1 Introduction
De Haan [1] recently described the occurrence of parietal pits in colubrid snakes of the subfamily Psammophiinae from seven species belonging to four genera. Drawings of these structures [2] in the psammophine snake Rhamphiophis maradiensis Chirio & Ineich, 1991 were previously published in this species description, without the authors explicitly noting them. These small apertures, numbering two to four, are located in the parietal plates of only some individuals belonging to some different species of that snake group. These structures are not sexually dimorphic. According to de Haan's observations (op. cit.), when present in a specimen, pits are permanent and do not vary in size and shape during the life span of the animal. Their function is unknown. De Haan [1] suggests that they are used in sensory perception, because they are located in the head area, but such an explanation requires a histological investigation. The hypothesis that considers them as apical stigmata to facilitate the process of skin shedding was rejected by this author.
During a study of head plate conformation in colubroid snakes, we observed the occurrence of similar structures in Atretium schistosum (Daudin, 1803), a presumably non-psammophine colubrid snake. Atretium Cope, 1861 is a genus of Asiatic colubrid consisting of two species: A. schistosum and Atretium yunnanensis Anderson, 1879. Atretium schistosum is an endemic species occurring on the Indian subcontinent, from India, Nepal and Sri Lanka. It is also reported from Myanmar, Malaysia, probably an erroneous locality, and from the Chinese province of Yunnan, which is undoubtedly a record of A. yunnanensis [3]. Atretium schistosum is a diurnal and ovoviviparous species restricted to freshwater habitats [3], which feeds on fish and small amphibians. In Sri Lanka, the species has been reported from some estuaries and even in coastal waters [4]. Its ecology is different from that of the psammophine snakes, which generally live in arid to semi-arid areas, but some species also occur in humid forests, seldom near water. Psammophine snakes are mainly distributed in Africa, whereas Atretium is found only in Asia.
After examination of the 12 specimens of A. schistosum available in the collection of the Paris Natural History Museum (MNHN), we concluded that these parietal pits appear to be homologous with those encountered in the Psammophiinae. Since Atretium schistosum may be only distantly related to the Psammophiinae, we here formulate a novel hypothesis to explain the function of these structures, accounting for their sporadically occurrence and discuss their distribution within the colubroid snake clade.
2 Material and methods
Measurements were taken to the nearest 0.1 mm with an electronic caliper. Drawings were made using a light chamber fixed to a LEICA MS5 binocular microscope. The cephalic plate nomenclature used follows that of Chippaux [5]. Specimens examined during this study are all deposited at the MNHN, Paris, and are preserved in 75% ethanol. Twelve specimens were examined: MNHN 582, 1946.64 and 1994.1075, India, Pondichéry; MNHN 612, 1994.2342–3, India, Bengal; MNHN 1890.481, Sri Lanka; MNHN 1902.165, India, Coromandel; MNHN 1999.8089 and 7000, Madagascar?; MNHN 3519 and 7414, Philippines?
3 Results
3.1 Parietal pits
Among the 12 specimens of Atretium schistosum available in the MNHN collections, only two females (16.6%) show parietal pits (MNHN 612 and MNHN 1946.64) (Table 1). One specimen (MNHN 612) presents two pits on the left parietal plate, meeting at the posterior part, forming a Y-shaped structure. The right parietal plate of this specimen is devoid of pits (Fig. 1b and d). The second specimen (MNHN 1946.64) shows a pit in the centre of each parietal plate (Fig. 1a and c). De Haan [1] mentioned the existence of small vesicles present along the bottom of the parietal pit. These are visible when the superficial level of the old epidermis is removed. These structures were not visible because the Paris specimens are relatively old and their state of preservation has not conserved the fragile parts. The similarity of the parietal pits observed in Atretium schistosum with comparable structures mentioned by de Haan [1] is evident in their shape, location, size and number. Such similarity appears to be homologous between these structures, suggesting possible inheritance from a common ancestor. De Haan [1] also noted that these parietal pits can occur symmetrically (47% of the specimens) or asymmetrically (53%); the specimens of A. schistosum examined here are in accordance with this observation.
Features of specimens of Atretium schistosum in MNHN collections. Parietal pits (PP): presence (P) or absence (A); Gular pits (GP): presence (P) or absence (A); sex of adult specimens obtained by tail dissection: (M) male, (F) female and (J) juvenile; TL: tail length; SVL: snout-vent length. Specimens showing parietal pits are indicated in bold
MNHN | PP | GP | Sex | TL | SVL |
7414 | A | P | F | 141 | 487 |
582 | A | A | F | 138 | 459 |
1994.1075 | A | P | M | 157 | 344 |
1999.8089 | A | P | M | 165 | 381 |
7000 | A | P | M | 115+ | 358 |
1902.165 | A | P | J | 77 | 194 |
1890.481 | A | P | J | 42 | 114 |
3519 | A | P | M | 114 | 262 |
1946.64 | P | A | F | 100 | 524 |
612 | P | P | F | 144+ | 508 |
1994.2342 | A | P | F | 142 | 616 |
1994.2343 | A | P | F | 167 | 585 |
![](/biologies/article/CRBIOL_2006__329_3_180_0/jpg/src/tex/figures/gr001.jpg)
Location of the parietal pits in Atretium schistosum. (A, C) MNHN 1946.64; (B, D) MNHN 612. Scale bars = 2 mm.
3.2 Gular pits
Out of 10 of the 12 examined specimens, other structures were observed, including small protuberances located on the chin, at the level of the inferior labial scales and the mental plates, gular plates and symphysials, but also on some of the first ventral plates (Fig. 2, Table 1). Such structures are also encountered in some psammophine snakes, as noted by de Haan [6]. The simultaneous occurrence of both these structures in the same species seems to argue in favour of them being functionally linked. De Haan (op. cit.) suggested that they could have a function in chemical olfactory marking.
![](/biologies/article/CRBIOL_2006__329_3_180_0/jpg/src/tex/figures/gr002.jpg)
Location of the gular pits in Atretium schistosum (MNHN 7000). Scale bar = 1 mm.
4 Discussion
4.1 Parietal pits: an earlier origin, and a wider distribution within snakes than expected
The exact position of the genus Atretium inside colubroid snakes is still debated, this genus having never been included in any phylogenetical analysis. According to Underwood (pers. commun. in [4]), the genus should be classified in the subfamily Xenodontinae. In the light of recent data [7,8], such a hypothesis is untenable and can reasonably be rejected, phylogenetic relationships of that subfamily showing that it is restricted to the New World. Two other subfamilies were suggested to include Atretium, the Natricinae, as suggested by Deuve [3], or the Colubrinae, as proposed by De Silva [4]. The last hypothesis, never formulated until now, would consist in including Atretium inside, or close to the psammophine, but given the high morphological, ecological and biogeographical differences between those two groups, this possibility appears to be very few probable. So, in the light of our observations, the occurrence of parietal pits could no more be taken as a unique synapomorphy of the Psammophiinae as suggested by de Haan [1]. These structures, probably glandular or sensory, should rather be considered as regressed organs constituting a plesiomorphy of the wider snake group of colubroids. Indeed, given that psammophine snakes are more closely related to the elapids and the atractaspidids than to most of the other colubrids [9], these pits could have been present at the base of the colubroid lineage and then regressed in most groups. Such a hypothesis is valid, whether Atretium is a natricine or a colubrine.
4.2 How is the presence of such structure explained?
Two plausible hypotheses are here considered in order to account for the sporadic occurrence of parietal pits as well in Psammophiinae than in A. schistosum.
(1) It could be an atavistic phenomenon. According to Hall [10], atavisms are the reappearance of ancestral characteristics in individual members of a species. They constitute proof that the genetic and developmental information originally used in the production of such characteristics has not been lost during evolution, but lies quiescent within the genome and in the processes of embryonic development. This occasionally resurgent trait may or may not be functionally expressed. By way of examples, the domestic horse, Equus caballus, can occasionally possess supernumerary digits [11], and the development of teeth in chick embryos can be experimentally induced by transplanting mouse neural crest cells [12]. In colubroid snakes, parietal pits could occasionally ‘reappear’ in some individuals (as could be the case in Atretium and among some Psammophiinae); some snake lineages would be more likely to produce such atavistic individuals. The low number of occurrences of pits within one species seems to indicate that they no longer have a functional role, as is often the case for several complex atavistic organs. Caution should be exercised, however, when interpreting the occurrence of these pits in only two colubroid lineages. These could in fact exist in other lineages, but they may be scarcely visible, and thus have not attracted the attention of herpetologists. A similar example is provided by the recent discovery of an external epidermoid supralabial gland present in all species of the viperid genus Echis [13,14]. These snakes have been previously examined by many herpetologists, yet the gland not noticed, although the gland aperture is visible without magnification. That is why it would be interesting to search for the presence of parietal pits in the most basal lineages of Alethinophidians (homalopsids, viperids, xenodermatids, boids, etc.) in order to determine whether their occurrence is more widespread in the basal clades of snakes.
(2) The second hypothesis considers these structures as permanent organs by colubroid snakes at least. They could be present permanently but in a discreet way, hidden by the tegument. Only after an injury, or an anomaly in the embryonic development, or even during some pathologies, will these structures open to the exterior. Those parietal pits could then play an unsuspected secretory or sensorial role.
Smith [15] described the presence of nuchal glands in 11 species of Asian natricine snakes of the genus Balanophis M. Smith, 1938, Macropisthodon Boulenger, 1839 and Rhabdophis Fitzinger, 1843. Those dorsal paired glands are distributed in the neck (and could also extend to the whole length of the body in some species). They could exude an irritant secretion in order to repulse potential predators. However, contrary to the parietal pits, those organs have never been observed directly on the head of any specimen.
Concerning the presence of gular pits, de Haan [1] formulated several hypotheses regarding their function. One of these considers the pits as ‘contact joints’, which allow the snake to shed correctly, in retaining the skin to shed until the most favourable moment for shedding. Another hypothesis suggests that pits could play a role in sexual recognition during precopulatory parades and during copulation itself. Indeed, among many snakes, the male lays his head flat on that of the female during the copulation parade (Fig. 3). The supposed glandular gular pores, presumably secretory structures, are then in contact with the parietal pits of the female, which perhaps receive chemical signals or sensory information. This hypothesis seems less probable, because the frequency of occurrence of parietal pits is low inside the one species. Moreover, the hypothesis of parietal pits hidden under the parietal plate is incompatible with the transmission of chemical information from the gular pits of one individual to the receptor organs located in the parietal pits of another.
![](/biologies/article/CRBIOL_2006__329_3_180_0/jpg/src/tex/figures/gr003.jpg)
‘Head-on-head’ mating position.
5 Conclusion
Occurrence of epidermoid glands in snakes may be more frequent than previously thought. Such structures are just beginning to be documented in snakes. Their function is currently unknown. Histological studies underway by de Haan will allow a better knowledge of their function. It is important that herpetologists be aware of the possible existence of such structures in order to be able to look for them, allowing a better knowledge of their occurrence among snakes.
Acknowledgements
The authors are grateful to Jean-Pierre Gasc (MNHN) and Elizabeth Scott (American Museum of Natural History) for their interesting comments and corrections on the manuscript.