Corallus congruence of morphology, trophic ecology, and phylogeny henderson et al (2013 in press) by Luis Alejandro Rodriguez J.

bs_bs_banner

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

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 1

Section of Vertebrate Zoology, Milwaukee Public Museum, 800 W. Wells Street, Milwaukee, WI 53233, USA 2 Biology 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 recent studies have provided an inconclusive picture about the relationship between morphology and trophic ecology in these snakes. To construct a more complete picture, we conducted the first study of morphology and diet to consider all nine species. Using adult specimens from museum collections, we examined several morphometric and meristic variables and their possible relationship to Corallus diets. Broadly, we found three basic morphologies within the genus: 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 in C. annulatus and C. blombergii, which may be indicative of endotherm generalists. These morphological and dietary patterns exhibit a strong degree of congruence with a recent molecular phylogeny of Corallus and highlight a 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 (Colston et al., 2013) of nine currently recognized species distributed from south-eastern Guatemala in northern Central America to southeastern Brazil in South America, on continental and oceanic islands, and at elevations between sea level and about 1000 m above sea level. These moderately sized boids (adult snout– vent length ~1.0–2.0 m) are relatively slender with laterally compressed bodies, thin necks, and large heads featuring long recurved teeth on the anteriormost portions of the maxilla and mandibles. As their common name implies, they are arboreal and occur in forested habitats ranging from arid Acacia scrub to primary rainforest, in mangrove swamps, fruit

*Corresponding author. E-mail: henderson@mpm.edu

orchards, along gallery forests and riparian zones in Brazilian cerrado and caatinga, and urban and suburban situations where they will sometimes seek shelter in human dwellings (Henderson, 2002). Prey is encountered during the night via active and ambush foraging, with some species employing both strategies. Corallus diets are largely comprised of lizards, birds, marsupials, rodents, and/or bats; prey is killed by constriction and, like all snakes, they are gape-limited. Several species undergo ontogenetic shifts in diet (e.g. lizards to rodents), some feed on birds and mammals, and others are stenophagic for mammals as adults (Henderson & Pauers, 2012). Amongst the squamates, snakes are the most trophically specialized group, eating a smaller range of prey taxa compared with the more generalized diets of lizards and amphisbaenians (Gans, 1983). This trophic specialization is manifested in a variety of morphological attributes, including the relative proportions and/or general construction of the head

R. W. HENDERSON ET AL.

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 genus Corallus face a significant morphological constraint due to their arboreal lifestyle, which must be further reconciled with their modes of foraging. One study of interest with regards to morphology and diet in the genus Corallus is that of Pizzatto, Marques & Martins (2007), who examined the morphology, meristics, and habitat usage of several species of South American boine snakes, including three species of Corallus (C. batesii [Gray, 1860], C. cropanii [Hoge, 1954], and C. hortulanus [Linnaeus, 1758]). Their findings indicated that some aspects of the overall 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 known from only a small number of specimens, was considered to be semi-arboreal. Some aspects of the morphology of C. cropanii are consistent with a somewhat more terrestrial habit, given its relatively thicker body and smaller number of subcaudals than its congeners. When diet was considered, however, C. cropanii had much in common with C. batesii; both may be stenophagous for mammals as adults, and both have relatively long heads to accommodate this diet. Corallus hortulanus, conversely, had a very short head, which Pizzatto et al. (2007) believed to be indicative of its generalist diet. Based on these three species, then, these authors present a somewhat equivocal picture of ecomorphology within Corallus. In this study, we strive to assemble a clearer, more refined picture of the relationship between morphology and diet among species of Corallus. Over many years, the senior author and others have examined hundreds of specimens of Corallus, and an extensive amount of morphological, meristic, and trophic data has been accumulated through these efforts. We here take the opportunity to relate these data to a recently generated Corallus phylogeny (Colston et al., 2013) and to address two questions: (1) are differences in morphological and meristic characters associated with trophic differences among species of Corallus, and (2) are morphology, diet, and phylogeny congruent within the genus?

METHODS Specimens of all nine currently recognized species of Corallus were examined from museum collections. To control for ontogenetic changes in both diet and the relative proportions of the body, we restricted our analyses to only those individuals with a snout–vent length (SVL) > 999 mm. We measured head width

(HW) and length (HL, measured from the tip of the snout to the quadrato-articular articulation = jaw length; we consider this the most reliable measure of the trophic appendage), SVL, mid-body circumference (MBC, measured with a string on specimens not obviously distorted by preserving fluid), and tail length (TL). We also counted three traditional meristic characters that had the potential to be important in foraging and predation: number of mid-body dorsal scale rows (DSR), number of ventral scales (VENT), and number of subcaudal scales (SC). Morphometric and meristic data were examined using principal components analysis (PCA). Both types of data were analysed separately, and were factored using the correlation matrix; the morphometric variables (SVL, HW, HL, MBC, and TL) were log10transformed before analysis. This produced two sets of loadings, one each for morphometric and meristic data. To visualize differences in body shape and proportions among species, we plotted morphological PC 2, which should represent shape and not size, versus meristic PC 1. To visualize differences between the two major adult diets, we classified each species as either mammal or mammal and bird consumers and plotted morphological PC 1 versus meristic PC 1. Information on 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 mitochondrial (two genes) and nuclear data (three genes) and all taxonomic relationships were well supported in both Bayesian (posterior probability, PP, > 0.95) and maximum-liklihood (bootstrap value > 80) analyses. Although the authors recognize the paraphyly created due to C. grenadensis and C. cookii being nested within C. hortulanus, no taxonomic analyses addressing their species validity has been performed with molecular data (i.e. using species tree methods or coalescent species delimitation), and given the strong morphological support for their recognition as distinct, herein we consider them as such.

RESULTS DIET Henderson & Pauers (2012) compiled 271 prey records from all nine species based on dissection of field-collected specimens or on field-based observations. These included two frogs (0.7% of total), 69 lizards (mostly Anolis; 25.5%), one snake (a pit-viper; 0.4%), 65 birds (including bananaquits, tanagers, and parrots; 24.0%), and 134 mammals (marsupials, rodents, a carnivore, and bats; 49.4%). Diet and geographical distribution for each species are briefly summarized in Table 1.

MORPHOLOGY, TROPHIC ECOLOGY, AND PHYLOGENY IN TREEBOAS

Table 1. Diet and distribution for species of Corallus Prey sample size

Species

Diet juveniles + subadults → adults

C. annulatus C. batesii C. blombergii C. caninus

Birds, Small Birds, Small

C. cookii C. cropanii C. grenadensis C. hortulanus

Lizards, rodents → rodents Marsupials Lizards, rodents → rodents Birds, bats → birds, marsupials, rodents, bats Birds, mammals → lizards, birds, mammals

C. ruschenbergerii

mammals mammals → marsupials, rodents mammals mammals → marsupials, rodents

Meristic PC 1

Species 0

C. annulatus C. batesii C. blombergii C. caninus C. cookii C. cropanii C. grenadensis C. hortulanus C. ruschenbergerii

-1 -2 -3 -2

-1 0 1 2 Morphological PC 2

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

MORPHOLOGY

AND MERISTICS

Corallus batesii, C. caninus (Linnaeus, 1758), and C. cropanii have relatively longer and wider heads and relatively larger mid-body circumferences than the other species, as well as relatively short tails (although rivalled by C. annulatus [Cope, 1876] and C. blombergii [Rendahl and Vestergren, 1941] in this character). Conversely, the other six species have narrower and shorter heads, and more slender bodies, with C. cookii (Gray, 1842) and C. grenadensis (Barbour, 1914) having the narrowest and shortest heads and C. grenadensis being the most slender member of the genus (Table 2). The PC loadings for the morphometric characters are shown in Table 3. As four of the five morphometric variables load highly and positively onto PC 1,

5 15 3 4 9 1 79 126 27

Distribution Central America, Colombia Amazonia Ecuador Guianas, eastern and southern Venezuela, north-eastern Brazil St. Vincent south-eastern Brazil Grenada Bank Guianas, Amazonia, Atlantic forest Costa Rica, Panama, northern Colombia, northern Venezuela, Trinidad, Tobago, Isla Margarita

interpreting PC 1 as size is reasonable; PC 1 accounts for 67.32% of the variance in the morphometric dataset. PC 2, which accounts for 25.94% of the variance, comprises the body shape component of the 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 this factor. The loadings for the meristic PCA are shown in Table 4. Meristic PC 1 explains 78.00% of the variance, and is highly influenced by all three meristic characters. Ventral (0.953) and subcaudal scales (0.933) both load highly and positively on meristic PC 1, while the number of dorsal scale rows (-0.750) loads strongly and negatively. When plotted against each other, morphological PC 2 and meristic PC 1 create three distinct clusters of species (Fig. 1). The species with longer bodies and tails, and higher numbers of ventral and subcaudal scales (C. cookii, C. grenadensis, C. hortulanus, and C. ruschenbergerii [Cope]), form a distinct cluster in the upper left quadrant of the plot. Species with shorter bodies and tails, and a higher number of dorsal scale rows (C. batesii, C. caninus, and C. cropanii), are clustered in the lower right quadrant. A final cluster consisting of the remaining species, C. annulatus and C. blombergii, is somewhat intermediate in relation to the other two clusters. A plot of morphological PC 1 versus meristic PC 1 illustrates the differences in morphology and size between the two diets (Fig. 2A). In general, mammal specialists differ from those species that eat both mammals and birds with regards to meristic characteristics. Mammal specialists tend to have a higher number of dorsal scale rows, whereas mammal/bird eaters have higher numbers of ventral and subcaudal

C. annulatus C. batesii C. blombergii C. caninus C. cookii C. cropanii C. grenadensis C. hortulanus C. ruschenbergerii

Species

HW 23.50 ± 1.94 (6) 33.28 ± 4.27 (20) 21.40 ± 1.41 (2) 33.21 ± 9.74 (7) 18.97 ± 2.83 (9) 38.47 ± 2.81 (3) 17.97 ± 2.53 (22) 23.02 ± 4.33 (38) 30.06 ± 7.19 (31)

MBC

95.33 ± 16.34 (6) 131.50 ± 24.10 (20) 90.50 ± 0.71 (2) 145.86 ± 22.82 (7) 87.67 ± 10.97 (9) 130.33 ± 23.50 (3) 78.27 ± 12.95 (22) 92.42 ± 20.67 (38) 119.16 ± 27.45 (31)

TL 237.75 ± 35.98 (4) 224.90 ± 32.70 (20) 193.50 ± 10.61 (2) 250.40 ± 35.43 (5) 301.20 ± 37.29 (5) 190.33 ± 5.69 (3) 286.07 ± 31.41 (15) 317.66 ± 34.42 (35) 330.00 ± 53.34 (25)

HL 43.40 ± 5.51 (6) 58.78 ± 7.98 (20) 39.10 ± 0.57 (2) 68.09 ± 10.20 (7) 33.66 ± 2.92 (9) 60.53 ± 3.20 (3) 32.98 ± 3.62 (22) 40.43 ± 5.50 (38) 50.84 ± 9.44 (31)

253.50 ± 2.07 (6) 199.17 ± 6.78 (18) 271.50 ± 0.71 (2) 203.14 ± 5.01 (7) 269.78 ± 3.63 (9) 189.50 ± 14.85 (2) 263.36 ± 2.32 (22) 277.55 ± 8.61 (38) 262.27 ± 5.47 (30)

VENT

1251.17 ± 166.57 (6) 1252.45 ± 175.48 (20) 1198.00 ± 2.83 (2) 1404.71 ± 223.73 (7) 1163.44 ± 70.47 (9) 1199 ± 131.39 (3) 1141.77 ± 104.69 (22) 1265.26 ± 192.59 (38) 1467.23 ± 266.42 (31)

SVL

52.33 ± 1.86 (6) 70.25 ± 3.60 (20) 51.50 ± 0.71 (2) 66.57 ± 2.99 (7) 43.56 ± 3.01 (9) 30.33 ± 1.53 (3) 40.68 ± 1.62 (22) 54.71 ± 2.29 (38) 43.36 ± 2.52 (31)

DSR

-1

Meristic PC 1

84.20 ± 2.68 (5) 70.10 ± 5.32 (20) 79.50 ± 0.71 (2) 75.43 ± 2.76 (7) 115.40 ± 3.29 (5) 52.00 ± 1.00 (3) 109.88 ± 4.41 (16) 117.53 ± 6.49 (34) 105.92 ± 4.14 (24)

Table 2. Morphological and meristic values (mean + SD) for nine species of Corallus; the parenthetical number following the mean is sample size

4 R. W. HENDERSON ET AL.

-3 -2

-2 Gut Contents Mammals Only Mammals and Birds

-1

-2 Species

C. batesii C. cookii C. cropanii C. grenadensis

-1 Morphological PC 1

0 1 2 3

Figure 2. A, plot of morphological PC 1 versus meristic PC 1 in species of Corallus that, as adults, specialize in mammalian prey versus those that take birds and mammals. B, as A, but restricted to those species that predominantly or exclusively take mammals as adults. See text for additional details.

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

DISCUSSION

These results document for the first time the patterns of morphology and their relationship to diet for each member of the genus Corallus. There seem to be three basic morphologies for Corallus species. The first, exhibited by C. cookii, C. grenadensis, C. hortulanus,

MORPHOLOGY, TROPHIC ECOLOGY, AND PHYLOGENY IN TREEBOAS

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

Mid-body circumference Head width Head length Snout–vent length Tail length % variance explained

PC 1

PC 2

PC 3

PC 4

PC 5

0.939 0.934 0.936 0.826 0.229 67.32

0.145 0.232 0.282 -0.483 -0.954 25.94

-0.118 0.224 0.055 -0.228 0.168 2.94

-0.286 0.079 0.075 0.176 -0.091 2.66

0.027 0.134 -0.188 0.042 -0.040 1.15

Table 4. Meristic principal component loadings

Ventral scutes Subcaudal scales Dorsal scale rows % variance explained

PC 1

PC 2

PC 3

0.953 0.933 -0.750 78.00

0.223 0.303 0.661 19.31

0.206 -0.194 0.020 2.69

and C. ruschenbergerii, features a short, narrow head and a long, slender body. While two of these slender species, C. hortulanus and C. ruschenbergerii, were found to prey upon both mammals and birds throughout their lives, C. cookii and C. grenadensis were found to prey upon lizards as juveniles and subadults and almost strictly upon mammals as adults. The second body type comprises a relatively stouter body with a long, wide head. This morphology was found in C. batesii, C. caninus, and C. cropanii, each of which typically feeds on larger mammalian prey. Finally, C. annulatus and C. blombergii have morphologies intermediate to the other two groups, and they may be endotherm generalists. What is perhaps most remarkable about these morphological and, to some extent, dietary patterns, is the degree to which they are congruent with a recent molecular phylogeny of the genus (Colston et al., 2013).

DIET,

MORPHOLOGY, AND MERISTICS

Species of Corallus are nocturnal predators of vertebrates, and all probably exploit both ectothermic and endothermic prey, although predation on ectotherms occurs most frequently as juveniles and subadults. Corallus batesii and C. caninus are the only members of the genus for which we had at least three documented prey items and for which we did not document avian prey. All identified prey items for C. batesii and C. caninus are nocturnal (including the reptiles Thecadactylus rapicauda and Bothrops atrox). This suggests that, unlike other species of Corallus, these two are probably ambush foragers throughout their lives (that is, nocturnally active prey

is more likely to be taken by nocturnal ambushforaging snakes rather than active foragers; Henderson, 2002; Sorrell, 2009); this is supported by available field observations of C. batesii (L.J. Vitt, in litt., 31.x.11; Martins & Oliveira, 1998). If so, that would greatly reduce opportunities for locating sleeping and nestling birds. The low number of ventral scales in C. batesii, C. caninus, and C. cropanii relative to their congenerics also suggests a more sedentary foraging mode, and the girths of C. batesii and C. caninus may preclude efficient active foraging; specifically, they cannot achieve the stealth exhibited by more slender treeboas when actively stalking nocturnally quiescent prey (Yorks et al., 2003; Henderson, Treglia & Powell, 2007). Corallus cropanii remains the most enigmatic member of the genus, largely due to its rarity; only five specimens have been collected since its description nearly 60 years ago. It has obvious shared similarities with C. batesii and C. caninus (MBC, HW, HL, VENT), but even fewer subcaudals than either of those two species and the mean number of dorsal scale rows is less than half the number for C. batesii and C. caninus, and the fewest for any species in the genus. Corallus cropanii might not be as arboreal as other members of the genus (Pizzatto et al., 2007; Machado-Filho et al., 2011), possibly spending substantial time on the ground. The larger heads and greater mid-body circumferences in C. batesii and C. caninus, along with the higher number of dorsal scale rows (characteristic of species that exploit large prey; e.g. Pough & Groves, 1983), all suggest that these two species are capable of capturing, subduing, and ingesting larger and more powerful prey species than other members of the genus. In an ecomorphological analysis of boine snakes that occur in the Neotropics, Madagascar, and Pacific islands (seven genera, 17 species including three species of Corallus), Pizzatto et al. (2007) found that, among South American species, C. batesii had a relative body circumference similar to those of terrestrial (Epicrates spp.) and aquatic (Eunectes spp.) boines; Corallus is the sister group to Epicrates and Eunectes (Burbrink, 2005; Colston et al., 2013). They also found that the mammal specialist C. batesii

R. W. HENDERSON ET AL.

Table 5. Large vs. small species of Corallus Variable

d.f.

Mid-body circumference Error Head width Error Head length Error Snout–vent length Error Tail length Error

0.598 0.909 0.817 0.860 0.750 0.637 0.042 0.508 0.057 0.866

1 112 1 112 1 112 1 112 1 112

0.598 0.008 0.817 0.008 0.750 0.006 0.042 0.005 0.057 0.008

MANOVA, all variables were log10-transformed before analysis (Wilks’ l = 0.395; F5,

had the longest relative head length, whereas vertebrate generalists (C. hortulanus and the anaconda, Eunectes murinus) had proportionately the smallest heads. Corallus hortulanus has the widest geographical range of any species in the genus (about five million km2; 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, and rodents as adults; Henderson, 2002; Pizzatto, Marques & Facure, 2009) of any species in the genus. It is long-tailed and small-headed (relative to C. batesii and C. caninus), with a body circumference greater than the West Indian species but smaller than the mammal specialists. Like C. hortulanus, C. ruschenbergerii is a vertebrate generalist (taking large lizards, birds, marsupials, rodents, carnivores, and bats) and they share similar morphologies, but C. ruschenbergerii is larger (longer SVL, larger body circumference, head width, and head length); C. hortulanus has a greater number of dorsal scale rows. The West Indian C. cookii and C. grenadensis are the two most slender species with the smallest heads, and their juvenile to subadult diets consist largely of Anolis lizards that they locate by active foraging as the lizards sleep on slender branches. They are the only species of Corallus that have diets comprising a high percentage of ectotherms. The morphological transition to a more slender body in C. grenadensis (compared with the closely related C. hortulanus) was not proximally caused by a change in behaviour and, as noted in the boid genus Epicrates which also exhibits a shift in diet from mammals to lizards in some West Indian taxa, behaviour ‘could only influence the maintenance (and subsequent propagation) or suppression of variants already existing in a population’ (Rodríguez-Robles & Greene, 1996). At the age/size classes of the West Indian species that are eating

108

73.706

0.000

106.420

0.000

131.879

0.000

9.343

0.003

7.395

0.008

= 33.318; P ⱕ 0.001).

anoles, the mainland taxa of similar age/size classes are exploiting birds, rodents, marsupials, and bats (Henderson, 2002; Henderson & Pauers, 2012). Although their adult diets largely comprise introduced rodents, we are reluctant to call them mammalian specialists as lizards form such a large percentage of their diets as juveniles and subadults and they are occasionally taken by adults. The reliance of C. cookii and C. grenadensis on lizard prey may be geographically imposed as a consequence of prey availability (Henderson & Pauers, 2012); they occur on islands that are depauperate in mammals but harbour amazingly dense Anolis populations (e.g. Harris et al., 2004). Corallus annulatus and C. blombergii share morphological and meristic similarities with both the vertebrate generalists and the mammal specialists, and they fall between them in Figure 1. They are somewhat heavier-bodied than the generalists, have head lengths similar to C. hortulanus and C. ruschenbergerii, tail lengths and subcaudal numbers closer to the specialists, and mid-body scale row and ventral counts like the generalists. As we have few documented prey records for these two species, assessing the relationship between diet and morphology would be premature.

SIZE,

DIET, AND DISTRIBUTION

The nine species of Corallus exhibit significant differences in head size and mid-body circumference. These traits clearly are implicated in trophic ecology and also demonstrate some geographical trends (Table 5). The large-bodied species (C. batesii and C. caninus and perhaps C. cropanii) have adult diets that are restricted to mammals (marsupials and rodents); C. ruschenbergerii exhibits a broader diet but, like the other three, is capable of subduing and ingesting larger prey items. These four species are allopatric to

MORPHOLOGY, TROPHIC ECOLOGY, AND PHYLOGENY IN TREEBOAS one another, but all are sympatric with one of the more slender species. Corallus hortulanus is broadly sympatric (and probably syntopic) with C. batesii, C. caninus, and C. cropanii, and marginally sympatric with C. ruschenbergerii, which also is sympatric with C. annulatus in portions of their respective ranges (see range maps in Henderson, 2002). Size differences between species that are sympatric/ syntopic and occupy the same adaptive zone should minimize competition for the same or similar trophic resources. Although specialization on Anolis lizards by West Indian Corallus is, based on morphology and behaviour, a true specialization, Henderson & Pauers (2012) suggested that the importance of lizards in their diets was, on the one hand, geographically imposed due to the depauperate mammal faunas of the St. Vincent and Grenada banks, as well as the reduced avian and chiropteran faunas relative to the South American mainland. Alternatively, the spectacular population densities of Anolis lizards on St. Vincent and Grenada may have precluded any necessary reliance on avian or chiropteran prey by subadult West Indian Corallus as compared with the mainland taxa C. hortulanus and, albeit with fewer prey records, C. annulatus and C. ruschenbergerii. Furthermore, most macrostomatan snakes in the West Indies prey on Anolis either throughout their lives or at least while subadults (Henderson & Crother, 1989; Henderson & Powell, 2009).

PHYLOGENY Colston et al.’s (2013) molecular phylogeny of all currently known species of Corallus except C. blombergii allows us to compare morphological and molecular data and relate those data with the trophic ecology (foraging, diet) of species of Corallus. In their phylogeny, there are three distinct evolutionary events with differing ecological and morphological consequences for the members of each clade. In the first, the common ancestor of the C. annulatus – C. ruschenbergerii – C. hortulanus clade diverged from 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 concordance with this divergence in morphology, the dietary niche that originally included large mammalian prey broadened to include avian prey as well. Secondly, the intermediate morph gave rise to the small, narrow-headed and slender-bodied morph exhibited by C. grenadensis and C. cookii. This morphological evolution was accompanied by the third event, a dietary reversion to specialization for mammalian prey in the ancestor of these two taxa. Of great interest is the fact that the morphological and meristic data (Fig. 1) exhibit a remarkable con-

gruence with Colston et al.’s (2013) molecular phylogeny (Fig. 3). The large-headed, heavier-bodied, shorttailed, mammal specialist C. caninus is basal to all other species and is sister to the mammal specialist C. batesii (Vidal et al., 2005; Henderson, Passos & Feitosa, 2009). Corallus cropanii is closely aligned with those two species and Pizzatto et al. (2007), based on two proposed phylogenetic hypotheses (Kluge, 1991; Burbrink, 2005), determined that the common ancestor of boines was stout, short-tailed, and with a moderately long head; that is, in some respects not unlike the most basal species of Corallus. Corallus annulatus and C. blombergi are each other’s closest relative (Henderson et al., 2001). The sister species C. grenadensis and C. cookii are West Indian endemics, lizard and rodent predators, relatively slender-bodied, small-headed, long-tailed, and are sister to euryphagic C. hortulanus. Those three species share morphological and meristic characters with euryphagic C. ruschenbergerii and form a clade that is sister to the latter species. Five species (C. cookii, C. grenadensis, C. hortulanus, C. ruschenbergerii, C. annulatus) exhibit active and ambush foraging behaviour, whereas C. batesii, C. caninus, and, probably, C. cropanii are strictly ambush foragers. It is instructive to contrast the diets of other arboreal boids and pythonids with those of Corallus. The Australasian pythonid Morelia viridis and the Neotropical boid C. caninus are often offered as examples of convergent evolution. In both species juveniles are red or yellow and adults are green with white markings, relatively heavy-bodied, arboreal, perch on branches in a distinctive coil, and are ambush predators. Unlike C. caninus and C. batesii which are stenophagous throughout their lives for mammals, M. viridis exhibits an ontogenetic shift in diet from lizards to mammals, with birds taken infrequently (Wilson, 2007; Natusch & Lyons, 2012). A more germane comparison is with the sister group of Corallus, which includes the genera Epicrates and Eunectes (Burbrink, 2005; Colston et al., 2013). While the available dietary data for both Epicrates and Eunectes are not as extensive as those for Corallus, it is known that the largely ground-dwelling species of Epicrates occurring on the South American mainland are euryphagic, taking frogs, lizards, birds and their eggs, rodents, and bats (Vitt & Vangilder, 1983; Martins & Oliveira, 1998; Starace, 1998; Pizzatto et al., 2009). In the West Indies, juveniles of both large and small species of Epicrates (ten species) show a strong proclivity for Anolis lizards and adults of three species (E. fordii, E. granti, E. gracilis) prey on anoles throughout their lives (Henderson et al., 1987; Chandler & Tolson, 1990; Henderson & Powell, 2009). The anacondas (Eunectes), like mainland

R. W. HENDERSON ET AL. C. grenadensis

C. cookii

C. hortulanus

C. ruschenbergerii

C. annulatus C. cropanii

C. batesii

= C. caninus

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

Epicrates, are euryphagous. They are known to prey on fishes, lizards, snakes, turtles, crocodilians, and wide taxonomic and size ranges of birds (including eggs) and mammals (Strimple, 1993; Strüssmann, 1997; Martins & Oliveira, 1998; Henderson, 2002). Thus, the mainland sister taxa lack trophic specialization, not unlike, for example, C. hortulanus. Conversely, some West Indian Epicrates exhibit a specialization for Anolis lizards that also appears in West Indian Corallus.

ogy, then, seems to minimize potential competition for resources among sympatric species by restricting snakes of a particular morphotype to a particular diet. Further, both diet and morphology can be mapped onto a molecular phylogeny of Corallus, indicating that these ecomorphological patterns are the results of evolutionary diversification within the genus. Our results also highlight the evolutionary insights that a multi-disciplinary approach can provide, even when investigating a relatively small group of closely related species.

SUMMARY While not very diverse, the genus Corallus is broadly distributed throughout much of the Neotropics and congenerics are often found in sympatry. We demonstrate that, despite overlapping geographical distributions, these species exhibit specialized morphologies that are strongly related to diet. Morphol-

ACKNOWLEDGEMENTS We are grateful to Ligia Pizzatto and Laurie Vitt for their generosity in sharing data; their contributions greatly enhanced the amount of information with which we were able to work. Jorge Valencia provided information on foraging behaviour in Corallus blomb-

MORPHOLOGY, TROPHIC ECOLOGY, AND PHYLOGENY IN TREEBOAS ergii, and William Lamar shared observations on C. batesii and C. hortulanus. For comments and suggestions on earlier versions of the manuscript we are grateful to Robert Powell, Paul Hampton, and anonymous reviewers. Recent fieldwork with West Indian Corallus has been generously funded by the Windway Foundation.

REFERENCES Burbrink FT. 2005. Inferring the phylogenetic position of Boa constrictor among the Boinae. Molecular Phylogenetics and Evolution 34: 167–180. Chandler CR, Tolson PJ. 1990. Habitat use by a boid snake, Epicrates monensis, and its anoline prey, Anolis cristatellus. Journal of Herpetology 24: 151–157. Colston TJ, Grazziotin FG, Shepard DB, Vitt LJ, Colli GR, Henderson RW, Hedges SB, Bonatto S, Zaher H, Burbrink FT. 2013. Molecular systematics and historical biogeography of tree boas (genus Corallus spp.). Molecular Phylogenetics and Evolution 66: 953–959. Gans C. 1983. Snake feeding strategies and adaptations – conclusions and prognosis. American Zoologist 23: 455–460. Hampton PM. 2011. Comparison of cranial form and function in association with diet in natricine snakes. Journal of Morphology 272: 1435–1443. Harris BR, Yorks DT, Bohnert CA, Parmerlee Jr. JS, Powell R. 2004. Population densities and structural habitats in lowland populations of Anolis lizards on Grenada. Caribbean Journal of Science 40: 31–40. Henderson RW. 2002. Neotropical treeboas: natural history of the Corallus hortulanus complex. Malabar: Krieger Publishing Co. Henderson RW, Crother BI. 1989. Biogeographic patterns of predation in West Indian colubrid snakes. In: Woods CA, ed. Biogeography of the West Indies: past, present, and future. Gainesville, FL: Sandhill Crane Press, 479– 517. Henderson RW, Höggren M, Lamar WW, Porras L. 2001. Distribution and variation in the treeboa Corallus annulatus (Serpentes: Boidae). Studies on the Neotropical Fauna and Environment 36: 39–47. Henderson RW, Noeske-Hallin TA, Crother BI, Schwartz A. 1988. The diets of Hispaniolan colubrid snakes II. Prey species, prey size, and phylogeny. Herpetologica 44: 55– 70. Henderson RW, Noeske-Hallin TA, Ottenwalder JA, Schwartz A. 1987. On the diet of Epicrates striatus on Hispaniola, with notes on E. fordi and E. gracilis. Amphibia-Reptilia 8: 251–258. Henderson RW, Passos P, Feitosa D. 2009. Geographic variation in the Emerald Treeboa, Corallus caninus (Squamata: Boidae). Copeia 2009: 572–582. Henderson RW, Pauers MJ. 2012. On the diets of Neotropical treeboas (Squamata: Boidae: Corallus). South American Journal of Herpetology 7: 172–180. Henderson RW, Powell R. 2009. Natural history of West

Indian reptiles and amphibians. Gainesville, FL: University Press of Florida. Henderson RW, Treglia ML, Powell SD. 2007. Corallus cookii (St. Vincent Treeboa). Foraging. Herpetological Review 38: 466. Kluge AG. 1991. Boine snake phylogeny and research cycles. Miscellaneous Publications of the Museum of Zoology, University of Michigan 178: 1–58. Machado-Filho PR, Duarte MR, do Carmo LF, Franco FL. 2011. New record of Corallus cropanii (Boidae: Boinae): a rare snake from the Vale do Ribeira, State of São Paulo, Brazil. Salamandra 47: 122–115. Martins M, Marques OAV, Sazima I. 2002. Ecological and phylogenetic correlates of feeding habits in Neotropical pitvipers of the genus Bothrops. In: Schuett GW, Höggren M, Douglas ME, Greene HW, eds. Biology of the vipers. Eagle Mountain, UT: Eagle Mountain Publishing, 307–328. Martins M, Oliveira ME. 1998 [1999]. Natural history of snakes in forests of the Manaus Region, Central Amazonia, Brazil. Herpetological Natural History 6: 78–150. Natusch DJD, Lyons JA. 2012. Relationships between ontogenetic changes in prey selection, head shape, sexual maturity, and colour in an Australian python (Morelia viridis). Biological Journal of the Linnean Society 107: 269–276. Pizzatto L, Marques OAV, Facure K. 2009. Food habits of Brazilian boid snakes: overview and new data, with special reference to Corallus hortulanus. Amphibia-Reptilia 30: 533–544. Pizzatto L, Marques OAV, Martins M. 2007. Ecomorphology of boine snakes, with emphasis on South American forms. In: Henderson RW, Powell R, eds. Biology of the boas and pythons. Eagle Mountain, UT: Eagle Mountain Publishing, 35–48. Pough FH, Groves JD. 1983. Specialization of the body form and food habits of snakes. American Zoologist 23: 443–454. Rodríguez-Robles JA, Greene HW. 1996. Ecological patterns in Greater Antillean macrostomatan snake assemblages, with comments on body-size evolution in Epicrates (Boidae). In: Powell R, Henderson RW, eds. Contributions to West Indian herpetology: a tribute to Albert Schwartz. Ithaca, NY: Contributions to Herpetology Society for the Study of Amphibians and Reptiles, 12: 339–357. Savitzky AH. 1983. Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. American Zoologist 23: 397–409. Sorrell GG. 2009. Diel movement and predation activity patterns of the Eyelash Palm-Pitviper (Bothriechis schlegelii). Copeia 2009: 105–109. Starace F. 1998. Guide des Serpents et Amphisbènes de Guyana. Guadeloupe et Guyana: Ibis Rouge Editions. Strimple PD. 1993. Overview of the natural history of the Green Anaconda (Eunectes murinus). Herpetological Natural History 1: 25–35. Strüssmann C. 1997. Habitos alimentares da sucuriamarela, Eunectes notaeus Cope, 1862, no pantanal matogrossense. Biociencias 5: 35–52.

R. W. HENDERSON ET AL.

Vidal N, Henderson RW, Delmas A-S, Hedges SB. 2005. A phylogeny of the emerald treeboa (Corallus caninus). Journal of Herpetology 39: 500–503. Vincent SE, Herrel A, Irschick DJ. 2004. Sexual dimorphism in head shape and diet in the cottonmouth snake (Agkistrodon piscivorus). Journal of the Zoological Society of London 264: 53–59. Vitt LJ, Vangilder LD. 1983. Ecology of a snake community in northeastern Brazil. Amphibia-Reptilia 4: 273–296. Voris HK, Voris HH. 1983. Feeding strategies in marine snakes: an analysis of evolutionary, morphological,

behavioral and ecological differences. American Zoologist 23: 411–425. Wilson D. 2007. Foraging ecology and diet of an ambush predator: the Green Python (Morelia viridis. In: Henderson RW, Powell R, eds. Biology of the boas and pythons. Eagle Mountain, UT: Eagle Mountain Publishing, 141– 150. Yorks DT, Williamson KE, Henderson RW, Powell R, Parmerlee Jr. JS. 2003. Foraging behavior in the arboreal boid Corallus grenadensis. Studies on the Neotropical Fauna and Environment 38: 167–172.