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 / Catalogue number/specimen details / Olfactory bulb/Cerebral hemisphere greatest diameters / Olfactory ratio (%) / Femur length (mm) / Body mass (kg)Allosauroidea
Allosaurus fragilis / Cast of UUVP 294
UUVP 5961 (Franzosa, 2004: fig. 28) / Length/Depth / 51.6
50 / 860 (UUVP 6000 in Paul, 1988) / 1468.77
Acrocanthosaurus atokensis / OMNH 10146 (Franzosa and Rowe, 2005: fig. 2) / Length/Depth / 58.1 / ~1153 (Stovall and Langston, 1950) / 3777.58
Carcharodontosaurus saharicus / SGM-Din 1 (endocast) / Depth/Length / 56 / ~1450 (Sereno et al., 1996) / 7905.47
Giganotosaurus carolinii / MUCPv-CH-1 (CT scan slices) / Length/Length / 57.7 / 1430 (Sereno et al., 1996) / 7559.49
Ceratosauria
Ceratosaurus magnicornis / MWC 1 (Sanders and Smith, 2005: fig. 13) / Length/Length / 48.1 / 630 (Madsen and Welles, 2000) / 538.86
Majungasaurus crenatissimus / FMNH PR 2100 (Sampson and Witmer, 2007: fig. 18) / Length/Length / 48.3 / Sampson and Witmer (2007) / 1130
Tyrannosauroidea
Dilong paradoxus / IVPP V14243 (CT scan slices) / Length/Length / 27 / 181 (Xu et al., 2004) / 9.69
Albertosaurus sarcophagus / TMP 81.9.1 (frontoparietal) / Length/Length* / 71* / 1020 (ROM 807, Currie, 2003) / 2545.13
Gorgosaurus libratus / TMP 67.14.3
(frontoparietal) / Length/Length* / 68.5* / 1040 (NMC 2120, Currie, 2003) / 2709.45
Tarbosaurus bataar / Cast of PIN 46104 / Depth/Length / 65.1 / 970 (PIN 551-3, Paul, 1988) / 2164.60
Tyrannosaurus rex / AMNH 5029 (subadult endocast)
FMNH PR 2081 (Brochu and Ketcham, 2003: digital endocast) / Depth/Length / 66.5
71 / 980 (AMNH 30564, Erickson et al., 2004)
1321 (Brochu, 2003) / 2237.33
5855.30
Ornithomimosauria
Garudimimus brevipes / GIN 100/13
(CT scan slices) / Length/Length / 28.8 / 371 (Kobayashi and Barsbold, 2005) / 97.84
Ornithomimus edmontonensis / TMP 95.110.1
(CT scan slices) / Length/Length / 31.4 / 426 / 152.74
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
Oviraptoridae
Citipati osmolskae / IGM 100/978 (Franzosa, 2004: fig. 30) / Depth/Length / 31.5 / ~405 (IGM 100/1004, G.M. Erickson personal communication 2008) / 129.78
Dromaeosauridae
Saurornitholestes langstoni / TMP 74.10.5
(endocast) / Length/Length / 34.8 / 214 / 16.62
Bambiraptor feinbergi / KUVP 129737 (Burnham, 2004: fig. 3.2) / Length/Length / 28.5 / 118 (Burnham, 2004) / 2.44
Velociraptor mongoliensis / GIN 100/24
(CT scan slices) / Length/Length / 35.7 / 200 (GIN 100/25, Paul, 1988) / 13.36
Troodontidae
Troodon formosus / 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
Aves
Archaeopteryx lithographica / BMNH 37001 (Dominguez Alonso et al., 2004: fig. 3) / Length/Length / 17.1 / 60.5 (Paul, 1988) / 0.28
Alligatoridae / Skull length (mm)
Alligator mississippiensis / UF 98341
UF 105541
UF 87885
(braincases) / Length/Depth / 49.8
54.3
55.1 / 434
367.5
311.5 / 161.60
90.60
50.90
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