- Email: [email protected]
Foraging modes of Mesozoic birds and non-avian theropods
Magazine R911
Correspondences
Foraging modes of Mesozoic birds and non-avian theropods Christopher L. Glen1,* and Michael B. Bennett1 The origin and early evolution of birds has been a major topic in evolutionary biology. In the 20th century, evolutionary scenarios posited either ground-based bird ancestors or tree- dwelling ancestors. This has since been recognised as a false dichotomy [1]. We suggest that part of the problem is the loose categorisation of many extant bird species as either ground or tree locomotors when considering hind-limb function [2–7]. In reality these are not mutually exclusive alternatives. Many extant birds exhibit different degrees of ground- and tree- based behaviours. We thus propose they can be better placed on a spectrum — rather than a dichotomy — according to the extent of ground and/or tree foraging they exhibit. To test this system we analysed the toe claws of 249 species of Holocene birds, revealing that claw curvature increases as tree foraging becomes more predominant. Improved claw morphometrics allow more direct comparisons between extant and extinct birds in order to infer the behaviours of the latter. In contrast to previous studies [2–6], we find that claw curvatures of Mesozoic birds and closely related non-avian theropod dinosaurs, differ significantly from Holocene arboreal birds and more closely resemble those of Holocene ‘ground-foraging’ birds. We hypothesise that for extant birds that forage on foot, the claw of toe III will show an adaptation that strongly correlates to the proportion of ground-based and/or tree-based foraging a species exhibits, rather than other aspects of life-style. In both birds
and non-avian theropods toe III is always present, acting as the central weight-bearing toe during locomotion [8], and undergoes less specialisation than other toes. A circle can be accurately fitted to the dorsal rim of bird claws [7], allowing consistent measurement of the ‘claw angle’ (γ) between the radii that extend to the tip and the claw base (Supplemental data). We dispensed with the behavioural categories ‘grounddwellers’, ‘perchers’ and ‘climbers’ [2–7], which represent an oversimplification of a complex eco-morphological/behavioural spectrum that fails to account for the large number of birds that spend much time both in trees and on the ground (Figure 1A). In fact, the centre of the spectrum ranges continuously from species that spend most time on the ground through to those that spend most time in trees. Also, nearly all such ‘dual-mode’ birds rely on flight for travel or escape while the hindlimbs are most
active during foraging. For these birds, foraging mode will thus be most crucial for hind-limb locomotor adaptation. Based on published descriptions, we categorised Holocene bird species according to the proportion of ground or tree foraging they exhibit (Supplemental data). We examined the claw curvatures of bird species from the orders Columbiformes and Cuculiformes, as both are sufficiently speciose and diverse in behaviour and body mass (M). Other speciose orders, e.g. Psittaciformes and Passeriformes, have foot specialisations that would confound such analysis. Columbiformes and Cuculiformes include species that can be placed in all four foraging subcategories: ‘dedicated ground foragers’ (Gg); ‘predominantly ground foragers’ (Ga); ‘predominantly arboreal foragers’ (Ag); ‘dedicated arboreal foragers’ (Aa) (Figure 1B). To complete the full range of γ, ‘ground-based birds’ (GB), limited to foraging on the
Increasing arboreality
A
Climbers
Conventional behavioural categories
Perchers Ground-dwellers Tree foraging >50%
B Foraging categories
Ground foraging >50%
GB
C Taxa
Ground-based bird orders (Struthiornithiformes, Ciconiiformes, Gruiformes and Galliformes)
Gg
Ga G
*
Ag
Aa A
Pigeons and doves (Columbiformes) and Cuckoos and allies (Cuculiformes)
V True woodpeckers (Picinae) that forage on vertical trunks Current Biology
Figure 1. Categorisation of recent bird species in the comparative dataset. (A) In previous studies categorisation of a bird species as either ‘ground-dweller’ or ‘percher’ required summarisation of potentially disparate aspects of behaviour and morphology [2–5,7], with emphasis on the ‘ability/inability’ to perch. However, many ‘perchers’ visit the ground and some ‘ground-dwellers’ can perch. (B) Birds were placed into six categories (GB, Gg, Ga, Ag, Aa and V) based the degree of ground or tree foraging; GB = ‘ground-based’ birds, limited to foraging on the ground; Gg = ‘dedicated ground foragers’; Ga = ‘predominantly ground foragers’; Ag = ‘predominantly arboreal foragers’; Aa = ‘dedicated arboreal foragers’; V = ‘vertical surface foragers’. The four intermediate subcategories were subsequently grouped as G (‘ground foragers’) and A (‘arboreal foragers’) after a significant difference in mean claw angles was found between the subcategories Ga and Ag (divide marked *). Note divide ‘*’ is further to the right than the transition between conventional ‘ground-dwellers’ and ‘perchers’ categories in (A). (C) Taxonomic composition.
Current Biology Vol 17 No 21 R912
birds’ than in the ‘non-avian theropods’, there is no obvious correlation between γ and how the genera are sorted (i.e. ancestral to derived) in potentially different phylogenetic schemes. Assuming this diverse group directly or indirectly represents the ancestral lineage of extant birds, these data suggest that the specialised arboreal claw function exhibited in ‘arboreal’ and ‘vertical surface foragers’ is a derived feature, and smaller γ is the ancestral condition. In summary, as pedal claw angle is independent of scale and phylogeny, it is a reliable indicator of the predominant mode of hindlimb-based foraging. Our findings suggest early birds foraged predominantly on the ground, rather than supporting previous suggestions of arboreal claw adaptations, which appear to have evolved later in the lineage. Figure 2. Claw angles of Holocene birds compared to non-avian dinosaurs and early birds. (A,B) Columbiformes (81 species; 95% of Holocene genera) and Cuculiformes (62 species; 86% of Holocene genera) grouped according to their foraging behaviours (n = 451). Within both orders successive increases in tree foraging correlate with larger claw angles. (C) The relationship between foraging behaviour and claw angle, extending from ground-based birds (GB), through ‘ground foragers’ (G = Gg + Ga) and ‘arboreal foragers’ (A = Ag + Aa) to ‘vertical surface foragers’ (V). Birds with claw angles under about 100° are restricted to ground foraging or exhibit limited tree foraging. (D) Measured (γ) and estimated claw angles (γest, calculated from γu; Supplemental data) of Mesozoic genera are all lower than those of birds that predominantly forage in trees, except for the Sapeornis estimate. Fossil genera (Supplemental data) are arranged left to right approximating an ‘ancestral to derived’ order based on a consensus of available published information (filled circles (γ); empty circles (γu); grey triangles (γest)).
ground, as well as ‘vertical surface foragers’ (V) were included, which exhibit the lowest and highest observed values of γ, respectively (Figures 1 and 2C). We found that γ is positively correlated with an increasing proportion of tree foraging within Columbiformes and Cuculiformes. This is the first clear indication of this trend at an ordinal level (Figure 2). Cuculiformes displayed a 3.8° higher mean claw angle than Columbiformes, though no significant phylogenetic signal could be found within the combined dataset using phylogenetic generalised least squares analysis (Supplemental data). Any scaling relationship between γ and M was small or absent within each foraging category. Although mean γ was not significantly different between the Gg and Ga (P = 0.118) and the
Aa and Ag (P = 0.073) categories, differences between categories in all other paired comparisons were highly significant (P < 0.001). This suggests that γ reliably resolves Columbiformes and Cuculiformes into behavioural groups of ‘arboreal foragers’ (A, comprising Ag and Aa) and ‘ground foragers’ (G, comprising Gg and Ga). For fossil claws, if their sheaths are preserved in situ, γ can be measured directly. Otherwise, estimated claw angles (γest) can be calculated from the claw angle of the ungual bone (γu) using the relationship γ = 1.54 γu that we determined from a broad analysis of X-radiographs of extant birds. All 12 Mesozoic genera were found to have claw angles within the GB to G range (Figure 2C,D), with the possible exception of Sapeornis. Other than the slightly higher average γ in ‘Mesozoic
Supplemental data Supplemental data including experimental procedures are available at http://www.current-biology.com/cgi/ content/full/17/21/R911/DC1 References 1. Padian, K. (2001). Stages in the origin of bird flight: Beyond the arboreal-cursorial dichotomy. In New Perspectives on the Origin and Early Evolution of Birds, J. Gauthier and L.F. Gall, eds. (New Haven: Peabody Museum of Natural History), pp. 255–272. 2. Ostrom, J.H. (1974). Archaeopteryx and the origin of flight. Q. Rev. Biol. 49, 27–47. 3. Yalden, D.W. (1985). Forelimb function in Archaeopteryx. In The Beginnings of Birds, M.K. Hecht, J.H. Ostrom, G. Viohl, and P. Wellnhofer, eds. (Eichstätt: Freunde des Jura-Museums Eichstätt), pp. 91–97. 4. Peters, D.S., and Görgner, E. (1992). A comparative study on the claws of Archaeopteryx. LA. Co. Mus. Sci. Ser. 36, 29–37. 5. Feduccia, A. (1993). Evidence from claw geometry indicating arboreal habits of Archaeopteryx. Science 259, 790–793. 6. Yalden, D.W. (1997). Climbing Archaeopteryx. Archaeopteryx 15, 107–108. 7. Pike, A.V.L., and Maitland, D.P. (2004). Scaling of bird claws. J. Zool. (Lond.) 262, 73–81. 8. Hopson, J.A. (2001). Ecomorphology of avian and nonavian theropod phalangeal proportions: Implications for the arboreal versus terrestrial origin of bird flight. In New Perspectives on the Origin and Early Evolution of Birds. J. Gauthier and L.F. Gall, eds. (New Haven: Peabody Museum of Natural History), pp. 211–235. 1School
of Biomedical Sciences, The University of Queensland, St. Lucia, Queensland 4072, Australia. *E-mail: [email protected]
Correspondences
Foraging modes of Mesozoic birds and non-avian theropods Christopher L. Glen1,* and Michael B. Bennett1 The origin and early evolution of birds has been a major topic in evolutionary biology. In the 20th century, evolutionary scenarios posited either ground-based bird ancestors or tree- dwelling ancestors. This has since been recognised as a false dichotomy [1]. We suggest that part of the problem is the loose categorisation of many extant bird species as either ground or tree locomotors when considering hind-limb function [2–7]. In reality these are not mutually exclusive alternatives. Many extant birds exhibit different degrees of ground- and tree- based behaviours. We thus propose they can be better placed on a spectrum — rather than a dichotomy — according to the extent of ground and/or tree foraging they exhibit. To test this system we analysed the toe claws of 249 species of Holocene birds, revealing that claw curvature increases as tree foraging becomes more predominant. Improved claw morphometrics allow more direct comparisons between extant and extinct birds in order to infer the behaviours of the latter. In contrast to previous studies [2–6], we find that claw curvatures of Mesozoic birds and closely related non-avian theropod dinosaurs, differ significantly from Holocene arboreal birds and more closely resemble those of Holocene ‘ground-foraging’ birds. We hypothesise that for extant birds that forage on foot, the claw of toe III will show an adaptation that strongly correlates to the proportion of ground-based and/or tree-based foraging a species exhibits, rather than other aspects of life-style. In both birds
and non-avian theropods toe III is always present, acting as the central weight-bearing toe during locomotion [8], and undergoes less specialisation than other toes. A circle can be accurately fitted to the dorsal rim of bird claws [7], allowing consistent measurement of the ‘claw angle’ (γ) between the radii that extend to the tip and the claw base (Supplemental data). We dispensed with the behavioural categories ‘grounddwellers’, ‘perchers’ and ‘climbers’ [2–7], which represent an oversimplification of a complex eco-morphological/behavioural spectrum that fails to account for the large number of birds that spend much time both in trees and on the ground (Figure 1A). In fact, the centre of the spectrum ranges continuously from species that spend most time on the ground through to those that spend most time in trees. Also, nearly all such ‘dual-mode’ birds rely on flight for travel or escape while the hindlimbs are most
active during foraging. For these birds, foraging mode will thus be most crucial for hind-limb locomotor adaptation. Based on published descriptions, we categorised Holocene bird species according to the proportion of ground or tree foraging they exhibit (Supplemental data). We examined the claw curvatures of bird species from the orders Columbiformes and Cuculiformes, as both are sufficiently speciose and diverse in behaviour and body mass (M). Other speciose orders, e.g. Psittaciformes and Passeriformes, have foot specialisations that would confound such analysis. Columbiformes and Cuculiformes include species that can be placed in all four foraging subcategories: ‘dedicated ground foragers’ (Gg); ‘predominantly ground foragers’ (Ga); ‘predominantly arboreal foragers’ (Ag); ‘dedicated arboreal foragers’ (Aa) (Figure 1B). To complete the full range of γ, ‘ground-based birds’ (GB), limited to foraging on the
Increasing arboreality
A
Climbers
Conventional behavioural categories
Perchers Ground-dwellers Tree foraging >50%
B Foraging categories
Ground foraging >50%
GB
C Taxa
Ground-based bird orders (Struthiornithiformes, Ciconiiformes, Gruiformes and Galliformes)
Gg
Ga G
*
Ag
Aa A
Pigeons and doves (Columbiformes) and Cuckoos and allies (Cuculiformes)
V True woodpeckers (Picinae) that forage on vertical trunks Current Biology
Figure 1. Categorisation of recent bird species in the comparative dataset. (A) In previous studies categorisation of a bird species as either ‘ground-dweller’ or ‘percher’ required summarisation of potentially disparate aspects of behaviour and morphology [2–5,7], with emphasis on the ‘ability/inability’ to perch. However, many ‘perchers’ visit the ground and some ‘ground-dwellers’ can perch. (B) Birds were placed into six categories (GB, Gg, Ga, Ag, Aa and V) based the degree of ground or tree foraging; GB = ‘ground-based’ birds, limited to foraging on the ground; Gg = ‘dedicated ground foragers’; Ga = ‘predominantly ground foragers’; Ag = ‘predominantly arboreal foragers’; Aa = ‘dedicated arboreal foragers’; V = ‘vertical surface foragers’. The four intermediate subcategories were subsequently grouped as G (‘ground foragers’) and A (‘arboreal foragers’) after a significant difference in mean claw angles was found between the subcategories Ga and Ag (divide marked *). Note divide ‘*’ is further to the right than the transition between conventional ‘ground-dwellers’ and ‘perchers’ categories in (A). (C) Taxonomic composition.
Current Biology Vol 17 No 21 R912
birds’ than in the ‘non-avian theropods’, there is no obvious correlation between γ and how the genera are sorted (i.e. ancestral to derived) in potentially different phylogenetic schemes. Assuming this diverse group directly or indirectly represents the ancestral lineage of extant birds, these data suggest that the specialised arboreal claw function exhibited in ‘arboreal’ and ‘vertical surface foragers’ is a derived feature, and smaller γ is the ancestral condition. In summary, as pedal claw angle is independent of scale and phylogeny, it is a reliable indicator of the predominant mode of hindlimb-based foraging. Our findings suggest early birds foraged predominantly on the ground, rather than supporting previous suggestions of arboreal claw adaptations, which appear to have evolved later in the lineage. Figure 2. Claw angles of Holocene birds compared to non-avian dinosaurs and early birds. (A,B) Columbiformes (81 species; 95% of Holocene genera) and Cuculiformes (62 species; 86% of Holocene genera) grouped according to their foraging behaviours (n = 451). Within both orders successive increases in tree foraging correlate with larger claw angles. (C) The relationship between foraging behaviour and claw angle, extending from ground-based birds (GB), through ‘ground foragers’ (G = Gg + Ga) and ‘arboreal foragers’ (A = Ag + Aa) to ‘vertical surface foragers’ (V). Birds with claw angles under about 100° are restricted to ground foraging or exhibit limited tree foraging. (D) Measured (γ) and estimated claw angles (γest, calculated from γu; Supplemental data) of Mesozoic genera are all lower than those of birds that predominantly forage in trees, except for the Sapeornis estimate. Fossil genera (Supplemental data) are arranged left to right approximating an ‘ancestral to derived’ order based on a consensus of available published information (filled circles (γ); empty circles (γu); grey triangles (γest)).
ground, as well as ‘vertical surface foragers’ (V) were included, which exhibit the lowest and highest observed values of γ, respectively (Figures 1 and 2C). We found that γ is positively correlated with an increasing proportion of tree foraging within Columbiformes and Cuculiformes. This is the first clear indication of this trend at an ordinal level (Figure 2). Cuculiformes displayed a 3.8° higher mean claw angle than Columbiformes, though no significant phylogenetic signal could be found within the combined dataset using phylogenetic generalised least squares analysis (Supplemental data). Any scaling relationship between γ and M was small or absent within each foraging category. Although mean γ was not significantly different between the Gg and Ga (P = 0.118) and the
Aa and Ag (P = 0.073) categories, differences between categories in all other paired comparisons were highly significant (P < 0.001). This suggests that γ reliably resolves Columbiformes and Cuculiformes into behavioural groups of ‘arboreal foragers’ (A, comprising Ag and Aa) and ‘ground foragers’ (G, comprising Gg and Ga). For fossil claws, if their sheaths are preserved in situ, γ can be measured directly. Otherwise, estimated claw angles (γest) can be calculated from the claw angle of the ungual bone (γu) using the relationship γ = 1.54 γu that we determined from a broad analysis of X-radiographs of extant birds. All 12 Mesozoic genera were found to have claw angles within the GB to G range (Figure 2C,D), with the possible exception of Sapeornis. Other than the slightly higher average γ in ‘Mesozoic
Supplemental data Supplemental data including experimental procedures are available at http://www.current-biology.com/cgi/ content/full/17/21/R911/DC1 References 1. Padian, K. (2001). Stages in the origin of bird flight: Beyond the arboreal-cursorial dichotomy. In New Perspectives on the Origin and Early Evolution of Birds, J. Gauthier and L.F. Gall, eds. (New Haven: Peabody Museum of Natural History), pp. 255–272. 2. Ostrom, J.H. (1974). Archaeopteryx and the origin of flight. Q. Rev. Biol. 49, 27–47. 3. Yalden, D.W. (1985). Forelimb function in Archaeopteryx. In The Beginnings of Birds, M.K. Hecht, J.H. Ostrom, G. Viohl, and P. Wellnhofer, eds. (Eichstätt: Freunde des Jura-Museums Eichstätt), pp. 91–97. 4. Peters, D.S., and Görgner, E. (1992). A comparative study on the claws of Archaeopteryx. LA. Co. Mus. Sci. Ser. 36, 29–37. 5. Feduccia, A. (1993). Evidence from claw geometry indicating arboreal habits of Archaeopteryx. Science 259, 790–793. 6. Yalden, D.W. (1997). Climbing Archaeopteryx. Archaeopteryx 15, 107–108. 7. Pike, A.V.L., and Maitland, D.P. (2004). Scaling of bird claws. J. Zool. (Lond.) 262, 73–81. 8. Hopson, J.A. (2001). Ecomorphology of avian and nonavian theropod phalangeal proportions: Implications for the arboreal versus terrestrial origin of bird flight. In New Perspectives on the Origin and Early Evolution of Birds. J. Gauthier and L.F. Gall, eds. (New Haven: Peabody Museum of Natural History), pp. 211–235. 1School
of Biomedical Sciences, The University of Queensland, St. Lucia, Queensland 4072, Australia. *E-mail: [email protected]