Contributions to Zoology, 70 (3) 139-146 (2001)
SPB Academic Publishing bv, The Hague
studies Ecological on a population of the water snake Grayia smythii in a
of rainforest swamp the Niger Delta, Nigeria
Godfrey+C. Akani¹ & Luca Luiselli²
'Department ofBiological Sciences, Rivers State University ofScience and Technology, P.M.B. 5080, Port
2 Harcourt, Rivers State, Nigeria, e-mail:[email protected]; Centre of Environmental Studies
“Demetra”, via dei Cochi 48/B, 1-00133 Rome, Italy: F.I.Z.V., via Olona 7, 1-00198 Rome, Italy; and Mu- nicipal Museum of Natural History, piazza A. Frezza 6, 1-00030 Capranica Prenestina, Rome, Italy, email: [email protected] (corresponding author)
Keywords: Grayia smythii, Colubridae, snakes, ecology, Nigeria
Abstract Introduction
The few of snakes of the The ecology of the water snake, Grayia smythii (Reptilia: species aquatic genus
occurring in a seasonal rainforest of the Colubridae) swamp Grayia constitute a systematically problematic
Niger Delta (southern Nigeria) was investigated between De- group of Colubridae that is endemic to tropical cember 1998 and March 2000. Females and males were similar Africa (Boulenger, 1909). They have been con- in body sizes (SVL) and head sizes, but males had tails the sidered as belonging to subfamily Grayini significantly longer than females. The diet was constituted only
and fish. The but also with some by frogs majorprey type was Xenopus tropicalis, (Meirte, 1992), “lycodontines”
followed and Clarias Adult sex-ratio by Tilapia sp. sp. was morphological affinities to South American 1:1. Sloughing ofskin and ovipositions occurred in dry season, xenodontines (e.g. McDowell, 1987). Although in the humid enclosure of buttress roots amongst leaf litters. these snakes notori- locally abundant, aquatic are from 8 14 with of Fecundity ranged to eggs per female, a mean ously difficult to catch, and their ecology is known 10 = smallest female eggs (SD 1.8). The gravid was 78.2 cm
SVL. laid in batches ofthree in for a few and anecdotal comments Eggs were to four eggs at a site, only general
at three different sites. The size ofthe least two to eggs averaged (e.g. see Cansdale, 1961; Isemonger, 1962; Pit-
3.1 cm in length, 2.1 cm in width, and had a fresh weight ranging man, 1974; Villiers, 1975). from 18,2 22.1 Maternal size influenced the to g. significantly Grayia smythii (= smithii, cf. Meirte, 1992, for of number eggs produced by female,but not their average size. a discussion on its correct name) is one of the com- There was a statistically significant negative correlation bet-
monest water snake of seasonal number of and size. Predators ofthis snake species rainforest ween eggs mean egg
at area herons fishermen. and bodies of the the study were and swamps permanent water Niger
Delta basin and south-eastern flank of Nigeria
(Butler and Reid, 1986, 1990; Luiselli et ah, 1998;
Contents Akani et ah, 1999). Like other rainforest snakes,
its and there persecution goes on unabated, are
Abstract 139 conservation considerations hardly any (Akani et
Introduction 139 ah, 1999). Moreover, the meat was described as a
Study area , 140 several rural households and delicacy by may Methods 141
be traded on. Results 141 possibly
Limited data Morphometry 141 ecological on Nigerian specimens
Food habits 142 are available only in Dunger (1971), Butler and Sex-ratio and reproductive biology 142 Reid (1986, 1990), and in more recent studies by Sloughing cycles 144 Luiselli and Akani (1999), Akani et ah (1999), and Discussion 144„ Luiselli et ah (1998). Acknowledgements 146 In view of References 146 the significance of Grayia smythii in
the ecosystem dynamic of the seasonal rainforest
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this Table I. Means and Standard Deviation of physico-chemical swamps (Luiselli et al., 1998), study was con- parameters ofthe seasonal freshwater at Rumuosi (Rivers ducted in order to provide basic information on its swamp State, Nigeria), where the ecology of Grayia smythii has been biometrics, habitat characteristics, food habits, studied. Ranges are in parentheses. reproduction and behaviour.
Parameter Wet Season Dry Season
= (N = 65) (N 57)
area Study Air Temperature (°C) 25.6 ± 1.5 30.8 ± 1.8
(24 - 29) (27.6 - 33)
The Water (°C) 25.1 + 0.8 28.5 ± 1.1 data presented here are based on a field study Temperature
(24 - 26.1) (26.2 - 30,4) from carried out during the wet and dry seasons, PH 5.6 ± 0.9 6.2 + 1.3 December 1998 to March 2000. The study area (4.8 - 6.6) (5.0 - 6.8)
30 ha of is a seasonal rainforest (about surface) Electricity pS/cm 15.7 ± 5.4 24.7 ± 6.8
located 5 km - - swamp at Rumuosi, approximately 1 Conductivity (10.0 23.0) (12.8 30.5)
Salinity 0(0) 0(0) on the northern flank of Port Harcourt (04° 45' N, Transmittance at 98 ± 1.3 97+1.8 004° OT E), the capital city of Rivers State, Nige-
420 p (%) (97.2 - 99.5) (96.0 - 98.9) ria. The vegetation is essentially secondary forest, Dissolved Oxygen (rag/1) 0.5 + 0.2 0.5 ± 0.2 characterized such flora as by Pterocarpus sp., (0- 1.0) (0- 1,0)
14.1 Raphia sp., Triumphetta eriophlebia, Mitragyna TDS (mg/1) 12.2 ± 2.5 ± 2.0
which broad and (10.0 - 13.1) (12.0 - 16.8) stipulosa, etc. have leaves, grow
Total Alkalinity as adventitious roots as the water level rises. On the CaC03 (mg/1) 14.8 ± 3.2 16.2 ± 2.6 slightly elevated spots, the trees Triplichiton sclero-
- (12.0 - 18.6) (13.1 19.3) Terminalia xylon, Khaya sp., superba, Mitragyna ciliata are found. The undergrowth is lush and dominated by pterophytes (ferns), shrubs, herbs, and sedges. Due to the shading effect of the crown, Shrimp, leeches, amphibians (Xenopus tropicalis,
similar to light conditions were twilight even at Ptychadena spp., Hoplobatrachus occipitalis, Bufo midday. Another significant feature of the swamp maculatus, Bufo regularis, and undetermined
is that the forest floor is interspersed with several Hyperoliidae tree-frogs), fish (families Clariidae,
natural and man-made ponds of varying depths and Cichlidae, Malapteruridae, Phractolaemidae, Cypri-
surfaces, often bordered by hydrophytes. nodontidae), reptiles (Agama agama, Mabuya affi-
The Rumuosi on cf. swamp depends exclusively nis, Psammophis phillipsi, Natriciteres variegata,
rainfall during wet season (May-October) for its Natriciteres fuliginoides, Gastropyxis smaragdina,
link all and small water supply and has no at to other water Naja nigricollis, Causus maculatus), bodies. Inundation of the swamp usually occurs mammals(Crocidura nigeriae, Crocidurapoensis,
/ which area of over 25 by July August, during an Mus musculoides, Lemniscomys sp., Rattus rattus)
be encroaches into in the ha may underwater. Floodwater are found in the swamp or immediate sur-
farmlands serious dam- neighbouring causing crop roundings (Akani and Luiselli, unpublished trap- age. The water is lentic, generally shallow but deeper ping data). Apart for fishermen (who catch these
in in the ponds, and is brown colour. By dry sea- snakes with no return valves), the major natural
85% the son (Novcmbcr-April) over of swamp dries predators of Grayia smythii at the study area were
the Thick that out, leaving water only in deep ponds. herons, were observed to prey even on adult
Nile monitors cushions of dry leaves are common due to increased specimens from the water surface.
leaf abscission in the dry season. The surface of (Varanus niloticus ornatus) were also observed
covered with float- other of the ponds at this time is green preying on adult Grayia smythii in areas
Lemna Azolla and ing macrophytes, including sp.,. sp., the Niger Delta, cobras (Naja nigricollis and
lotus, these snakes Ceratophyllum demersum, Nymphaea etc. Naja melanoleuca) also may prey on
dissolved and Total in and known to Water temperature, pH, oxygen, as they can forage water are eat
Dissolved Solid (TDS), and Alkalinity, measured occasionally on snakes (Luiselli and Angelici,
in in situ, are presented Table 1. 2000).
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Methods
Samples of Grayia smythii were collected both by
traps and by capture of specimens encountered
during standardized routes throughout the study
area. Specimens trapped were captured by means of 12 basket traps with no return valves (fishing
gears commonly used in the area), set amongst barricades (approximately I m high) that entirely
surrounded the As swamp perimeter. already ex-
the varied plained, swamp perimeter considerably
between seasons. These barricades were made of
palm fronds obtained from the Oil palm tree, Elaeis Fig. I. Correlation between body length (SVL, cm) and tail guineensis and reeds. The traps were set for 65 in length Grayia smythii from the study area.For statistical details, days in the dry season, and for 57 days in the wet see text. season in both shallow and deeper waters. They
were set by 8.00 am each day and inspected by the
same time the following day. Other sources of the
specimens included fishermen’s catch, both when
the inundated the swamp was and when ponds were
bailed in dry season. All captured individuals were
taken to the research laboratory at Department of
Biological Sciences, Rivers State University of
and Science Technology (Port Harcourt), not more
than two hours after collection. Morphometric
measurements (snout-vent length (SVL), tail length
(tL), head length (HD), head width (HW), and body
mass were recorded from all the captured speci-
mens. The specimens that had died were already Fig. 2. Correlation between body length (SVL, cm) and head dissected for determination of stomach sex, con- length in Grayia smythii from the study area. For statistical details,
see text. tents, fecundity, egg sizes, etc.
Statistical analyses were done by a SPSS and a
STATISTICA for Windows PC packages, with all males differed significantly from the females in
tests being two tailed and alpha set at 5%. Means terms of body proportions (Fig. 1). Single-factor
followed of are by ± one Standard Deviation. analysis covariance (with sex as the factor, and
SVL as the covariate) showed that for the same
body length, female Grayia smythii had shorter tails Results than males (ANCOVA on ordinate intercepts: F =
19.201, DFn = 1, DFd = 21,P< 0.0001). Indeed,
the in Morphometry two sexes differed significantly terms of mean
= tL / SVL ratio (males: x 0.485 ± 0.019, N = 15,
SVLs = + were measured in 16adult males and 17 adult range 0.458-0.525; females: x 0.413 0.023, N
females from the = intersexual study population. Females aver- 16, range 0.388-0.472; differences
aged slightly longer SVL than males (x = 74.48 ± significant at P < 0.000001, Student t-test with df
13.23 cm 69.35 ± 1 1.62 but = On versus cm), the inter- 29). the other hand, the two sexes were simi-
sexual differences did not attain statistical signifi- lar in terms of head size relative to SVL (single-
cance (t = 1.18, df = P = 31, 0.247). Moreover,- factor ANCOVA with sex as the factor and SVL
SVL and although tL = were highly correlated (in as the covariate: F= 3.217, DFn 1, DFd = 27, P
the > two at least P < = In sexes, r 0.74, 0.00001), the 0.834; Fig. 2). fact the mean HD / SVL ratios
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Table It. Summary ofthe data on food habits ofGrayia smythii are forced to fold as they are being swallowed, Rumuosi seasonal freshwater from the swamp. which the The helps ingestion process. largest prey
which measured 11.3 ingested was a Tilapia sp. Prey itemsHems Frequency of Percent of
Occurrence Occurrence cm in total length, and 3.5 cm wide.
Although there were abundant aquatic insects, 33 15.0 Tilapia sp. and in the of leech, shrimps ponds, none these ClariasGlorias 22 10.0 sp. were found in snakes’ stomach. 4 20.020.0 species any PtychadenaPlychadena sp.
Xenopus tropicalis 66 30.030,0
AmiranAnuran tadpoles 2 10.0
Undetermined frogs 33 15.0 Sex-ratio and reproductive biology TOTAL 20 100.0
Adultsex-ratio (16 malesand 17 females) was found
in the = 1:1 were almost identical two sexes (males: x to be (binomial test, P > 0.9).
0.049 ± N = fe- 0.0031, 16, range 0.046-0.057; The bulk of the females caught in dry season
= males: = 0.049 ± N 0.038- = x 0.006, 17, range (73.3%, total N 15) were gravid. Females with
intersexual differences: Student with in December = 0.063; t-test eggs were captured (N 1), January
= = = df 31, t 0.12, P 0.906). (N = 1), February (N = 7), and March (N = 2).
The mean SVL of the gravid females was 81.77 ±
= 6.02 cm (N 11, range 77.2 - 98 cm), and their
429.0 Food habits mean body mass was ± 146.88 g(range 325-
The 800 g). average fecundity was 10.0 ± 1.8 eggs
the female The when in the Dietary data of Grayia smythii at study area is per (range 8-14). eggs, summarized in Table 2. gonad, were elliptical in shape and yellowish to
A total of 33 snake stomachs (16 males and 17 orange in colour. The smallest female to produce females) were examined, and 13 of them (39.4%; eggs measured 77.2 cm SVL and 108.6 cm total
325 and had 9 well 7 of males and 6 of females) were completely empty. length, weighed g, developed
Contingency table analysis revealed that the two eggs in the ovary.
did not differ in terms of were laid end of March in the enclo- sexes significantly pro- Eggs by
> of buttress portion of specimens with prey in stomachs (P sure roots amongst leaf litters close to
0.3). Five of 11 gravid females had food in the the pond (N = 8 clutches observed). In practice,
the burrows stomach. The proportion of gravid females con- eggs were deposited in small on sandy
In taining food (45.4%) was lower than that of non- soil, and were covered by abundant leaf litter. gravid females (100%, N = 6), and suggests a re- all cases observed (N= 8), they were laid in batches duction of three to four in the feeding rates of the specimens with eggs at a site, which means that a
female its in least three eggs. may oviposit eggs at two to
found different sites that the clutch size Grayia smythii was to prey exclusively (given average upon fish (25%) and anurans, either tadpoles or of each female was approximately 10 eggs. The
size of the in metamorphs (75%). The major fish prey was Tila- eggs averaged 3.1 cm length, 2.1 cm
followed Clarias and the in and had fresh from 18.2 pia sp. by sp., major width, a weight ranging
which is to 22.1 amphibian prey was Xenopus tropicalis, g. abundant in the of coincides with swamp. Dietary composition Grayia smythii oviposition period
2 the P > It the hottest in the two sexes was similar (% test, 0.6). was period swamp (Table 1), and it is observed stomachs that increase in would enhance that all preys found in snake likely temperature were oriented towards the hatchabi of the with their heads poste- 1 ity eggs. rior direction of the snake, which implies that Grayia Maternal size (SVL) influenced significantly the
number of = swallows its prey’s head first. With this habit of eggs produced by female (r 0.66, N swallowing, it is clear that the dorsal spines of the = 11, P < 0.01; regression equation: number of
= cichlid fish - + x or the pectoral spine of the clariid fish eggs 6.96 0.204 SVL; Fig. 3), but not their
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3. Correlation between maternal size and number of in eleven the For Fig. eggs Grayia smythii females from study area. statistical
details, see text.
4. Fig. Correlation between maternal size and mean size in eleven from the For statistical egg Grayia smythii females study area.
details, see text.
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5. Correlation between number of female and in eleven females from the Fig. eggs produced by mean egg size Grayia smythii study
area. For statistical details, see text.
size = N = able data the of average (egg length) (r 0.237, !!,/’> quantitative on ecology Grayia
= - 0.231 0.036 0.1; regression equation: egg size + smythii. Thus, based on the data presented here, a
detailed overview of of x SVL; Fig. 4). However, there was a statistically its ecology is now worthy
significant negative correlation between number discussion. of each female and mean In terms of data showed that eggs produced by egg morphometry, our
= N= P in size (r -0.407, 11, < 0.05; regression equa- males and females were similar body sizes, but
tion; egg size = 4.635-0.199 x number of eggs; differed in body proportions, with males having
Fig. 5). longer tails relative to SVLs. Schmidt (1923) re-
ported that males were longer than females (maxi-
153.5 mum size was cm for the longest male and
Sloughing cycles 135.0 cm for the longest female), which is clearly
contradicted by our own data. Indeed, the maxi-
size in Sloughed skins were always found a few meters mum our sample was attained by a female
3.2 TV = the total whereas the maximum size (0 to m, 14) away from pond, and (138.3 cm length),
under shade. Sloughed skins were found mainly attained by a male was 121.8 cm total length. the during the dry months (December to February), Moreover, largest individuals in our popula-
tion which indicate in this were much smaller than the ones re- may a rapid growth season, largest
in corded Schmidt and Laurent and a pre-oviposition sloughing phase the adult by (1923, see above) by
females. (1956: 167.0 cm total length), whereas they were
similar to the largest specimen observed by Danger
(1972) in Nigeria (142.2 cm total length). How-
the Luiselli Discussion ever, largest specimen captured by et
in Eket al. (1998) (Akwa-Ibom State, Nigeria) ex-
ceeded 160 cm in total Although based on a relatively small sample size, length. The fact that male had our study has probably added significantly to avail- Grayia smythii longer
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tails than females is universal trend in a nearly Delta females that were captured during the wet
colubrid snakes, including species (Shine, 1994). season (May to August, N= 24) were non-gravid,
Our of feed exclu- and it confirms population Grayia smythii definitely that egg-laying may take
and fish, with a in the sively upon frogs preponderance place only dry season. The ecological sig- of the former versus the latter. This evidence is nificance of this pattern is likely linked to the diet
consistent with the for other of the fully few dataavailable offsprings. In fact, as the newborns feed
(Luiselli as well Nigerian populations et ah, 1998), probably on tadpoles and small fish, it is likely as with anecdotal accounts see that find easier to previous (e.g. they may prey upon these or-
Cansdale, In Leston and 1961). Ghana, Hughes ganisms when, just a few weeks after their birth,
(1968) cat-fish as a of the reported prey Grayia smythii, ponds start to be fully inundated and most of whereas Cansdale (1961) found that have Xenopus the anurans their breeding season.
and Clarias are the of The fact that maternal size tropicalis sp. preferred prey and number of eggs this snake. The latter was also true for our popu- produced are highly positively correlated is not
lation. Butler and Reid found fish remains (1990) surprising, as it appears to be a nearly universal in several from the forests of specimens Nigeria. trend in snakes (e.g. see Luiselli and Angelici, 2000;
The of lack intersexual differences in dietary com- Luiselli et al., 2000). The negative correlation position in our also is consistent with between clutch population size and mean egg size has already the minor sexual size dimorphism and the similar been observed in the European Natrix natrix head sizes in the two sexes. In fact, intersexual (Luiselli, unpubl. data), and seems to be quite
with dietary divergence is often correlated diver- equivalent to the pattern observed in the live-bearing in absolute gence body size or in head size (Shine, Thamnophis butleri, where larger clutches produced
1991). It is that the adult females smaller 1986, noteworthy young (Ford and Killebrew, 1983). How-
also continued to con- the lack of correlation forage during pregnancy, ever, positive between fe-
in trary to what of snakes male size and mean size does happens many species egg not mirror data studied to date (e.g. see Saint Girons, 1952). How- of several oviparous snakes from elsewhere, where
their ever, feeding rates are probably reduced, at such a correlation was detected (e.g. see Plummer, least on the basis of the evidence and Akani of a lower per- 1984; et al., 2001 for another Nigerian centage of gravid specimens containing food in forest species). Especially noteworthy is the comparison to non-gravid specimens. The still behaviour exhibited by reproductive females that unresolved their systematic position of Grayia unfortu- deposit clutch in more than one nest site, rather
does allow than the nately not useful comparisons of its ovipositing whole clutch in the same site feeding with those of other at once. It patterns phylogeneti- is clearly demonstrated by our findings related of cally species. small batches of 3-4 eggs at each site, that is
The fact that adult sex-ratio was 1:1 is consis- much less than the minimum number of eggs (8) tent with data available for most snake species produced by the smallest female examined during studied to date, including other forest the Predation after is Nigerian present study. laying a pos- species (e.g. see Luiselli and 2000; Luiselli the small Angelici, sibility to explain numbers of eggs at et al., 2000). each site that should be the rejected. In fact, gen-
Our data demonstrated that of Ni- eral reproduction conditions of all the nest sites examined by us gerian is seasonal and = indicated that the Grayia smythii strongly (N 8) nest sites were clearly synchronous, and that most females should be able violated earlier not by any predator, including also to reproduce every year, as suggested by the high ants or other insects. This oviposition behaviour percent of the is well frequency adult females that were known in chelonians (e.g. Emys orbicu- gravid the season. The data avail- cf. Zuffi and during dry only laris, Odetti, 1998), but, to our knowl- able for also Nigerian Grayia smythii suggests that edge, has never been recordedbefore in free-ranging e in gg-laying should occur season snakes. dry Although very preliminary, our findings toon of a single on 7 December that this captive specimen suggest is likely an important reproduc-
1969, sec Butler and The adult tive Reid, 1990). Niger strategy of Grayia smythii, possibly linked to
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Luiselli Akani GC. 1999. Habitats of in the the need to reduce egg mortality due to predation L, snakes
rainforests of Eket (Akwa-Ibom State, south-eastern (by monitorlizards, othersnakes, birds, mongooses, Nigeria). Herpetozoa II: 99-107. in etc) and to desiccation dry season. Luiselli L, Akani GC, Capizzi I). 1998. Food resource
of of snakes in partitioning a community a swamp-
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Acknowledgements 133.
Luiselli L, Angclici I'M. 2000. Ecological relationships in
two Afrotropical cobra species (Naja melanoleuca and This research study was financiallysupported by Aquater S.p.A., Naja Ecosystem s.r.l., the Institute Demetra, T.S.K.J.Nigeria ltd (Lagos nigricollis). Canad. J. Zool. 78: 191-198. and Port Harcourt) and, indirectly, by ENI Group environmental Luiselli L, Angelici FM, Akani GC. 2000. Large elapids Department. The Federal Department ofForestry, Port Harcourt, the of Jameson’s and arboreality: ecology green mamba is thanked for having permitted to capture the specimens studied (Dendroaspis jamesoni) in an Afrotropical forested region. in this Critical reviews ofthis paper. manuscript were provided Contrih. Zool. 69: 147-155. by two anonymous referees, DrFrancesco M. Angelici, Dr Dario McDowell SB. 1987. Systematics. In: Seigel, R.A., Collins, Capizzi, Dr Ernesto Filippi, Dr Zena Tooze, and Dr Massimo J.T., and Novak, S.S., eds. Snakes, ecology and evolu- Capula. Dr Joe Butler provided us with some crucial references, tionary biology. MacMillan, New York, pp. 3-50. and Dr Zena Tooze polished the English style. Meirte I). 1992. Cles de determination des serpents d’Afrique.
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