Electronic Supplementary Material - Zelenitsky et al.
Relationships between olfactory ratio and general habits in birds
Early work on olfactory ratios in birds revealed associations between olfactory ratio and
foraging, diet, nesting, or breeding habits (Cobb 1960; Bang 1971; Bang & Wenzel 1985),
although lacked rigorous statistical analyses. A subsequent study (Healy & Guilford 1990)
attempted to examine statistical correlations between olfactory bulb length (not olfactory ratio)
and general habits (activity timing, diet, nest type, development, nest dispersion, migratory
behaviour) of birds and found a significant correlation only between olfactory bulb length and
activity timing (nocturnality and crepuscularity). Although Healy & Guilford (1990) conducted
statistical analyses of olfactory bulb length in relation to general habits of birds, they did not
truly test the associations between olfactory bulb size and ecological parameters established by
Cobb (1960) and Bang (1971). Even though Healy & Guilford (1990) may have used the
olfactory bulb lengths of species reported by Cobb (1960) and Bang (1971), they averaged these
values to the family level to address the phylogenetic relationships of taxa in their analyses, an
approach now considered invalid (Martins & Garland 1991). Furthermore, they used different
parameters (e.g., development, migratory behavior) and different groupings within a given
parameter from those established by Bang (1971). For example, Healy & Guilford’s (1990) diet
categories (fruit, foliage, invertebrates, lower vertebrates, plant material + invertebrates,
invertebrates + lower vertebrates + higher vertebrates + carrion) were distinctly different from
Bang’s (1971) diet categories (carnivorous + piscivorous, vegetarian + frugivorous,
insectivorous, granivorous, omnivorous). Therefore, the fact that Healy & Guilford (1990) used
different parameters (and different categories within these parameters) than those used by Bang
(1971) could explain, in part, the difference in correlation/relationships between olfactory bulb
size and ecological parameters between these two studies.
Data Analysis and Acquisition
Justification for use of olfactory ratios in theropods: Olfactory ratios rather than volumes were
used to quantify olfactory bulb size in extinct theropods because: 1) volumetric data cannot be
obtained from specimens that are incomplete or the sphenethmoid is unossified (in
maniraptoriforms); and 2) olfactory ratios have been used widely for birds in the literature, and
are the standard for the quantification of olfactory bulb size in behavioural studies (e.g., Bang &
Wenzel, 1985; Healy & Guilford 1990; Verheyden & Jouventin 1994; Steiger et al. 2008).
Changes in cerebral hemisphere size through theropod evolution (Larsson et al. 2000; Larsson
2001) could be used as an argument to invalidate the use of olfactory ratios based on the
assumptions that: 1) changes were restricted to the cerebral hemispheres and were not mirrored
in the olfactory apparatus; and 2) the same cerebral hemisphere dimension (e.g. length) is
compared among all taxa, such that evolutionary changes in shape could be missed. Whereas
there is no published study supporting or falsifying the first assumption, the use of the greatest
cerebral diameter, regardless of its dimension (length, width, and depth), allows for some of the
cerebral morphological differences between taxa to be accounted. As such, olfactory ratios can
reasonably be used as a proxy for the importance of olfaction relative to other senses irrespective
of whether changes occur in olfactory bulb size (i.e numerator of ratio) or in cerebral
hemisphere size (i.e. denominator of ratio).
Olfactory ratio calculations: Olfactory ratios were obtained from absolute measurements of
braincases, endocasts, or from measurements of CT-scan slices. Ratios were also determined
from illustrations of three-dimensional digital reconstructions of the endocranial cavity. For the
latter, linear dimensions were acquired from the same aspect (i.e. dorsal or lateral view) of the
endocast without conversion to original dimensions (in cm) in order to avoid errors due to
imprecision of scale bars. Thus, although the true dimensions of the endocranial cavity were not
determined for illustrations, the proportion between the olfactory and cerebral regions is
accurate. Olfactory ratios obtained from illustrations produced results comparable to those
obtained from measurements on specimens/casts of related taxa, thus justifying their validity.
The source/specimen number of the olfactory ratio data is indicated under “catalogue number” in
Table S1.
Olfactory ratio calculations for some specimens require explanation due to specimen
preservation. The olfactory ratio of one of the Tyrannosaurus rex endocasts (AMNH 5029) may
be underestimated because the depth of the olfactory bulb is uncertain due to a missing
sphenethmoid. The olfactory ratios of Albertosaurus sarcophagus and Gorgosaurus libratus
were derived from fronto-parietal complexes that preserve neither the depth of the olfactory
bulbs nor the entire length of the cerebral hemispheres; consequently, these olfactory ratios
should be considered maximum values. In Troodon formosus, the insertion site of the
mesethmoid and olfactory bulb impressions on the frontals reveal that the olfactory bulbs
occupied approximately 60% of the total length of the olfactory fossa; consequently the length of
the olfactory fossa was adjusted proportionally to reflect the true length of the olfactory bulbs. In
Saurornitholestes langstoni, the posterior portion of the endocast is unknown; consequently, its
olfactory ratio should be considered an approximation.
Independent contrast methods: A branch length of one was assigned to the phylogeny for
independent contrasts (Figure S1). Albertosaurus and Gorgosaurus were not included in the
independent contrast analysis because of the uncertainty of their olfactory ratios and body
masses. For taxa in which several individuals were studied, specimens of Allosaurus (UUVP
5961), Tyrannosaurus rex (FMNH PR 2081), and Troodon (TMP 86.36.4) were considered
because either their body mass estimates were the least subject to uncertainty (Allosaurus and
Tyrannosaurus) or their olfactory ratio was close to the mean value of all individuals (Troodon).
Least-squares regression of the standardized, positivized independent contrasts of olfactory ratio
and body mass (slope = 0.1237, r = 0.87) is presented (Figure S2). To reconstruct the ancestral
state of the common ancestor of Dilong and tyrannosaurids, the tree was rerooted to place that
node at the base of the tree and the number of branch lengths deleted in the process was added to
the overlying branch, following the method of Garland et al. (1999).
Figure S1. Phylogeny used to calculate phylogenetic independent contrasts of olfactory ratio on
body mass for 19 theropod species. The topology of the tree was obtained from Holtz &
Osmólska (2004) and Kobayashi & Barsbold (2005). Numbers indicate nodes and tips.
Figure S2. Relationship between phylogenetic independent contrasts of the olfactory ratio on
body size for 19 theropod species. Numbers refer to the nodes in Figure S1.
Institutional abbreviations for Table S1.
AMNH, American Museum of Natural History, New York City, NY; BMNH, British Museum
of Natural History, London, UK; FMNH PR, Field Museum of Natural History, Chicago, IL;
GIN, Paleontological Center of Mongolia, Ulaan Bataar, Mongolia; IGM, Institute of Geology,
Mongolian Academy of Sciences, Ulaan Bataar, Mongolia; IVPP, Institute of Vertebrate
Paleontology and Paleoanthropology, Beijing, China; KUVP, Kansas University Natural History
Museum, Lawrence, KS; MUCPv-CH, Museo de la Universidad Nacional del Comahue, El
Chocón collection, Neuquén; MWC, Museum of Western Colorado, Fruita, CO; NMC, Canadian
Museum of Nature, Ottawa; OMNH, Oklahoma Museum of Natural History, Norman, OK; PIN,
Palaeontological Institute, Moscow; ROM, Royal Ontario Museum, Toronto, Ontario; SGM,
Ministère de l’Énergie et des Mines, Rabat, Morocco; TMP, Royal Tyrrell Museum of
Palaeontology, Drumheller, Alberta; UF, University of Florida, Gainesville, FL; UUVP,
University of Utah Museum of Natural History, Salt Lake City, UT; ZPAL, Institute of
Paleobiology of the Polish Academy of Sciences, Warsaw, Poland.
Table S1. Calculated olfactory ratios and body masses of theropod and crocodylian specimens
studied. Source is provided for specimens measured and when body mass is based on published
femur length or different specimens from endocasts. Body mass estimates for theropods are
based on femur length, following Christiansen and Fariña’s (2004) method, except for
Majungasaurus where a published estimate based on femur circumference is used; body mass
estimates for Alligator are based on skull length following Farlow et al.’s (2005) method.
Asterisk indicates maximum values as it was not possible to determine the full length of the
cerebral hemispheres and depth of the olfactory bulbs in Albertosaurus and Gorgosaurus
because measurements were made on frontoparietal complexes.
Taxon
Allosauroidea
Allosaurus fragilis
Acrocanthosaurus
atokensis
Carcharodontosaurus
saharicus
Giganotosaurus
carolinii
Ceratosauria
Ceratosaurus
magnicornis
Majungasaurus
crenatissimus
Tyrannosauroidea
Dilong paradoxus
Albertosaurus
sarcophagus
Catalogue
number/specimen
details
Olfactory
bulb/Cerebral
hemisphere
greatest
diameters
Olfactory
ratio (%)
Cast of UUVP
294
UUVP 5961
(Franzosa, 2004:
fig. 28)
OMNH 10146
(Franzosa and
Rowe, 2005: fig.
2)
SGM-Din 1
(endocast)
Length/Depth
51.6
50
Femur length
(mm)
Body mass (kg)
860 (UUVP
6000 in Paul,
1988)
1468.77
Length/Depth
58.1
~1153 (Stovall
and Langston,
1950)
3777.58
Depth/Length
56
~1450 (Sereno
et al., 1996)
7905.47
MUCPv-CH-1
(CT scan slices)
Length/Length
57.7
1430 (Sereno et
al., 1996)
7559.49
MWC 1 (Sanders
and Smith, 2005:
fig. 13)
FMNH PR 2100
(Sampson and
Witmer, 2007:
fig. 18)
Length/Length
48.1
538.86
Length/Length
48.3
630 (Madsen
and Welles,
2000)
Sampson and
Witmer (2007)
IVPP V14243
(CT scan slices)
TMP 81.9.1
(frontoparietal)
Length/Length
27
9.69
Length/Length*
71*
Length/Length*
68.5*
181 (Xu et al.,
2004)
1020 (ROM
807, Currie,
2003)
1040 (NMC
2120, Currie,
2003)
970 (PIN 551-3,
Paul, 1988)
Gorgosaurus libratus
TMP 67.14.3
(frontoparietal)
Tarbosaurus bataar
Cast of PIN
46104
Depth/Length
65.1
Tyrannosaurus rex
AMNH 5029
(subadult
endocast)
FMNH PR 2081
Depth/Length
66.5
71
980 (AMNH
30564, Erickson
et al., 2004)
1321 (Brochu,
1130
2545.13
2709.45
2164.60
2237.33
5855.30
(Brochu and
Ketcham, 2003:
digital endocast)
Ornithomimosauria
Garudimimus brevipes
2003)
GIN 100/13
(CT scan slices)
Length/Length
28.8
Ornithomimus
edmontonensis
TMP 95.110.1
(CT scan slices)
Length/Length
31.4
Dromiceiomimus
brevitertius
NMC 12228
(endocast)
Length/Length
29.4
468 (Russell,
1972)
206.79
Struthiomimus altus
TMP 90.26.1
(CT scan slices)
Length/Length
32.5
486
277.97
IGM 100/978
(Franzosa, 2004:
fig. 30)
Depth/Length
31.5
~405 (IGM
100/1004, G.M.
Erickson
personal
communication
2008)
129.78
TMP 74.10.5
(endocast)
Length/Length
34.8
214
16.62
KUVP 129737
(Burnham, 2004:
fig. 3.2)
GIN 100/24
(CT scan slices)
Length/Length
28.5
118 (Burnham,
2004)
2.44
Length/Length
35.7
200 (GIN
100/25, Paul,
1988)
13.36
TMP 79.8.1
TMP 86.36.4
NMC 12340
AMNH 6174
(frontoparietals)
Length/Length
33.2
33.5
32.6
33
320 (MOR 748,
D.J. Varricchio
personal
communication
2008)
60.76
BMNH 37001
(Dominguez
Alonso et al.,
2004: fig. 3)
Length/Length
17.1
60.5 (Paul,
1988)
0.28
Oviraptoridae
Citipati osmolskae
Dromaeosauridae
Saurornitholestes
langstoni
Bambiraptor feinbergi
Velociraptor
mongoliensis
Troodontidae
Troodon formosus
Aves
Archaeopteryx
lithographica
Alligatoridae
Alligator
mississippiensis
UF 98341
UF 105541
UF 87885
Length/Depth
49.8
54.3
55.1
371 (Kobayashi
and Barsbold,
2005)
426
Skull length
(mm)
434
367.5
311.5
97.84
152.74
161.60
90.60
50.90
(braincases)
References
Bang, B. G. 1971. Functional anatomy of the olfactory system in 23 orders of birds. Acta Anat.
79, 1-76.
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.
Brochu, C. A. 2003. Osteology of Tyrannosaurus rex: Insights from a nearly complete skeleton
and high-resolution computed tomographic analysis of the skull. J. Vert. Paleont. 22 (Suppl.,
Memoir 7), 1-138.
Brochu, C. A. & Ketcham, R. A. 2003. Computed tomographic analysis of the Tyrannosaurus
rex skull. Society of Vertebrate Paleontology Memoir 7:CD-ROM.
Burnham, D. A. 2004. New information on Bambiraptor feinbergi (Theropoda:
Dromaeosauridae) from the Late Cretaceous of Montana. In Feathered dragons: Studies on
the transition from dinosaurs to birds (eds P. J. Currie, E. B. Koppelhus, M. A. Shugar & J.
L. Wright), pp. 67-111. Bloomington, IN: Indiana University Press.
Christiansen, P. & Fariña. R. A. 2004. Mass prediction in theropod dinosaurs. Hist. Biol. 16, 8592.
Cobb, S. 1960. A note on the size of the avian olfactory bulbs. Epilepsia 1, 394-402.
Currie, P. J. 2003. Allometric growth in tyrannosaurids (Dinosauria: Theropoda) from the Upper
Cretaceous of North America and Asia. Can. J. Earth Sci. 40, 651-665.
Dominguez Alonso, P. D., 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.
Erickson, G. M., Makovicky, P. J., Currie, P. J., Norell, M. A., Yerby, S. A. & Brochu, C. A..
2004. Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature
430, 772-775.
Farlow, J. O., Hurlburt, G. R., Elsey, R. M., Britton, A. R. C. & Langston, Jr., W. 2005. Femoral
dimensions and body size of Alligator mississippiensis: Estimating the size of extinct
mesoeucrocodylians. J. Vert. Paleont. 25, 354-369.
Franzosa, J. W. 2004. Evolution of the brain in Theropoda (Dinosauria). Ph.D. dissertation,
University of Texas at Austin, Austin, Texas.
Franzosa, J. & Rowe ,T. 2005. Cranial endocast of the Cretaceous theropod dinosaur
Acrocanthosaurus atokensis. J. Vert. Paleont. 25, 859-864.
Garland, T., Jr., Midford, P. E. & Ives, A. R. 1999. An introduction to phylogenetically based
statistical methods, with a new method for confidence intervals on ancestral values. Amer.
Zool. 39, 374-388.
Healy, S., & Guilford, T. 1990. Olfactory-bulb size and nocturnality in birds. Evolution 44, 339346.
Holtz, T. J., Jr. & Osmólska, H. 2004. Saurischia. In The Dinosauria, 2nd edition (eds D. B.
Weishampel, P. Dodson & H. Osmólska), pp. 21-24. Berkeley, CA: University of California
Press.
Kobayashi, Y. & Barsbold, R. 2005. Reexamination of a primitive ornithomimosaur,
Garudimimus brevipes Barsbold, 1981 (Dinosauria:Theropoda) from the Late Cretaceous of
Mongolia. Can. J. Earth Sci. 42, 1501–1521.
Larsson, H. C. E. 2001. Endocranial anatomy of Carcharodontosaurus saharicus (Theropoda:
Allosauroidea) and its implications for theropod brain evolution. In Mesozoic vertebrate life
(eds D. H. Tanke and K. Carpenter), pp. 19-33. Bloomington, IN: Indiana University Press.
Larsson, H. C. E., Sereno, P. C. & Wilson, J. A. 2000. Forebrain enlargement among nonavian
theropod dinosaurs. J. Vert. Paleont. 20, 615-618.
Martins, E. P. & Garland, T., Jr. 1991. Phylogenetic analyses of the correlated evolution of
continuous characters: a simulation study. Evolution 45, 534-557.
Madsen, J. H., Jr. & Welles, S. P. 2000. Ceratosaurus (Dinosauria, Theropoda), a revised
osteology. UT Geol. Surv. Misc. Publ. 00-2, 1-80.
Paul, G. S. 1988. Predatory dinosaurs of the world. New York, NY: Simon and Schuster.
Russell, D. A. 1972. Ostrich dinosaurs from the Late Cretaceous of Western Canada. Can. J.
Earth Sci. 9, 375-402.
Sampson, S. D. & Witmer, L. M. 2007. Craniofacial anatomy of Majungasaurus crenatissimus
(Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. J. Vert. Paleont. 27
(Suppl., Memoir 8), 32-102.
Sanders, R. K. & Smith, D. K.. 2005. The endocranium of the theropod dinosaur Ceratosaurus
studied with computed tomography. Acta Palaeontol. Pol. 50, 601-616.
Sereno, P. C., Dutheil, D. B., Iarochene, M., Larsson, H. C. E., Lyon, G. H., Magwene, P. M.,
Sidor, C. A., Varricchio, D. J. & Wilson, J. A. 1996. Predatory dinosaurs from the Sahara
and Late Cretaceous faunal differentiation. Science 272, 986–991.
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, doi:
10.1098/rspb.2008.0607.
Stovall J. W. & Langston, W., Jr. 1950. Acrocanthosaurus atokensis, a new genus and species of
Lower Cretaceous Theropoda from Oklahoma. Am. Midl. Nat. 43, 696-728.
Verheyden, C. & Jouventin, P. 1994. Olfactory behavior of foraging procellariiforms. The Auk
111, 285-291.
Xu, X., Norell, M. A., Kuang, X., Wang, X., Zhao, Q. & Jia, C. 2004. Basal tyrannosauroids
from China and evidence for protofeathers in tyrannosauroids. Nature 431, 680-684.