reproductive and trophic ecology of an assemblage of aquatic and
TRANSCRIPT
Reproductive and Trophic Ecology of an Assemblage of Aquatic and
Semi-Aquatic Snakes in Tonle Sap, Cambodia
Sharon E. Brooks1, Edward H. Allison2, Jennifer A. Gill3, and John D. Reynolds4
We studied the reproductive and trophic ecology of a group of aquatic and semi-aquatic snakes that face severehunting pressure in Cambodia. Over a two-year period we sampled hunters’ catches, measuring and dissecting a total of8982 specimens of seven snake species, five of which belong to the family Homalopsidae. The seven species—Enhydrisenhydris, Enhydris longicauda, Homalopsis buccata, Enhydris bocourti, Erpeton tentaculatus, Xenochrophis piscator, andCylindrophis ruffus—all inhabit Tonle Sap Lake, the largest lake in South-East Asia. All species are sexually dimorphic ineither body size or tail length. The larger species, E. bocourti and H. buccata, have a larger size at maturity, and the non-homalopsids, X. piscator and C. ruffus, have the highest and lowest fecundities, respectively. Clutch size increasessignificantly with female body size in all species, and with body condition in E. enhydris. Our data also suggest thatrelative investment in reproduction increases with size in E. enhydris, which has the largest sample size. All speciesexcept one are synchronized in their timing of reproduction with the seasonally receding flood waters of the lake. Therewas variation in both the frequency of feeding and the prey size and type among species, with the homalopsids moresimilar to one another than to the other non-homalopsid species. The prey to predator mass ratio ranged from 0.04 to0.1 in the homalopsids, compared to 0.15 to 0.17 in the non-homalopsids. There was also variation in the feedingfrequency between the sexes that differed between species and six species continued to feed while gravid. Thesedetailed life history analyses can help provide a basis for assessing conservation options for these heavily exploitedspecies.
TONLE Sap Lake in Cambodia is home to anassemblage of aquatic and semi-aquatic snakes thatare heavily exploited and traded as a food supply for
the numerous crocodile farms surrounding the lake (Stuartet al., 2000). As a result of the growing demand from thisindustry over the last 20 years, this exploitation nowrepresents the world’s largest snake hunting operation, withan estimated 6.9 million snakes removed annually (Brookset al., 2007a, 2007b), yet it proceeds without knowledge ofthe basic population biology of the species involved. Thisstudy aims to increase our understanding of the reproduc-tive and trophic ecology of these snake populations as partof a program to assess the severity of this threat.
Five of the species in this community belong to the familyHomalopsidae. There is also a member of the Natricidae(Xenochrophis) and a member of the Cylindrophiidae(Cylindrophis). Homalopsidae consists of approximately 37viviparous species distributed throughout South and South-East Asia from India to North Australia (Gyi, 1970; Voris etal., 2002; Murphy, 2007). The greatest diversity andabundance is in South-East Asia, where the snakes arelargely found in lowland freshwater habitats (Voris andKarns, 1996). Homalopsids can comprise a large part of thevertebrate biomass of the aquatic systems they inhabit(Voris and Karns, 1996), and there is speculation that somespecies may thrive in areas dominated by human activitiessuch as rice cultivation, which may provide suitable habitatand food supplies (Gyi, 1970; Murphy and Voris, 1994).While there is a growing literature on the ecology ofhomalopsid species (Jayne et al., 1995; Voris and Karns,1996; Murphy et al., 1999; Karns et al., 1999–2000),reviewed by Murphy (2007), the Cambodian populationshave received little attention since the work of Saint Girons
in the 1970’s (Saint Girons and Pfeffer, 1971; Saint Girons,1972).
Tonle Sap Lake is the largest wetland in South-East Asiaand exhibits an extraordinary seasonal fluctuation in waterlevel and size. As a result of the rising waters of the MekongRiver during the monsoon season each year, the Tonle SapRiver reverses and Mekong water flows into the Tonle SapLake, inundating a large expanse of forest (Bonheur andLane, 2002). This lake receives intense fishing pressure, andit has been suggested that homalopsids thrive in such areasdue to reductions in size composition of fish communities,increasing the snakes’ food supply while decreasing theabundance of their natural predators (Murphy, 2007).However, in recent years, decreasing fish catches from thelake have led to human exploitation of several snake species,primarily to provide food for the growing number ofcrocodile farms, and some snake species now face thelikelihood of population declines (Brooks et al., 2007a).While most of the species in this study are widely distributedthroughout the region, the Tonle Sap Water Snake, Enhydrislongicauda, is endemic to the Tonle Sap Lake and River. Thestatus of this species has not been assessed, but its limiteddistribution and high level of exploitation throughout itsrange raises strong conservation concerns.
The extreme level of exploitation of snakes at this studysite allowed assessment of a large number of specimens thathad been killed during routine hunting operations. Here weexplore life history variation within and among speciesthroughout the year, to identify breeding seasons and todescribe the ecological traits of this aquatic and semi-aquaticsnake community. Inter-specific comparisons are includedas they can be useful for predicting how species will differ intheir response to exploitation. The large sample sizes
1 Department of Geography, University of Cambridge, CB2 3EN, Cambridge, U.K.; E-mail: [email protected]. Sendreprint requests to this address.
2 The WorldFish Center, P.O. Box 500, GPO, 10670 Penang, Malaysia, and School of Development Studies, University of East Anglia, NorwichNR4 7TJ, U.K.
3 School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, U.K.4 Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada.Submitted: 20 April 2007. Accepted: 11 June 2008. Associate Editor: G. Haenel.F 2009 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CE-07-102
Copeia 2009, No. 1, 7–20
available for some species have allowed us to adopt someanalytical approaches used by fish biologists for studies ofpopulation dynamics.
MATERIALS AND METHODS
Study site.—Biological monitoring programs were based atChong Khneas landing site in Siem Reap province on thenorthern side of Tonle Sap Lake in Cambodia. This is themost important location for snakes being transported fromthe lake as a result of the high number of crocodile farms inSiem Reap province.
Study species.—We purchased a total of 8982 dead snakesfrom traders on a weekly basis during two hunting seasonsthat extended from June 2004 to March 2005 and June 2005to March 2006. Seven species that occur regularly in thetrade were included in the study, with sample sizes that varyaccording to their abundance in catches. We measured(snout to vent length [SVL] and total length), weighed, andsexed 4356 Enhydris enhydris, 1634 Enhydris longicauda, 1609Homalopsis buccata, 141 Enhydris bocourti, 869 Erpetontentaculatus, 234 Xenochrophis piscator, and 139 Cylindrophisruffus. We analyzed each species for sexual dimorphism ofbody mass, length, and tail length and for the relationshipbetween body length and mass, which we square-roottransformed. Only non-reproductive females were used inanalyses using mass, as the mass of the clutch could bias theresults.
Sampling issues.—We sampled snakes by haphazardly select-ing crates of snakes as they arrived at the landing site toensure the data were as representative of catch compositionas possible. The size composition of the catch is influencedby the size-selective capture technique. The gill nets used inTonle Sap capture a large range of sizes of reproductive-agedindividuals of most species, but large adults of the two largerspecies, H. buccata and E. bocourti, are not caught by thismethod. For these two species, we therefore sampled thelarger adults from those that had been caught by baitedhooks and traps.
Reproductive biology.—For each female we recorded thereproductive state as inactive, vitellogenic, or embryonic.Embryonic eggs were categorized as follows: A1—eggfertilized and oviducal but no embryo yet visible, A2—smallembryo present, A3—scales present on the embryonic snake,A4—pigmentation of the embryonic snake present but notcomplete and brain still visible, A5—fully developed,resembling a neonate. This classification was adapted fromthe 37 stages identified in Thamnophis sirtalis (Zehr, 1962).We considered females as reproductively mature when theycontained vitellogenic follicles or oviducal eggs or showedevidence of being post-partum, indicated by a thickened andmuscular oviduct. Reproductively inactive females showed aribbon-like oviduct. However, as the oviduct regresses aftereach reproductive bout, mature females that have bredpreviously but have yet to thicken their oviduct in thisseason would be scored as immature, resulting in a slightbias in this method, particularly if females do not breedevery year (Harlow and Taylor, 2000; Keogh et al., 2000).
There is no standard method for determining the size orage at maturity in reptiles. Often the minimum size at whichgravid or reproductively active individuals are observed is
used as an indication, which we include here for compar-ative purposes (Fitzgerald et al., 1993; Blouin-Demers et al.,2002). However, variation between individuals in size atmaturity makes this method heavily sample-size dependent.We therefore also adopted a more representative andstatistically robust method, which is widely used in fisheriesresearch (Jennings et al., 2001), to estimate the length atwhich 50% of the female population is mature (SVL50),based on a logistic regression of the length of mature versusimmature females:
P Mð Þ~ 1.
1 z e{ a z b SVLð Þð Þ� �
,
where P(M) is the probability of being mature, a is the y-intercept, and b is the coefficient for the predictor variable(SVL). The SVL when the probability of being mature is 50%
was then calculated as:
SVL ~ a=b:
An alternative indicator of size is mass, which might bemore appropriate for comparisons among species, due todifferences in shape. As our mass measurements includedgravid females, we could not use the above method to makedirect calculations of the mass at which 50% of the femalepopulation is mature. Instead, we used length–mass rela-tionships within each species to convert the length at 50%
female maturity to mass at 50% female maturity.
We measured the right testis of dissected males andestimated volume from length and width based on theformula for a prolate spheroid (vol 5 4/3p (K teste length) N(K teste width)2 (Harlow and Taylor, 2000). As the mass ofthe gonads was unknown, the gonadosomatic index (GSI),which is a measure of the mass of the testis relative to themass of the animal, could not be calculated. Instead wecalculated the testis volume per 100 g snake in order to takeaccount of the varying size of males.
Trophic ecology.—We examined stomach contents of indi-viduals of all seven species between June 2004 and March2006. Presence or absence of food items was noted andidentified into broad taxonomic groups where possible.When prey items were intact, we weighed and measuredthem and where possible identified the species. We retrieved277 intact prey items, of which 249 were from the stomachsof three species; E. enhydris, E. longicauda, and H. buccata. Allof the data in these analyses were checked for a normaldistribution and log transformed where necessary.
RESULTS
Sexual dimorphism and sex ratios.—All species, except H.buccata, show sexual dimorphism of body size with femalessignificantly longer and/or heavier than males (Table 1).The lack of sexual size dimorphism in H. buccata and E.bocourti with regard to length is likely to be the result ofinsufficient sampling in the upper range of body size by thesize-selective gill net fishery. Sexual size dimorphism isreflected in the maximum sizes of individuals in our sampleswhere females are two to three times heavier than males.This difference is also illustrated in the mass–lengthrelationships, where females of all species except C. ruffusaccrue a greater mass per unit length increase (Table 1). Allspecies, other than C. ruffus, exhibit significant sex differ-
8 Copeia 2009, No. 1
Tab
le1.
Sex
Ratios
an
dSexu
ally
Dim
orp
hic
Traits
ofth
eSeve
nW
ate
rSn
ake
Sp
eci
es.
Sex
ratios
are
rep
ort
ed
as
the
nu
mb
er
ofm
ale
s/fe
male
s.W
here
two
valu
es
are
giv
en
,th
ese
rep
rese
nttw
osa
mp
les
of
smalle
rsn
ake
s(c
ap
ture
dby
gill
net;
25
–86
cmSV
L)an
dla
rger
on
es
(captu
red
by
baited
ho
oks
an
dtr
aps;
56
–1
35
cmSV
L).T
he
linear
rela
tio
nsh
ips
betw
een
mass
an
dSV
Lare
giv
en
.Pva
lues
are
deri
ved
fro
mt–
test
sco
mp
ari
ng
diffe
ren
ces
betw
een
the
sexe
sfo
rm
ass,
SV
L,an
dta
ille
ngth
(***
*P
,0
.00
01
,**
*P
,0
.00
1,**
P,
0.0
1,*
P,
0.0
5).
Sp
eci
es
Sex
ratio
(M:F
)
Sq
rtm
ass
(y)
2Sq
rtSV
L(x
)re
gre
ssio
neq
uatio
n(R
2)
Mass
(g)
mean
61
SE
(max)
SV
L(c
m)
mean
61
SE
(max)
Tail
len
gth
as
pro
po
rtio
no
fSV
Lm
ean
61
SE
fem
ale
male
fem
ale
male
Pfe
male
male
Pfe
male
male
P
Enhyd
risen
hyd
ris1
.44
y5
3.9
38
x2
17
.61
7(0
.70
)y
52
.85
4x
2
10
.74
7(0
.54
)
97
.86
1.2
(33
5)
n5
11
54
81
.56
0.5
(28
5)
n5
24
48
****
50
.56
0.2
(74
.1)
n5
18
26
47
.66
0.1
(69
.3)
n5
23
71
***
0.2
86
0.0
01
0.3
26
0.0
01
***
Enhyd
rislo
ngic
auda
0.8
3y
54
.81
0x
2
21
.25
8(0
.79
)y
54
.14
3x
2
17
.02
5(0
.57
)
15
0.9
62
.6(5
18
)n
58
92
11
7.5
64
.6(2
60
)n
57
25
****
48
.96
0.2
(89
)n
59
11
44
.26
0.2
(59
.7)
n5
69
1
****
0.2
76
0.0
02
0.3
46
0.0
02
****
Hom
alo
psi
sbucc
ata
1.1
8/
0.7
2y
54
.10
9x
2
19
.43
4(0
.80
)y
53
.83
5x
2
17
.47
8(0
.78
)
24
2.4
65
.5(1
74
0)
n5
73
0
24
9.8
63
.8(6
15
)n
57
22
NS
74.0
60.5
(134.5
)n
5875
74.0
60.5
(100.0
)n
5698
NS
0.2
96
0.0
02
0.3
46
0.0
02
****
Enhyd
risboco
urt
i1
.2/
0.5
5y
54
.94
7x
2
21
.32
(0.9
1)
y5
3.6
71
x2
13
.19
2(0
.65
)
26
7.9
63
1.8
(11
10
)n
56
5
19
6.9
61
4.7
(55
9)
n5
71
*57.3
62.6
(105)
n5
70
53
.26
1.7
(98
.5)
n5
71
NS
0.1
56
0.0
06
0.2
26
0.0
08
****
Erpet
on
tenta
cula
tus
1.0
6y
53
.55
9x
2
14
.93
9(0
.62
)y
53
.46
0x
2
14
.38
6(0
.54
)
10
4.1
62
.3(3
87
)n
53
23
81
.86
1.3
(29
7)
n5
44
3
****
50
.16
0.3
(77
.5)
n5
36
6
45
.96
0.2
(70
)n
53
80
****
0.4
36
0.0
04
0.5
26
0.0
04
****
Xenoch
rophis
pis
cato
r0
.70
y5
4.8
1x
2
25
.18
(0.7
8)
y5
3.6
01
x2
15
.58
6(0
.66
)
16
0.1
61
0.1
(62
0)
n5
10
6
10
3.1
63
.8(2
22
)n
59
8
****
60.6
61.0
(89)
n5
113
50
.46
0.7
(67
)n
57
5
****
0.3
66
0.0
12
0.4
16
0.0
11
***
Cyl
indro
phis
ruffus
0.5
4y
53
.69
x2
16
.22
(0.4
1)
y5
5.3
1x
2
29
.05
(0.7
3)
22
4.4
68
.0(4
10
)n
57
9
22
0.9
61
0.5
(37
9)
n5
48
NS
71
.56
0.8
(86
.4)
n5
78
68
.66
1.2
(80
.5)
n5
37
*0
.02
16
0.0
03
0.0
19
6
0.0
00
4N
S
Brooks et al.—Ecology of exploited snakes 9
ences in tail length, with males having considerably longertails—a widely reported sexually dimorphic trait in snakes(Table 1).
The sex ratios reported here show considerable variationbetween species and, for five of the seven, they deviatesignificantly from 1:1, with E. enhydris the most male-biasedand C. ruffus the most female-biased (Table 1). In H. buccataand E. bocourti, the observed sex ratio shifts from male-biased in smaller snakes (first value) to female-biased inlarger snakes (second value), and therefore sex ratios becomeskewed in favor of the females at upper ranges of body sizes.
Size at maturity.—For all species other than C. ruffus, theSVL50 could be estimated using logistic regression. Thesevalues are converted into mass at maturity (Table 2) usingthe linear length–mass relationships given in Table 1. Therewas considerable variation among the species in mass atmaturity, with H. buccata and E. bocourti maturing at a muchlarger size than the other species, and E. tentaculatusfollowed by E. enhydris maturing at the smallest size. Sizeat maturity for males is unknown for all species as we didnot record any immature males.
Reproductive output.—Females of all species exhibit a strongpositive relationship between clutch size and body size(Fig. 1). An ANCOVA with clutch size as the dependentvariable, species as a factor, and SVL as a covariate showedthat clutch sizes differed significantly between species(F6,1069 5 5.33, P , 0.0001). Bonferroni-corrected post hoccomparisons showed X. piscator had significantly largerclutch sizes than all other species, and C. ruffus, E. bocourti,and H. buccata had significantly smaller clutches than theother species (P , 0.05). An interaction effect between SVLand species demonstrated that there were significantdifferences between the species in the relationship betweenclutch size and SVL (F6,1069 5 15.78, P , 0.0001), with themost notable difference being the weak relationship shownby E. longicauda (Fig. 1).
The potential ranges of fecundities can be estimated fromthe linear fit of clutch size against SVL and using the
estimated size at maturity as a minimum and the maximumobserved female body size as a maximum (Fig. 2). The size-selective capture method may influence the estimated meanclutch size for some of the populations, particularly H.buccata and E. bocourti. Figure 2 illustrates considerablevariation in fecundity among species, with the non-homa-lopsids, X. piscator and C. ruffus, showing the highest andlowest fecundities, respectively. The homalopsids had inter-mediate clutch sizes, which appear similar to one another.
Body condition (BC), measured as mass of females withlitters removed divided by SVL, has a significant positiverelationship with clutch size (CS) in E. enhydris (CS 5
5.41(BC) 2 2.11, R2 5 0.35, F1,197 5 101.3, P , 0.0001) andthe same trend is apparent in E. longicauda, although therelationship is weaker (CS 5 2.60(BC) + 5.57, R2 5 0.36, F1,9
5 5.0, P , 0.052). Sample sizes were too small to test forrelationships in the other species.
An ANCOVA with egg stage as a fixed factor and SVL as acovariate showed that, for any given size of snake, clutchsizes of vitellogenic eggs are significantly larger than thoseof embryonic eggs in E. enhydris (F1,647 5 493.7, P , 0.0001).Enhydris longicauda shows a similar trend of a reduction inclutch size from vitellogenic to embryonic stages, but thiswas not significant (F1,183 5 0.66, P 5 0.42; Table 3). For E.enhydris the decline in clutch size occurs post-fertilization, aspost hoc analysis of a one-way ANOVA shows that thenumber of eggs at stages A2 to A5 are significantly lowerthan those at the vitellogenic (yolk) or fertilized (A1) stage(F5,671 5 17.63, P , 0.0001). In contrast, for E. longicaudathere is some decline in clutch size between vitellogenic andfertilized eggs and then again between fertilized and fullterm embryos (A5), although these differences are notstatistically significant (F2,189 5 1.56, P 5 0.21). For bothof these examples, there is greater variation for the moredeveloped stages due to smaller sample sizes. No significantdifferences were seen between the clutch sizes of vitellogen-ic and embryonic eggs in any of the other species, althoughthis may partly be an artifact of low sample sizes,particularly for E. bocourti and C. ruffus. Xenochrophis piscatoris oviparous and therefore does not appear in this analysis.
Table 2. The Estimated Size at Maturity of Water Snakes from Logistic Regression Models of Percentage Mature Females in Relation to Snout–VentLength (SVL). SVL at 50% maturity (SVL 50) is shown and converted to mass at 50% maturity (Mass 50) using the linear relationships given in Table 1(** P , 0.0001, * P , 0.01). Exp b represents the change in probability of an individual being mature with a unit change in SVL according to themodel for each species. The % predicted correctly indicates how accurately the model can predict maturity based on SVL. The minimum size (SVL) ofmature females observed is also shown with the total number of mature females observed (n).
SpeciesMinimum SVL atmaturity (cm) (n)
SVL50 (SVL atmaturity (cm))
Log-likelihood
Chi-squared Exp b (95% CI)
% predictedcorrectly
Mass50 (Mass atmaturity (g))
Enhydris enhydris 41.0 (836) 48.73** 392.6 194.8 1.387(1.302–1.478)
80.8 96.44**
Enhydris longicauda 38.8 (319) 44.75** 461.5 88.6 1.207(1.153–1.263)
74.6 119.23**
Homalopsis buccata 67.2 (291) 81.26** 369.5 493.3 1.411(1.337–1.490)
89.1 310.05**
Enhydris bocourti 66.5 (16) 71.32** 12.7 31.7 1.198(1.053–1.362)
90.6 418.39**
Erpeton tentaculatus 37.8 (188) 47.23** 250.7 68.6 1.287(1.196–1.384)
74.1 90.55**
Xenochrophis piscator 45.4 (38) 60.51* 69.9 3.4 1.052(0.995–1.113)
54.7 149.40*
Cylindrophis ruffus 61.2 (37) 63 (P50.1) 32.1 2.5 1.153(0.953–1.395)
79.4 170.50
10 Copeia 2009, No. 1
Fig. 1. Fecundity–body length relationships for seven snake species. Clutch size is measured as the number of eggs per breeding bout and iscombined for vitellogenic and embryonic eggs. Each data point represents a gravid female. Linear regression equations and R2 values can be found inTable 3.
Brooks et al.—Ecology of exploited snakes 11
The relative clutch mass (RCM), calculated as the mass ofthe clutch/maternal mass, was derived from females con-taining embryonic eggs for four of the species. This is ameasure of the reproductive effort made by a female perbreeding bout. Cylindrophis ruffus shows a considerablyhigher RCM than the others, and H. buccata exhibits thelowest (Table 3). Enhydris enhydris showed a slight positiverelationship between RCM and body length (RCM 5
0.004(SVL) 2 0.078, R2 5 0.11, F1,200 5 25.94, P , 0.0001).A similar trend was seen in E. longicauda, although thesample size was small and the relationship was notstatistically significant (RCM 5 0.008(SVL) 2 0.217, R2 5
0.04, F1,9 5 0.41, P 5 0.54). SVL is strongly correlated withmass, which is the denominator for RCM. Existence of apositive relationship therefore provides evidence that therelative investment in reproduction increases with anincrease in body size. There were insufficient data todetermine if this relationship existed in the other species.
Neonate size also varies significantly between species(F3,174 5 22.72, P , 0.0001) with the largest species, E.bocourti, producing larger offspring (Table 3). No full-termneonates were observed in individuals of H. buccata, E.tentaculatus, or X. piscator.
Timing of reproduction.—All species, except C. ruffus, breed atthe same time. Females undergo vitellogenesis in Novemberand December, which matches the timing of the seasonalreduction in water levels in the lake (Fig. 3). Developingembryos were observed in successive months, and, althoughthis varies between species, embryogenesis appears to betaking place mostly in February and March. Enhydris enhydrisis an exception because it displays two breeding seasons. Thefirst period of vitellogenesis occurs as the water starts to risein July and August with embryogenesis taking place betweenAugust and October, and the second period matches theother five species (Fig. 3). In all species, peaks in testis sizeare synchronized with female vitellogenesis (Fig. 3). For E.enhydris, this occurs in both July and December, and for allother species, except for C. ruffus, the peaks occur betweenOctober and December.
Trophic ecology.—The diet of this assemblage shows astriking difference between the five homalopsids and thetwo non-homalopsids, X. piscator and C. ruffus (Table 4).Whereas the homalopsids fed nearly exclusively on fishes,the other two species ate a significant amount of non-fishprey (Table 4). Xenochrophis piscator has the most diversediet, with the major components being fish (77%) and frogs(16%). For C. ruffus, 40% of the diet was composed of snakesand 60% eels (family Synbranchidae). The prey species ofsnake identified were E. enhydris (80%) and E. tentaculatus(20%), n 5 5. One individual of H. buccata contained a frogin its stomach.
In total, ten fish families were identified within thestomachs of this snake assemblage, with the two common-est families being Cyprinidae (minnows and carps) andOsphronoemidae (gouramies). Of the cyprinids, all fish
Table 3. Reproductive Allocation for Seven Water Snake Species. R2 values and linear regression equations are given for the relationships betweenclutch size and body size shown in Figure 1 (* P , 0.05, ** P , 0.001, *** P , 0.0001). Mean sizes of vitellogenic and embryonic clutches are given.Mean relative clutch mass (RCM) and neonate length are given for species for which data exist.
Species
Clutch size–SVL relationship
Clutch size Mean relativeclutch mass(litter mass /
maternal mass)(61 SE)
Meanneonate totallength (cm)
(61 SE)
Vitellogenic Embryonic
R2 Linear equation RangeMean
(6 1 SE) RangeMean
(6 1 SE)
Enhydris enhydris 0.43 *** y 5 0.602x–20.28 4–34 13.5 6 0.30(n 5 414)
2–28 10.6 6 0.32(n 5 263)
0.15 6 0.001(n 5 213)
18.9 6 0.16(n 5 75)
Enhydris longicauda 0.44 *** y 5 0.865x–25.98 6–44 19.4 6 0.57(n 5 179)
5–24 16.23 6 1.2(n 5 13)
0.15 6 0.03(n 5 12)
17.5 6 0.33(n 5 23)
Homalopsis buccata 0.39 *** y 5 0.404x–23.98 4–23 11.7 6 0.35(n 5 106)
4–24 12.4 6 1.1(n 5 19)
0.10 6 0.02(n 5 5)
Enhydris bocourti 0.72 * y 5 0.345x–16.88 6–20 13.6 6 2.66(n 5 5)
11 11.0 (n 5 1) 25.0 6 0.14(n 5 4)
Erpeton tentaculatus 0.28 *** y 5 0.432x–9.834 3–29 12.2 6 0.49(n 5 79)
6–29 13.9 6 1.21(n 5 24)
Xenochrophis piscator 0.73 *** y 5 1.24x–46.075 9–74 33 6 3.28(n 5 29)
Cylindrophis ruffus 0.90 ** y 5 0.293x–11.869 4 4 (n 5 1) 6–14 9.4 6 0.85(n 5 9)
0.41 6 0.04(n 5 8)
19.4 6 0.23(n 5 76)
Fig. 2. Fecundity ranges for seven snake species, based on the linearregressions of clutch size (number of eggs) versus SVL shown in Fig. 1.Minimum values are based on the estimated clutch size at length atmaturity (Table 2) and maximum values are based on the estimatedclutch sizes at maximum observed female length. The mean observedclutch sizes are also shown.
12 Copeia 2009, No. 1
species belonged to the genus Trichogaster and of theophronoemids most belonged to the genera Henichorynchus(56%), Cyclocheilichthys (19%), and Opsarius (15%).
Across all species, prey size increased with snake SVL. Atwo-factor ANCOVA was conducted using both prey length
and prey mass as the dependent variable, with sex andspecies of snake as factors and SVL as the covariate. Only E.enhydris, E. longicauda, and H. buccata were included in thisanalysis due to the low sample sizes for all other species.Unsurprisingly, snakes with a larger SVL consumed larger
Fig. 3. Breeding seasons for the seven snake species. The bars represent the percentage of all females that were reproductive, including vitellogenic(white bars) and embryonic (solid bars). The line represents the mean testis volume 6 standard error. Data shown are from June 2004 until March2006 and no data exist for April and May 2005. The sparse amount of data for 2004, for all species except E. enhydris, is the result of lower samplingeffort that year. The graph in the bottom left-hand corner illustrates the seasonal fluctuation of water level in the lake (data extracted from MRC/FINWater Utilisation program, 2000).
Brooks et al.—Ecology of exploited snakes 13
Tab
le4.
Die
tary
Data
for
Bo
thSexe
so
fA
llSeve
nSp
eci
es.
%co
nta
inin
gfo
od
repre
sen
tsfe
ed
ing
frequ
en
cy.
Pre
ysi
ze(l
en
gth
and
weig
ht)
take
nfr
om
asm
alle
rsa
mp
leo
fin
tact
pre
yitem
s.Pre
yty
pe
identified
into
bro
adta
xono
mic
gro
up
san
din
tofish
fam
ilies
for
asm
alle
rsu
b-s
amp
le.
Enh
ydri
sen
hyd
ris
Enh
ydri
slo
ng
ica
ud
aH
om
alo
psi
sb
ucc
ata
Enh
ydri
sb
oco
urt
iEr
peto
nte
nta
cula
tus
Xen
och
rop
his
pis
cato
rC
ylin
dro
ph
isru
ffu
s
MF
MF
MF
MF
MF
MF
MF
%co
nta
inin
gfo
od
(n)
42
.0(2
34
1)
53
.3(1
65
8)
44
.4(7
20
)4
7.6
(90
6)
38
.1(7
07
)4
3.3
(87
4)
44
.1(6
8)
47
.1(6
8)
34
.1(4
43
)3
3.7
(42
4)
75
.3(9
7)
60
.7(1
35
)2
0.8
(48
)1
7.1
(88
)N
um
ber
of
mea
sure
dpre
y2
55
81
44
14
96
25
43
22
41
7M
ean
pre
yle
ngt
h6
SE(m
m)
69
.36
3.4
81
.96
2.8
79
.56
6.3
93
.76
3.5
97
.66
2.8
11
0.3
6
5.3
92
.76
23
.38
0.5
6
26
.64
9.4
6
1.2
10
1.0
6
40
.99
7.9
6
44
.96
9.9
6
15
.15
7.8
10
6.3
6
57
.6M
ean
pre
yw
eigh
t6
SE(g
)3
.26
0.2
77
.16
0.6
37
.76
1.8
10
.76
1.3
15
.16
1.4
21
.36
3.4
13
.56
6.0
10
.96
4.4
2.2
6
0.4
10
.76
7.7
9.0
6
4.1
12
.76
2.4
61
.05
1.5
6
10
.5Pre
yty
pes
No.id
entif
ied
tobro
adta
xonom
icgp
30
73
76
80
15
31
39
19
91
51
03
33
72
84
75
15
%Se
rpen
te0
00
00
00
00
00
04
0.0
42
.3%
Anura
n0
00
00
0.5
00
00
14
.31
7.0
00
%Roden
t0
00
00
00
00
03
.63
.20
0%
Bird
00
00
00
00
00
02
.10
0%
Inse
ct0
00
00
00
00
00
2.1
00
%Fi
sh1
00
10
01
00
10
01
00
99
.51
00
10
01
00
10
08
2.1
75
.56
0.0
57
.7N
umbe
rfis
hid
entif
ied
tofa
mily
26
34
11
35
50
66
54
21
03
03
%Fa
mily
Anab
antid
ae3
.98
.81
8.2
17
.15
6.0
59
.10
00
00
33
.30
0%
Fam
ilyB
agrid
ae0
00
8.6
00
20
.00
50
.00
00
00
%Fa
mily
Chan
nid
ae0
00
2.9
6.0
9.1
00
00
00
00
%Fa
mily
Cyp
rinid
ae7
3.1
52
.92
7.3
42
.92
.03
.00
00
00
00
0%
Fam
ilyM
asta
cem
bili
dae
00
00
03
.00
00
00
00
0%
Fam
ilyN
andid
ae3
.91
1.8
18
.22
.90
00
00
00
00
0%
Fam
ilyO
sphro
nem
idae
19
.22
6.5
36
.42
5.7
36
.02
5.8
40
.05
0.0
50
.01
00
.00
33
.30
0%
Fam
ilyPan
gasi
idae
00
00
00
02
5.0
00
00
00
%Fa
mily
Silir
idae
00
00
00
20
.00
00
00
00
%Fa
mily
Synbra
nch
idae
00
00
00
20
.02
5.0
00
03
3.3
01
00
.0
14 Copeia 2009, No. 1
prey (prey length F1,232 5 62.78, P , 0.0001, log prey weightF1,234 5 45.79, P , 0.0001), but both species identity and sexhad an independent effect on prey size (species effect: preylength F2,232 5 4.49, P , 0.05, log prey mass F2,234 5 10.37, P, 0.0001 and sex effect: prey length F3,232 5 3.21, P , 0.05,log prey mass F3,234 5 3.68, P , 0.05). Homalopsis buccataconsumed much larger prey, followed by E. longicauda withE. enhydris consuming the smallest prey. Females of allspecies consumed larger prey than males both in absoluteterms (Table 4) and after controlling for SVL (statisticsabove). Analyses of prey to predator mass ratios showedthat the two non-homalopsids ate much larger prey itemsrelative to their body size than did the homalopsids (Fig. 4).
Contingency table analysis revealed that there weresignificant differences between the species in their feedingfrequency (x2
6 5 86.74, P , 0.0001), with most of thevariation resulting from the low count for C. ruffus (Fig. 5).Within some species, there were significant differencesbetween the sexes; E. enhydris and H. buccata showedsignificantly higher feeding frequencies in females and lessin males than expected (x2
1 5 48.88, P , 0.0001 and x21 5
4.37, P , 0.05, respectively), and X. piscator showedsignificantly higher feeding frequencies in males and lessin females than expected (x2
1 5 72.03, P , 0.0001; Fig. 5).Comparisons were also made between feeding frequenciesfor breeding and non-breeding females. When breeding, E.enhydris fed less frequently (x2
1 5 25.07, P , 0.0001) and E.longicauda fed more frequently (x2
1 5 7.0, P , 0.001). Nobreeding individuals of C. ruffus were found with food intheir stomachs, but this finding did not differ from the otherspecies due to the low number of breeding individualsencountered and the low feeding frequency for this species(x2
1 5 2.95, P 5 0.086; Fig. 5).
DISCUSSION
Sexual dimorphism and sex ratios.—All species are sexuallydimorphic either in overall size, with females heavier orlonger than males, or in tail length, with males havinglonger tails. Sexual size dimorphism may be the result offemales growing more quickly rather than living longer, ashas been shown in studies of northern water snakes, Nerodiasipedon (Weatherhead et al., 1995). The direction andmagnitude of sexual size dimorphism depends on relativebenefits and costs of growth and size in each sex (Andersson,1994). These are typically determined by size–fecunditybenefits in females and size–competitive benefits in males(Fairbairn, 1997; Szekely et al., 2004). We have shown strongsize–fecundity relationships in females of most species,suggesting that larger body size could be favored byselection for greater reproductive output. Cylindrophis ruffus,however, showed weak sexual size dimorphism, despite astrong size–fecundity relationship in females. It is possiblethat a large male size offers advantages that are absent in theother species, for example, through combat or displacementof other males in mating aggregations (Weatherhead et al.,1995). In species for which male–male combat has beenshown, males usually reach a larger size than females (Shine,1978, 1994a). Tail length relative to body length has beenshown to be another sexually dimorphic trait in many snakespecies, with males having longer tails than females, as aresult of sexual selection for male mating success (Shine etal., 1999). In this study, the lack of tail size dimorphism inC. ruffus again implies that this species may have a differentmating system than the others.
The size dimorphism exhibited by these snakes translatesinto changes in sex ratios with size for H. buccata and E.
Fig. 4. Prey mass relative to predator mass (6 standard error). Symbols a, b, and c denote homogeneous subsets to which the species belong,derived from post hoc analyses following a one-way ANOVA of mean prey/predator mass ratio. Those with different symbols are therefore statisticallysignificantly different from one another.
Brooks et al.—Ecology of exploited snakes 15
bocourti, and consequently size-selective capture techniqueswill be biased with regard to sex ratio. Most snakes show a1:1 sex ratio at birth, although skewed sex ratios have beenobserved in a few species (Shine and Bull, 1977). Sex ratiosare difficult to determine due to differing activity patternsbetween males and females (Shine, 1994b). Our study of E.enhydris is a case in point. This species may form matingaggregations during the breeding season, as indicatedthrough sightings by local fishers in Thailand (Murphy,2007), and it has also been reported that males are attractedto fishing traps containing females. Such behavior couldaccount for the strong male-biased sex ratio seen for thisspecies.
Size at maturity.—Size and age at maturity are key life historyvariables that affect population vulnerability to exploitation(Reynolds, 2003). We report both mass and length as sizeparameters. Mass may be a better indication of inter-specificvariation in age at maturity, as it indicates the biomass thatmust be accumulated before a female is able to breed and isindependent of body shape. Enhydris bocourti, whichmatures at a smaller length than H. buccata, has aconsiderably greater mass at maturity. Similarly, E. long-icauda, which matures at a relatively small length comparedto the other similar-sized homalopsids, has a greater mass atmaturity. The use of mass, however, may be confounded bycurrent body condition and stomach contents, which willvary independently of the sexual maturity of the snake.
Reproductive output and strategies.—The clutch sizes andmean relative clutch mass (RCM) reported here for E.enhydris are considerably lower than those documentedpreviously in this lake (Murphy et al., 2002). This cannot beexplained solely by differences in sample sizes because,despite our large sampling effort with this species, we didnot find any female with a litter size as large as in thisprevious study. This suggests that there may have been some
reduction in fecundity between the years of the two studies.Nonetheless, the clutch sizes and RCM values reported herefor the Cambodian populations of E. enhydris are stillconsiderably larger than those reported for this species inboth Thailand and Myanmar (Murphy et al., 2002). TheTonle Sap Lake in Cambodia is famous for its productivefisheries (Lim et al., 1999; Lamberts, 2006), and it istherefore possible that there is a more abundant supply offish available to the snakes here than in other parts of theirrange. This could increase their body condition and accountfor the greater clutch sizes observed in Cambodia, comparedwith Thailand and Myanmar.
The clutch sizes shown for H. buccata are consistent withthe ranges seen in previous studies (Berry and Lim, 1967),and the larger average clutch size in our study may be due toa greater sampling of adults, which are sought and traded fortheir skins. Since Berry and Lim did not present size–fecundity relationships, we cannot test whether this is thecorrect explanation, but this underscores the importance ofreporting fecundities as a function of body size. Clutch sizesfor E. tentaculatus are higher than previously recorded, withdocumented litter sizes ranging from 5 to 12 (Martinez andBehler, 1988), compared to the range of 3 to 29 shown here.The range of SVL of females in our study is considerablyhigher, and this could account for the difference.
Relative clutch mass (RCM) is used as a measure ofreproductive effort and is often thought to reflect trade-offsin allocation of resources among maintenance, storage,growth, and reproduction. The low RCM values reportedhere for the homalopsid species support previous research,which showed that aquatic viviparous snakes have a lowerlevel of reproductive investment than terrestrial egg-layingspecies (Seigel and Fitch, 1984; Shine, 1988). The longreproductive season of viviparous species and the mobilityrestriction of a large clutch mass when swimming aresuggested to have resulted in selection for a low RCM. Thisis further supported by the higher RCM value reported here
Fig. 5. Proportion of individuals containing food in the stomachs. This is shown for males, females, non-breeding and breeding females for allspecies separately. Values above bars denote sample sizes. Where the number of females in the sample is greater than the sum of the breeding andnon-breeding females, this is due to missing data on the reproductive status of females due to putrefication of specimens.
16 Copeia 2009, No. 1
for C. ruffus and the large clutch size of X. piscator, the moreterrestrial species within this assemblage.
Life history theory predicts a trade-off between clutch sizeand offspring size, as has been reported within and amongspecies (Fleming and Gross, 1990; Olsson and Shine, 1997;Kolm et al., 2006). Across the species in this study, we seesuggestions of a negative trend between offspring size andnumber, but this is confounded by variation in maternalbody size between the species. Our study suggests that H.buccata and E. bocourti show a lower reproductive effort thanthe other homalopsids, as a result of their smaller clutchsizes at maturity. This is reflected in the low RCM of H.buccata. This has strong conservation implications for therelative vulnerability of these larger-bodied species (Brookset al., 2007a). The relationship between RCM and body sizeseen in E. enhydris suggests that reproductive effort increaseswith age, at least for this species. This suggests that theallocation of resources to reproduction changes over time,perhaps with more energy being allocated to growth earlieron in life, given the advantages of large body size for lifetimereproductive success.
The reduction in clutch sizes between vitellogenic andembryonic staged females shown for two of the species inthis study, E. enhydris and E. longicauda, indicates a lack ofefficiency in converting eggs into neonate snakes. It isunclear whether this difference is due to lack of fertilization,or whether eggs are aborted post-fertilization. There is noevidence that squamate reptiles are able to resorb abortiveeggs, based on the functional morphology of the oviduct(Blackburn, 1998). Observations made during our study ofsolidified vitellogenic eggs in the oviduct alongside devel-oping embryonic eggs in E. enhydris further support the viewthat abortive eggs would be expelled rather than resorbed.
Reproductive synchrony and timing.—The flood pulse in river-floodplain systems is considered the principal driving forcebehind the seasonal patterns in productivity of the flora andfauna of this region (Junk et al., 1989). The reproductivesynchrony of all species except for C. ruffus thereforesuggests that the flood pulse may be driving the seasonalreproduction of this snake assemblage. Based on estimates ofthe gestation period of E. enhydris as 2 to 2.5 months, and H.buccata as 2 to 3 months (Saint Girons and Pfeffer, 1971;Saint Girons, 1972), we expect that for all species except forC. ruffus, parturition occurs during the dry season betweenApril and June. The newborn neonates would therefore bepresent in the floodplain at the onset of the rainy season(May to June), prior to or just as the Mekong water floodsthe lake. This is when the majority of fish species within thefloodplain of Tonle Sap reproduce (Lim et al., 1999). Thetiming of reproduction by the snakes may therefore betimed to match the presence of optimal conditions for thenewborn snakes, such as availability of prey items (fish fry)and the presence of nursery conditions when the grasslandsare beginning to flood. This information can help to informconservation management strategies, such as closed huntingseasons to protect species during the breeding season(Brooks et al., 2007a).
The seasonal changes in testis volume reported hereprovide evidence for seasonal sperm production in thesesnakes. For most species, males show peak testicular activitybetween October and December prior to the presence ofovarian eggs in females. Spermatogenic cycles in thehomalopsids can therefore be said to be pre-nuptial,
whereby testis mass peaks prior to ovulation, a characteristicof many tropical snake populations (Maunaga et al., 2003).For all species in this study, sperm production occurs whilethe majority of females are undergoing vitellogenesis.However, given the likelihood that the females have theability to retain sperm (Sever and Ryan, 1999), thissynchronized timing of sperm production by the males tothe female’s fertile period is likely to be the result of spermcompetition.
Females of E. enhydris appear to breed all year round, butthere are two distinct peaks per year. This concurs withprevious studies of this species (Saint Girons and Pfeffer,1971; Murphy et al., 2002). It is unknown whether a singlefemale is capable of breeding twice a year or whether thepattern stems from different individuals breeding at differ-ent times. We observed females that contained fat storeswhen heavily gravid, whereas, in most snakes, fat storesbecome depleted during vitellogenesis (Scott et al., 1995). Itis likely that this is typical of tropical aquatic snakes thatshow a high frequency of feeding, even while gravid, thusenabling them to undergo vitellogenesis soon after parturi-tion.
Cylindrophis ruffus is the only species in this assemblagethat does not breed when the lake is receding, but issynchronized with the first breeding season of E. enhydris.We speculate that this species could be out of synchronywith flooding periods in order to synchronize with theperiods of productivity of their prey, which include theother snakes in this assemblage.
Trophic ecology.—Previous studies of the two non-homalop-sids in this assemblage show them both to be top predators,with X. piscator feeding largely on frogs, and C. ruffus oncaecilians and other snakes (Kupfer et al., 2006). Thismatches our findings, although eels and other fish comprisea significant proportion of their diet. The local Khmer namefor X. piscator is ‘poh sumlap gon gaeb’ which literallytranslates as ‘snake that eats frog.’ Cylindrophis ruffus haspreviously been reported to be a predator of homalopsids(Voris and Murphy, 2002; Karns et al., 2005) but has neverbeen reported to prey on E. tentaculatus. This snake hasclearly specialized to a diet of relatively large elongated preyitems, i.e., snakes and eels.
The homalopsids in this study are almost entirelypiscivorous. This is in accordance with what was previouslyknown for these species, although Deuve (1970) reportedcrustaceans in the stomachs of H. buccata in Laos, along withfish and frogs (Voris and Murphy, 2002). There is a great dealof overlap between the fish diet of this snake communityand the fish composition taken by the fishery on Tonle Sap,with species of the family Cyprinidae dominating both (Limet al., 1999). This highlights a potential connection betweenhuman fishing activities and the snake populations. TonleSap Lake is currently undergoing intense fishing at levelsthat may be unsustainable (Bonheur and Lane, 2002), andthis is likely to have conservation implications for this snakeassemblage. However, based on this study, the homalopsids,although restricted to a diet of fish, appear to be fairly non-specialized feeders, which should increase their resilience tosuch effects.
The prey-to-predator mass ratios reported here for homa-lopsids are lower than for other groups of snakes (Rodrıguez-Robles et al., 1999; Greene and Rodrıguez-Robles, 2003), andgiven that larger prey items are available, at least for the
Brooks et al.—Ecology of exploited snakes 17
smaller of the species, this suggests they are restricted intheir choice of prey with regard to size. Other homalopsidshave been shown to consume relatively small prey items(Jayne et al., 1988), and some have been shown to tear largeprey items into smaller pieces, thus overcoming gapelimitations (Jayne et al., 2002).
Sex differences in feeding biology shown in this study canbe explained by sexual dimorphism in body size, with thelarger snakes taking larger prey items. However, it has beensuggested in other studies that the difference in choice ofprey size between males and females may drive this sexualsize dimorphism (Shetty and Shine, 2002; Shine et al., 2002).In this study we see considerable overlap between the sexesin their choice of prey, providing no evidence that malesand females follow separate allometric trajectories withregard to prey size.
We found high and consistent feeding rates throughoutthe wet season, even through pregnancy, which matchesprevious studies of tropical aquatic snakes (Shine et al.,2004; Karns et al., 2005). The homalopsids do not bask, andtheir body temperature remains very stable (Murphy et al.,1999; Karns et al., 2002). They may therefore need to feedcontinuously to sustain this metabolic rate as they cannotseek out cooler refuges to digest food slowly. Cylindrophisruffus, which feeds on larger prey, is more likely to berestricted in feeding while gravid, due to the physiologicalconstraint of containing both eggs and large food items.This would also account for the lack of females observedwith vitellogenic follicles or developing embryos as, if theyare not feeding while gravid, they presumably may remaininactive to reduce their vulnerability to predators. The factthat females with full-term neonates were captured indicatesthat this species starts moving at this stage, perhaps insearch of a suitable habitat to give birth.
Xenochrophis piscator, which also feeds on large food items,appears to continue feeding while undergoing vitellogene-sis. However, we did not find any individuals with enlargedfollicles containing a large food item in its stomach. In factall of the vitellogenic females with full stomachs containedpartially digested material that could not be measured oridentified, and all of the data on prey size for this speciescame from non-breeding individuals. It is therefore possiblethat this species switches to smaller food items, such as fish,as it undergoes vitellogenesis.
ACKNOWLEDGMENTS
We thank H. Voris, J. Murphy, and B. Stuart from the FieldMuseum of Natural History, Chicago and D. Karns fromHanover College, Chicago, who assisted us greatly withsetting up the methodologies for this project and for sharingtheir knowledge of homalopsid snakes. In particular wethank J. Murphy and D. Karns who advised us in the field inCambodia. We are grateful to C. Poole, J. Walston, S. Visal,H. Sovannara, and L. Kheng from the Wildlife ConservationSociety Cambodia program and K. Davies, F. Goes, and Y.Pathomrath from the Sam Veasna Center for WildlifeConservation for their logistical and technical supportthroughout this research project. Most of all we thank ourfield assistants in Cambodia, K. Prokrotey, S. Van, B. Touch,V. Kranh, and C. Chea for their concerted efforts in the field.This work was funded by the Research Fellowship Programof the Wildlife Conservation Society in New York, the Northof England Zoological Society, and two U.K. Research
Councils (NERC and ESRC). This is WorldFish contributionnumber 1879.
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