This art icle was downloaded by: [ J.D. Daza] On: 07 Decem ber 2012, At : 03: 51 Publisher: Taylor & Francis I nform a Lt d Regist ered in England and Wales Regist ered Num ber: 1072954 Regist ered office: Mort im er House, 37- 41 Mort im er St reet , London W1T 3JH, UK Journal of Natural History Publicat ion det ails, including inst ruct ions f or aut hors and subscript ion inf ormat ion: ht t p: / / www. t andf online. com/ loi/ t nah20 Six species of Amazonian Woodcreepers (Aves: Dendrocolaptidae) preying upon lizards and frogs V. M. S. Kupriyanov , G. R. Rocha-Brit o a d , J. D. Daza b & E. Höf ling , A. M. Bauer b , R. Gaban-Lima c a a Depart ament o de Zoologia, Inst it ut o de Biociências, Universidade de São Paulo, São Paulo, Brazil b Villanova Universit y, Depart ment of Biology, Villanova, PA, USA c Inst it ut o de Ciências Biológicas e da Saúde and Museu de Hist ória Nat ural, Universidade Federal de Alagoas, Alagoas, Brazil d Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil To cite this article: V. M. S. Kupriyanov , J. D. Daza , A. M. Bauer , R. Gaban-Lima , G. R. Rocha-Brit o & E. Höf ling (2012): Six species of Amazonian Woodcreepers (Aves: Dendrocolapt idae) preying upon lizards and f rogs, Journal of Nat ural Hist ory, 46: 47-48, 2985-2997 To link to this article: ht t p: / / dx. doi. org/ 10. 1080/ 00222933. 2012. 717646 PLEASE SCROLL DOWN FOR ARTI CLE Full t erm s and condit ions of use: ht t p: / / www.t andfonline.com / page/ t erm s- andcondit ions This art icle m ay be used for research, t eaching, and privat e st udy purposes. Any subst ant ial or syst em at ic reproduct ion, redist ribut ion, reselling, loan, sub- licensing, syst em at ic supply, or dist ribut ion in any form t o anyone is expressly forbidden. The publisher does not give any warrant y express or im plied or m ake any represent at ion t hat t he cont ent s will be com plet e or accurat e or up t o dat e. The accuracy of any inst ruct ions, form ulae, and drug doses should be independent ly verified wit h prim ary sources. The publisher shall not be liable for any loss, act ions, claim s, proceedings, dem and, or cost s or dam ages what soever or howsoever caused arising direct ly or indirect ly in connect ion wit h or arising out of t he use of t his m at erial. Journal of Natural History Vol. 46, Nos. 47–48, December 2012, 2985–2997 Six species of Amazonian Woodcreepers (Aves: Dendrocolaptidae) preying upon lizards and frogs Viviane M.S. Kupriyanova , Juan D. Dazab* , Aaron M. Bauerb , Renato Gaban-Limac , Guilherme R. Rocha-Britod and Elizabeth Höflinga a Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil; b Villanova University, Department of Biology, Villanova, PA, USA; c Instituto de Ciências Biológicas e da Saúde and Museu de História Natural, Universidade Federal de Alagoas, Alagoas, Brazil; d Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil Downloaded by [J.D. Daza] at 03:51 07 December 2012 (Received 3 March 2012; final version received 30 July 2012; printed 6 December 2012) Dietary data from a large sample of woodcreepers (16 spp., n = 139), revealed that six species of dendrocolaptids occasionally feed upon lizards and frogs. These birds, which are mainly insectivorous, encounter and feed on lizards while perching on tree trunks, probably in association with army-ant swarm feeding behaviour. Frog intake may be related to declines in the abundance of invertebrate prey. The bones recovered were identified as one small species of gecko, Gonatodes humeralis, and at least one anuran. We estimate that in the entire sample, about eight lizards and two frogs were ingested. The partially digested gecko material allows determination of which bones are more resistant to digestion, although it is possible that these elements were differentially retained in the stomach. These elements correspond to the more frequently preserved bones in the fossil record of geckos, indicating that the same portions of the skeleton persist under the processes of both digestion and fossilization. Keywords: insectivorous birds; lizard; frog; stomach contents; Amazon Basin Introduction Woodcreepers are passerine birds that have the conspicuous habit of climbing trees; however, they occasionally descend, chiefly to enter nesting or roosting cavities, or when foraging in association with ant swarms. Only a few species, particularly those frequenting open areas, regularly forage on the ground (Marantz et al. 2003). In the Amazon, these birds feed mainly on small arthropods, especially crickets and beetles (Chapman and Rosenberg 1991; Macedo-Mestre 2002). Strong-billed species are capable of feeding on hard-backed beetles and small vertebrates such as frogs and lizards (Feduccia 1973). In the Amazon, vertebrate predation by Neotropical passerines is poorly documented (Chapman and Rosenberg 1991; Lopes et al. 2005), although predation of frogs and lizards has been documented for more than 50% of insectivorous birds dwelling in the Panamanian understorey (Poulin et al. 2001). There are only a few reports of insectivorous birds from the Amazon Basin consuming lizards and frogs (Chapman and Rosenberg 1991; Macedo-Mestre 2002). However, these studies provide little detail and prey are identified only by their common name, corresponding to higher taxonomic levels (i.e. Order or Suborder). Here we *Corresponding author. Email: juand.daza@gmail.com ISSN 0022-2933 print/ISSN 1464-5262 online © 2012 Taylor & Francis http://dx.doi.org/10.1080/00222933.2012.717646 http://www.tandfonline.com Downloaded by [J.D. Daza] at 03:51 07 December 2012 2986 V.M.S. Kupriyanov et al. Figure 1. Sampling localities along the margin of the rivers Tapajós and Teles Pires. See Table 2 for complete information. report the details of predation upon lizards and frogs by six species of dendrocolaptids sampled in six localities in the Brazilian Amazon Basin along the rivers Tapajós and Teles Pires (Figure 1). The relatively large number of bones recovered allows us to quantify the number of prey ingested and to provide a more precise identification using comparative material from known species of amphibians and reptiles from this region. We were able to determine these skeletal elements to the species level in the case of lizards, and since these were more numerous, we were also able to determine which bones were more resistant to digestion and to draw parallels with differential preservation of bony elements under conditions of fossilization. Methods A large sample (n = 139) of stomach (proventriculus and gizzard) contents of 16 species of woodcreepers was examined (Table 1). All stomach samples were obtained by field expeditions to different regions of the Amazon Basin (Figure 1) and deposited in the collections of the Museu Nacional do Rio de Janeiro-UFRJ (MNRJMNA), the Museu de Zoologia, Universidade de São Paulo (MZUSP) and the Museu Paraense Emílio Goeldi (MPEG), all in Brazil. Bird specimens were fixed in 4% formalin and transferred to 70% ethanol approximately 20 days later. Stomachs were removed and placed in separate jars, also containing 70% ethanol. Samples were examined with the aid of a stereomicroscope (Nikon SMZ 800). The skeletal material was washed in water and any muscle remains Journal of Natural History 2987 Table 1. Total number of bird stomachs sampled indicating the number of animals that were found to be either saurophagous (lizard eating) or anurophagous (frog eating). Downloaded by [J.D. Daza] at 03:51 07 December 2012 Species Campylorhamphus procurvoides Deconychura longicauda Deconychura stictolaema Dendrocincla fuliginosa Dendrocincla merula Dendrocolaptes certhia Dendrocolaptes hoffmannsii Glyphorhynchus spirurus Lepidocolaptes albolineatus Sittasomus griseicapillus Xiphocolaptes promeropirhynchus Xiphorhynchus elegans Xiphorhynchus guttatus Xiphorhynchus obsoletus Xiphorhynchus picus Xiphorhynchus spixii Total n Number of saurophagous birds Number of anurophagous birds 1 4 2 20 12 8 1 50 2 1 3 6 15 1 3 10 139 – – 1 3 1 – – – – – – 1 – – – – 6 – – – – – – – – – – 1 – 1 – – – 2 were removed manually. The dried osteological specimens were photographed with a ® Sony Cyber-shot DSC-W300, with multiple shots taken at different focal planes and combined into a single image with CombineZ 5.3 (Hadley 2006). To identify the vertebrate prey we considered the adult size and morphological characters of the herpetological groups occurring in the areas sampled and compared these with the specimens recovered. As we could not discount predation on juveniles, we also considered the degree of ossification of the material recovered to distinguish the remains of juveniles of larger prey species from those of similar-sized adults of smaller species. The skeletal material was compared with museum specimens and literature descriptions of species distributed in the sampled areas. For some specimens digital radiographs were obtained using a KevexTM PXS10-16W X-ray source and ® Varian Amorphous Silicon Digital X-RayDetector PaxScanH 4030 set to 130 kV at 81 mA. Museum abbreviations used: AMNH, American Museum of Natural History (New York, NY, USA); JFBM, James Ford Bell Museum, University of Minnesota (Saint Paul, MN, USA); MPEG, Museu Paraense Emílio Goeldi (Belém, Brazil); MNRJ/MNA, Museu Nacional, Universidade Federal do Rio de Janeiro, Museu Nacional Anatômica (Rio de Janeiro, Brazil); MZUSP, Museu de Zoologia, Universidade de São Paulo (São Paulo, Brazil); NHMUK, The Natural History Museum (London, UK); RT, Richard Thomas, personal collection (San Juan, Puerto Rico); USNM, United States National Museum of Natural History (Washington DC, USA). Material used for comparison. Sk, skeletonized specimen; C&S, cleared and stained; XR, digital X-ray. Sphaerodactylidae: Chatogekko amazonicus (C&S = USNM 200664, USNM 288764, USNM 289031, XR = USNM 200661, USNM 2988 V.M.S. Kupriyanov et al. 288763); Coleodactylus brachystoma (C&S = MZUSP no data); Gonatodes humeralis (C&S = RT 01198, XR = USNM 94980); Lepidoblepharis heyerorum (XR = USNM 217635). Phyllodactylidae: Thecadactylus rapicauda (Sk = AMNH R-59722, AMNH R-75824, AMNH R-85312, NHMUK 59.9.6). Gekkonidae: Lygodactylus gutturalis (C&S = AMNH R-10294, AMNH R-10297, AMNH R-10333); Lygodactylus picturatus (Sk = JFBM 15818 ); Hemidactylus mabouia (Sk = AMNH R-102426, C&S = RT 13861–13863). We used two species of Lygodactylus from Africa in lieu of the morphologically similar American endemic Lygodactylus klugei because of the lack of osteological preparations of this species in the collections reviewed. Downloaded by [J.D. Daza] at 03:51 07 December 2012 Results In the animals sampled, only four stomachs were found empty. The most common prey categories were Coleoptera (13.8%), Araneae (13.0%), Orthoptera (12.1%), Hymenoptera (10.5%) and Isoptera (10.5%), the bulk of the remaining diet comprised other arthropods and occasionally vertebrates (Kupriyanov et al. 2011). Of the species of woodcreepers sampled, 12.5% were found to prey on frogs (Xiphocolaptes promeropirhynchus, Xiphorhynchus guttatus), whereas 25% preyed on geckos (Dendrocincla fuliginosa, Dendrocincla merula, Deconychura stictolaema, Xiphorhynchus elegans). From the entire sample of stomachs we recovered the bones of at least eight lizards and two frogs (Table 2). Based on their similar size and morphology, we identified all lizard bones as belonging to a single species of gecko. The identification to the Gekkota is based on the presence of marginal bones with isodont dentition and blunt crowns, tubular frontals fused dorsally and ventrally, and dentary bones with a fused Meckelian canal. Seven species of geckos from three different families have been recorded in the States of Pará, Rondônia and Mato Grosso: Sphaerodactylidae: Chatogekko amazonicus, Coleodactylus brachystoma, Gonatodes humeralis, Lepidoblepharis heyerorum; Gekkonidae: Lygodactylus wetzli, Hemidactylus mabouia; Phyllodactylidae: Thecadactylus rapicauda (Nascimento et al. 1987; Ávila-Pires 1995; Uetanabaro et al. 2007; Gamble et al. 2008, Silva et al. 2009; Ávila-Pires et al. 2010; Gamble, Bauer et al. 2011; Santos et al. 2011; Silva et al. 2011). The digested material corresponds to Gonatodes humeralis (Figure 2). The identification of the skeletal material is based on characters that define the New World clade Sphaerodactylini, including postcranial characters such as the pubic portion of the innominate bone with a large and ventrally directed pectineal process (Noble 1921; Daza and Bauer 2012), and cranial characters such as a very long dentary bone that overlaps the surangular and the compound bone laterally, and surangular and compound bone partially fused and forming an external mandibular fenestra (Daza et al. 2008; Gamble, Daza et al. 2011). Gonatodes humeralis can be differentiated from the other sphaerodactyls from the area (i.e. Chatogekko amazonicus, Coleodactylus brachystoma and Lepidoblepharis heyerorum) by its larger adult size (41 mm snout–vent length versus a maximum of 34 mm in the other species; Ávila-Pires 1995; Vitt et al. 1997), maxilla with a wider facial process (instead of very narrow) and a postorbitofrontal with more angular lateral margin including a small ventrolateral process (instead of having a rounded lateral margin as in other sphaerodactyls). The number of frog species in the area is about five times the number of geckos (Sociedade Brasileira de Herpetologia 2012). We cannot meaningfully identify these Downloaded by [J.D. Daza] at 03:51 07 December 2012 Table 2. Predator, prey and the bones recovered from each animal ingested. Predator Prey Sample Gonatodes humeralis (n = 1) MPEG 64098 Dendrocincla fuliginosa Gonatodes humeralis (n = 1) MZUSP 87611 Dendrocincla fuliginosa Gonatodes humeralis (n = 2) MZUSP 87617 Dendrocincla merula Gonatodes humeralis (n = 1) MZUSP 87625 maxilla (L1), pterygoid (R1), postorbitofrontal (L1, Fig. 2C), dentary (R1, L1, Fig. 2F), compound bone (R1), humerus (R1, L1), femur (R1), tibia (R1, L1, Fig. 2M), ulna (?, Fig. 2J), radius (?, Fig. 2K) maxilla (L1), prefrontal (L1, Fig. 2B), postorbitofrontal (L1), frontal, pterygoid (R1, Fig. 2E), dentary (R1, L1), humerus (R1), ulna (?), radius (?). maxilla (R2, L1), frontal, dentary (R2, L2), compound bone + surangular (R2, L1, Fig. 2G), humerus (R1, L1, Fig. 2I), femur (R2, L1). maxilla (R1, L1, Fig. 2A), frontal (Fig. 2D), dentary (L1), compound bone + surangular (R1, L1), innominate bone, pelvis (R1, L1, Fig. 2H), humerus (R1, L1), femur (L1, Fig. 2L) Locality and collection dates Key to lettered localities (see Figure 1) State of Pará, left margin of river Arapiuns, Santarém city, Comunidade São Francisco (2◦ 32′ 9.60" S, 55◦ 19′ 19.16" W) A State of Pará, right margin of river Teles Pires, Jacareacanga town, (9◦ 13′ 34" S, 56◦ 59′ 54" W) 24 February 2009 C State of Mato Grosso, left margin of river Teles Pires, Paranaíta town (9◦ 19′ 04" S, 56◦ 46′ 53" W) 30 September 2008 State of Mato Grosso, left margin of river Teles Pires, Paranaíta town (9◦ 19′ 18" S, 56◦ 46′ 55" W) 2 December 2009 E F (Continued) Journal of Natural History 2989 Dendrocincla fuliginosa Bones recovered Downloaded by [J.D. Daza] at 03:51 07 December 2012 Table 2. (Continued). Prey Sample Bones recovered Deconychura stictolaema Gonatodes humeralis (n = 1) MNRJ/MNA 4431 ulna (?) Xiphorhynchus elegans Gonatodes humeralis (n = 2) MZUSP 87663 maxilla (L1), dentary + compound bone fragment (R1), humerus (R1, L1), femur (R2, L1), radius (?). Xiphorhynchus guttatus Anura (indeterminate) (n = 1) MZUSP 87657 radio-ulna, illium, indeterminate element. Xiphocolaptes promeropirhynchus Hylidae (n = 1) MPEG 64127 premaxilla (Fig. 3A), maxilla (L1, Fig. 3B), frontoparietal (Fig. 3C), dentary (R1, L1, Figs. 3D, 3E), indeterminate cranial elements? (Figs. 3F, 3G, 3H, 3I), presacral vertebrae (Figs. 3J–3Q), atlas (Fig. 3J), sacrum (Fig. 3Q), scapula (Fig. 3R), radio-ulna (Fig. 3S), illium (R1, Fig. 3T), femur (R2, L1, Fig. 3U), indeterminate postcranial bones (Fig. 3V). Locality and collection dates State of Pará, right margin of river Teles Pires, Jacareacanga town (9◦ 13′ 34" S, 56◦ 59′ 54" W) 24 February 2009 State of Mato Grosso, left margin of river Teles Pires, Paranaíta town (9◦ 19′ 18" S, 56◦ 46′ 55" W) 30 September 2009 State of Pará, right margin of river Teles Pires, Jacareacanga town (9◦ 13′ 40" S, 56◦ 59′ 48" W) 24 February 2009 State of Pará, left margin of river Tapajós, Igarapé Aricoré, Escrivão, Aveiro town (3◦ 25′ 22.80" S, 55◦ 21′ 18.00" W) 11 December 2007 Key to lettered localities (see Figure 1) C G D B L and R indicate left and right, respectively, number after letters indicate the number of bones recovered. The number of prey is the minimum number estimated, as different bones might belong to different prey specimens. 2990 V.M.S. Kupriyanov et al. Predator Downloaded by [J.D. Daza] at 03:51 07 December 2012 Journal of Natural History 2991 Figure 2. Sample of gecko bones (Gonatodes humeralis) recovered in the stomach contents of dendrocolaptid birds. (A) Right maxilla; (B) left prefrontal; (C) left postorbitofrontal; (D) frontal; (E) right pterygoid; (F) left dentary; (G) right compound bone + surangular; (H) left and right innominate bone (pelvis); (I) left humerus; (J) ulna; (K) radius; (L) left femur; (M) left tibia. B, C, E, F, G, I, J, K, M recovered from Dendrocincla fuliginosa, A, D, H, L recovered from Dendrocincla merula. Scale bar 10 mm. remains to the level of species, but we observed seven diagnostic characters in the most complete specimen (Figure 3) and tentatively identify it as a member of the Family Hylidae, this lowers the number of candidate species to about 15. The characters observed are: eight presacral vertebrae, presacral vertebrae I and II not fused, Downloaded by [J.D. Daza] at 03:51 07 December 2012 2992 V.M.S. Kupriyanov et al. Figure 3. Frog bones (Hylidae?) recovered in the stomach contents of dendrocolaptid bird Xiphocolaptes promeropirhynchus. (A) Premaxilla; (B) maxilla; (C) frontoparietal; (D, E) dentaries; (F–I) indeterminate cranial elements; (J–Q) presacral vertebrae; (J) atlas; (Q) sacrum; (R) scapula; (S) radio-ulna; (T) illium; (U) femur; (V) indeterminate postcranial bones. Scale bar 10 mm. cervical cotyles of atlas widely separated, sacrum with dilated diapophyses, bicondylar articulation with urostyle, teeth present in both premaxilla and maxilla, frontoparietal co-ossified as indicated by substantial ornamentation (Trueb 1970; Gaudin 1974; Holman 2003; Jared et al. 2005). The gecko material recovered allows us to determine which bones persist during the digestive process. Of the 52 bones recovered, representing at least eight individuals, 17.3% were humeri, 13.4% dentaries and maxillae, 11.5% each were compound bones and femora. The rest of the bones recovered were less well represented (Figure 4). Discussion Woodcreepers feed primarily on insects that browse on tree trunks. Predation on vertebrates such as lizards (Anolis, Ameiva) by insectivorous birds has been generally regarded to be opportunistic, especially in the ant-follower families – e.g. Cuculidae, Dendrocolaptidae, Formicariidae, Thraupidae (Willis and Oniki 1978; Chapman and Rosenberg 1991; Chesser 1995; Poulin et al. 2001), and lizard predation has not been Downloaded by [J.D. Daza] at 03:51 07 December 2012 Journal of Natural History 2993 Figure 4. Above, digital X-ray of Gonatodes humeralis (USNM 568677) indicating the bones from the gecko skeleton that are more resistant to digestion. Below, histogram indicating the total number and percentage of bones recovered from at least eight geckos preyed upon by six birds. Scale bar 10 mm. observed outside this context (Willis 1967, 1972a, b, 1973). Predation on small vertebrates may also be related to the reproductive season and the availability of arthropods, for example Poulin et al. (2001) suggest that the low intake of lizards during avian nesting activities might be influenced by a decrease in foraging at army-ant swarms during that period. So, lizard intake is opportunistic, but based more on frequency of encounter, related to ant swarm feeding, than on lizard availability per se. The same authors indicate that predation on frogs is also opportunistic, especially when invertebrates are less abundant. The bird species recorded as predators of lizards and frogs in this study have variable foraging behaviours. Dendrocincla woodcreepers are known as specialized followers of army-ant swarms throughout much of Amazonia (Willis 1972). The remaining species join mixed-species flocks in the understorey and sub-canopy and are relatively sporadic at army-ant swarms (Munn 1985; Marantz et al. 2003). The two larger woodcreeper species that fed on vertebrates (Xiphorhynchus guttatus and Xiphocolaptes promeropyrrhynchus) have relatively larger bills and are known to forage principally while climbing trunks and vines, picking items from the surface or even probing into the wood or other substrates such as bromeliads and lichen (Pierpont 1983; Marantz et al. 2003). Bill morphology and foraging behaviour may increase the possibilities in finding small vertebrates, such as nocturnal anurans, while they are inactive. Downloaded by [J.D. Daza] at 03:51 07 December 2012 2994 V.M.S. Kupriyanov et al. The generally low frequency of lizards and frogs registered in the diets of these birds supports the opportunistic vertebrate predator hypothesis. For example, specialized army-ant followers, especially Dendrocincla fuliginosa, which forms dominant hierarchies near the swarms, perch on tree trunks to wait for swarms. This species has been reported as a predator of the scansorial lizard Anolis limifrons in Panama (Poulin et al. 2001). Similarly in the Amazon Basin, it is possible that Dendrocincla spp. preys on G. humeralis as consequence of both predator and prey occurring together in the same microhabitat (i.e., tree-trunks), which correlates with the scansorial habits typical of this family of birds, and this gekkotan clade. Gonatodes humeralis is a climbing gecko (Vitt et al. 1997, 2000), differing ecologically from larger congeners, such as G. hasemani, which use lower perches such as fallen logs (Vitt et al. 2000). Gonatodes have more prominent exposed claws (Rivero-Blanco 1979; Leal et al. 2010) than other Sphaerodactylini such as Chatogekko amazonicus, Coleodactylus brachystoma and Lepidoblepharis heyerorum in which claws are covered by a sheath of scales, a character developed to different degrees in species dwelling in the leaf litter (Parker 1926; Vanzolini 1957; Kluge 1995; Gamble, Daza et al. 2011). This difference in digital morphology seems to characterize climbers versus leaf-litter dwellers among sphaerodactyls and ungual sheaths may assist the latter when moving across leaf surfaces (Vitt et al. 2005). Gonatodes humeralis has been hypothesized to use arboreal habitats to avoid predation from terrestrial lizard-eating snakes like Drymoluber dichrous (Vitt et al. 2000). Alternatively, it has been argued that this species selects trees with large trunks because these have deeper leaf litter at the base which acts as a refuge against predation (Miranda et al. 2010), despite the fact that this species is found in the diets of many leaf litter lizards and snakes (e.g. Ameiva ameiva, Drymoluber, Bothrops, Clelia, Mastigodryas and Bothriopsis; Dixon and Soini 1975; Martins 1991; Ávila-Pires 1995). Our results are not consistent with the hypothesis of Vitt et al. (2000) that tree trunks are used as shelter from terrestrial predators. Although the cryptic coloration of G. humeralis, especially in females and juveniles, renders individuals almost invisible on trunks and limbs of trees (Ávila-Pires 1995; Vitt et al. 1997), its microhabitat preference obviously exposes it to avian predators. Gonatodes humeralis predation by birds has not been reported before. The absolute size of comparable bones of the prey (e.g. maxillae, femora) indicates that the frogs consumed are larger than the geckos. Geckos were probably swallowed whole, because their bodies are slender and more elongated than that of frogs; the larger beaks of Xiphocolaptes promeropirhynchus and Xiphorhynchus guttatus undoubtedly confer upon these birds the capability of handling and disarticulating larger prey, or eating small frogs in one piece; this capability increases the range of food items that can be consumed. According to Poulin et al. (2001) birds with long bills (as observed in the two species in question) were more likely to feed on frogs, an observation supported by the strong correlations between morphological variables such as bill length and size of vertebrate prey in other insectivorous birds. Furthermore, there is a single report where a small frog identified to species (Hyla myotympanum) was consumed by Xiphocolaptes promeropirhynchus (Marantz et al. 2003). Geckos are lightly built and relatively paedomorphic lizards; this is probably the reason why their skeletons are rarely preserved in the fossil record (Evans 2003). With the material recovered from this study, we were able to evaluate the relative persistence of different portions of the skeleton in the woodcreepers’ stomachs. There is a Journal of Natural History 2995 strong parallel between the bones recovered most commonly in the bird stomachs (i.e. maxillae, dentaries, compound bones and frontals; Figure 4, Table 2) and the most frequently recovered bones in 22 species of Cenozoic fossil gekkotans (i.e. maxillae, dentaries and frontals; Hoffstetter 1946; Rage 1978; Estes 1983; Hutchinson 1997; Albino 2005; Augé 2005). This suggests that the gekkotan skeleton responds similarly to different decay process (i.e. digestion and fossilization), favouring the idea that bone resistance to digestion or decomposition as opposed to differential retention accounts for the particular elements recovered from the stomachs of woodcreepers. Downloaded by [J.D. Daza] at 03:51 07 December 2012 Acknowledgements We thank R. Montero, L. Allcock, and an anonymous reviewer for their comments that improved this manuscript. L. Ponssa (Instituto de Herpetología, FML) for her help identifying the frog bones. We also thank the following curators for access to material under their care: R. Thomas (personal collection) K. de Queiroz (USNM), D. Frost and D. Kizirian (AMNH), C. McCarthy (NHMUK), K. Kozak (JFBM), L.F. Silveira (MZUSP), M. Raposo (MNRJ), and A. Aleixo (MPEG). S. Raredon and K. Tighe (USNM) kindly assisted us obtaining the X-rays. JDD and AMB were supported by the Lemole Endowed Chair funds and National Science Foundation grant DEB 0844523. VK was benefited from research fellowship from Capes. GRRB was supported by Capes/Faperj PAPD post-doctoral fellowship, and E.H. from CNPq grant. References Albino A. 2005. A Late Quaternary lizard assemblage from the southern Pampean region of Argentina. J Vert Pal. 25(1):185–191. Augé ML. 2005. Évolution des lézards du Paléogène en Europe. Mém Mus Natl Hist Nat. 192:1–369. Ávila-Pires TCS. 1995. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zool Verh. 299(20):1–706. Ávila-Pires TCS, Hoogmoed MS, Rocha WA. 2010. Notes on the vertebrates of northern Pará, Brazil: a forgotten part of the Guianan Region, I. Herpetofauna. Bol Mus Paraense Emílio Goeldi, Ser Ciênc Nat. 5(1):13–112. Chapman A, Rosenberg KV. 1991. Diets of four sympatric Amazonian woodcreepers (Dendrocolaptidae). Condor 93(4):904–915. Chesser RT. 1995. Comparative diets of obligate ant-following birds at a site in Northern Bolivia. Biotropica 27(3):382–390. Daza JD, Abdala V, Thomas R, Bauer AM. 2008. Skull anatomy of the miniaturized gecko Sphaerodactylus roosevelti (Squamata: Gekkota). J Morphol. 239(11):1340–1364. Daza JD, Bauer AM. 2012. A new amber-embedded sphaerodactyl gecko from Hispaniola, with comments on the morphological synapomorphies of the Sphaerodactylidae. Breviora 529:1–28. Dixon JR, Soini P. 1975. The reptiles of the upper Amazon Basin, Iquitos region, Peru. Milwaukee Pub Mus Contrib Biol Geol. 4(12):1–58. Estes R. 1983. Handbuch der Paläoherpetologie. 10A. Sauria terrestria, Amphisbaenia. Stuttgart: Gustav Fischer Verlag. 249 pp. Evans SE. 2003. At the feet of the dinosaurs: the early history and radiation of lizards. Biol Rev. 78(4):513–551. Feduccia A. 1973. Evolutionary trends in the Neotropical ovenbirds and woodhewers. Ornithol Monogr. 13(1973): iv + 1–69. Downloaded by [J.D. Daza] at 03:51 07 December 2012 2996 V.M.S. Kupriyanov et al. Gaudin AJ. 1974. An osteological analysis of Holarctic tree frogs, family Hylidae. J Herpetol. 8(2):141–152. Gamble T, Bauer AM, Colli GR, Greenbaum E, Jackman TR, Vitt LJ, Simons AM. 2011. Coming to America: multiple origins of the New World geckos. J Evol Biol. 24(2):231–244. Gamble T, Daza JD, Colli GR, Vitt LJ, Bauer AM. 2011. A new genus of miniaturized and pug-nosed gecko from South America (Sphaerodactylidae: Gekkota). Zool J Linn Soc. 163(4):1244–1266. Gamble T, Simons AM, Colli GR, Vitt LJ. 2008. Tertiary climate change and the diversification of the Amazonian gecko genus Gonatodes (Sphaerodactylidae, Squamata). Mol Phyl Evol. 46(1):269–277. Hadley A. 2006. CombineZ5.3 Program and documentation. [Accessed 20 June 2012]. Available from: http://www.hadleyweb.pwp.blueyonder.co.uk. Holman JA. 2003. Fossil frogs and toads of North America. Bloomington (IN): Indiana University Press. xiii + 246 pp. Hoffstetter R. 1946. Sur les Gekkonidae fossils. Bull Mus Natl Hist Nat. 18:195–203. Hutchinson MN. 1997. The first fossil pygopod (Squamata, Gekkota), and a review of mandibular variation in living species. Mem Queensland Mus. 41(2):355–366. Jared C, Antoniazzi MM, Navas CA, Katchburian E, Freymüller E, Tambourgi DV, Rodrigues MT. 2005. Head co-ossification, phragmosis and defence in the casque-headed tree frog Corythomantis greening. J Zool (London). 265(1):1–8. Kluge AG. 1995. Cladistic relationships of sphaerodactyl lizards. Am Mus Novit. 3139:1–23. Kupriyanov VMS, Gaban-Lima R, Alvarenga H, Höfling E. 2011. Analysis of the stomach content of woodcreepers (Passeriformes: Dendrocolaptidae) collected in the Brazilian Amazonian region. Book of abstracts, 11th Congress of Neotropical Ornithology. 2011 Nov 8–14; Cusco, Peru. The Neotropical Ornithological Society - Unión de Ornitólogos del Perú, Cusco. p. 375. Leal F, Tarazona OA, Ramírez-Pinilla MP. 2010. Limb development in the gekkonid lizard Gonatodes albogularis: a reconsideration of homology in the lizard carpus and tarsus. J Morphol. 271(11):1328–1341. Lopes LE, Fernandes AM, Marini MA. 2005. Predation on vertebrates by Neotropical passerine birds. Lundiana 6(1):57–66. Macedo-Mestre LA. 2002. Dieta de aves insetívoras terrestres e a disponibilidade de presas em fragmentos florestais amazônicos [MSc dissertation]. [São Carlos, Brazil], Universidade Federal de São Carlos. Marantz CA, Aleixo A, Bevier LR, Patten MA. 2003. Family Dendrocolaptidae (Woodcreepers). In: del Hoyo, J. et al., editors. Handbook of the birds of the world, Volume 8, Broadbills to Tapaculos. Barcelona: Lynx Edicions. p. 358–447. Martins M. 1991. The lizards of Balbina, Central Amazonia, Brazil: a qualitative analysis of resource utilization. Stud Neotrop Fauna Environm. 26(3):179–190. Miranda JP, Ricci-Lobão A, Rocha CFD. 2010. Influence of structural habitat use on the thermal ecology of Gonatodes humeralis (Squamata: Gekkonidae) from a transitional forest in Maranhão, Brazil. Zoologia (Curitiba). 27(1):35–39. Munn CA. 1985. Permanent canopy and understory flocks in Amazonia: species composition and population density. Ornithol Monogr. 36:683–712. Nascimento FP, Ávila-Pires TCS, Cunha OR. 1987. Os répteis da área de Carajás, Pará, Brasil (Squamata). Bol Mus Paraense Emílio Goeldi, Sér Zool. 3(1):33–65. Noble GK. 1921. The bony structure and phyletic relations of Sphaerodactylus and allied lacertilian genera, with the description of a new genus. Am Mus Novit. (4):1–16. Parker HW. 1926. The Neotropical lizards of the genera Lepidoblepharis, Pseudogonatodes, Lathrogecko, and Sphaerodactylus, with the description of a new genus. Ann Mag Nat Hist. Series (9) 17:291–301. Downloaded by [J.D. Daza] at 03:51 07 December 2012 Journal of Natural History 2997 Pierpont N. 1983. Interspecific dominance and the structure of woodcreeper guilds. Am Zool. 23(4):1001. Poulin B, Lefebvre G, Ibañez R, Jaramillo C, Hernández C, Rand AS. 2001. Avian predation upon lizards and frogs in a Neotropical forest understory. J Trop Ecol. 17(1):21–40. Rage JC. 1978. La pouche à Phosphate de Ste-Néboule (Lot) et sa faune de vértebrés du Ludien supérieur. 5. Squamates. Palaeovertebrata. 8(2–4):201–215 Rivero-Blanco CV. 1979. The Neotropical lizard genus Gonatodes Fitzinger (Sauria: Sphaerodactylinae) [PhD dissertation]. [College Station (TX)]: Texas A&M University. Santos MM, Ávila RW, Kawashita-Ribeiro RA. 2011. Checklist of the amphibians and reptiles in Nobres municipality, Mato Grosso state, central Brazil. Herpetol Notes. 4:455–461. Silva FM, Menks AC, Prudente ALC, Costa JCL, Travassos AEM, Galatti U. 2011. Squamate reptiles from municipality of Barcarena and surroundings, State of Pará, north of Brazil. Checklist 7(3):220–226. Silva-Jr NJ, Cintra CED, Silva HLR, Costa MC, Souza CA, Pachêco-Jr AA, Gonçalves FA. 2009. Herpetofauna, Ponte de Pedra Hydroelectric Power Plant, states of Mato Grosso and Mato Grosso do Sul, Brazil. Checklist 5(3):518–525. Sociedade Brasiliera de Herpetologia. 2012 Lista de anfíbios do Brasil [Internet]. [Accessed 20 June 2012]. Available from: http://www.sbherpetologia.org.br/. Trueb L. 1970. Evolutionary relationships of casque-headed tree frogs with co-ossified skulls (family Hylidae). Univ Kansas Pub Mus Nat Hist. 1970(18):547–716. Uetanabaro M, Souza FL, Landgref Filho P, Beda AF, Brandão RA. 2007. Anfíbios e répteis do Parque Nacional da Serra da Bodoquena, Mato Grosso do Sul, Brasil. Biota Neotrop. 7(3): 279–289. Vanzolini PE. 1957. O gênero Coleodactylus (Sauria, Gekkonidae). Pap Avul Zool (São Paulo). 13(1):1–17. Vitt LJ, Sartorius SS, Ávila-Pires TCS, Zani PA, Espósito MC. 2005. Small in a big world: ecology of leaf-litter geckos in New World tropical forest. Herpetol Monogr. 19:137–152. Vitt LJ, Souza RA, Sartorius SS, Ávila-Pires TCS, Espósito MC. 2000. Comparative ecology of sympatric Gonatodes (Squamata: Gekkonide) in the Western Amazon of Brazil. Copeia 2000(1):83–95. Vitt LJ, Zani PA, Monteiro de Barros AA. 1997. Ecological variation among populations of the gekkonid lizard Gonatodes humeralis in the Amazon Basin. Copeia 1997(1):32–43. Willis EO. 1967. The behavior of Bicolored Antbirds. Univ California Pub Zool. 79:1–132. Willis EO. 1972a. The behavior of Plain-brown Woodcreepers, Dendrocincla fuliginosa. Wilson Bull. 84(4):377–420. Willis EO. 1972b. The behavior of Spotted Antbirds. Ornithol Monogr. 10:1–162. Willis EO. 1973. The behavior of Ocellated Antbirds. Smithsonian Contrib Zool. (144):1–57. Willis EO, Oniki Y. 1978. Birds and army ants. Ann Rev Ecol Syst. 9:243–26.