Analysis of skull morphometric characters in diurnal raptors (Accipitriformes and Falconiformes)

Open access


Diurnal birds of prey (Accipitriformes and Falconiformes) has traditionally been known as comprising a single order. Recently, this classification has been used in the non-taxonomic sense as referring to a convergent group of birds that are largely classified as predatory birds. Although these birds are similar in their morphology, the species differ in their foraging methods and prey preference. The cranial shape and the physical attributes determine the efficiency of the resource use. The aim of this study is to increase our knowledge of the relationship between skull shape, prey preference, and foraging habits. A geometric morphometric approach was used to analyse two-dimensional cranial landmarks. We used principal component (PC) analyses on measurements that may be related to prey preference and foraging habits. The PCs are resulted described the relative height of the skull and beak, the variation in the relative size, the orientation and robustness of the lacrimal bone, the variation in the relative size of the neurocranium compared to the viscerocranium, and the orientation of the palatine bone. The dietary categories significantly overlap. The skull morphology reflects more on foraging habits than diet or prey preference.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Adams D. C. Rohlf F. J. & Slice D. E. 2004. Geometric morphometrics: ten years of progress following the ‘revolutionʼ. – Italian Journal of Zoology 71(1): 5–16. DOI: 10.1080/11250000409356545

  • Anderson R. A. McBrayer L. D. & Herrel A. 2008. Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure. – Biological Journal of the Linnean Society 93(4): 709–720. DOI: 10.1111/j.1095-8312.2007.00905.x

  • Andersson M. & Norberg R. Å. 1981. Evolution of reversed sexual size dimorphism and role partitioning among predatory birds with a size scaling of flight performance. – Biological Journal of the Linnean Society 15(2): 105–130. DOI: 10.1111/j.1095-8312.1981.tb00752.x

  • Andersson M. 1994. Sexual Selection. – Princeton University Press Princeton NJ Ballejo F. Lambertucci S. A. Trejo A. & De Santis L. J. 2018. Trophic niche overlap among scavengers in Patagonia supports the condor-vulture competition hypothesis. – Bird Conservation International 28(3): 390–402. DOI: 10.1017/S0959270917000211

  • Bakaloudis D. E. Vlachos C. G. & Holloway G. J. 1998. Habitat use by Short-toed Eagles Circaetus gallicus and their reptilian prey during the breeding season in Dadia Forest (north-eastern Greece). – Journal of Applied Ecology 35(6): 821–828. DOI: 10.1111/j.1365-2664.1998.tb00001.x

  • Barker F. K. Cibois A. Schikler P. Feinstein J. & Cracraft J. 2004. Phylogeny and diversification of the largest avian radiation. – Proceedings of the National Academy of Sciences 101(30): 11040–11045. DOI: 10.1073/pnas.0401892101

  • Baumel J. J. 1993. Handbook of avian anatomy: Nomina Anatomica Avium. – Publications of the Nuttall Ornithological Club (USA) no. 23.

  • Benkman C. W. 2003. Divergent selection drives the adaptive radiation of Crossbills. – Evolution 57(5): 1176–1181. DOI: 10.1111/j.0014-3820.2003.tb00326.x

  • Bergmann F. Amaral H. Pinto D. Chivittz C. & Tozetti A. 2013. Foraging activity of the Snail Kite Rostrhamus sociabilis (Aves: Accipitridae) in wetlands of southern Brazil. – Brazilian Journal of Biology 73(2): 245–252. DOI: 10.1590/s1519-69842013000200004

  • Bielefeldt J. Rosenfield R. N. & Papp J. M. 1992. Unfounded assumptions about diet of the Cooper’s Hawk. – The Condor 94(2): 427–436. DOI: 10.2307/1369215

  • Bijleveld M. 1974. Birds of prey in Europe. – Macmillan International Higher Education

  • Brathwaite D. H. 1992. Notes on the weight flying ability habitat and prey of Haast’s Eagle (Harpagornis moorei). – Notornis 39(4): 239–247.

  • Brown C. J. & Plug I. 1990. Food choice and diet of the Bearded Vulture Gypaetus barbatus in southern Africa. – South African Journal of Zoology 25: 169–177. DOI: 10.1080/02541858.1990.11448207

  • Cade T. J. & Digby R. D. 1982. The falcons of the world. – Harper Collins Colwell R. K. 2000. Rensch’s rule crosses the line: convergent allometry of sexual size dimorphism in hummingbirds and flower mites. – American Naturalist 156: 495–510. DOI: 10.1086/303406

  • Cracraft J. Barker F. K. Braun M. J. Harshman J. Dyke G. J. Feinstein J. Stanley S. Cibois A. Schikler P. Beresford P. García-Moreno J. Sorenson M. D. Yuri T. & Mindell D. P. 2004. Phylogenetic relationships among modern birds (Neornithes). – In: Cracraft J. Donoghue M. J. & Donoghue M. M. (eds.) Assembling the tree of life. – New York Oxford University Press pp. 468–489.

  • Cramp S. 1980. Handbook of the birds of Europe the Middle East and North Africa: the birds of the western Palearctic Vol. 2. Hawks to bustards. – Oxford University Press

  • Csermely D. & Gaibani G. 1998. Is foot squeezing pressure by two raptor species sufficient to subdue their prey? – Condor 100(4): 757–763. DOI: 10.2307/1369762

  • Csermely D. Bertè L. & Camoni R. 1998. Prey killing by Eurasian Kestrels: the role of the foot and the significance of bill and talons. – Journal of Avian Biology 29(1): 10–16. DOI: 10.2307/3677335

  • Csermely D. & Rossi O. 2006. Bird claws and bird of prey talons: Where is the difference? – Italian Journal of Zoology 73(1): 43–53. DOI: 10.1080/11250000500502368

  • Dixon A. Richards C. & King A. 2018. Diet of Peregrine Falcons (Falco peregrinus) in relation to temporal and spatial variation in racing pigeon availability in Wales. – Ornis Hungarica 26(2): 188–200. DOI: 10.1515/orhu-2018-0028

  • Dumont E. R. 2003. Bats and fruit: an ecomorphological approach. – In: Kunz T. H. & Fenton M. B (eds.) Bat Ecology. – University of Chicago Press Chicago pp. 398–429.

  • Fabbri M. Koch N. M. Pritchard A. C. Hanson M. Hoffman E. Bever G. S. Balanoff A. M. Morris Z. S. Field D. J. Camacho J. Rowe T. B. Norell M. A. Smith R. M. Abzhanov A. & Bhullar B-A. S. 2017. The skull roof tracks the brain during the evolution and development of reptiles including birds. – Nature Ecology & Evolution 1(10): 1543–1550. DOI: 10.1038/s41559-017-0288-2

  • Fowler D. W. Freedman E. A. & Scannella J. B. 2009. Predatory functional morphology in raptors: interdigital variation in talon size is related to prey restraint and immobilisation technique. – PloS One 4(11): e7999. DOI: 10.1371/journal.pone.0007999

  • Gende S. M. Wilson M. F. & Jacobsen M. 1997. Reproductive success of Bald Eagles (Haliaeetus leucocephalus) and its association with habitat or landscape features and weather in southeast Alaska. – Canadian Journal of Zoology 75(10): 1595–1604. DOI: 10.1139/z97-786

  • Graham I. M. Redpath S. M. & Thirgood S. J. 1995. The diet and breeding density of Common Buzzards Buteo buteo in relation to indices of prey abundance. – Bird Study 42(2): 165–173. DOI: 10.1080/00063659509477162

  • Graves G. R. 2017. Sexual monomorphism in wing loading and wing aspect ratio in Black Vulture (Coragyps atratus) and Turkey Vulture (Cathartes aura). – Proceedings of the Biological Society of Washington 130(1): 240–249. DOI: 10.2988/17-00018

  • Grant P. R. Abbott I. Schluter D. Curry R. L. & Abbott L. K. 1985. Variation in the size and shape of Darwin’s finches. – Biological Journal of the Linnean Society 25(1): 1–39. DOI: 10.1111/j.1095-8312.1985.tb00384.x

  • Guangdi S. I. Dong Y. Ma Y. & Zhang Z. 2015. Shape similarities and differences in the skulls of scavenging raptors. – Zoological Science 32(2): 71–177. DOI: 10.2108/zs130253

  • Hackett S. J. Kimball R. T. Reddy S. Bowie R. C. Braun E. L. Braun M. J. & Huddleston C. J. 2008. A phylogenomic study of birds reveals their evolutionary history. – Science 320(5884): 1763–1768. DOI: 10.1126/science.1157704

  • Hammer Ø. Harper D. A. T. & Ryan P. D. 2001. PAST: paleontological statistics software package for education and data analysis. – Palaeontologia Electronica 4: 1–9.

  • Haring E. Kvaløy K. Gjershaug J. O. Røv N. & Gamauf A. 2007. Convergent evolution and paraphyly of the hawk eagles of the genus Spizaetus (Aves Accipitridae) – phylogenetic analyses based on mitochondrial markers. – Journal of Zoological Systematics and Evolutionary Research 45(4): 353–365. DOI: 10.1111/j.1439-0469.2007.00410.x

  • Helbig A. J. Seibold I. Bednarek W. Gaucher P. Ristow D. Scharlau W. Schmidl D. & Wink M. 1994. Phylogenetic relationships among falcon species (genus Falco) according to DNA sequence variation of the cytochrome b gene. – In: Meyburg B-U. & Chancellor R. D. (eds.) Raptor Conservation Today WWGBP/The Pica Press pp. 593–599.

  • Heesy C. P. 2004. On the relationship between orbit orientation and binocular visual field overlap in mammals. – The Anatomical Record Part A: Discoveries in Molecular Cellular and Evolutionary Biology 281(1): 1104–1110. DOI: 10.1002/ar.a.20116

  • Herrel A. Podos J. Huber S. K. & Hendry A. P. 2005. Bite performance and morphology in a population of Darwin’s finches: implications for the evolution of beak shape. – Functional Ecology 19(1): 43–48. DOI: 10.1111/j.0269-8463.2005.00923.x

  • Hertel F. 1995. Ecomorphological indicators of feeding behavior in recent and fossil raptors. – The Auk 112(4): 890–903. DOI: 10.2307/4089021

  • Hille S. M. Korner-Nievergelt F. Bleeker M. & Collar N. J. 2016. Foraging behaviour at carcasses in an Asian vulture assemblage: towards a good restaurant guide. – Bird Conservation International 26(3): 263–272. DOI: 10.1017/S0959270915000349

  • Hinsley S. A. Bellamy P. E. & Moss D. 1995. Sparrowhawk Accipiter nisus prediction and feeding site selection by its. – Ibis 137(3): 418–422. DOI: 10.1111/j.1474-919X.1995.tb08042.x

  • Houston D. C. 1986. Scavenging efficiency of Turkey Vultures in tropical forest. – The Condor 88(3): 318–323. DOI: 10.2307/1368878

  • Hull C. 1991. A Comparison of the morphology of the feeding apparatus in the Peregrine Falcon Falco peregrinus and the Brown Falcon Falco berigora (Falconiformes). – Australian Journal of Zoology 39(1): 67–76. DOI: 10.1071/ZO9910067

  • Itämies J. & Mikkola H. 1972. The diet of Honey Buzzards Pernis apivorus in Finland. – Ornis Fennica 49: 7–10.

  • Jarvis E. D. Mirarab S. Aberer A. J. Li B. Houde P. Li C. Ho S. Y. W. Faircloth B. C. Nabholz B. Howard J. T. Suh A. et al. & Zhang G. 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. – Science 346(6215): 1320–1331. DOI: 10.1126/science.1253451.

  • Jones M. P. Pierce K. E. & Ward D. 2007. Avian vision: a review of form and function with special consideration to birds of prey. – Journal of Exotic Pet Medicine 16(2): 69–87. DOI: 10.1053/j.jepm.2007.03.012

  • Korpimäki E. 1985. Prey choice strategies of the Kestrel Falco tinnunculus in relation to available small mammals and other Finnish birds of prey. – Annales Zoologici Fennici 22(1): 91–104.

  • Kotymán L. Solt S. Horváth É. Palatitz P. & Fehérvári P. 2015. Demography breeding success and effects of nest type in artificial colonies of Red-footed Falcons and allies. – Ornis Hungarica 23(1): 1–21. DOI: 10.1515/orhu-2015-0001

  • Kulemeyer C. Asbahr K. Gunz P. Frahnert F. & Bairlein F. 2009. Functional morphology and integration of corvid skulls-a 3D geometric morphometric approach. – Frontiers of Zoology 6: 2. DOI: 10.1186/1742-9994-6-2

  • Kruuk H. 1967. Competition for food between vultures of East Africa. – Ardea 55(17): 1–193.

  • Ladyguin A. 2000. The morphology of the bill apparatus in the Steller’s Sea Eagle. – In: Ueta M. & McGrady M. J. (eds.) First Symposium on Steller’s and White-tailed Sea Eagles in East Asia. – Wild Bird Society of Japan Tokyo Japan pp. 1–10.

  • Lindberg P. & Odsjö T. 1983. Mercury levels in feathers of Peregrine Falcon Falco peregrinus compared with total mercury content in some of its prey species in Sweden. – Environmental Pollution Series B Chemical and Physical 5(4): 297–318. DOI: 10.1016/0143-148X(83)90023-X

  • Martin G. R. 2007. Visual fields and their functions in birds. – Journal of Ornithology 48(Suppl. 2.): S547–S562. DOI: 10.1007/s10336-007-0213-6

  • Marugán-Lobón J. & Buscalioni Á. D. 2006. Avian skull morphological evolution: exploring exo- and endocranial covariation with two-block partial least squares. – Zoology 109(3): 217–230. DOI: 10.1016/j.zool.2006.03.005

  • Massemin S. Korpimäki E. & Wiehn J. 2000. Reversed sexual size dimorphism in raptors: evaluation of the hypotheses in kestrels breeding in a temporally changing environment. – Oecologia 124(1): 26–32. DOI: 10.1007/s004420050021

  • McBrayer L. D. 2004. The relationship between skull morphology biting performance and foraging mode in Kalahari lacertid lizards. – Zoological Journal of the Linnean Society 140(3): 403–416. DOI: 10.1111/j.1096-3642.2003.00106.x

  • McCormack J. E. Harvey M. G. Faircloth B. C. Crawford N. G. Glenn T. C. & Brumfield R. T. 2013. A phylogeny of birds based on over 1500 loci collected by target enrichment and high-throughput sequencing. – PLoS One 8(1): e54848. DOI: 10.1371/journal.pone.0054848

  • Mindell D. P. Fuchs J. & Johnson J. A. 2018. Phylogeny taxonomy and geographic diversity of diurnal raptors: Falconiformes Accipitriformes and Cathartiformes. – In: Sarasola J. H. Grande J. M. & Negro J. J. (eds.) Birds of Prey. Biology and conservation in the XXI. century Springer pp. 3–32.

  • Møller A. P. & Garamszegi L. Z. 2012. Sexual selection range size and population size. – Ornis Hungarica 20(1): 1–25. DOI: 10.2478/orhu-2013-0001

  • Moreno-Opo R. Margalida A. Arredondo A. Guil F. Martín M. Higuero R. & Guzman J. 2010. Factors influencing the presence of the Cinereous Vulture Aegypius monachus at carcasses: food preferences and implications for the management of supplementary feeding sites. – Wildlife Biology 16(1): 25–35. DOI: 10.2981/09-037

  • Mueller H. C. 1990. The evolution of reversed sexual dimorphism in size in monogamous species of birds. – Biological Reviews 65: 553–585. DOI: 10.1111/j.1469-185X.1990.tb01238.x

  • Nagy J. & Tökölyi J. 2014. Phylogeny historical biogeography and the evolution of migration in accipitrid birds of prey (Aves: Accipitriformes). – Ornis Hungarica 22(1): 15–35. DOI: 10.2478/orhu-2014-0008

  • Newton I. 1978. Feeding and development of Sparrowhawk Accipiter nisus nestlings. – Journal of Zoology 184(4): 65–487. DOI: 10.1111/j.1469-7998.1978.tb03302.x

  • O’Rourke C. T. Hall M. I. Pitlik T. & Fernández-Juricic E. 2010. Hawk eyes I: diurnal raptors differ in visual fields and degree of eye movement. – PLoS One 5(9): e12802. DOI: 10.1371/journal.pone.0012802

  • Owens I. P. F. & Hartley I. R. 1998. Sexual dimorphism in birds: why are there so many different forms of dimorphism? – Proceedings of the Royal Society B 265: 397–407. DOI: 10.1098/rspb.1998.0308

  • Pecsics T. Laczi M. Nagy G. & Csörgő T. 2017. The cranial morphometrics of the wildfowl (Anatidae). – Ornis Hungarica 25(1): 44–57. DOI: 10.1515/orhu-2017-0004

  • Pecsics T. Laczi M. Nagy G. Kondor T. & Csörgő T. 2018. Analysis of skull morphometric characters in Owls (Strigiformes). – Ornis Hungarica 26(1): 41–53. DOI: 10.1515/orhu-2018-0003

  • Pomichal K. Vági B. & Csörgő T. 2014. A case study on the phylogeny and conservation of Saker Falcon. – Ornis Hungarica 22(1): 1–14. DOI: 10.2478/orhu-2014-0007

  • Prum R. O. Berv J. S. Dornburg A. Field D. J. Townsend J. P. Lemmon E. M. & Lemmon A. R. 2015. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. – Nature 526(7574): 569–573. DOI: 10.1038/nature15697

  • Puzović S. 2008. Nest occupation and prey grabbing by Saker Falcon (Falco cherrug) on power lines in the province of Vojvodina (Serbia). – Archives of Biological Sciences 60(2): 271–277. DOI: 10.2298/ABS0802271P

  • Rohlf F. J. 2010. TpsDig version 2.16. – Department of Ecology and Evolution State University of New York Stony Brook USA

  • Schüz E. & König C. 1983. Old World vultures and man. – In: Wilbur S. R. & Jackson J. A. (eds.) Vulture biology and management. – Berkley Los Angeles: University of California Press University of California Press pp. 461–496.

  • Si G. Dong Y. Ma Y. & Zhang Z. 2015. Shape similarities and differences on the skull of scavenging raptors. – Zoological Science 32(2): 171–177. DOI: 10.2108/zs130253

  • Sulkava S. Tornberg R. & Koivusaari J. 1997. Diet of the White-tailed Eagle Haliaeetus albicilla in Finland. – Ornis Fennica 74(2): 65–78.

  • Sun Y. Si G. Wang X. Wang K. & Zhang Z. 2018. Geometric morphometric analysis of skull shape in the Accipitridae. – Zoomorphology 137: 445–456. DOI: 10.1007/s00435-018-0406-y

  • Sustaita D. & Hertel F. 2010. In vivo bite and grip forces morphology and prey-killing behavior of North American accipiters (Accipitridae) and falcons (Falconidae). – Journal of Experimental Biology 213(15): 2617–2628. DOI: 10.1242/jeb.041731

  • Szövényi G. 2015. Orthopteran insects as potential and preferred preys of the Red-footed Falcon (Falco vespertinus) in Hungary. – Ornis Hungarica 23(1): 48–57. DOI: 10.1515/orhu-2015-0004

  • Tóth L. 2014. Numerical response of the Common Buzzard Buteo buteo to the changes in abundance of small mammals. – Ornis Hungarica 22(1): 48–56. DOI: 10.2478/orhu-2014-0010

  • Van der Meij M. A. A. & Bout R. G. 2004. Scaling of jaw muscle size and maximal bite force in finches. – Journal of Experimental Biology 207(16): 2745–2753. DOI: 10.1242/jeb.01091

  • Verwaijen D. Van Damme R. & Herrel A. 2002. Relationships between head size bite force prey handling efficiency. – Functional Ecology 16(6): 842–850. DOI: 10.1046/j.1365-2435.2002.00696.x

  • Ward A. B. Weigl P. D. & Conroy R. M. 2002. Functional morphology of raptor hindlimbs: implications for resource partitioning. – The Auk 119(4): 1052–1063.

  • Yuri T. Kimball R. T. Harshman J. Bowie R. C. Braun M. J. Chojnowski J. L. Han K-L. Hackett S. J. Huddleston Ch. J. Moore W. S. Reddy S. Sheldon F. H. Steadman D. W. Witt Ch. C. & Braun E. L. 2013. Parsimony and model-based analyses of indels in avian nuclear genes reveal congruent and incongruent phylogenetic signals. – Biology 2(1): 419–444. DOI: 10.3390/biology2010419

  • Zelditch M. Swiderski D. Sheets D. H. & Fink W. 2004. Geometric Morphometrics for Biologists: A primer. – Elsevier Academic Press Waltham MA.

  • Zusi R. L. 1993. Patterns of diversity in the avian skull. – In: Hanken J. & Hall B. K. The Skull Vol. 2. Patterns of Structural and Systematic Diversity. – University of Chicago Press pp. 391–437.

  • Zweers G. A. Berkhoudt H. & Berge J. V. 1994. Behavioral mechanisms of avian feeding. – In: Bels V. L. Chardon M. & Vandewalle P. 1994. Biomechanics of feeding in vertebrates. – Springer Berlin Heidelberg pp. 241–279.

Journal information
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 292 292 15
PDF Downloads 242 242 18