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Evolution of Bill Size in Relation to Body Size in Toucans and Hornbills (Aves: Piciformes and Bucerotiformes)

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Evolution of Bill Size in Relation to Body Size in Toucans and Hornbills (Aves: Piciformes and Bucerotiformes) ZOOLOGIA 31 (3): 256–263, June, 2014 http://dx.doi.org/10.1590/S1984-46702014000300007 Evolution of bill size in relation to body size in toucans and hornbills (Aves: Piciformes and Bucerotiformes) Austin L. Hughes Department of Biological Sciences, University of South Carolina, Columbia SC 29205 USA. E-mail: [email protected] ABSTRACT. Evidence that the bill of the Toco Toucan, Ramphastos toco Statius Muller, 1776, has a specialized role in heat dissipation suggests a new function for the large and light-weight bill of the toucan family (Piciformes: Ramphastidae). A prediction of this hypothesis is that bill length in toucans will increase with body mass at a rate greater than the isometric expectation. This hypothesis was tested in a phylogenetic context with measurements of skeletal elements in adult males of 21 toucan species. In these species, 64.3% of variance in relative skeletal measurements was accounted for by the contrast between bill and body size. Maxilla length and depth increased with body mass at a greater than isometric rate relative to both body mass and other linear skeletal measures. By contrast, no such trend was seen in a parallel analysis of 24 hornbill species (Bucerotiformes), sometimes considered ecological equivalents of toucans. The unique relationship between bill size and body mass in toucans supports the hypothesis that the evolution of a heat dissipation function has been a persistent theme of bill evolution in toucans. KEY WORDS. Allometry; heat dissipation; Ramphastidae. The adaptive significance of the large and remarkably plesiomorphic function of the avian bill. In the Ramphastidae, light-weight bill of members of the Neotropical toucan family it might be hypothesized that the ancestral heat-dissipation (Piciformes: Ramphastidae) has been the subject of much specu- function has become elaborated by the evolution of a highly lation (SHORT & HORNE 2001, TATTERSALL et al. 2009). Although modifiable vascular radiator (TATTERSALL et al. 2009). On this VAN TYNE (1929: 39) suggested that the toucan’s bill has no hypothesis, the emergence of this vascular adaptation has been “especial adaptive function”, a number of adaptive hypoth- an additional factor favoring the evolution of large bill size in eses have been proposed. BÜHLER (1995) proposed that the bill’s toucans, in conjunction with other selective pressures such as large size and serrated edges originally evolved primarily as an frugivory and signaling. Relatively little is known of toucans’ adaptation for reaching and grasping fruit; later “tooth-like” thermal biology in nature, but the family is entirely Neotropi- markings on the bill may have evolved as adaptations to mini- cal in distribution, and most species inhabit tropical lowland mize mobbing by other birds when toucans prey on their nests forests (SHORT & HORNE 2001), where high daily maximum tem- (SICK 1993, BÜHLER 1995). SHORT & HORNE (2001) suggested a simi- peratures occur year-round (GRUBB & WHITMORE 1996). lar evolutionary sequence, while emphasizing the likely im- Consistent with a role for the toucan bill in heat-dissi- portance of species-specific bill markings in species recognition pation, TATTERSALL et al. (2009) presented evidence that bill and courtship. Toucan bills are often brightly colored, and a length in juvenile and adult Toco Toucan increases as a func- few species show sexual dimorphism in bill coloration (SHORT tion of body mass at a rate greater than the isometric expecta- & HORNE 2001). When bill color dimorphism occurs it is usu- tion; i.e., greater than an exponent of 1/3 expected for a linear ally not very marked (SHORT & HORNE 2001), but its presence dimension (ALEXANDER 1971). Likewise, SYMONS & TATTERSALL suggests that sexual selection may be another evolutionary force (2010) provided evidence that across toucan species bill length acting on toucan bills, at least in some species. increases as a function of body mass at a rate greater than lin- A further contribution to understanding the function of ear expectation, using published data on 34 species of the toucan’s bill was provided by evidence that the bill of the Ramphastidae. Such a relationship is expected if the bill plays Toco Toucan, Ramphastos toco Statius Muller, 1776, serves as a a role in dissipating body heat, since metabolic rate increases key surface area for heat dissipation (TATTERSALL et al. 2009), with body mass with an exponent between 2/3 and 1.0, de- which the bird can use to regulate body temperature by con- pending on activity level (GLAZIER 2008). trolling blood flow. There is evidence that bills of a variety of Here I analyze the evolution of bill size in relation both avian taxa can function in heat dissipation (HAGAN & HEATH to the size of other major skeletal elements and to body mass 1980, SCOTT et al. 2008, GREENBERG et al. 2012a, b, GREENBERG & across the family Ramphastidae in order to test the hypothesis DANNER 2013), suggesting that heat dissipation may be a of isometry against an alternative consistent with the bill’s 2014 Sociedade Brasileira de Zoologia | www.sbzoologia.org.br | www.scielo.br/zool All content of the journal, except where identified, is licensed under a Creative Commons attribution-type BY-NC. Evolution of bill size in relation to body size in toucans and hornbills 257 proposed role in heat dissipation, using statistical methods that control for phylogenetic relationships. A phylogenetic ap- proach makes it possible to test the hypothesis that there has been a trend toward bill sizes greater than the isometric expec- tation throughout the evolution of this family. The hornbills (Bucerotiformes) are considered Old World ecological equiva- lents of the toucans, filling similar ecological niches in their respective ecosystems; most members of both families are cav- ity-nesting frugivores of tropical forests, and the two families have convergently evolved large slightly downcurved bills (KEMP 1995, KINNAIRD & O’BRIEN 2007). Because of these ecological parallels, I conduct a similar analysis with hornbills to com- pare the patterns of bill evolution relative to body size in the two groups of large-billed tropical birds. By comparing pattern of bill allometry in these two families, I test for a distinctive pattern of bill evolution in toucans, which would be consis- 1 tent with the hypothesis that the toucan’s bill plays an excep- tionally highly developed role in heat dissipation. MATERIAL AND METHODS Measurements were made on complete skeletal specimens of adult males belonging to 21 species of toucans (Piciformes: Ramphastidae) and on complete skeletons of adult males of 24 species of hornbills (Bucerotiformes: Bucorvidae and Bucerotidae) from the U.S. National Museum of Natural History. The same measurements were also made on adult females of 16 of the toucan species and 14 of the hornbill species; since the patterns were similar for males and females, only the results for males are reported here. As an outgroup to root the phylogenetic tree of toucans, two species of New World barbets (Piciformes: Capitonidae) were used, Capito aurovirens (Cuvier, 1829) and 2 Semnornis ramphastinus (Jardine, 1855) (Fig. 1). As an outgroup Figures 1-2. Phylogenies of species used in analyses: (1) phyloge- to root the phylogenetic tree of hornbills, the Eurasian Hoopoe, ny of toucans (Ramphastidae), rooted with two species of barbet, Upupa epops Linnaeus, 1758, (Upupiformes: Upupidae) was used Capito aurovirens and Semnornis ramphastinus; (2) phylogeny of (Fig. 2). Species were included based on available specimens but hornbills (Bucerotiformes), rooted with Upupa epops. sampled all major lineages of both toucans and hornbills (Figs 1 and 2). Because no comprehensive molecular phylogeny of tou- abilities, Bayesian posterior probabilities, or both. Preliminary cans has been published, the phylogeny of toucans (Fig. 1) analyses using the phylogeny of Ramphastos from HAFFER (1974, was derived from a combination of published DNA sequence- 1997) showed essentially identical results to those based on based phylogenies. The relationships among the ramphastid the phylogeny of PATANÉ et al. (2009); only the latter results are genera were based on NAHUM et al. (2003); see also PATANÉ et al. reported here. (2009). Relationships within the genus Ramphastos were based In the case of toucans and barbets, the following nine skel- on PATANÉ et al. (2009); see also WECKSTEIN (2005). Relationships etal measurements were made by digital caliper (BAUMEL 1993): within Pteroglossus and Baillonius were based on EBERHARD & 1) maxilla length, measured from the dorsal junction of the max- BERMINGHAM (2005) and PATEL et al. (2011). Relationships within illa with the cranium to the tip of the bill (Rostrum maxillare); 2) Aulacorhynchus were based on BONACCORSO et al. (2011); and maxilla depth, measured at the point of widest dorsal to ventral those within Andigena and Selenidera were based on LUTZ et al. depth; 3) maxilla width, measured at the point of greatest lateral (2013). The phylogeny of hornbills (Fig. 2) was based on the width; 4) cranium length, measured from the dorsal junction of DNA sequence phylogeny of GONZALEZ et al. (2013). Most the maxilla with the cranium to the posterior end (Proeminentia branching patterns indicated in Figs 1 and 2 were strongly sup- cerebellaris) of the cranium; 5) cranium width, measured at the ported in the original phylogenetic analyses by bootstrap prob- point of greatest lateral width; 6) sternum, measured from Apex ZOOLOGIA 31 (3): 256–263, June, 2014 258 A.L. Hughes carinae to Margo caudalis; 7) synsacrum, measured from the ante- (i.e., the allometric exponent) of any linear skeletal measure rior edge of Ala preacetabularis to the posterior edge of Ala ischii; on any other linear skeletal measure is 1.0. The isometric ex- 8) femur, measured from the proximal point of Crista trochanteris pectation for b in a log-log regression of a linear measure on to the distal point of Condylus lateralis; and 9) tibiotarsus, mea- body mass (predicted to be proportional to body volume) is 1/ sured from the proximal point of Facies gastrocnemialis to Inci- 3 (ALEXANDER 1971).
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