar 1952, figs 4 and 5; Majumdar and Saxena 1961, figs 5 and 6; Sinha 1979, 366, figs 2-7). According to Kappers et al. (1960, 354) this high number of taste buds in cyprinids is associated with a hypertrophy of the visceral afferent roots of the glossopharyngeal (IX) and vagus (X) nerves. This further correlates with the fact that the facial and vagal lobes of the brain are usually well developed in cyprinids (see e.g. A1 Hussaini 1949, 112).

Taste buds, unlike mucous cells, do not seem to vary appreciably in numbers during ontogeny. According to Girgis (1952 b, 361) mucous cells of the buccal cavity and anterior pharynx are [in Labeo horie]: . . . numerous in young specimens and less so in the older ones'. Strangely, Seghal (1965, 265) reports that in L. calbasu mucous cells are equally numerous in the buccal and pharyngeal regions, while taste buds are less numerous in the pharyngeal region. Seghal's (1965) findings are, so far, unconfirmed.

Functional analysis (1) Buccopharynx in general: The researches of several authors (Sarbahi 1939, A1 Hussaini 1949, Majumdar 1952, Okada and Kubota 1956, Majumdar and Saxena 1961; Girgis 1952 a) show that the buccopharynx in adult cyprinids is divisible into: (a) a mucous secreting buccal region (mucous cells comprise ca 80% of the entire buccal coat in Labeo rohita according to Sarbahi 1939, 100) with a few scattered taste buds. In fishes which have a vomero-palatine organ these taste buds are con- centrated on the free margins of lamellae and on epithelial ridges, especially the

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raised border to the pharynx; (b) a dorsal pharyngeal cushion which apparently secretes less mucous than the buccal region, but is rich in gustatory cells, especially on the papillae. The morpho-plan of a mucous secreting buccal region and a gustatory pharyngeal region is general for teleosts (e.g. see Kapoor and Evans 1975) and, in cyprinids at least, this is consistent with the idea of anterior boli-formation coupled with a posterior taste and sorting system. Certainly, Dorier and Bellon (1951-52) consider that one main function of the dorsal pharyngeal region is gustatory (see also Hara 1971 and Vasilevskaya and Pavlov 1971); peristaltic movements of the dorsal pharyngeal cushion evidently also aid in deglutition (Girgis 1952a, 314). Jara (1957, I963) and Matthes (1963, 10) have proposed a curious additional hypothesis that the dorsal and ventral pharyngeal cushions act together as a press preventing inflow of water to the gut. This notion appears to be dispensable.

(2) Vomero-palatine organ: A survey of the literature shows that there are three principal ways in which the organ is supposed to function: in respiration; in a sensory capacity; in feeding. These hypotheses are, of course, not mutually exclusive but each wiI1 be considered separately:

(a) Respiratory hypothesis: Majumdar (1952) and Majumdar and Saxena (1961) suggest that the vomero-palatine organ, in conjunction with the papillae of the dorsal pharyngeal cushion, provides an accessory respiratory surface. On the face of it, this is a reasonable hypothesis, at least by analogy with respiratory structures in allied taxa. Johansen et al: (1968), for example, have shown that richly vascularized papillar outgrowths in the oro-branchial chamber of the electric eel (Electrophorus electrieus; Ostariophysi) are vital to respiration. But Johansen arrived at his conclusion from physiological data and from the fact that papillar outgrowths in the electric eel are associated with air-gulping at the surface and with vestigial gills Which are unimportant in gas exchange. However, Majumdar (1952) and Majumdar and Saxena (1961), in order to test their hypothesis, conducted a series of respiratory experiments which, in my view, were ill-conceived. Certainly, the results obtained from these experiments in no way support the respiratory hypothesis. The only acceptable evidence for a respiratory function would be a demonstrated increase in the physiological oxygen titre in the blood of the efferent (as compared to the afferent) capillaries of both lamellae and papillae. As far as can be ascertained, such experiments have not been conducted. Therefore, it is not possible to confirm or deny the respiratory hypothesis.

However, one point suggestive of a respiratory function is that the vomero- palatine organ is greatly regressed in adults oflabeine species which live in torrential and presumably oxygen-rich, streams (personal observation). (This regressed condition can also be explained in terms of feeding habits (see p. 506).) Nevertheless, there is no histological evidence to show that lamellae or papillae contain air spaces (cf. Electrophorus) or are more richly vascularized than the rest of the tissue roofing the buccopharynx; and vestigial gills are not known in cyprinids. Also, in living Labeo senegalensis, L. coubie and L. tibestii, at least, the vomero-palatine organ is not suffused with red as one might expect from a richly vascularized structure (personal observation). Labeo never show gulping behaviour nor do they fare conspicuously well under anoxic conditions in dry-season pools--they gasp for air at the surface as do most fishes (personal observations in the field, West Africa).

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(b) Sensory hypothesis: Girgis (1952 a, 334) states that: 'The position and shape of the lamellar organ of the palate suggest some specialized sensory function.' Nevertheless, Girgis finds the nerve endings in lamellar epithelium to be similar to those in adjacent tissue and from this he concludes that a specialized sensory function is, after all, improbable. Girgis does not state what sort of sense organs he was looking for but taste buds are likely candidates. Sinha (1979) has, on the basis of scattered taste buds found on free lamellar margins,postulated a gustatory function. On Sinha's histological data, this function must exist (even if limited) but there is no suggestion that concentrations of taste buds on lamellae are greater than on other epithelial ridges in the buccopharynx. I t is difficult to argue, therefore, that the vomero-palatine organ serves a specialized gustatory function.

Thines (1969, 86) considers that, in cavernicolous Garra-like cyprinids, the presence and degree of development of 'L'organe palatal' (?=vomero-palatine organ) is positively correlated with an increased number o f 'pores olfactifs'. In support of his opinion Thines gives two citations. I have checked these references and find that neither of them deals, even indirectly, with the vomero-palatine organ. The evidence for an olfactory function is slight.

A1 Hussaini (1949, 119, 126) has described paired 'palatine cushions' occurring in Gobio just posterior to the maxillary valve. This author reports an experiment where gravel particles sucked in with the respiratory current are immediately rejected as soon as they touch the palatine cushions. I t does not seem that the palatine cushions of Gobio are homologous with the labeine vomero-palatine organ; nevertheless, it may be that there is some functional correspondence between these structures.

(c) Trophic hypothesis: Matthes (1963, 13) states that: 'The regular form of the vomero-palatine organ suggests some specialized function in relation to feeding; however, no voluntary muscle being present, any active function is excluded.' Matthes further proposes that the precise function might be in "passively mixing' small food particles (e.g. algal cells and fragments) with mucous (see also comments in Kapoor et al. 1975, 121; Kapoor and Evans 1975, 79). Matthes does not, however, clearly formulate this hypothesis and it is difficult to be sure of his exact meaning. I challenge Matthes' assertion that an active role is impossible. Striated muscle fibres are present as a longitudinal arrangement in the cyprinid buccopharyngeal mucosa and these fibres are probably responsible for the systaltic movements which pass over the buccopharyngeal roof in freshly slaughtered fishes (personal observations and Majumdar 1952; Jara 1957, 1963; King 1975). Longitudinal lateral ridges, especially when developed anteriorly as membranous folds, are particularly rich in striated muscle fibres (personal observation, see also Sarbahi I939; Majumdar and Saxena 1961, fig. 4).

My hypothesis is (to develop and restate Matthes' original idea) that the vomero- palatine organ is concerned in bolus-formation by the active co-mixing of precipitat- ing mucous secretions with ingested particles (food and sediment). Obviously, this revised hypothesis requires experimental validation which may not be easy to obtain. In the absence of experimental proof, ecological observations lend support to the trophic hypothesis. First, all cyprinids which have the organ are essentially microphagous and feed on aufwuchs, a matted complex of algae (the major component), microscopic animals, organic detritus and inorganic particles which forms a slimey covering over various substrata, e.g. rocks, sand, macrophytes. Particular substrates determine the detailed composition of an aufwuchs com-

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munity (Bayly and Williams 1973; Fryer 1959, 165). The particular size of aufwuchs particles that a fish ingests will thus vary, depending on the habitat as set by substrate and water velocity.

Second, epipelic aufwuchs browsers usually have well-developed vomero- palatine organs (e.g. Labeo niloticus, L. horie, L. senegalensis , Cirrhinus spp., Osteochilus spp.). The size of silt particle ingested on medium-fine to coarse substrates is (on the Whitworth scale) about 0" 125-1"00 mm. In labeine species which feed on substrates coarser than this the vomero-palatine organ is poorly developed, e.g. Labeo rohita which includes in its diet up to 11% of small benthonic crustaceans (Das and Moitra 1963). Cavernicolous Garra-like cyprinids (i.e. Typhlogarra and Iranocypris) may provide another example of this principle. These species are (from their general facies and from their restricted habitat) deposit feeders but they do not show a highly developed vomero-palatine organ. A comparison was made between specimens of blind, de-pigmented hypogean Garra barreimiae (B.M.N.H. Reg. No. 1980: 11.27:12-71) and their sighted, pigmented epigean counterparts (1977.12.13:557-578). The vomero-palatine organ occurs in a regressed state in specimens from both samples but (allowing for size differences) regression is more extreme in the hypogean population.

Third, in epilithic aufwuchs scrapers the vomero-palatine organ is, in the adult, present in a more or less regressed condition. I gain the impression from general oro-mandibular morphology and from personal observations in the field that torrenticolous aufwuchs scrapers (e.g. Labeo sorex, many Garra species) are more microphagous than are labeine species which occur in less turbulent habitats (e.g. Labeo coubie) [see also Matthes 1963, 11]. In accord with this observation is the fact that adult specimens of torrenticolous labcine species have an extremely regressed vomero-palatine organ whereas other species from less turbulent and less trophically restricted habitats have the organ better developed.

The picture which emerges, then--albeit from a limited body of evidence--is that the maximum development of the vomero-palatine organ is seen in fishes whose particle intake is neither 'too large' nor 'too small'. Supporting the notion that particle size is critical in a mucous precipitation system, is the observation by Moriarty et al. (1973, 310) that in some microphytophagous cichlid fishes: 'Collection of particles from the incurrent water involves a mucous filtration mechanism which may well depend upon the particle size.' An analogous system possibly exists among the larvae of certain amphibians. Wassersug (1972) notes that pharyngeal (mucous secreting) epithelial ridges are particularly well developed in those anuran tadpoles which feed by uttraplanktonic entrapment (particles~< 120/~m). However, these ridges are not well developed in the highly specialized aufwuchs scraping tadpoles of the genus Ascophus which inhabit torrential streams.

P hylogenetic analysis Previous researchers have given no consideration to the systematic or phylo-

genetic value of the vomero-palatine organ. Of the 1,500 to 2,000 species of cyprinid fish (representing about 400 nominal genera) a vomero-palatine organ occurs in as many as 300 species (representing about 13 nominal genera). That is to say, a large proportion of cyprinids (15-20~o) have the organ. Curimatid characoids are the only other ostariophysan group which has a structure comparable to the vomero-palatine organ (Vari personal communication). I t seems likely that the organ in curimatids is a parallelism associated with the deposit feeding habits in this group. Although the

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Vomero-palatine organ in cyprinids 507

cyprinid vomero-palatine organ may, in some cases, be regressed (and hence difficult to recognize) its taxonomic distribution is regular. For example, the organ occurs, without exception, in over 100 species of Labeo. In all representative labeine genera, the organ has essentially the same 'bauplan', ontogeny, and histological structure and occurs in the same position, i.e. it is homologous.

The vomero-palatine organ is taxonomically-useful in that it constantly characterizes a large assemblage of cyprinids. Further, it is of phylogenetic importance because it is a shared specialization or synapomorphy which unites the group it characterizes (sensu Hennig 1979). This synapomorphy, then, sets the hypothesis that fishes which have a vomero-palatine organ share an immediate common ancestor which also had the organ. Three other synapomorphies, of congruent taxonomic distribution, lend support to this idea: the neural complex of the Weberian apparatus in direct contact with the supra~ccipital region of the skull; the terete process of the basioccipital bone, and the superficial labial fold developed posterior to the lower jaw Reid (1978). This last synapomorphy contributes to the 'Labeo-like' appearance which characterizes all organ-bearing fish. 'Labeine cyprinids' is, therefore, a convenient informal name for the entire monophyletic assemblage which includes: Labeo, Osteochilus, Labeobarbus, Tylognathus, Cirrhinus, Garra, Semilabeo, Crossocheilus, Paracrossocheilus, TypMogarra, Mekon41ina , Iranocypris and Epalzeorhynchos. I t is probable that Barbichthys Bleeker, 1859 also belongs with the labeine cyprinids but this is the subject of ongoing research (Reid in M.S.). A number of cyprinid genera which have a superficially labeine appearance can be safely excluded from this assemblage because they lack the necessary synapomorphies: Prolabeo, Prolabeops, Oreodaimon, Capoeta, Varicorhinus and 'rubber-lipped' species of Barbus.

The plesiomorphic condition of the vomero-palatine organ is reckoned to be a low number (4 or 5) of lamellar pairs (in Tylognathus); the lamellar count increasing to 7 + 2 in derived labeine groups and reaching ca 26 in Epalzeorhynchos and the Labeo bicolor species-group. The incrassate nature of the lamellae in Tyloganthus is uniquely derived, i.e. an autapomorphy.

In rheophilic aufwuchs scrapers (species of Labeo and Garra) the vomero-palatine organ is usually rudimentary in adults, and Matthes (1963, 12) considers this to be a primitive condition. I do not share this view. I t has been argued above (p. 506) that the degree of development of the organ is associated with the size of ingested particles (food and sediment) which, in turn, is controlled by ecological factors such as substrate and water velocity. Rheophilic species apparently ingest very fine particles and this fact correlates with an ontogenetic regression of the vomero- palatine organ. This pattern of regression is repeated in transformation series of species in habitats ranging from slow-flowing water (e.g. Labeo niloticus; organ well developed) to brisk flows (e.g.L. coubie; organ slightly regressed) to rapid flows (e.g. L. forskalii; organ markedly regressed) to torrential flows (e.g.L. sorex; organ extremely regressed). From these ecological, ontogenetic and transformational data, I argue that the rudimentary organ seen in rheophilic species is a derived or apomorphic condition. Certainly, rheophilic species are in most other aspects of their morphology and in their ecology, the most specialized of labeine species. Furthermore, if we accept the generic integrity of Labeo and Garra, then this apomorphic (regressed) condition of the organ must have evolved twice, in- dependently. This is the most economical assumption, as there is ample morpholo- gical evidence to show that Labeo and Garra are each monophyletic taxa (Reid 1978).

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508 G. MeG. Reid

I t may well be tha t a more detailed comparative study of the elements which comprise the vomero-palatine organ will reveal more apomorphies of use in further sub-dividing or identifying labeine cyprinids. Finally, it should be noted that labeine cyprinids are confined to the tropical-old-world, i.e. North American and European cyprinid taxa do not have a vomero-palatine organ. This implies tha t the organ evolved after vicariance events which separated the tropical-old-world from North American and Europe bu t before events which isolated Africa from Asia. This notion should be of use in future biogeographic analyses of cyprinids.

Summary The vomero-palatine organ is a peculiar fleshy structure which occurs on the

buccopharyngeal roof of 15-20% of cyprinid fish species. Researchers have advanced three main hypotheses for the function of the organ: respiratory, sensory and trophie. From a study of comparative biology a trophic function is most likely, but there are points in favour of the two remaining ideas. I t is suggested tha t the organ is primarily concerned in bolus-formation by the active co-mixing of precipitating mucous secretions with ingested particles (food and sediment). Comparative studies also show the organ to be of taxonomic use. I t is a shared specialization (synapomorphy) which unites the labeine group it characterizes. The vomero-palatine organ is found in a regressed state in rheophilic algae-scraping species of Labeo and Garra. Using standard cladistic arguments and ecological da ta on feeding habits, it is suggested that this regression is a derived condition (autapomorphy) which has evolved independently in these two genera. Finally, the fact tha t the vomero-palatine organ is restricted to a large monophyletic group of tropical-old-world cyprinids is of biogeographic significance.

Acknowledgments I must thank Dr. P. H. Greenwood, Dr. K. E. Banister and Mr. Gordon Howes

(Fish Section, British Museum of Natural History) who read and criticized the manuscript. I am also grateful to Dr. R. P. Vari (Division of Fishes, Smithsonian Insti tution, Washington} for providing me with some unpublished information on curimatids. Mrs. Noreen Brewster kindly typed the final draft. The Trustees of the B.M.N.H. were good enough to let me use the facilities of the Fish Section. I gratefully acknowledge financial support from a Science Research Council, Research Studentship. Additional support for the completion of this work was generously p r o v i d e d b y Merseyside County Museums.

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