Evolution of olfaction in non-avian theropod dinosaurs and birds

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1725, 2011, Pages 3625-3634

  Zelenitsky, Darla K ^a   Therrien, François ^a,b   Ridgely, Ryan C ^c   McGee, Amanda R ^a   Witmer, Lawrence M ^c  

^a UNIVERSITY OF CALGARY   (Canada)

^b ROYAL TYRRELL MUSEUM OF PALAEONTOLOGY   (Canada)

^c OHIO UNIVERSITY   (United States)

Author keywords

Archaeopteryx; Aves; Basal birds; Olfactory bulb; Olfactory ratio; Theropoda

Indexed keywords

BIRD; CLADISTICS; CRETACEOUS; DINOSAUR; EVOLUTIONARY BIOLOGY; FLIGHT; FORAGING BEHAVIOR; FOSSIL RECORD; HYPOTHESIS TESTING; MASS EXTINCTION; OLFACTION; SURVIVAL; VISION;

ARCHAEOPTERYX; AVES; DINOSAURIA; THEROPODA;

EID: 80855129635     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0238     Document Type: Article

References (117)

1. Britt, B. B., Makovicky, P. J., Gauthier, J. & Bond, N. 1998 Postcranial pneumatization in Archaeopteryx. Nature 395, 374-376. (doi:10.1038/26469)
2. Currie, P. J. 1987 Bird-like characteristics of the jaws and teeth of troodontid theropods (Dinosauria, Saurischia). J. Vertebr. Paleontol. 7, 72-81. (doi:10.1080/02724634.1987.10011638)
3. Erickson, G. M., Rauhut, O. W. M., Zhou, Z., Turner, A. H., Inouye, B. D., Hu, D. & Norell, M. A. 2009 Was dinosaurian physiology inherited by birds? Reconciling slow growth in Archaeopteryx. PLoS ONE 4, e7390. (doi:10.1371/journal.pone.0007390)
4. Ji, Q., Currie, P. J., Norell, M. A. & Ji, A. 1998 Two feathered dinosaurs from northeastern China. Nature 393, 753-761. (doi:10.1038/31635)
5. Kurochkin, E. N., Dyke, G. J., Saveliev, S. V., Pervushov, E. M. & Popov, E. V. 2007 A fossil brain from the Cretaceous of European Russia and avian sensory evolution. Biol. Lett. 3, 309-313. (doi:10.1098/ rsbl.2006.0617)
6. Norell, M. A., Clark, J. M., Chiappe, L. M. & Dashzeveg, D. 1995 A nesting dinosaur. Nature 378, 774-776. (doi:10.1038/378774a0)
7. Norell, M. A., Makovicky, P. J. & Clark, J. M. 1997 A Velociraptor wishbone. Nature 389, 447. (doi:10.1038/ 38918)
8. O'Connor, P. M. & Claessens, L. P. A. M. 2005 Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs. Nature 436, 253-256. (doi:10.1038/nature03716)
9. Ostrom, J. H. 1976 Archaeopteryx and the origin of birds. Biol. J. Linn. Soc. 8, 91-182. (doi:10.1111/j. 1095-8312.1976.tb00244.x)
10. Sato, T., Cheng, Y., Wu, X., Zelenitsky, D. K. & Hsiao, Y. 2005 A pair of shelled eggs inside mother dinosaur. Science 308, 375. (doi:10.1126/science.1110578)
11. Varricchio, D. J., Jackson, F., Borkowski, J. J. & Horner, J. R. 1997 Nest and egg clutches of the dinosaur Troodon formosus and the evolution of avian reproductive traits. Nature 385, 247-250. (doi:10.1038/385247a0)
12. Varricchio, D. J., Moore, J. R., Erickson, G. M., Norell, M. A., Jackson, F. D. & Borkowski, J. J. 2008 Avian paternal care had dinosaur origin. Science 322, 1826-1828. (doi:10.1126/science.1163245)
13. Xu, X. & Norell, M. A. 2004 A new troodontid dinosaur from China with avian-like sleeping posture. Nature 431, 838-841. (doi:10.1038/nature02898)
14. Xu, X., Zhou, Z.-H. & Prum, R. O. 2001 Branched integumental structures in Sinornithosaurus and the origin of feathers. Nature 410, 200-204. (doi:10.1038/ 35065589)
15. Domínguez Alonso, P., Milner, A. C., Ketcham, R. A., Cookson, M. J. & Rowe, T. B. 2004 The avian nature of the brain and inner ear of Archaeopteryx. Nature 430, 666-669. (doi:10.1038/nature02706)
16. Milner, A. C. & Walsh, S. A. 2009 Avian brain evolution: new data from palaeogene birds (Lower Eocene) from England. Zool. J. Linn. Soc. 155, 198-219. (doi:10.1111/j.1096-3642.2008.00443.x)
17. Walsh, S. & Milner, A. 2010 Halcyornis toliapicus (Aves: Lower Eocene, England) indicates advanced neuromorphology in Mesozoic Neornithes. J. Syst. Paleontol. 9, 173-181.
18. Turner, C. H. 1892 A few characteristics of the avian brain. Science 19, 16-17 (doi:10.1126/science.ns-19. 466.16)
19. Edinger, T. 1951 The brains of the Odontognathae. Evolution 5, 6-24. (doi:10.2307/2405427)
20. Pearson, R. 1972 The avian brain. London, UK: Academic Press.
21. Wenzel, B. M. 1971 Olfaction in birds. In Handbook of sensory physiology (ed. L. M. Beidler), pp. 432-448. New York, NY: Springer-Verlag.
22. Caro, S. P. & Balthazart, J. 2010 Pheromones in birds: myth or reality? J. Comp. Physiol. A 196, 751-766. (doi:10.1007/s00359-010-0534-4)
23. Hagelin, J. C. & Jones, I. L. 2007 Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 124, 741-761. (doi:10.1642/0004-8038(2007)124 [741:BOAOCS]2.0.CO;2)
24. Roper, T. J. 1999 Olfaction in birds. In Advances in the study of behavior (eds P. J. B. Slater, J. S. Rosenblatt, C. T. Snowden & T. J. Roper), pp. 247-332. New York, NY: Academic Press.
25. Bang, B. G. & Cobb, S. 1968 The size of the olfactory bulb in 108 species of birds. Auk 85, 55-61.
26. Bang, B. G. & Wenzel, B. M. 1985 Nasal cavity and olfactory system. In Form and function in birds (eds A. S. King & J. McLelland), pp. 195-225. New York, NY: Academic Press.
27. Cobb, S. 1960 A note on the size of the avian olfactory bulbs. Epilepsia 1, 394-402. (doi:10.1111/j.1528-1157. 1959.tb04276.x)
28. Bang, B. G. 1971 Functional anatomy of the olfactory system in 23 orders of birds. Acta Anat. 58, 1-76.
29. Wenzel, B. M. & Meisami, E. 1987 Number, size, and density of mitral cells in the olfactory bulbs of the northern fulmar and rock dove. In Olfaction and taste (eds S. Roper & J. Atema), pp. 700-702. New York, NY: Annals of the New York Academy of Sciences.
30. Brochu, C. A. 2000 A digitally-rendered endocast for Tyrannosaurus rex. J. Vertebr. Paleontol. 20, 1-6. (doi:10.1671/0272-4634(2000)020[0001:ADREFT]2. 0.CO;2)
31. Franzosa, J. W. 2004 Evolution of the brain in Theropoda (Dinosauria). PhD thesis, University of Texas at Austin, Austin, TX, USA.
32. Witmer, L. M. & Ridgely, R. C. 2009 New insights into the brain, braincase, and ear region of tyrannosaurs, with implications for sensory organization and behavior. Anat. Rec. 292, 1266-1296. (doi:10.1002/ar.20983)
33. Zelenitsky, D. K., Therrien, F. & Kobayashi, Y. 2009 Olfactory acuity in theropods: palaeobiological and evolutionary implications. Proc. R. Soc. B 276, 667-673. (doi:10.1098/rspb.2008.1075)
34. Edinger, L. 1908 The relations of comparative anatomy to comparative psychology. J. Comp. Neurol. 18, 437-457. (doi:10.1002/cne.920180502)
35. Jerison, H. J. 1973 Evolution of the brain and intelligence. New York, NY: Academic Press.
36. Buschhüter, D., Smitka, M., Puschmann, S., Gerber, J. C., Witt, M., Abolmaali, N. D. & Hummel, T. 2008 Correlation between olfactory bulb volume and olfactory function. Neuroimage 42, 498-502. (doi:10.1016/ j.neuroimage.2008.05.004)
37. Clark, L., Avilova, K. V. & Beans, N. J. 1993 Odor thresholds in passerines. Comp. Biochem. Physiol. A 104, 305-312. (doi:10.1016/0300-9629(93)90322-U)
38. Hammock, J. 2005 Structure, function and context: the impact of morphometry and ecology on olfactory sensitivity. PhD thesis, Massachusetts Institutie of Technology, Boston, MA, USA.
39. Mackay-Sim, A. & Royet, J. P. 2006 Structure and function of the olfactory system. In Olfaction and the brain (eds W. Brewer, D. Castle & C. Pantelis), pp. 3-27. Cambridge, UK: Cambridge University Press.
40. Mori, K., Nagao, H. & Yoshihara, Y. 1999 The olfactory bulb: coding and processing of odor molecule information. Science 286, 711-715. (doi:10.1126/science. 286.5440.711)
41. Steiger, S. S., Fidler, A. E. & Kempenaers, B. 2009 Evidence for increased olfactory receptor gene repertoire size in two nocturnal bird species with welldeveloped olfactory ability. BMC Evol. Biol. 9, 117. (doi:10.1186/1471-2148-9-117)
42. Steiger, S. S., Fidler, A. E., Valcu, M. & Kempenaers, B. 2008 Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? Proc. R. Soc. B 275, 2309-2317. (doi:10.1098/rspb.2008.0607)
43. Larsson, H. C. E., Sereno, P. C. & Wilson, J. A. 2000 Forebrain enlargement among nonavian theropod dinosaurs. J. Vertebr. Paleontol. 20, 615-618. (doi:10.1671/ 0272-4634(2000)020[0615:FEANTD]2.0.CO;2)
44. Portmann, A. 1947 Etudes sur la ce ́re ́bralisation chez les oiseaux. Alauda 15, 1-15.
45. Pontzer, H. 2007 Effective limb length and the scaling of locomotor cost in terrestrial animals. J. Exp. Biol. 210, 1752-1761. (doi:10.1242/jeb.002246)
46. Tickle, P., Nudds, R. & Codd, J. 2009 Uncinate process length in birds scales with resting metabolic rate. PLoS ONE 4, e5667. (doi:10.1371/journal.pone.0005667)
47. Head, J. J., Bloch, J. I., Hastings, A. K., Bourque, J. R., Cadena, E. A., Herrera, F. A., Polly, P. D. & Jaramillo, C. A. 2009 Giant boid snake from the Palaeocene neotropics reveals hotter past equatorial temperatures. Nature 457, 715-717. (doi:10.1038/nature07671)
48. Sánchez-Villagra, M. R., Aguilera, O. & Horovitz, I. 2003 The anatomy of the world's largest extinct rodent. Science 301, 1708-1710. (doi:10.1126/science. 1089332)
49. Hamano, K., Iwasaki, N., Takeya, T. & Takita, H. 1993 A comparative study of linear measurement of the brain and three-dimensional measurement of brain volume using CT scans. Pediatr. Radiol. 23, 165-168. (doi:10. 1007/BF02013822)
50. Whalley, H. C. & Wardlaw, J. M. 2001 Accuracy and reproducibility of simple cross-sectional linear and area measurements of brain structures and their comparison with volume measurements. Neuroradiology 43, 263-271. (doi:10.1007/s002340000437)
51. Ali, F., Zelenitsky, D. K., Therrien, F. & Weishampel, D. B. 2008 Homology of the 'ethmoid complex' of tyrannosaurids and its implications for the reconstruction of the olfactory apparatus of non-avian theropods. J. Vertebr. Paleontol. 28, 123-133. (doi:10.1671/0272-4634(2008)28[123:HOTECO]2.0.CO;2)
52. Hagelin, J. C. 2004 Observations on the olfactory ability of the Kakapo Strigops habroptilus, the critically endangered parrot of New Zealand. Ibis 146, 161-164. (doi:10.1111/j.1474-919X.2004.00212.x)
53. Iwaniuk, A. N. & Nelson, J. E. 2002 Can endocranial volume be used as an estimate of brain size in birds? Can. J. Zool. 80, 16-23. (doi:10.1139/z01-204)
54. Witmer, L. M., Chatterjee, S., Franzosa, J. & Rowe, T. 2003 Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425, 950-953. (doi:10.1038/nature02048)
55. Dunning Jr, J. B. 2008 CRC handbook of avian body masses, 2nd edn. Boca Raton, FL: CRC Press.
56. Paige, H. D., Anderson, J. F. & Rahn, H. 1979 Scaling of skeletal mass to body mass in birds and mammals. Am. Nat. 113, 103-122. (doi:10.1086/283367)
57. Hinić-Frlog, S. & Motani, R. 2010 Relationship between osteology and aquatic locomotion in birds: determining modes of locomotion in extinct Ornithurae. J. Evol. Biol. 23, 372-385. (doi:10.1111/j.1420-9101. 2009.01909.x)
58. Therrien, F. & Henderson, D. M. 2007 My theropod is bigger than yours or not: estimating body size from skull length in theropods. J. Vertebr. Paleontol. 27, 108-115. (doi:10.1671/0272-4634(2007)27[108: MTIBTY]2.0.CO;2)
59. Smith, R. J. 1999 Statistics of sexual size dimorphism. J. Hum. Evol. 36, 423-459. (doi:10.1006/jhev.1998. 0281)
60. Felsenstein, J. 1985 Phylogenies and the comparative method. Am. Nat. 125, 1-15. (doi:10.1086/284325)
61. Midford, P. E., Garland Jr, T. & Maddison, W. P. 2008. PDAP package of MESQUITE, v. 1.13. See http://mesquiteproject.org/pdap_mesquite/index.html.
62. Maddison, W. P. & Maddison, D. R. 2008. MESQUITE: a modular system for evolutionary analysis, v. 2.5. See http://mesquiteproject.org.
63. Garland Jr, T., Dickerman, A. W., Janis, C. M. & Jones, J. A. 1993 Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42, 265-292.
64. Hackett, S. J. et al. 2008 A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763-1768. (doi:10.1126/science.1157704)
65. Livezey, B. C. & Zusi, R. L. 2007 Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zool. J. Linn. Soc. 149, 1-95. (doi:10. 1111/j.1096-3642.2006.00293.x)
66. Baker, A. J., Pereira, S. L. & Paton, T. A. 2007 Phylogenetic relationships and divergence times of Charadriiformes genera: multigene evidence for the Cretaceous origin of at least 14 clades of shorebirds. Biol. Lett. 3, 205-210. (doi:10.1098/rsbl.2006.0606)
67. Benz, B. W., Robbins, M. B. & Peterson, A. T. 2006 Evolutionary history of woodpeckers and allies (Aves: Picidae): placing key taxa on the phylogenetic tree. Mol. Phylogenet. Evol. 40, 389-399. (doi:10.1016/j. ympev.2006.02.021)
68. Donne-Gousse, C., Laudet, V. & Hanni, C. 2002 A molecular phylogeny of Anseriformes based on mitochondrial DNA analysis. Mol. Phylogenet. Evol. 23, 339-356. (doi:10.1016/S1055-7903(02)00019-2)
69. Ericson, P. G. P. et al. 2006 Diversification of Neoaves: integration of molecular sequence data and fossils. Biol. Lett. 2, 543-547. (doi:10.1098/rsbl.2006.0523)
70. Ericson, P. G. P., Jansen, A.-L., Johansson, U. S. & Ekman, J. 2005 Inter-generic relationships of the crows, jays, magpies and allied groups (Aves: Corvidae) based on nucleotide sequence data. J. Avian Biol. 36, 222-234. (doi:10.1111/j.0908-8857.2001.03409.x)
71. Ericson, P. G. P. & Johansson, U. S. 2003 Phylogeny of Passerida (Aves: Passeriformes) based on nuclear and mitochondrial sequence data. Mol. Phylogenet. Evol. 29, 126-138. (doi:10.1016/S1055-7903(03)00067-8)
72. Griffiths, C. S., Barrowclough, G. F., Groth, J. G. & Mertz, L. A. 2007 Phylogeny, diversity, and classification of the Accipitridae based on DNA sequences of the RAG-1 exon. J. Avian Biol. 38, 587-602. (doi:10. 1111/j.2007.0908-8857.03971.x)
73. Jonsson, K. A. & Fjeldsa, J. 2006 A phylogenetic supertree of oscine passerine birds (Aves: Passeri). Zool. Scr. 35, 149-186. (doi:10.1111/j.1463-6409. 2006.00221.x)
74. Kennedy, M. & Page, R. D. M. 2002 Seabird supertrees: combining partial estimates of procellariiform phylogeny. Auk 119, 88-108. (doi:10.1642/0004-8038(2002)119[0088:SSCPEO]2.0.CO;2)
75. Kennedy, M., Valle, C. A. & Spencer, H. G. 2009 The phylogenetic position of the Galápagos cormorant. Mol. Phylogenet. Evol. 53, 94-98. (doi:10.1016/j.ympev. 2009.06.002)
76. Lee, P. L. M., Clayton, D. H., Griffiths, R. & Page, R. D. M. 1996 Does behavior reflect phylogeny in swiftlets (Aves: Apodidae)? A test using cytochrome b mitochondrial DNA sequences. Proc. Natl Acad. Sci. USA 96, 7091-7096. (doi:10.1073/pnas.93.14.7091)
77. Livezey, B. C. 1998 A phylogenetic analysis of the Gruiformes (Aves) based on morphological characters with an emphasis on the rails (Rallidae). Phil. Trans. R. Soc. Lond. B 353, 2077-2151. (doi:10.1098/rstb.1998. 0353)
78. Nunn, G. B. & Stanley, S. E. 1998 Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Mol. Biol. Evol. 15, 1360-1371.
79. Payne, R. B. 2005 The cuckoos. New York, NY: Oxford University Press.
80. Reddy, S. & Cracraft, J. 2007 OldWorld shrike-babblers (Pteruthius) belong with New World vireos (Vireonidae). Mol. Phylogenet. Evol. 44, 1352-1357. (doi:10.1016/j. ympev.2007.02.023)
81. Trewick, S. A. 1997 Flightlessness and phylogeny amongst endemic rails (Aves: Rallidae) of the New Zealand region. Phil. Trans. R. Soc. Lond. B 352, 429-446. (doi:10.1098/rstb.1997.0031)
82. Wright, T. F. et al. 2008 A multilocus molecular phylogeny of the parrots (Psittaciformes): support for a Gondwanan origin during the Cretaceous. Mol. Biol. Evol. 20, 2141-2156. (doi:10.1093/molbev/ msn160)
83. Ericson, P. G. P. 2000 Systematic revision, skeletal anatomy, and paleoecology of the New World early Tertiary Presbyornithidae (Aves: Anseriformes). Paleobios 20, 1-23.
84. Zhou, Z. & Li, F. Z. Z. 2010 A new Lower Cretaceous bird from China and tooth reduction in early avian evolution. Proc. R. Soc. B 277, 219-227. (doi:10. 1098/rspb.2009.0885)
85. Dyke, G. & Van Tuinen, D. 2004 The evolutionary radiation of modern birds (Neornithes): reconciling molecules, morphology and the fossil record. Zool. J. Linn. Soc. 148, 153-177. (doi:1111/j.1096- 3642.2004.00118.x)
86. Csiki, Z., Vremir, M., Brusatte, S. L. & Norell, M. A. 2010 An aberrant island-dwelling theropod dinosaur from the Late Cretaceous of Romania. Proc. Natl Acad. Sci. USA 107, 15 357-15 361. (doi:10.1073/ pnas.1006970107)
87. Bang, B. G. 1960 Anatomical evidence for olfactory function in some species of birds. Nature 188, 547-549. (doi:10.1038/188547a0)
88. Hutchison, L. V. & Wenzel, B. M. 1980 Olfactory guidance in foraging by procellariiforms. Condor 82, 314-319. (doi:10.2307/1367400)
89. Stager, K. E. 1964 The role of olfaction in food location by the turkey vulture, Cathartes aura. Los Angeles Co. Mus. Contrib. Sci. 81, 1-63.
90. Gagliardo, A., Ioalé, P., Savini, M. & Wild, M. 2008 Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young. J. Exp. Biol. 211, 2046-2051. (doi:10. 1242/jeb.017608)
91. Jorge, P. E., Marques, P. A. M. & Phillips, J. B. 2009 Activational effects of odours on avian navigation. Proc. R. Soc. B 276, 45-49. (doi:10.1098/rspb.2009. 1521)
92. Papi, F. 1976 The olfactory navigation system of the homing pigeon. Verh. Dtsch. Zool. Ges. 69, 184-205.
93. Papi, F. 1990 Olfactory navigation in birds. Experientia 46, 352-363. (doi:10.1007/BF01952168)
94. Wallraff, H. G. 1982 The homing mechanism of pigeons. Nature 300, 293-294. (doi:10.1038/300293a0)
95. Berger, C. 2003 Sphenisciformes (Penguins). In Grzimek's animal life encyclopedia: birds I, vol. 8 (eds M. Hutchins, J. A. Jackson, W. J. Brock & D. Olendorf), pp. 147-158, 2nd edn. Farmington Hills, MI: Gale Group.
96. Hosner, P. 2003 Gaviiformes (Loons). In Grzimek's animal life encyclopedia: birds I vol. 8 (eds M. Hutchins, J. A. Jackson, W. J. Brock & D. Olendorf), pp. 159-167, 2nd edn. Farmington Hills, MI: Gale Group.
97. Grubb,T. C. 1972 Smell and foraging in shearwaters and petrels. Nature 237, 404-405. (doi:10.1038/237404a0)
98. Grubb, T. C. 1974 Olfactory navigation to the nesting burrow in Leach's petrel (Oceanodroma leucorhoa). Anim. Behav. 22, 192-202. (doi:10.1016/S0003- 3472(74)80069-2)
99. Lequette, B., Verheyden, C. & Jouventin, P. 1989 Olfaction in subantarctic seabirds: its phylogenetic and ecological significance. Condor 91, 732-735. (doi:10. 2307/1368131)
100. Nevitt, G. A., Losekoot, M. & Weimerskirch, H. 2008 Evidence for olfactory search in wandering albatross (Diomedea exulans). Proc. Natl Acad. Sci. USA 105, 4576-4581. (doi:10.1073/pnas.0709047105)
101. Verheyden, C. & Jouventin, P. 1994 Olfactory behavior of foraging procellariiforms. Auk 111, 285-291.
102. Nevitt, G. A., Veit, R. R. & Kareiva, P. 1995 Dimethyl sulphide as a foraging cue for Antarctic procellariiform seabirds. Nature 376, 681-682. (doi:10.1038/ 376680a0)
103. Grubb, T. C. 1973 Colony location by Leach's petrel. Auk 90, 78-82.
104. Grubb, T. C. 1979 Olfactory guidance of Leach's storm petrel to the breeding island. Wilson Bull. 91, 141-143.
105. Benham, W. B. 1906 The olfactory sense in Apteryx. Nature 74, 222-223. (doi:10.1038/074222b0)
106. Cunningham, S. J., Castro, I. & Potter, M. A. 2009 The relative importance of olfaction and remote touch in prey detection by North Island brown kiwis. Anim. Behav. 78, 899-905. (doi:10.1016/j.anbehav.2009. 07.015)
107. Wenzel, B. M. 1968 Olfactory prowess of the kiwi. Nature 220, 1133-1134. (doi:10.1038/2201133a0)
108. Davies, S. J. J. F. 2002 Ratites and tinamous. New York, NY: Oxford University Press.
109. Martin, G. R. & Katzir, G. 1995 Visual fields in ostriches. Nature 374, 19-20. (doi:10.1038/374019a0)
110. Bonadonna, F. & Bretagnolle, V. 2002 Smelling home: a good solution for burrow-finding in nocturnal petrels? J. Exp. Biol. 205, 2519-2523.
111. Bonadonna, F., Cunningham, G. B., Jouventin, P., Hesters, F. & Nevitt, G. A. 2003 Evidence for nestodour recognition in two species of diving petrel. J. Exp. Biol. 206, 3719-3722. (doi:10.1242/jeb.00610)
112. Jouventin, P., Mouret, V. & Bonadonna, F. 2007 Wilson's storm petrels Oceanites oceanicus recognise the olfactory signature of their mate. Ethology 113, 1228-1232. (doi:10.1111/j.1439-0310.2007.01444.x)
113. Martin, G., Rojas, L. M., Ramirez, Y. & McNeil, R. 2004 The eyes of oilbirds (Steatornis caripensis): pushing at the limits of sensitivity. Naturwissenschaften 91, 26-29. (doi:10.1007/s00114-003-0495-3)
114. Emery, N. J. 2006 Cognitive ornithology: the evolution of avian intelligence. Phil. Trans. R. Soc. B 361, 23-43. (doi:10.1098/rstb.2005.1736)
115. Lefebvre, L., Nicolakakis, N. & Boire, D. 2002 Tools and brains in birds. Behaviour 139, 939-973. (doi:10. 1163/156853902320387918)
116. Lefebvre, L., Whittle, P., Lascaris, E. & Finkelstein, A. 1997 Feeding innovations and forebrain size in birds. Appl. Anim. Behav. Sci. 53, 549-560.
117. Timmermans, S., Lefebvre, L., Boire, D. & Basu, P. 2000 Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav. Evol. 56, 196-203. (doi:10.1159/ 000047204)