reproductive ecology of dipsadine snakes, with emphasis on south ...

REPRODUCTIVE ECOLOGY OF DIPSADINE SNAKES, WITHEMPHASIS ON SOUTH AMERICAN SPECIES

LIGIA PIZZATTO1,4,5, MAURICIO CANTOR

2, JULIANA LIMA DE OLIVEIRA3, OTAVIO A. V. MARQUES

4,VINICIUS CAPOVILLA

2, AND MARCIO MARTINS3

1Pos-Graduacao em Ecologia, Depto. de Zoologia, Universidade Estadual de Campinas, CP 6109, 13083-970, Campinas,SP, Brazil

2Graduacao em Ciencias Biologicas, Depto. de Zoologia, Universidade Estadual de Campinas, CP 6109, 13083-970,Campinas, SP, Brazil

3Departamento de Ecologia, Instituto de Biociencias, Universidade de Sao Paulo, Rua do Matao, Travessa 14 s/n,05508-090, Sao Paulo, SP, Brazil

4Laboratorio Especial de Ecologia e Evolucao, Instituto Butantan, Av. Dr. Vital Brazil 1500, 05503-900, Sao Paulo, SP, Brazil

ABSTRACT: A relatively large amount of variation occurs in the reproductive ecology of tropical snakes, andthis variation is generally regarded as being a consequence of seasonality in climate and prey availability. Insome groups, even closely related species may differ in their reproductive ecology; however, in others itseems to be very conservative. Here we explore whether characters related to reproduction arephylogenetically constrained in a monophyletic group of snakes, the subfamily Dipsadinae, which rangesfrom Mexico to southern South America. We provide original data on reproduction for Leptodeira annulata,Imantodes cenchoa, and three species of Sibynomorphus from southern, southeastern and central Brazil, anddata from literature for other species and populations of dipsadines. Follicular cycles were seasonal inAtractus reticulatus, Dipsas albifrons, Hypsiglena torquata, Leptodeira maculata, L. punctata, Sibynomor-phus spp. and Sibon sanniola from areas where climate is seasonal. In contrast, extended or continuousfollicular cycles were recorded in Dipsas catesbyi, D. neivai, Imantodes cenchoa, Leptodeira annulata, andNinia maculata from areas with seasonal and aseasonal climates. Testicular cycles also varied from seasonal(in H. torquata) to continuous (in Dipsas spp., Leptodeira annulata, L. maculata, N. maculata andSibynomorphus spp.). Most dipsadines are small (less than 500 mm SVL), and females attain sexual maturitywith similar relative body size than males. Sexual dimorphism occurred in terms of SVL and tail length inmost species, and clutch size tended to be small (less than five eggs). Combat behavior occurs in Imantodescenchoa, which did not show sexual size dimorphism. Reproductive timing, for both females and males,varied among species but in general there were no differences between the tribes of Dipsadinae in most ofthe reproductive characteristics, such as mean body size, relative size at sexual maturity, sexual size and taildimorphism, duration of vitellogenesis or egg-carrying in oviducts.

Key words: Dipsadinae; Fecundity; Follicular cycle; Reproduction; Sexual size dimorphism; Sexual taildimorphism; Testicular cycle

REPRODUCTIVE cycles of snakes vary fromhighly seasonal to continuous. In temperateareas, snakes usually reproduce only duringthe warmer months (usually spring) and manyspecies present nonannual cycles. In tropicalareas, however, cycles tend to be morevariable (Fitch, 1982; Seigel and Ford,1987). This higher variability can be partiallyexplained by greater climatic complexity(Greene, 1997) and food availability in tropicalareas (Santos et al., 2005; Seigel and Ford,1987). Climatic factors may be an importantvariable affecting seasonality in reproductivecycles of tropical snakes (Pizzatto andMarques, 2002, 2006). For example, Brownand Shine (2006) provided evidence that, for a

colubrid snake from tropical Australia (Tropi-donophis mairii), abiotic factors such asseasonal availability of moist incubation con-ditions were more important than bioticfactors (e.g., higher predation on eggs orhatchlings, or food availability for hatchlings)on influencing reproductive timing.

Recent studies on the evolution of ecolog-ical characters in Neotropical snakes haveshown that characters related to defenseagainst predators seem to have diversifiedapparently quickly in Neotropical snakes, witha large amount of variation within clades (e.g.,Martins, 1996). In contrast, habitat andmicrohabitat use, as well as diet and manyother characters related to feeding, seem to beconservative, i.e., they have experienced fewchanges during the lineage’s history and,consequently, the snake groups studied show5 CORRESPONDENCE: e-mail, [email protected]

Herpetologica, 64(2), 2008, 168–179

E 2008 by The Herpetologists’ League, Inc.

168

little contemporary variation in these charac-ters (e.g., Martins et al., 2001, 2002). Charac-ters related to reproduction in Neotropicalsnakes seem to be relatively conservative insome phylogenetic lineages (Almeida-Santosand Salomao, 2002; Almeida Santos at al.,2006; Marques, 1996; Marques et al., 2006;Pizzatto and Marques, 2007; Pizzatto et al.,2007a, 2008), although in other groups evenclosely related species may differ widely intheir reproductive ecology (e.g., Marques,1996). Despite the efforts to study thereproductive biology of tropical snakes in thelast few decades (e.g., Balestrin and Di-Bernardo, 2005; Marques, 1996; Pizzatto andMarques, 2002; Vitt, 1987), it is still notpossible to recognize patterns in many groups,especially in areas where species diversity ishigh, such as in the Neotropics (but seeAlmeida-Santos and Salomao, 2002).

The subfamily Dipsadinae (Vidal et al.,2000; Zaher, 1999) is composed of small,slender snakes which occur from Mexico tosouthern South America (Ferrarezzi, 1994;Zaher, 1999). The monophyletism of Dipsa-dinae is suggested by both morphological andmolecular data (Cadle, 1984; Vidal et al., 2000;Wallach, 1995; Zaher, 1999), and the subfam-ily is apparently the sister group of all otherxenodontines (Vidal et al., 2000). Two appar-ently monophyletic clades comprise the Dip-sadinae: the tribes Dipsadini, composed ofaglyphous, relatively smaller, earthworm/mol-lusk-eating snakes (e.g., Adelphicos, Atractus,Geophis, Ninia, Tropidodipsas, Sibon, Dipsasand Sibynomorphus), and Leptodeirini, whichis composed of aglyphous or opisthoglyphous,relatively larger, lizard/frog-eating snakes(e.g., Eridiphas, Hypsiglena, Imantodes, Lep-todeira and Pseudoleptodeira (see Cadle,1984; Cadle and Greene, 1993; Ferrarezzi,1994; Martins and Oliveira, 1999; Rodrıguez-Robles et al., 1999; Vidal et al., 2000; Vitt,1996; Zaher, 1999).

As a further attempt to understand theextent to which reproductive characters ofNeotropical snakes are conservative (cf. Al-meida-Santos and Salomao, 2002), we hereexplored the variation in reproductive ecologyin the subfamily Dipsadinae based on originaland literature data. Specifically, our aim is to:(1) conduct an overview of reproductive

characters, such as sexual maturity anddimorphism, body sizes, reproductive cyclesand clutch size in snakes of the tribeDipsadini; and (2) investigate how thosecharacters differ between the tribes Dipsadiniand Leptodeirini.

MATERIALS AND METHODS

Original data on adult Leptodeira annulata(n 5 181), Imantodes cenchoa (n 5 36),Sibynomorphus mikanii (n 5 144), S. neu-wiedi (n 5 126), and S. ventrimaculatus (n 5111) were obtained from specimens deposit-ed in the collections of Instituto Butantan(IB), Museu de Historia Natural da Uni-versidade Estadual de Campinas (ZUEC),Universidade Federal de Santa Maria(ZUFSM), Pontifıcia Universidade Catolicado Rio Grande do Sul (MCP), and Museu deHistoria Natural do Capao da Imbuia(MHNCI). Specimens of L. annulata werecollected in a range of localities between 11u479 N and 23u 359 S, and 39u 439 E and 56u059 W; those of I. cenchoa are from 21u 119 Nto 26u 559 S and 45u 249 E to 52u 069 W; S.mikanii from 20u 169 N to 23u 589 S and 45u429 E to 51u 209 W; S. neuwiedi from 20u 219N to 25u 009 S and 40u 399 E to 49u 429 W;and S. ventrimaculatus from 27u 289 N to 30u529 S and 51u 019 E to 54u 289 W. For eachsnake we collected data on: (1) snout–ventlength (SVL), (2) length of the right testis, (3)diameter of deferent duct, proximal to thecloaca, (4) diameter of the largest ovarianfollicle or oviductal egg, and (5) number ofwell developed follicles in secondary vitello-genesis (.10 mm) and eggs.

Gravid S. mikanii and S. neuwiedi receivedat Instituto Butantan (IB) were kept incaptivity until oviposition. Data on otherspecies of dipsadines were obtained frompublished papers. In these cases we used onlyinformation that confirmed reproductive tim-ing and fecundity in each species. Manypublished sources were not used because theyrepresent only a few, or casual, records thatwere not conclusive or comparable to ourdata. Data on testicular cycles of Hypsiglenatorquata, Leptodeira maculata, L. punctataand Ninia maculata came from histologicalanalyses (Diller and Wallace, 1986; Goldberg,2001, 2004a,b).

June 2008] HERPETOLOGICA 169

Females were considered mature if theyhad follicles in secondary vitellogenesis, ovi-ductal eggs (cf. Shine, 1978) or foldedoviducts (which indicate recent oviposition).Males were considered mature when they hadturgid testes and convoluted deferent ducts(cf. Shine, 1980; Slip and Shine, 1988). Asexual size dimorphism index (SSD) wascalculated according to Shine (1994): meanbody size of the largest sex divided by meanbody size of the smallest sex, minus one. Byconvention, positive values represent femaleslarger than males and negative values repre-sent males larger than females (Shine, 1994).

Size at maturity, represented by the SVL ofthe smallest mature snake in the samples, andrelative tail length were presented as theproportions of the mean body size andanalyzed after transformation to the arcsineof their squared root. All variables were testedfor normality and homoscedasticity prior toanalyses (Zar, 1999).

Sexual dimorphism was investigated interms of mean SVL, proportional size atmaturity (PSM) and relative tail length(RTL). We compared these variables betweensexes, using two-tailed t-Student test (Zar,1999). Sexual dimorphism in tail length wasanalyzed in L. annulata, I. cenchoa andSibynomorphus spp. with ANCOVA, usingtail length as the dependent variable, SVL asthe covariate, and sex as the factor (Zar, 1999).This analysis was not performed for the otherspecies because we did not have access to theraw data sets.

We used the Student’s t-test (Zar, 1999) totest for differences in mean SVL, PSM, RTL,SSD, clutch size, and duration of reproductivecycles between the tribes and RTL betweenhabitat use categories (terrestrial/fossorial andarboreal/semi-arboreal). To test whether SSDwas affected by body size, we used linearregressions, separately for males and females(Zar, 1999). To test whether clutch size isaffected by body size in L. annulata, I.cenchoa and Sibynomorphus spp., we usedlinear regressions. Data were log-transformedas required (Zar, 1999).

Testis length indicates sperm production(cf. Volsøe, 1944), and deferent duct diametercan indicate sperm storage (Almeida-Santos etal., 2006; Sever et al., 2002; Yokoyama and

Yoshida, 1993). Variation in testis length anddiameter of deferent duct (dependent vari-ables) were compared among seasons (factors)using ANCOVA because both variables weresignificantly correlated to snake SVL (covari-ate) (Zar, 1999).

RESULTS

Mean body sizes of adult snakes differedamong species in the dipsadines (Table 1). Allspecies, except I. cenchoa had a mean SVL ,600 mm, and the smallest species was N.maculata (mean SVL 5 226 mm; Table 1).When mean SVL is compared between theDipsadina and the Leptodeirina, neither thoseof females (means 403.6 and 517.6 mm,respectively) nor those of males (means 372.7and 457.8 mm, respectively) were significantlydifferent (t 5 21.50, P 5 0.156; t 5 21.04, P5 0.318; respectively). Males were significantlysmaller than females in all species (L. annulata,t 5 8.09, df 5 179, P , 0.001; S. mikanii, t 59.05, df 5 147, P , 0.001; S. neuwiedi, t 59.25, df 5 125, P , 0.001; S. ventrimaculatus, t5 9.48, df 5 110, P , 0.001; see originalpapers for results for other species), except forI. cenchoa (t 5 0.25, df 5 34, P 5 0.801).

Sexual size dimorphism ranged from 0.009in I. cenchoa to 0.27 in S. ventrimaculatus.The value of SSD was lower than 0.1 in allspecies of Dipsas, in I. cenchoa and in apopulation of L. annulata from the BrazilianAmazon (Table 1). Sexual size dimorphismwas not significantly different between Dipsa-dini and Leptodeirini (means 0.159 and 0.156;t 5 0.06, P 5 0.955). Sexual size dimorphismdecreased with increasing snake size; snakesize explained about one third of the variationin SSD in males (r2 5 0.35, P 5 0.034) andone fifth in females (r2 5 0.18, P , 0.001).Females of most species attained sexualmaturity at 75–85% of mean adult SVL andmales at 70–80% (Table 1), and this intersex-ual difference was not significant (t 5 1.42, P5 0.168). When the proportion of mean adultSVL at which sexes attained sexual maturity iscompared between the Dipsadini and theLeptodeirini, neither females (means 79.3 and77.3%, respectively) nor males (means 77.0and 73.1%) were significantly different (t 50.49, P 5 0.640, t 5 20.70, P 5 0.500;respectively).

170 HERPETOLOGICA [Vol. 64, No. 2

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Relative tail length of male and femalesnakes did not differ significantly betweenDipsadini and Leptodeirini (means 22.6%and 30.0% of body length for females, and27.5% and 35.3% for males; t 5 20.92, P 50.388, and t 5 20.966, P 5 0.371, respectively;Table 2). When all species of Dipsadinae areconsidered together, tails were significantlylonger in arboreal and semi-arboreal speciesthan in fossorial and terrestrial species, both forfemales and males (medians 34.5% and 17.4%of body length for females, and 39.0% and21.8% for males; t 5 24.03, P 5 0.005, and t 524.18, P 5 0.004, respectively; Table 2). Tailswere also significantly longer in males than infemales of L. annulata, I. cenchoa, S. mikanii,S. neuwiedi, and S. ventrimaculatus (AN-COVA, all F . 2.0, all P , 0.025) and in otherdipsadines (Table 2, for statistical analyses, seedata in original papers).

Among the Leptodeirina, in Leptodeiraannulata, follicles in secondary vitellogenesiswere found from late February and March toearly December and oviductal eggs from May

to August (Fig. 1A). In I. cenchoa, vitellogenicfollicles were found in September and eggswere recorded from November to January(Fig. 1B). Among the Dipsadina, seasonalvitellogenesis was recorded for S. mikaniiand S. neuwiedi mostly from July to Decem-ber and eggs were recorded from late Augustto February (Fig. 1C,D). In S. ventrimacula-tus, vitellogenesis was shorter, occurringmostly from October to December, and eggswere recorded from October to February(Fig. 1E). Thus, a seasonal reproductive cycle,with vitellogenesis restricted to the warmerand rainier months of the year, was observedin Sibynomorphus spp. in our analyses, andalso in Atractus reticulatus, Dipsas albifrons(from coastal Atlantic Forest in southernBrazil), H. torquata, L. maculata, L. punctataand Sibon sanniola in literature data (seeFig. 2). In Dipsas catesbyi and D. neivai fromthe coastal Atlantic Forest in northeasternBrazil and in N. maculata from Costa Ricacycles were continuous (Fig. 2). Leptodeiraannulata, Geophis brachycephalus and prob-

TABLE 2.—Tail length (as % of SVL) in males and females, mean clutch size and habitat of dipsadine snakes.

Species Tail length (as % of SVL) Mean clutch size (6SD) Habitat Reference

DipsadiniAtractus reticulatus RR: 11.6%,

==: 15.7%12.7 6 0.8 (1–3, n 5 6) Fossorial Balestrin and

Di-Bernardo, 2005Dipsas albifrons — 3.9 6 1.8 (1–8, n 5 33) Arboreal Hartmann et al., 2002Dipsas catesbyi RR: 36.5%,

==: 39.0%22.0 6 0.82 (1–3, n 5 10) Arboreal Zug et al., 1979

Dipsas catesbyi — 3.63 6 1.66 (1–6, n 5 13) Arboreal Alves et al., 2005Dipsas neivai — 3.91 6 1.95 (1–8, n 5 22) Arboreal Alves et al., 2005Geophys brachycephalus RR: 17.3%, ==: — 4.2 6 1.17 (3–6, n 5 6) Terrestrial-

fossorialSasa, 1993

Ninia maculata — 2.9 6 1.1 (1–5, n 5 14) Semi-fossorial Goldberg, 2004bSibynomorphus mikanii RR: 20.4%,

==: 24.8%15.7 6 1.7 (3–10, n 5 29) Terrestrial This work

Sibynomorphus neuviedi RR: 26.9%,==: 31.1%1

6.4 6 2.4 (4–12, n 5 14) Semi-arboreal This work

Sibynomorphusventrimaculatus

RR: 22.7%,==: 26.8%1

4.8 6 1.0 (3–7, n 5 33) Terrestrial This work

Sibon sanniola — 3.1 6 0.70 (2–5, n 5 28) ? Kofron, 1983LeptodeiriniHypsiglena torquata RR: 15.0%,

==: 20.0%23.2 6 1.5 (1–6, n 5 9) Terrestrial Goldberg, 2001;

Runquist, 2002Imantodes cenchoa — 2.0 6 0.71 (1–3, n 5 5) Arboreal Zug et al., 1979Imantodes cenchoa RR: 45.0%,

==: 47.0%13.3 6 1.70 (1–7, n 5 13) Arboreal This work

Leptodeira annulata ==: 30.0%,==: 39.0%1

7.3 6 2.53 (3–13, n 5 23) Arboreal This work, but seealso Duellman, 1958

Leptodeira maculata — 8.7 6 1.5 (7–11, n 5 7) Arboreal Goldberg, 2004aLeptodeira punctata — 7.8 6 1.7 (6–11, n 5 9) Arboreal Goldberg, 2004a

1 Statistically significant differences.2 No statistical tests performed, but differences are apparent.


ably I. cenchoa had extended cycles (abouteight months; Fig. 2). Duration of vitellogen-esis, occurrence of oviductal eggs or theduration of complete reproductive period(months in which vitellogenesis and/or pres-ence of oviductal eggs occurred) did not differbetween Dipsadina (means 8.4, 7.1 and15.5 mo, respectively) and Leptodeirina (5.8,5.0 and 10.8 mo, respectively; t 5 1.82, P 50.093 for vitellogenesis duration, t 5 1.37, P 50.194 for duration of eggs in oviducts, and t 51.63, P 5 0.127 for the complete cycle).

Clutch size is relatively small in thedipsadines (Table 2) and is not significantlydifferent between the Dipsadini and theLeptodeirini (means 5.3 and 3.9 eggs, respec-tively; t 5 1.47, P 5 0.160). Clutch size wasnot different between terrestrial/fossorialsnakes and arboreal/semiarboreal ones (t 50.45, P 5 0.656). Snout–vent length wassignificantly related to clutch size in S. mikanii(r2 5 0.39, P 5 0.037; Fig. 3A), S. neuwiedi(r2 5 0.63, P 5 0.015; Fig. 3B), S. ventrima-culatus (r2 5 0.59, P , 0.001; Fig. 3C) and I.cenchoa (r2 5 0.68, P 5 0.010; Fig. 3E), butnot in L. annulata (data log-transformed, r2 50.34, P 5 0.101; Fig. 3D). When all speciesare considered together, clutch size seems not

to be a function of female SVL (Fig. 4). WhenI. cenchoa populations and D. neivai (all withlow relative fecundity) are removed from theanalysis the relationship between SVL andclutch size become positive and significant (r2

5 0.33, P 5 0.025, Fig. 4).Testis length and deferent duct diameter

did not differ significantly among seasons in L.annulata and Sibynomorphus spp. (Table 3),which indicates continuous sperm productionand absence of sperm storage by males. Dataon I. cenchoa were not sufficient to compareeither right testis length or deferent ductdiameter among seasons.

Sperm production occurred throughoutthe year in the Dipsadini and in spring-summer in the only species of Leptodeirinistudied. Sperm was found in the deferent ductthroughout the year in all Dipsadini except N.maculata (in which it occurred in spring-autumn), and in spring-summer in bothspecies of Leptodeirini studied (Table 4).

DISCUSSION

In all species of the subfamily Dipsadinaefor which data on size at sexual maturity wereavailable, males and females attained sexual

FIG. 1.—Seasonal variation in the diameter of the largest ovarian follicle (full circles) and oviductal eggs (emptycircles) in Leptodeira annulata, Imantodes cenchroa and Sibynomorphus spp. from Brazil. Triangles represent egg-laying in snakes received gravid at IB. Follicles above dotted line were in secondary vitellogenesis.


maturity at similar relative body sizes. Thedegree of sexual size dimorphism (SSD)decreased with increasing body size in thedipsadines. This pattern is opposite to thatfound in the tribe Xenodontini (Pizzatto et al.,

2008), a clade within the Xenodontinae (Vidalet al., 2000; Zaher, 1999). Males larger thanfemales or absence of sexual dimorphismusually occurs in species in which malesexhibit combat behavior during the mating

FIG. 2.—Reproductive cycles in Dipsadinae snakes. Lines: Vitellogenesis time. Boxes: Oviductal eggs or egg-laying.BRA 5 Brazil, USA 5 United States of America, MEX 5 Mexico, COR 5 Costa Rica. Full lines and boxes 5 observed,dotted lines and boxes 5 inferred.


season (Shine, 1994). The lowest SSD occursin Imantodes cenchoa and this is the onlyspecies in which the largest body size isattained by males and not females. Male-malefighting behavior and mating was recorded inthis species in October (spring) in theBrazilian Amazon (see Santos-Costa andPrudente, 2005) and, an aggregation of threemales and one female in a Peruvian rainforestin May (spring) (Doan and Arriaga, 1999) alsosuggest combat. Male-male ritual combat hasnot been reported in any other dipsadine,xenodontines, nor in the Heterodon-Faranciagroup, the basal lineage of both clades (seeVidal et al., 2000). Thus, either ritual combatremains unnoticed due to elusive habits of thesnakes and suboptimal research efforts or it isan autapomorphy of Imantodes cenchoa with-in this large clade of colubrids.

Sexual dimorphism also occurs in tail lengthin all species in both tribes (Dipsadini: A.reticulatus, Balestrin and Di-Bernardo, 2005;D. albifrons, Hartmann et al., 2002; D.catesbyi, Zug et al., 1979; Sibynomorphusspp., this study; Leptodeirini: H. torquata,Runquist, 2002; I. cenchoa, Zug et al., 1979,this study; L. annulata, Vitt, 1996, this study).A longer tail is expected in males due to thepresence of the hemipenes and their retractormuscles (King, 1989). However, in manyarboreal snakes this dimorphism is absent(Fowler and Salomao, 1994; Pizzatto andMarques, 2007) probably because a long tailmay be advantageous for arboreal life (Lilly-white and Henderson, 1993; Martins et al.,2001). Tail dimorphism occurs in both terres-trial and arboreal dipsadines, but tail isproportionally much longer in arboreal and

FIG. 3.—Relationship between clutch size and female snout–vent length in Leptodeira annulata, Imantodes cenchroaand Sibynomorphus spp. from Brazil.


semi-arboreal species of dipsadines than interrestrial and fossorial species, as observed inother studies (e.g., Hartmann and Marques,2005; Martins et al., 2001; Pizzatto andMarques, 2007; Pizzatto et al., 2007b).

Reproductive cycles vary among snakespecies and also can differ between femalesand males (Seigel and Ford, 1987). Dipsa-dines usually show seasonal reproductivecycles in females, but duration is variableamong species. Some species occurring inareas with a seasonal climate exhibit cyclesrestricted to the warm and rainier seasons, butL. annulata seems to have extended follicularcycles even in areas where climate is seasonal(e.g., southeastern and central Brazil between9u 349 N and 23u 359 S). In contrast, more

seasonal climates seem to restrict the femalecycles in some species, such as D. albifronsand S. ventrimaculatus from southern Brazil.These species show more restricted timing ofvitellogenesis than their congenerics fromlower latitudes.

Testicular cycles are not available for mostspecies of dipsadines; however, our dataindicate that it is variable within this subfam-ily. Hypsiglena torquata from temperate areashas a seasonal sperm production, occurring inthe warmest periods of the year. Despite therecords of seasonal sperm production in manytropical snakes (Fitch, 1982; Shine, 1977),most tropical species of dipsadines showcontinuous testicular activity. Cycles alsodiffered among sexes in the same species.For example, while females of Sibynomorphusspp. have seasonal cycles, males producesperm continuously, indicating that spermproduction is less costly than egg production(Trivers, 1972), at least in tropical snakes.

In general, dipsadine snakes produce smallclutches, probably because of the small size ofthese snakes. Also, the very slender body inarboreal species such as L. annulata and I.cenchoa can strongly reduce body cavity spaceto carry eggs, resulting in smaller clutches (seePizzatto et al., 2007b). Thus, although femalebody size is important in determining clutchsize for some species, other factors mayinfluence this trait (e.g., habitat use, feedinghabits, phylogeny).

Most reproductive characters we analyzedfor the dipsadines seem to be conservativewithin the tribe. The tribes Dipsadini andLeptodeirini did not differ in the amount ofSSD, the proportion of mean SVL at whichsexes attained sexual maturity, relative tail

FIG. 4.—Relationship between mean clutch size andmean female snout–vent length in Dipsadinae snakes.Circles 5 arboreal/semi-arboreal species, triangles 5terrestrial, squares 5 fossorial. Data from: Alves et al.,2005, Balestin and Di-Bernardo, 2005; Goldberg, 2001,2004a,b; Hartmann et al., 2002, Kofron, 1983; Sasa, 1993;Vitt, 1996; Zug et al., 1979; this work.

TABLE 3.—Statistical results of variation in right testis length and diameter of deferent duct among seasons in fourdipsadine snakes from Brazil.

Species Right testis length ANCOVA Deferent duct diameter ANCOVA

DipsadiniSibynomorphus mikanii Slopes: F3,32 5 0.11, P 5 0.954 Insufficient data

Intercept: F3,33 5 2.22, P 5 0.102Sibynomorphus neuwiedi Slopes: F3,25 5 1.01, P 5 0.403 Slopes: F3,22 5 0.20, P 5 0.827

Intercept: F3,26 5 0.96, P 5 0.423 Intercept: F3,23 5 2.58, P 5 0.076Sibynomorphus ventrimaculatus Slopes: F3,22 5 0.95, P 5 0.434 Slopes: F3,21 5 1.48, P 5 0.248

Intercept: F3,23 5 1.07, P 5 0.379 Intercept: F3,22 5 0.08, P 5 0.967LeptodeiriniLeptodeira annulata Slopes: F3,71 5 0.74, P 5 0.530 Slopes F3,69 5 1.86, P 5 0.144

Intercept: F3,72 5 0.80, P 5 0.495 Intercept: F3,70 5 0.49, P 5 0.688


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length of both sexes, duration of vitellogene-sis, egg-carrying period, duration of thecomplete reproductive cycle, and clutch size.However, tribes differ in the timing ofreproductive cycles in females and, apparent-ly, in the duration of sperm production inmales. Thus, reproduction as a whole seems tohave changed relatively little during thehistory of the dipsadines, as already observedin other monophyletic lineages of Neotropicalsnakes, e.g., the genera Bothrops (Almeida-Santos and Salomao, 2002) and Micrurus(Almeida-Santos et al., 2006).

Acknowledgments.—We thank S. Cechin (ZUFSM), M.Di-Bernardo (MCP), F. L. Franco (IB), J. C. Moura Leite(MHNCI) and I. Sazima (ZUEC), for permission toanalyze specimens under their care and Valdir Germano(IB) for help in the laboratory. S. Goldberg helped withliterature, B. Phillips and M. Crossland reviewed the textand made important comments. We also thank twoanonymous referees for helpful comments and sugges-tions. CNPq provided fellowships to MM, OAVM and MCand FAPESP provided fellowships to JLM and LP. Thisstudy was partly funded by FAPESP.

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.Accepted: 15 February 2008

.Associate Editor: Brad Moon


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