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Electronic Supplementary Material - Zelenitsky et al.

1. Accuracy of endocast-derived olfactory ratios

Because the braincase closely conforms to brain shape in birds [1, 2], olfactory ratios based on soft-tissue measurements should theoretically be comparable to olfactory ratios based on measurement of endocasts. To test this assumption, we compared endocast-derived olfactory ratios for Apteryx australis (USNM 18278) and Dromaius novaehollandiae (OUVC 10515) with published soft-tissue-derived values for these taxa [3]. For each taxon, the absolute difference between endocast-derived and soft-tissue-derived olfactory ratios was less than 1.0%, thus verifying that olfactory ratios derived from virtual endocasts are comparable to those derived from soft tissues.

Olfactory ratios for extinct theropods were calculated from endocranial measurements. Like birds, the brains of non-avian maniraptoriform theropods mostly filled the endocranial cavity [4-9] so endocranial proportions should accurately reflect brain proportions. For non-maniraptoriform theropods, we follow the assumption of Larsson et al.[10] that the size proportion between the soft-tissue structures of the brain are equal to the size proportion of the endocranial cavity housing them, even though their brains did not completely fill the endocranial cavity, as in extant crocodylians [11, 12]. Moreover, the disparity between the dimensions of the neural tissues of the telencephalon (which includes the olfactory bulb and cerebral hemispheres) in extant reptiles and the enclosing bony braincase is the smallest for any region of the brain [12]. Therefore, olfactory ratios of non-avian theropods, as we have calculated from measured endocasts, should accurately reflect the proportions of the cerebral hemispheres and olfactory bulbs [13].

2. High olfactory ratios and olfactory-associated behaviours

Among birds, olfaction is involved in a variety of behaviours, such as foraging, navigation, orientation, homing, individual recognition, social displays, predator avoidance, and nest material selection [14-17]. There is a tendency for olfactory-associated behaviours to be reported more often in birds with above average olfactory ratios [3, 18]. Here we wanted to test for significant correlations between olfactory ratios and the frequencies of specific olfactory behaviours (e.g., olfactory foraging, navigation, mate recognition, etc.) among the bird species considered in this study. This was not possible in most cases due to a general paucity of behavioural studies related to olfaction in birds [17]. The only behaviour we could test was olfactory foraging because it represents the only behaviour documented in a reasonable number of species (n = 13). We compared the olfactory ratios of birds known to practice olfactory foraging (i.e., Apteryx australia, Cathartes aura septentrionalis, Daption capense, Fulmarus glacialis, Oceanites oceanicus, Oceanodroma leucorhoa leucorhoa, Pachyptila desolata, Pagodroma nivea, Puffinus pacificus, Puffinus gravis, Phoebastria nigripes, Puffinus opisthomelas, Strigops habroptila) against those of all other birds, which primarily use other senses for foraging, through an independent sample t-test in PASW Statistics v. 17.0.2. For this analysis, although we could not find data on Puffinus opisthomelas, we considered it as part of the olfactory foraging group because at least six closely related species (P. gravis, P. griseus, P. creatops, P. bulleri, P. puffinus, P. tenuirostris) are reported to practice olfactory foraging [19]. Our results reveal that olfactory foraging species have significantly higher (p < 0.0001) olfactory ratios (mean = 30.6%) than other species (mean = 13.8%).



3. Institutional abbreviations

AMNH, American Museum of Natural History, New York City, NY; BMNH, Natural History Museum, London, UK; CMN, Canadian Museum of Nature, Ottawa; 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, University of Kansas Natural History Museum, Lawrence, KS; MOR, Museum of the Rockies, Bozeman, MT; MUCPv-CH, Museo de la Universidad Nacional del Comahue, El Chocón collection, Neuquén; MWC, Museum of Western Colorado, Fruita, CO; OMNH, Oklahoma Museum of Natural History, Norman, OK; OUVC, Ohio University Vertebrate Collection, Ohio University, Athens, OH; PIN, Paleontological Institute, Moscow; SGM, Ministère de l’Énergie et des Mines, Rabat, Morocco; TMP, Royal Tyrrell Museum of Palaeontology, Drumheller, Alberta; UMNH, Utah Museum of Natural History, Salt Lake City, UT; USNM, National Museum of Natural History, Smithsonian Institution, Washington, D.C.; UUVP, University of Utah Museum of Natural History, Salt Lake City, UT; YPM, Yale-Peabody Museum, New Haven, CT.



4. Phylogenetic independent contrasts

Least-squares regression of the standardized, positivized independent contrasts of olfactory ratio and body mass based on molecular and morphological phylogenies for Aves are presented below.



Figure S1. Least-squares regression of the standardized, positivized independent contrasts of olfactory ratio and body mass based on the molecular phylogeny for Aves (figure S3).



Figure S2. Least-squares regression of the standardized, positivized independent contrasts of olfactory ratio and body mass based on the morphological phylogeny for Aves (figure S4).



Figure S3. Molecular phylogeny of Aves used for maximum parsimony ancestral state reconstruction of olfactory ratios. Olfactory ratios for each node, except those for terminal taxa, are provided in table S3. Olfactory ratios for terminal taxa are listed in table S1.



Figure S4. Morphological phylogeny of Aves used for maximum parsimony ancestral state reconstruction of olfactory ratios. Olfactory ratios for each node, except those for terminal taxa, are provided in table S4. Olfactory ratios for terminal taxa are listed in table S1.



Table S1. Olfactory ratios and body masses of avian taxa considered in this study. Olfactory ratios for extant birds are sourced from Bang [3] and body masses are derived from Dunning [20], unless otherwise noted. Ordinal-level categories of living birds are based on the phylogeny of Hackett et al. [21], and follow the revised nomenclature of Chesser et al. [22]. Sources of olfactory ratios and body masses for extinct birds are provided in the text (see Materials and Methods). Limb-element lengths for extinct birds were measured by the authors, unless otherwise noted. Residuals for all birds were calculated relative to a phylogenetically-corrected least-squares regression of olfactory ratio against body mass for non-avian theropods (figure 2). Dagger “†” denotes fossil taxon. *From virtual endocast. **From Hagelin [23].


Taxon

Olfactory ratio (%)

Body mass (kg)


Olfactory ratio residual

Basal birds

 

 

 

Archaeopterygiformes†

 

 

 

Archaeopteryx lithographica† (BMNH 37001)

17.1

0.280

-0.01

Confuciusornithiformes†

 

 

 

Confuciusornis sanctus†(TMP 1998.14.2) (TMP 1998.14.1 mean humerus length = 63.65 mm)

17.9

0.277

0.01

Hesperornithiformes†

 

 

 

Hesperornis regalis† (KUVP 71012) (femur length = 105 mm; from Marsh [24])

15.3-21.3 mean=18.3 

10.608


-0.26 to -0.11 mean=-0.18 

Ichthyornithiformes†




 




Ichthyornis dispar† (YPM 1728) (mean of all known complete humeri = 62.4 mm; from Clarke [25])

18.1

0.350

0.00

Palaeognathae

 

 

 

Apterygiformes

 

 

 

Apteryx australis

34.3

2.330

0.18

Lithornithiformes†

 

 

 

Lithornis plebius† (USNM 336534) (humerus = 83 mm; from Houde [26])

36.5

0.480

0.29

Lithornis promiscuus† (USNM 391983) (USNM 336535 humerus = 112.7 mm; from Houde [26]

37.7

0.908

0.27

Tinamiformes

 

 

 

Eudromia elegans (OUVC 10602)

19.5*

0.695

0.00

Casuariformes

 

 

 

Dromaius novaehollandiae

26.3

34.200

-0.08

Struthioniformes

 

 

 

Rhea americana

19.1

23.000

-0.20

Struthio camelus (OUVC 10491)

19.2*

111.000

-0.28

Neognathae

 

 

 

Galliformes

 

 

 

Gallus gallus

15.4

0.904

-0.12

Bonasa umbellus

14.3

0.532

-0.12

Meleagris gallopavo/Meleagris gallopavo silvestris

13.5

6.050

-0.28

Anseriformes

 

 

 

Presbyornis sp. (USNM 299846) (humerus = 95.64 mm; from Ericson [27])

24.2

0.646

0.10

Aix sponsa

25.6

0.658

0.12

Polysticta stelleri

23.7

0.808

0.07

Anas carolinensis/Anas crecca carolinensis

20.0

0.341

0.05

Anas platyrhynchos

19.0

1.082

-0.04

Mergus serrator

15.0

1.022

-0.14

Caprimulgiformes

 

 

 

Caprimulgus vociferus

25.0

0.053

0.25

Steatornis caipensis

24.7

0.408

0.13

Caprimulgus asiaticus

22.0

0.042

0.20

Chaetura pelagica

18.8

0.024

0.17

Apus affinis/Apus affinis affinis

18.7

0.018

0.18

Cypsiurus parvus

18.7

0.014

0.19

Podicipediformes

 

 

 

Podiceps auritus

26.7

0.453

0.16

Podiceps ruficollis/Tachybaptus ruficollis philippensis

22.2

0.213

0.12

Phoenicopteriformes

 

 

 

Phoeniconaias minor/Phoenicopterus minor

21.7

1.500

0.00

Phaethontiformes

 

 

 

Phaethon aethereus

20.0

0.750

0.01

Columbiformes

 

 

 

Columba livia

21.2

0.355

0.07

Treron phoenicopterus

20.0

0.235

0.07

Columba livia domestica

18.2

0.355

0.00

Opisthocomiformes

 

 

 

Opisthocomus hoazin

24.2

0.696

0.09

Gruiformes

 

 

 

Tribonyx mortierii/Gallinula mortierii

26.1

1.293

0.09

Rallus limicola

25.6

0.084

0.23

Fulica atraatra

24.9

0.836

0.09

Tribonyx ventralis/Gallinula ventralis

23.9

0.387

0.12

Gallirallus australis/Gallirallus australis australis

24.2

0.852

0.08

Fulica americana

23.5

0.642

0.08

Porzana fusca

23.1

0.058

0.21

Porphyrio poliocephalus/Porphyrio porphyrio melanotis

23.4

0.988

0.06

Amaurornis phoenicurus

22.6

0.180

0.14

Porphyrio porphyrio/Porphyrio prophyrio porphyrio

21.1

0.797

0.02

Gallinula chloropus/Gallinula chloropus chloropus

20.0

0.305

0.05

Rallus longirostris/Rallus longirostris scottii

20.0

0.269

0.06

Rallus elegans/Rallus elegans elegans

20.0

0.361

0.05

Cuculiformes

 

 

 

Coccyzus americanus

21.1

0.064

0.16

Cuculus varius

20.7

0.103

0.13

Eudynamis scolopacea

19.4

0.167

0.07

Centropus sinensis

18.3

0.283

0.02

Gaviiformes

 

 

 

Gavia immer

20.0

4.980

-0.10

Sphenisciformes

 

 

 

Pygoscelis adeliae

16.7

4.850

-0.18

Procellariiformes

 

 

 

Pagodroma nivea

37.2

0.268

0.33

Oceanodroma leucorhoa leucorhoa

33.0

0.041

0.38

Oceanites oceanicus

33.3

0.032

0.40

Puffinu spacificus

30.9

0.388

0.23

Puffinus gravis

30.0

0.849

0.17

Pachyptila desolata

29.3

0.147

0.26

Diomedea nigripes/Phoebastria nigripes

28.6

3.195

0.08

Puffinus opisthomelas

29.4

0.408

0.21

Daption capensis/Daption capense

27.5

0.436

0.17

Fulmarus glacialis

27.1

0.613

0.15

Pelecanoides georgicus

17.7

0.121

0.05

Pelecaniformes

 

 

 

Phalacrocorax niger/Phalacrocorax sulcirostris

15.8

1.000

-0.11

Fregata magnificens

15.0

1.414

-0.15

Phalacrocorax carbolucidus

14.5

2.669

-0.20

Phalancrocorax auritus/Phalacrocrax auritus floridanus

10.3

1.674

-0.32

Sula bassana/Morus bassanus

9.6

3.000

-0.39

Pelecanus occidentalis

9.7

3.438

-0.39

Phalacrocorax urile

9.5

2.138

-0.37

Phalacrocorax pelagicus

8.0

1.857

-0.44

Nycticorax nycticorax

20.2

0.810

0.01

Charadriiformes

 

 

 

Turnix suscitator/Turnix suscitator leggei

12.5

0.051

-0.05

Vanellus indicus

22.0

0.181

0.12

Hydrophasianus chirurgus

20.0

0.164

0.09

Philohela minor/Scolopax minor

16.7

0.198

0.00

Larus argentatus

15.8

1.085

-0.12

Charadrius semipalmatus

15.0

0.047

0.03

Limnodromus griseus/Limnodromus griseus griseus

15.4

0.113

-0.01

Uria lomvia

15.0

0.964

-0.13

Capella gallinago/Gallina godelicata

14.3

0.122

-0.04

Fratercula artica

13.9

0.932

-0.16

Accipitriformes

 

 

 

Milvus migrans/Milvus migrans lineatus (Accipitridae)

15.0

0.836

-0.13

Pandion haliaetus (Accipitridae)

14.3

1.486

-0.18

Haliastur indus (Accipitridae)

12.5

0.529

-0.18

Coragyps atratus/Coragyps atratus atratus (Cathartidae)

16.7

2.159

-0.13

Cathartes aura/Cathartes aura septentrionalis (Cathartidae)

28.7

2.006

0.11

Coliiformes

 

 

 

Colius macrourus/Urocolius macrourus

9.7

0.046

-0.16

Strigiformes

 

 

 

Asio flammeus

19.4

0.347

0.04

Bubo virginianus/Bubo virginianus virginianus

18.0

1.355

-0.07

Otus asio/Megascops asio naevius

15.0

0.181

-0.04

Coraciiformes

 

 

 

Merops orientalis

18.8

0.015

0.19

Megaceryle alcyon/Ceryle alcyon

17.0

0.148

0.02

Upupa epops

14.7

0.061

0.01

Coracias benghalensis

14.3

0.158

-0.06

Bicanistes subcylidricus/Ceratogymna subcylindricus

7.7

1.201

-0.44

Megalaima asiatica

15.4

0.091

0.01

Micropternus brachyurus/Celeus brachyurus phaioceps

14.3

0.108

-0.04

Dendrocopos pubescens/Picoides pubescens

10.0

0.028

-0.12

Megalaima haemocephala/Megalaima haemacephala haemacephala

9.3

0.047

-0.18

Colaptes auratus/Colaptes auratus auratus

8.3

0.127

-0.28

Falconiformes

 

 

 

Falco peregrinus/Falco peregrinus anatum

20.0

0.815

0.00

Psittaciformes

 

 

 

Melopsittacus undulata

6.2

0.029

-0.33

Psittacula krameri

10.0

0.117

-0.19

Strigops habroptila

30.2**

1.750

0.14

Passeriformes

 

 

 

Pitta brachyurus (Suboscine)

18.2

0.056

0.11

Tephrodornis pondicerianus (Corvida)

17.9

0.020

0.15

Dicrurus adsimilis (Corvida)

16.5

0.040

0.08

Lanius schach (Corvida)

16.0

0.052

0.05

Pteruthius rufiventer (Corvida)

14.3

0.045

0.01

Oriolus xanthornus (Corvida)

13.3

0.056

-0.03

Coracina melanoptera (Corvida)

12.0

0.030

-0.04

Dendrocitta vagabunda/Dendrocitta vagabunda pallida (Corvida)

7.2

0.100

-0.33

Cyanocitta cristata (Corvida)

6.3

0.088

-0.38

Corvus brachyrhynchos (Corvida)

5.0

0.506

-0.88

Motacilla maderaspatensis (Passerida)

16.7

0.031

0.10

Hirundo rustica/Hirundo rustica rustica (Passerida)

15.0

0.018

0.08

Copsychus albospecularis inexpectatus (Passerida)

14.0

0.024

0.04

Motacilla flava/Motacilla flava beema (Passerida)

13.6

0.017

0.05

Sturnus malabaricus (Passerida)

12.7

0.040

-0.03

Nectarinia zeylonica/Leptocoma zeylonica (Passerida)

12.9

0.009

0.06

Cinclus cinclus/Cinclus cinclus aquaticus (Passerida)

10.7

0.060

-0.13

Estrilda amandava/Amandava amandava (Passerida)

10.0

0.010

-0.06

Sturnus vulgaris (Passerida)

9.7

0.086

-0.19

Quiscalus quiscula (Passerida)

9.4

0.106

-0.22

Gracula religiosa (Passerida)

7.7

0.192

-0.34

Turdus migratorius (Passerida)

8.6

0.079

-0.24

Molothrus ater/Molothrus ater artemisiae (Passerida)

7.1

0.043

-0.29

Turdoides caudatus/Turdoides caudatus caudatus (Passerida)

5.9

0.034

-0.36

Serinus canaria (Passerida)

6.0

0.024

-0.33

Passarella iliaca (Passerida)

5.8

0.032

-0.36

Zonotrichia albicollis (Passerida)

4.6

0.024

-0.44

Hesperiphona vespertina (Passerida)

4.0

0.060

-0.56

Passer domesticus (Passerida)

3.8

0.028

-0.53

Carpodacus purpureus (Passerida)

4.2

0.023

-0.48

Parus atricapillus/Poecile atricapillus (Passerida)

3.2

0.011

-0.56
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