Corallus congruence of morphology, trophic ecology, and phylogeny henderson et al (2013 in press)

On the congruence of morphology, trophic ecology,and phylogeny in Neotropical treeboas (Squamata:Boidae: Corallus)

ROBERT W. HENDERSON1*, MICHAEL J. PAUERS1 and TIMOTHY J. COLSTON2

1Section of Vertebrate Zoology, Milwaukee Public Museum, 800 W. Wells Street, Milwaukee, WI53233, USA2Biology Department, University of Mississippi, PO Box 1848, MS 38677, USA

Received 21 November 2012; revised 19 December 2012; accepted for publication 19 December 2012

Nine members of the Neotropical treeboa genus Corallus occur from Guatemala to south-eastern Brazil and recentstudies have provided an inconclusive picture about the relationship between morphology and trophic ecology inthese snakes. To construct a more complete picture, we conducted the first study of morphology and diet to considerall nine species. Using adult specimens from museum collections, we examined several morphometric and meristicvariables and their possible relationship to Corallus diets. Broadly, we found three basic morphologies within thegenus: a short, narrow head and a slender body (C. cookii, C. grenadensis, C. hortulanus, and C. ruschenbergerii),useful for exploiting a wide variety of prey; a relatively stout body with a long, wide head (C. batesii, C. caninus,and C. cropanii) associated with feeding on larger mammalian prey; and an intermediate morphology, found inC. annulatus and C. blombergii, which may be indicative of endotherm generalists. These morphological anddietary patterns exhibit a strong degree of congruence with a recent molecular phylogeny of Corallus and highlighta heretofore unexamined ecological diversification within Corallus. © 2013 The Linnean Society of London,Biological Journal of the Linnean Society, 2013, ••, ••–••.

ADDITIONAL KEYWORDS: Amazonia – diets – ecomorphology – meristics – snakes – West Indies.

INTRODUCTION

The Neotropical treeboa genus Corallus (Squamata:Boidae: Boinae) is a monophyletic group (Colstonet al., 2013) of nine currently recognized species dis-tributed from south-eastern Guatemala in northernCentral America to southeastern Brazil in SouthAmerica, on continental and oceanic islands, and atelevations between sea level and about 1000 m abovesea level. These moderately sized boids (adult snout–vent length ~1.0–2.0 m) are relatively slender withlaterally compressed bodies, thin necks, and largeheads featuring long recurved teeth on the anterior-most portions of the maxilla and mandibles. As theircommon name implies, they are arboreal and occurin forested habitats ranging from arid Acacia scrubto primary rainforest, in mangrove swamps, fruit

orchards, along gallery forests and riparian zones inBrazilian cerrado and caatinga, and urban and sub-urban situations where they will sometimes seekshelter in human dwellings (Henderson, 2002). Preyis encountered during the night via active andambush foraging, with some species employing bothstrategies. Corallus diets are largely comprised oflizards, birds, marsupials, rodents, and/or bats; preyis killed by constriction and, like all snakes, they aregape-limited. Several species undergo ontogeneticshifts in diet (e.g. lizards to rodents), some feed onbirds and mammals, and others are stenophagic formammals as adults (Henderson & Pauers, 2012).

Amongst the squamates, snakes are the mosttrophically specialized group, eating a smaller rangeof prey taxa compared with the more generalizeddiets of lizards and amphisbaenians (Gans, 1983).This trophic specialization is manifested in a varietyof morphological attributes, including the relativeproportions and/or general construction of the head*Corresponding author. E-mail: [email protected]

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Biological Journal of the Linnean Society, 2013, ••, ••–••. With 3 figures

© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, ••, ••–•• 1

and body, as well as overall body shape (e.g. Savitzky,1983; Voris & Voris, 1983; Henderson et al., 1988;Martins, Marques & Sazima, 2002; Vincent, Herrel &Irschick, 2004; Hampton, 2011). Snakes of the genusCorallus face a significant morphological constraintdue to their arboreal lifestyle, which must be furtherreconciled with their modes of foraging.

One study of interest with regards to morphologyand diet in the genus Corallus is that of Pizzatto,Marques & Martins (2007), who examined the mor-phology, meristics, and habitat usage of several speciesof South American boine snakes, including threespecies of Corallus (C. batesii [Gray, 1860], C. cropanii[Hoge, 1954], and C. hortulanus [Linnaeus, 1758]).Their findings indicated that some aspects of theoverall morphology of C. batesii and C. hortulanus,such as tail length and the number of subcaudal scales,were probably related to their use of arboreal habitats.Corallus cropanii, on the other hand, which is knownfrom only a small number of specimens, was consid-ered to be semi-arboreal. Some aspects of the morphol-ogy of C. cropanii are consistent with a somewhat moreterrestrial habit, given its relatively thicker body andsmaller number of subcaudals than its congeners.When diet was considered, however, C. cropanii hadmuch in common with C. batesii; both may be sten-ophagous for mammals as adults, and both haverelatively long heads to accommodate this diet. Coral-lus hortulanus, conversely, had a very short head,which Pizzatto et al. (2007) believed to be indicative ofits generalist diet. Based on these three species, then,these authors present a somewhat equivocal picture ofecomorphology within Corallus.

In this study, we strive to assemble a clearer, morerefined picture of the relationship between morphol-ogy and diet among species of Corallus. Over manyyears, the senior author and others have examinedhundreds of specimens of Corallus, and an extensiveamount of morphological, meristic, and trophic datahas been accumulated through these efforts. We heretake the opportunity to relate these data to a recentlygenerated Corallus phylogeny (Colston et al., 2013)and to address two questions: (1) are differences inmorphological and meristic characters associatedwith trophic differences among species of Corallus,and (2) are morphology, diet, and phylogeny congru-ent within the genus?

METHODS

Specimens of all nine currently recognized species ofCorallus were examined from museum collections. Tocontrol for ontogenetic changes in both diet and therelative proportions of the body, we restricted ouranalyses to only those individuals with a snout–ventlength (SVL) > 999 mm. We measured head width

(HW) and length (HL, measured from the tip of thesnout to the quadrato-articular articulation = jawlength; we consider this the most reliable measure ofthe trophic appendage), SVL, mid-body circumference(MBC, measured with a string on specimens not obvi-ously distorted by preserving fluid), and tail length(TL). We also counted three traditional meristic char-acters that had the potential to be important inforaging and predation: number of mid-body dorsalscale rows (DSR), number of ventral scales (VENT),and number of subcaudal scales (SC).

Morphometric and meristic data were examinedusing principal components analysis (PCA). Both typesof data were analysed separately, and were factoredusing the correlation matrix; the morphometric vari-ables (SVL, HW, HL, MBC, and TL) were log10-transformed before analysis. This produced two sets ofloadings, one each for morphometric and meristic data.To visualize differences in body shape and proportionsamong species, we plotted morphological PC 2, whichshould represent shape and not size, versus meristicPC 1. To visualize differences between the two majoradult diets, we classified each species as eithermammal or mammal and bird consumers and plottedmorphological PC 1 versus meristic PC 1. Informationon Corallus diets is from Henderson & Pauers (2012).

We used the phylogeny produced by Colston et al.(2013) for evolutionary relationships among Corallus.The phylogeny reported is based on both mitochon-drial (two genes) and nuclear data (three genes) andall taxonomic relationships were well supported inboth Bayesian (posterior probability, PP, > 0.95) andmaximum-liklihood (bootstrap value > 80) analyses.Although the authors recognize the paraphyly createddue to C. grenadensis and C. cookii being nestedwithin C. hortulanus, no taxonomic analyses address-ing their species validity has been performed withmolecular data (i.e. using species tree methods orcoalescent species delimitation), and given the strongmorphological support for their recognition as dis-tinct, herein we consider them as such.

RESULTSDIET

Henderson & Pauers (2012) compiled 271 preyrecords from all nine species based on dissection offield-collected specimens or on field-based observa-tions. These included two frogs (0.7% of total), 69lizards (mostly Anolis; 25.5%), one snake (a pit-viper;0.4%), 65 birds (including bananaquits, tanagers, andparrots; 24.0%), and 134 mammals (marsupials,rodents, a carnivore, and bats; 49.4%). Diet and geo-graphical distribution for each species are brieflysummarized in Table 1.

2 R. W. HENDERSON ET AL.

© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, ••, ••–••

MORPHOLOGY AND MERISTICS

Corallus batesii, C. caninus (Linnaeus, 1758), andC. cropanii have relatively longer and wider headsand relatively larger mid-body circumferences thanthe other species, as well as relatively short tails(although rivalled by C. annulatus [Cope, 1876] andC. blombergii [Rendahl and Vestergren, 1941] in thischaracter). Conversely, the other six species havenarrower and shorter heads, and more slender bodies,with C. cookii (Gray, 1842) and C. grenadensis(Barbour, 1914) having the narrowest and shortestheads and C. grenadensis being the most slendermember of the genus (Table 2).

The PC loadings for the morphometric charactersare shown in Table 3. As four of the five morphomet-ric variables load highly and positively onto PC 1,

interpreting PC 1 as size is reasonable; PC 1accounts for 67.32% of the variance in the morpho-metric dataset. PC 2, which accounts for 25.94% ofthe variance, comprises the body shape component ofthe dataset. Log-transformed tail length (-0.954)loads highly and negatively on PC 2, while snout–vent length (-0.483) is a moderate contributor to thisfactor. The loadings for the meristic PCA are shownin Table 4. Meristic PC 1 explains 78.00% of the vari-ance, and is highly influenced by all three meristiccharacters. Ventral (0.953) and subcaudal scales(0.933) both load highly and positively on meristicPC 1, while the number of dorsal scale rows (-0.750)loads strongly and negatively.

When plotted against each other, morphologicalPC 2 and meristic PC 1 create three distinct clustersof species (Fig. 1). The species with longer bodies andtails, and higher numbers of ventral and subcaudalscales (C. cookii, C. grenadensis, C. hortulanus, andC. ruschenbergerii [Cope]), form a distinct cluster inthe upper left quadrant of the plot. Species withshorter bodies and tails, and a higher number ofdorsal scale rows (C. batesii, C. caninus, and C. cro-panii), are clustered in the lower right quadrant. Afinal cluster consisting of the remaining species,C. annulatus and C. blombergii, is somewhat inter-mediate in relation to the other two clusters.

A plot of morphological PC 1 versus meristic PC 1illustrates the differences in morphology and sizebetween the two diets (Fig. 2A). In general, mammalspecialists differ from those species that eat bothmammals and birds with regards to meristic charac-teristics. Mammal specialists tend to have a highernumber of dorsal scale rows, whereas mammal/birdeaters have higher numbers of ventral and subcaudal

Table 1. Diet and distribution for species of Corallus

SpeciesDietjuveniles + subadults → adults

Preysamplesize Distribution

C. annulatus Birds, mammals 5 Central America, ColombiaC. batesii Small mammals → marsupials, rodents 15 AmazoniaC. blombergii Birds, mammals 3 EcuadorC. caninus Small mammals → marsupials, rodents 4 Guianas, eastern and southern

Venezuela, north-eastern BrazilC. cookii Lizards, rodents → rodents 9 St. VincentC. cropanii Marsupials 1 south-eastern BrazilC. grenadensis Lizards, rodents → rodents 79 Grenada BankC. hortulanus Birds, bats → birds, marsupials, rodents,

bats126 Guianas, Amazonia, Atlantic forest

C. ruschenbergerii Birds, mammals → lizards, birds,mammals

27 Costa Rica, Panama, northern Colombia,northern Venezuela, Trinidad, Tobago,Isla Margarita

-2 -1 0 1 2 3-3

-2

-1

0

1

2

Morphological PC 2

Mer

istic

PC

1 SpeciesC. annulatusC. batesiiC. blombergiiC. caninusC. cookiiC. cropaniiC. grenadensisC. hortulanusC. ruschenbergerii

Figure 1. Plot of morphological PC 2 and meristic PC 1 inspecies of Corallus; see text for details.

MORPHOLOGY, TROPHIC ECOLOGY, AND PHYLOGENY IN TREEBOAS 3


scales; individuals with both diets tend to have asimilar range of body size, as indicated by theirsimilar distributions along the morphological axis.Interestingly, a small grouping of mammal predatorsis clustered within the mammal/bird eaters (Fig. 2A).These individuals, while meristically similar to themammal/bird eaters, tend to be smaller than both thetypical mammal/bird eaters and the mammal special-ists. As a way to identify the species present in thiscluster, we replotted these data, using only themammal specialists; these smaller but meristicallydistinct mammalian predators are adult C. cookii andC. grenadensis (Fig. 2B).

DISCUSSION

These results document for the first time the patternsof morphology and their relationship to diet for eachmember of the genus Corallus. There seem to be threebasic morphologies for Corallus species. The first,exhibited by C. cookii, C. grenadensis, C. hortulanus,T

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1

Gut Contents

Species

Mammals Only

Mammals and Birds

C. batesiiC. cookiiC. cropaniiC. grenadensis

A

B

Figure 2. A, plot of morphological PC 1 versus meristicPC 1 in species of Corallus that, as adults, specialize inmammalian prey versus those that take birds andmammals. B, as A, but restricted to those species thatpredominantly or exclusively take mammals as adults. Seetext for additional details.



and C. ruschenbergerii, features a short, narrow headand a long, slender body. While two of these slenderspecies, C. hortulanus and C. ruschenbergerii, werefound to prey upon both mammals and birds through-out their lives, C. cookii and C. grenadensis werefound to prey upon lizards as juveniles and subadultsand almost strictly upon mammals as adults. Thesecond body type comprises a relatively stouter bodywith a long, wide head. This morphology was found inC. batesii, C. caninus, and C. cropanii, each of whichtypically feeds on larger mammalian prey. Finally,C. annulatus and C. blombergii have morphologiesintermediate to the other two groups, and they maybe endotherm generalists. What is perhaps mostremarkable about these morphological and, to someextent, dietary patterns, is the degree to which theyare congruent with a recent molecular phylogeny ofthe genus (Colston et al., 2013).

DIET, MORPHOLOGY, AND MERISTICS

Species of Corallus are nocturnal predators of verte-brates, and all probably exploit both ectothermic andendothermic prey, although predation on ectothermsoccurs most frequently as juveniles and subadults.Corallus batesii and C. caninus are the only membersof the genus for which we had at least three docu-mented prey items and for which we did not docu-ment avian prey. All identified prey items forC. batesii and C. caninus are nocturnal (including thereptiles Thecadactylus rapicauda and Bothropsatrox). This suggests that, unlike other species ofCorallus, these two are probably ambush foragersthroughout their lives (that is, nocturnally active prey

is more likely to be taken by nocturnal ambush-foraging snakes rather than active foragers;Henderson, 2002; Sorrell, 2009); this is supported byavailable field observations of C. batesii (L.J. Vitt, inlitt., 31.x.11; Martins & Oliveira, 1998). If so, thatwould greatly reduce opportunities for locating sleep-ing and nestling birds. The low number of ventralscales in C. batesii, C. caninus, and C. cropanii rela-tive to their congenerics also suggests a more seden-tary foraging mode, and the girths of C. batesii andC. caninus may preclude efficient active foraging; spe-cifically, they cannot achieve the stealth exhibited bymore slender treeboas when actively stalking noctur-nally quiescent prey (Yorks et al., 2003; Henderson,Treglia & Powell, 2007). Corallus cropanii remainsthe most enigmatic member of the genus, largely dueto its rarity; only five specimens have been collectedsince its description nearly 60 years ago. It hasobvious shared similarities with C. batesii andC. caninus (MBC, HW, HL, VENT), but even fewersubcaudals than either of those two species and themean number of dorsal scale rows is less than half thenumber for C. batesii and C. caninus, and the fewestfor any species in the genus. Corallus cropanii mightnot be as arboreal as other members of the genus(Pizzatto et al., 2007; Machado-Filho et al., 2011), pos-sibly spending substantial time on the ground.

The larger heads and greater mid-body circumfer-ences in C. batesii and C. caninus, along with thehigher number of dorsal scale rows (characteristic ofspecies that exploit large prey; e.g. Pough & Groves,1983), all suggest that these two species are capableof capturing, subduing, and ingesting larger and morepowerful prey species than other members of thegenus. In an ecomorphological analysis of boinesnakes that occur in the Neotropics, Madagascar, andPacific islands (seven genera, 17 species includingthree species of Corallus), Pizzatto et al. (2007) foundthat, among South American species, C. batesii had arelative body circumference similar to those of terres-trial (Epicrates spp.) and aquatic (Eunectes spp.)boines; Corallus is the sister group to Epicrates andEunectes (Burbrink, 2005; Colston et al., 2013). Theyalso found that the mammal specialist C. batesii

Table 3. Morphometric principal component loadings; all variables were log10-transformed before analysis

PC 1 PC 2 PC 3 PC 4 PC 5

Mid-body circumference 0.939 0.145 -0.118 -0.286 0.027Head width 0.934 0.232 0.224 0.079 0.134Head length 0.936 0.282 0.055 0.075 -0.188Snout–vent length 0.826 -0.483 -0.228 0.176 0.042Tail length 0.229 -0.954 0.168 -0.091 -0.040% variance explained 67.32 25.94 2.94 2.66 1.15

Table 4. Meristic principal component loadings

PC 1 PC 2 PC 3

Ventral scutes 0.953 0.223 0.206Subcaudal scales 0.933 0.303 -0.194Dorsal scale rows -0.750 0.661 0.020% variance explained 78.00 19.31 2.69



had the longest relative head length, whereas verte-brate generalists (C. hortulanus and the anaconda,Eunectes murinus) had proportionately the smallestheads.

Corallus hortulanus has the widest geographicalrange of any species in the genus (about five millionkm2; in contrast, the range of C. grenadensis is< 400 km2) and, throughout the course of its life,exhibits the most euryphagic diet (frogs, lizards,birds, and bats as juveniles; birds, marsupials, androdents as adults; Henderson, 2002; Pizzatto,Marques & Facure, 2009) of any species in the genus.It is long-tailed and small-headed (relative to C. ba-tesii and C. caninus), with a body circumferencegreater than the West Indian species but smallerthan the mammal specialists. Like C. hortulanus,C. ruschenbergerii is a vertebrate generalist (takinglarge lizards, birds, marsupials, rodents, carnivores,and bats) and they share similar morphologies, butC. ruschenbergerii is larger (longer SVL, larger bodycircumference, head width, and head length); C. hor-tulanus has a greater number of dorsal scale rows.

The West Indian C. cookii and C. grenadensis arethe two most slender species with the smallest heads,and their juvenile to subadult diets consist largely ofAnolis lizards that they locate by active foraging asthe lizards sleep on slender branches. They are theonly species of Corallus that have diets comprising ahigh percentage of ectotherms. The morphologicaltransition to a more slender body in C. grenadensis(compared with the closely related C. hortulanus) wasnot proximally caused by a change in behaviour and,as noted in the boid genus Epicrates which also exhib-its a shift in diet from mammals to lizards in someWest Indian taxa, behaviour ‘could only influence themaintenance (and subsequent propagation) or sup-pression of variants already existing in a population’(Rodríguez-Robles & Greene, 1996). At the age/sizeclasses of the West Indian species that are eating

anoles, the mainland taxa of similar age/size classesare exploiting birds, rodents, marsupials, and bats(Henderson, 2002; Henderson & Pauers, 2012).Although their adult diets largely comprise intro-duced rodents, we are reluctant to call them mam-malian specialists as lizards form such a largepercentage of their diets as juveniles and subadultsand they are occasionally taken by adults. The reli-ance of C. cookii and C. grenadensis on lizard preymay be geographically imposed as a consequence ofprey availability (Henderson & Pauers, 2012); theyoccur on islands that are depauperate in mammalsbut harbour amazingly dense Anolis populations (e.g.Harris et al., 2004).

Corallus annulatus and C. blombergii share mor-phological and meristic similarities with both thevertebrate generalists and the mammal specialists,and they fall between them in Figure 1. They aresomewhat heavier-bodied than the generalists, havehead lengths similar to C. hortulanus and C. ruschen-bergerii, tail lengths and subcaudal numbers closer tothe specialists, and mid-body scale row and ventralcounts like the generalists. As we have few docu-mented prey records for these two species, assessingthe relationship between diet and morphology wouldbe premature.

SIZE, DIET, AND DISTRIBUTION

The nine species of Corallus exhibit significant differ-ences in head size and mid-body circumference. Thesetraits clearly are implicated in trophic ecology andalso demonstrate some geographical trends (Table 5).The large-bodied species (C. batesii and C. caninusand perhaps C. cropanii) have adult diets that arerestricted to mammals (marsupials and rodents); C.ruschenbergerii exhibits a broader diet but, like theother three, is capable of subduing and ingestinglarger prey items. These four species are allopatric to

Table 5. Large vs. small species of Corallus

Variable SS d.f. MS F P

Mid-body circumference 0.598 1 0.598 73.706 0.000Error 0.909 112 0.008Head width 0.817 1 0.817 106.420 0.000Error 0.860 112 0.008Head length 0.750 1 0.750 131.879 0.000Error 0.637 112 0.006Snout–vent length 0.042 1 0.042 9.343 0.003Error 0.508 112 0.005Tail length 0.057 1 0.057 7.395 0.008Error 0.866 112 0.008

MANOVA, all variables were log10-transformed before analysis (Wilks’ l = 0.395; F5, 108 = 33.318; P � 0.001).



one another, but all are sympatric with one of themore slender species. Corallus hortulanus is broadlysympatric (and probably syntopic) with C. batesii,C. caninus, and C. cropanii, and marginally sympat-ric with C. ruschenbergerii, which also is sympatricwith C. annulatus in portions of their respectiveranges (see range maps in Henderson, 2002). Sizedifferences between species that are sympatric/syntopic and occupy the same adaptive zone shouldminimize competition for the same or similar trophicresources.

Although specialization on Anolis lizards by WestIndian Corallus is, based on morphology and behav-iour, a true specialization, Henderson & Pauers(2012) suggested that the importance of lizards intheir diets was, on the one hand, geographicallyimposed due to the depauperate mammal faunas ofthe St. Vincent and Grenada banks, as well as thereduced avian and chiropteran faunas relative to theSouth American mainland. Alternatively, the spec-tacular population densities of Anolis lizards on St.Vincent and Grenada may have precluded any neces-sary reliance on avian or chiropteran prey by sub-adult West Indian Corallus as compared with themainland taxa C. hortulanus and, albeit with fewerprey records, C. annulatus and C. ruschenbergerii.Furthermore, most macrostomatan snakes in theWest Indies prey on Anolis either throughout theirlives or at least while subadults (Henderson &Crother, 1989; Henderson & Powell, 2009).

PHYLOGENY

Colston et al.’s (2013) molecular phylogeny of all cur-rently known species of Corallus except C. blombergiiallows us to compare morphological and moleculardata and relate those data with the trophic ecology(foraging, diet) of species of Corallus. In their phyl-ogeny, there are three distinct evolutionary eventswith differing ecological and morphological conse-quences for the members of each clade. In the first,the common ancestor of the C. annulatus –C. ruschenbergerii – C. hortulanus clade divergedfrom the stout-bodied, long- and wide-headed morph(a morphology still found in C. batesii, C. caninus,and C. cropanii) into the intermediate morph. In con-cordance with this divergence in morphology, thedietary niche that originally included large mamma-lian prey broadened to include avian prey as well.Secondly, the intermediate morph gave rise to thesmall, narrow-headed and slender-bodied morphexhibited by C. grenadensis and C. cookii. This mor-phological evolution was accompanied by the thirdevent, a dietary reversion to specialization for mam-malian prey in the ancestor of these two taxa.

Of great interest is the fact that the morphologicaland meristic data (Fig. 1) exhibit a remarkable con-

gruence with Colston et al.’s (2013) molecular phylog-eny (Fig. 3). The large-headed, heavier-bodied, short-tailed, mammal specialist C. caninus is basal to allother species and is sister to the mammal specialistC. batesii (Vidal et al., 2005; Henderson, Passos &Feitosa, 2009). Corallus cropanii is closely alignedwith those two species and Pizzatto et al. (2007),based on two proposed phylogenetic hypotheses(Kluge, 1991; Burbrink, 2005), determined that thecommon ancestor of boines was stout, short-tailed,and with a moderately long head; that is, in somerespects not unlike the most basal species of Corallus.Corallus annulatus and C. blombergi are each other’sclosest relative (Henderson et al., 2001). The sisterspecies C. grenadensis and C. cookii are West Indianendemics, lizard and rodent predators, relativelyslender-bodied, small-headed, long-tailed, and aresister to euryphagic C. hortulanus. Those threespecies share morphological and meristic characterswith euryphagic C. ruschenbergerii and form a cladethat is sister to the latter species. Five species(C. cookii, C. grenadensis, C. hortulanus, C. ruschen-bergerii, C. annulatus) exhibit active and ambushforaging behaviour, whereas C. batesii, C. caninus,and, probably, C. cropanii are strictly ambushforagers.

It is instructive to contrast the diets of other arbo-real boids and pythonids with those of Corallus. TheAustralasian pythonid Morelia viridis and the Neo-tropical boid C. caninus are often offered as examplesof convergent evolution. In both species juveniles arered or yellow and adults are green with white mark-ings, relatively heavy-bodied, arboreal, perch onbranches in a distinctive coil, and are ambush preda-tors. Unlike C. caninus and C. batesii which are sten-ophagous throughout their lives for mammals,M. viridis exhibits an ontogenetic shift in diet fromlizards to mammals, with birds taken infrequently(Wilson, 2007; Natusch & Lyons, 2012). A moregermane comparison is with the sister group ofCorallus, which includes the genera Epicratesand Eunectes (Burbrink, 2005; Colston et al., 2013).While the available dietary data for both Epicratesand Eunectes are not as extensive as those for Cor-allus, it is known that the largely ground-dwellingspecies of Epicrates occurring on the South Americanmainland are euryphagic, taking frogs, lizards, birdsand their eggs, rodents, and bats (Vitt & Vangilder,1983; Martins & Oliveira, 1998; Starace, 1998;Pizzatto et al., 2009). In the West Indies, juveniles ofboth large and small species of Epicrates (ten species)show a strong proclivity for Anolis lizards and adultsof three species (E. fordii, E. granti, E. gracilis) preyon anoles throughout their lives (Henderson et al.,1987; Chandler & Tolson, 1990; Henderson & Powell,2009). The anacondas (Eunectes), like mainland



Epicrates, are euryphagous. They are known to preyon fishes, lizards, snakes, turtles, crocodilians, andwide taxonomic and size ranges of birds (includingeggs) and mammals (Strimple, 1993; Strüssmann,1997; Martins & Oliveira, 1998; Henderson, 2002).Thus, the mainland sister taxa lack trophic speciali-zation, not unlike, for example, C. hortulanus. Con-versely, some West Indian Epicrates exhibit aspecialization for Anolis lizards that also appears inWest Indian Corallus.

SUMMARY

While not very diverse, the genus Corallus is broadlydistributed throughout much of the Neotropicsand congenerics are often found in sympatry. Wedemonstrate that, despite overlapping geographicaldistributions, these species exhibit specialized mor-phologies that are strongly related to diet. Morphol-

ogy, then, seems to minimize potential competition forresources among sympatric species by restrictingsnakes of a particular morphotype to a particulardiet. Further, both diet and morphology can bemapped onto a molecular phylogeny of Corallus, indi-cating that these ecomorphological patterns are theresults of evolutionary diversification within thegenus. Our results also highlight the evolutionaryinsights that a multi-disciplinary approach canprovide, even when investigating a relatively smallgroup of closely related species.

ACKNOWLEDGEMENTS

We are grateful to Ligia Pizzatto and Laurie Vitt fortheir generosity in sharing data; their contributionsgreatly enhanced the amount of information withwhich we were able to work. Jorge Valencia providedinformation on foraging behaviour in Corallus blomb-

C. batesii

C. annulatus

C. cropanii

C. grenadensis

C. cookii

C. hortulanus

C. caninus

C. ruschenbergerii

+

+

=

=

=

=?

Figure 3. Phylogenetic tree based on molecular evidence (mitochondrial and nuclear loci) for species of Corallus (basedon Colston et al., 2013) and predominant prey groups for each species.



ergii, and William Lamar shared observations onC. batesii and C. hortulanus. For comments and sug-gestions on earlier versions of the manuscript we aregrateful to Robert Powell, Paul Hampton, and anony-mous reviewers. Recent fieldwork with West IndianCorallus has been generously funded by the WindwayFoundation.

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