J Comp Physiol A (2006) 192:1313–1326

DOI 10.1007/s00359-006-0161-2

ORIGINAL PAPER

The evolution of stereopsis and the Wulst in caprimulgiform birds: a comparative analysis

Andrew N. Iwaniuk · Douglas R. W. Wylie

Received: 27 March 2006 / Revised: 3 August 2006 / Accepted: 6 August 2006 / Published online: 30 August 2006© Springer-Verlag 2006

Abstract Owls possess stereopsis (i.e., the ability toperceive depth from retinal disparity cues), but its dis-tribution amongst other birds has remained largelyunexplored. Here, we present data on species variationin brain and telencephalon size and features of theWulst, the neuroanatomical substrate that subservesstereopsis, in a putative sister-group to owls, the orderCaprimulgiformes. The caprimulgiforms we examinedincluded nightjars (Caprimulgidae), owlet-nightjars(Aegothelidae), potoos (Nyctibiidae), frogmouths(Podargidae) and the Oilbird (Steatornithidae). Theowlet-nightjars and frogmouths shared almost identicalrelative brain, telencephalic and Wulst volumes as wellas overall brain morphology and Wulst morphologywith owls. SpeciWcally, the owls, frogmouths and owlet-nightjars possess relatively large brains and telence-phalic and Wulst volumes, had a characteristic brainshape and displayed prominent laminae in the Wulst.In contrast, potoos and nightjars both had relativelysmall brains and telencephala, and Wulst volumes thatare typical for similarly sized birds from other orders.The Oilbird had a large brain, telencephalon andWulst, although these measures were not quite as largeas those of the owls. This gradation of owl-like versusnightjar-like brains within caprimulgiforms has signiW-cant implications for understanding the evolution of

stereopsis and the Wulst both within the order andbirds in general.

Keywords Wulst · Caprimulgiformes · Evolution · Stereopsis · Strigiformes

Introduction

A series of neurophysiological, neuroanatomical andbehavioral experiments has demonstrated that owlspossess a visual system that is very similar to primates(van der Willigen et al. 1998) and cats insofar as it isdesigned to subserve stereopsis. At least two featuresof the owl visual system sets them apart from mostother birds. First, owl eyes are positioned frontally,such that they have a large area of binocular visual Weldoverlap [44 to >50° horizontally; Barn Owl (Tyto alba),Pettigrew and Konishi 1984; Tawny Owl (Strix aluco),Martin 1984; Northern Saw-whet Owl (Aegolius acadi-cus), Wylie et al. 1994]. Although all birds have somedegree of binocular overlap (Martin and Katzir 1999),the magnitude pales in comparison to that of owls(Martin and Coetzee 2004). Second, compared to otherspecies, owls have a grossly hypertrophied visual Wulst(Stingelin 1958; Karten et al. 1973; Pettigrew 1979;Iwaniuk and Hurd 2005), the putative homolog ofmammalian primary visual cortex (V1) (e.g., Shimizuand Karten 1993; Medina and Reiner 2000; Reineret al. 2005). Recordings from the owl Wulst reveal thatit is functionally like V1; Wulst neurons are selectivefor orientation, movement direction, spatial frequencyand binocular disparity (Pettigrew and Konishi 1976;Pettigrew 1979; Porciatti et al. 1990; Wagner and Frost1993; Nieder and Wagner 2000, 2001). Critically, the

A. N. Iwaniuk (&) · D. R. W. WylieDepartment of Psychology, University of Alberta, Edmonton, AB, Canada T6G 2E9e-mail: brainsize@yahoo.ca

D. R. W. WylieCentre for Neuroscience, University of Alberta, Edmonton, AB, Canada T6G 2E9

123

1314 J Comp Physiol A (2006) 192:1313–1326

vast majority (86%) of neurons are binocular andtuned to a particular disparity (Pettigrew 1979). Binoc-ular neurons are present in the Wulst of other species,but they are not as numerous as they are in owls (e.g.,Perisic et al. 1971; Pettigrew 1978; Wilson 1980; Den-ton 1981). Although the role of the Wulst in stereopsishas yet to be deWnitively proven, the available neuralevidence from owls suggests that the Wulst mediatesstereopsis.

While it is clear that the owls have evolved globalstereopsis (i.e., depth perception throughout all ormost of the visual Weld) independently from mammals(Pettigrew 1986), its evolution and phylogenetic distribu-tion within birds has not been investigated. Owls areconsidered by some to be closely related to the orderCaprimulgiformes (Sibley and Ahlquist 1990; Livezeyand Zusi 2001), which is a diverse assemblage of noc-turnal birds. Three families within the Caprimulgiformespossess frontal eye position comparable to owls: frog-mouths (Podargidae; binocular overlap = 50° horizon-tally; Wallman and Pettigrew 1985), owlet-nightjars(Aegothelidae) and Oilbird (Steatornis caripensis,Steatornithidae; binocular overlap = 38–50°, Pettigrewand Konishi 1984; Martin et al. 2004a, b). Nightjars(Caprimulgidae), on the other hand, have a narrowerbinocular visual Weld (25°; Martin et al. 2004b). Lastly,nothing is known about the visual Weld or abilities ofthe Wfth family: the potoos (Nyctibiidae).

Stereopsis is thought to be present in both owlet-nightjars and frogmouths (Pettigrew 1986) because oftheir frontal eye position and an area of binocularvisual overlap comparable to that of owls (Wallmanand Pettigrew 1985; Pettigrew 1986). However, thereare no behavioral studies that demonstrate stereopsisand no reports of electrophysiogical investigations ofthe Wulst for either family. With respect to the Oilbird,electrophysiological investigations failed to Wnd anybinocular neurons in the Wulst (Pettigrew and Konishi1984), despite the presence of a broad area of binocu-lar visual Weld overlap (Pettigrew and Konishi 1984;Martin et al. 2004a, b). Finally, Pettigrew (1986)reported that there was no evidence of binocular neu-rons in the Wulst of nightjars based on both electro-physiological and anatomical investigations, but detailsare lacking.

Given that both the owls and frogmouths possess agrossly enlarged Wulst (Pettigrew 1986; Iwaniuk andHurd 2005) and owls, and possibly frogmouths, pos-sess stereopsis (Pettigrew 1986), it is conceivable thatWulst enlargement underlies functional global stere-opsis. Currently, little is known about how the rela-tive size of the Wulst varies among birds and this isespecially true of caprimulgiforms. Stingelin (1958)

documented a large amount of variation in Wulst sizeand structure in birds, but did not provide anydetailed volumetric data for the Wulst or its constitu-ent regions and only included a single caprimulgiform(Caprimulgus europaeus). If claims of stereopsis inthe owlet-nightjar and frogmouth are correct (Petti-grew 1986), then we would expect to see an enlarge-ment of the Wulst in both families such that they aresimilar to owls. Similarly, the relative size of theWulst could indicate whether potoos have stereo-scopic vision or not. Enlargement of the Wulst canalso result in an increase in overall brain and telence-phalic volumes (Iwaniuk et al. 2005; Iwaniuk andHurd 2005) and changes in Wulst morphology (Sting-elin 1958). We therefore surveyed the Wve currentlyrecognized caprimulgiform families and examined thefollowing features: brain size and morphology, telen-cephalic size and Wulst size and morphology.

Methods

Specimens

Brain volumes were measured from Wxed brains aswell as endocranial volumes (Iwaniuk and Nelson2002) of skeletal specimens (Table 1). These dataincluded measurements from over 200 individualsrepresenting 18 caprimulgiform and 40 owl (Strigifor-mes) species. Fixed brains of a Spotted Nightjar(Eurostopodus argus), Barn Owl (Tyto alba) Boo-book Owls (Ninox boobook, n = 2) and Tawny Frog-mouths (Podargus strigoides, n = 3) were extractedfrom carcasses obtained as roadkills and from Heales-ville Sanctuary (Healesville, VIC, Australia). GreyPotoo (Nyctibius griseus), Oilbird, Pauraque (Nycti-dromus albicollis) and Feline Owlet-nightjar (Aegoth-eles insignis) specimens were loaned to us from theNational Museum of Natural History (Washington,DC, USA) and the Bishop Museum (Honolulu, HI,USA) and a Northern Saw-whet Owl was donated byB.J. Frost (see Table 2). The brains of all of themuseum specimens, which were all stored in 70% eth-anol for up to 45 years, were extracted and placedinto buVered 4% paraformaldehyde. They were sub-sequently placed into 30% sucrose in 0.1 M phos-phate buVered saline until they sank. The brains werethen embedded in gelatin and serially sectioned in thetransverse plane on a freezing stage microtome at40 �m. The sections were collected in 0.1 M phos-phate buVered saline, mounted onto gelatinizedslides, stained for Nissl substance with thionin andcoverslipped with Permount.

123

J Comp Physiol A (2006) 192:1313–1326 1315

Table 1 A list of the caprimulgiform and owl species measured, sample sizes and means of brain volume (mm3) and body mass (g)

Order Family Species n Brain volume(mm3)

Bodymass (g)

Caprimulgiformes Aegothelidae Australian owlet-nightjar Aegotheles cristatus 8 1,420 41.0Caprimulgidae Chuck-will’s-widow Caprimulgus carolinensis 9 1,360 109.5

European nightjar Caprimulgus europaeus 10 880 67.0Large-tailed nightjar Caprimulgus macrurus 9 1,010 78.0Whip-poor-will Caprimulgus vociferus 10 820 50.8Common nighthawk Chordeiles minor 10 850 57.1Spotted nightjar Eurostopodus argus 2 1,240 72.0Great eared-nightjar Eurostopodus macrotis 5 1,460 168.8White-throated nightjar Eurostopodus mystacialis 2 1,330 170.0Pennant-winged nightjar Macrodipteryx vexillarius 6 870 66.1Pauraque Nyctidromus albicollis 8 910 56.6Ocellated poorwill Nyctiphrynus ocellatus 3 740 39.0Band-tailed nighthawk Nyctiprogne leucopyga 4 510 23.0Common poorwill Phalaenoptilus nuttallii 2 530 51.6Nacunda nighthawk Podager nacunda 5 1,290 213.3

Nyctibiidae Grey potoo Nyctibius griseus 5 1,980 257.4Podargidae Tawny frogmouth Podargus strigoides 15 4,860 387.3Steatornithidae Oilbird Steatornis caripensis 1 3,900 414.0

Strigiformes Strigidae Saw-whet owl Aegolius acadicus 9 3,360 73.1Boreal owl Aegolius funereus 6 4,020 91.2African marsh owl Asio capensis 5 5,980 310.0Short-eared owl Asio Xammeus 26 5,300 309.8Long-eared owl Asio otus 12 5,310 214.7Burrowing owl Athene cunicularia 10 3,780 152.8Little owl Athene noctua 5 3,700 164Spotted eagle owl Bubo africanus 4 8,600 635.0Eurasian eagle owl Bubo bubo 5 17,090 2,686.0Great horned owl Bubo virginianus 40 14,730 1,415.8Ferruginous pygmy owl Glaucidium brasilianum 5 2,510 68.3Mountain pygmy owl Glaucidium gnoma 1 3,600 61.9Eurasian pygmy owl Glaucidium passerinum 6 2,590 58.5BuVy Wsh-owl Ketupa ketupu 1 12,750 770.0Elf owl Micrathene whitneyi 1 1,400 35.0Barking owl Ninox connivens 1 6,400 700.0Boobook owl Ninox booook 13 5,530 231.4Bismark hawk owl Ninox solomonis 3 4,380 130.0Moluccan hawk owl Ninox squamipila 1 4,400 175.7Powerful owl Ninox strenua 3 11,440 1,359.9Snowy owl Nyctea scandiaca 8 15,870 1,894.0Eastern screech owl Otus asio 9 4,910 180.5Indian scops owl Otus bakkamoena 5 4,040 139.1Tropical screech owl Otus choliba 3 3,410 121.5Moluccan scops owl Otus magicus 3 3,760 165.0Puerto Rican screech owl Otus nudipes 5 3,710 142.5Scops owl Otus scops 10 2,490 77.1Spectacled owl Pulsatrix perspicillata 1 10,600 873.0Tawny owl Strix aluco 5 9,080 426.0Grey owl Strix nebulosa 12 14,660 1,056.1Black and white owl Strix nigrolineata 5 7,400 527.5Ural owl Strix uralensis 5 11,210 784.5Barred owl Strix varia 10 12,550 700.0Mottled owl Strix virgata 4 6,100 229.5Northern hawk-owl Surnia ulula 5 7,480 286.4

Tytonidae Barn owl Tyto alba 11 6,510 354.7African grass owl Tyto capensis 3 5,230 419.0Eastern grass owl Tyto longimembris 1 5,250 478.0Australian masked owl Tyto novaehollandiae 9 8,470 766.6Greater sooty owl Tyto tenebricosa 3 12,700 671.5

123

1316 J Comp Physiol A (2006) 192:1313–1326

123

Tab

le2

A li

st o

f the

cap

rim

ulgi

form

and

ow

l fam

ilies

sur

veye

d fo

r st

ereo

psis

and

thei

r bo

dy m

asse

s (g

), b

rain

vol

umes

(m

m3 ),

tele

ncep

halic

vol

umes

(m

m3 )

and

Wul

st v

olum

es (

mm

3 )

Not

e th

at fo

r al

l spe

cies

, wit

h th

e ex

cept

ion

of th

e B

oobo

ok O

wl (

n=

2) a

nd T

awny

Fro

gmou

th (

n=

3), o

nly

one

spec

imen

was

mea

sure

d

USN

M N

atio

nal M

useu

m o

f Nat

ural

His

tory

, Was

hing

ton,

DC

, BB

M B

erni

ce B

isho

p M

useu

m, H

onol

ulu,

HI

Ord

erF

amily

Spec

ies

nB

ody

mas

s (g

)B

rain

vo

lum

e (m

m3 )

Tel

ence

phal

on

volu

me

(mm

3 )W

ulst

vo

lum

(mm

3 )

Wul

st/

Bra

in

volu

me

Wul

st/

Tel

ence

phal

on

volu

me

Sour

ce

Cap

rim

ulgi

form

esA

egot

helid

aeA

egot

hele

s in

sign

is1

–1,

540

1,10

7.99

363.

630.

2361

0.32

82T

his

stud

y (B

BM

NG

1013

65)

Cap

rim

ulgi

dae

Cap

rim

ulgu

s sp

.1

5373

434

2.75

51.6

20.

0703

0.15

06B

oire

(19

89)

Eur

osto

podu

s ar

gus

172

.098

242

6.73

59.3

00.

0604

0.13

90T

his

stud

y

Nyc

tidro

mus

al

bico

llis

156

.691

041

4.83

66.0

30.

0726

0.15

92T

his

stud

y (U

SNM

5042

11)

Nyc

tibi

idae

Nyc

tibiu

s gr

iseu

s1

257.

41,

980

1,00

4.67

176.

670.

0892

0.17

58T

his

stud

y (U

SNM

5041

84)

Pod

argi

dae

Pod

argu

s st

rigo

ides

338

7.0

5,31

13,

826.

811,

226.

890.

2310

0.32

06T

his

stud

y

Stea

torn

ithi

dae

Stea

torn

is

cari

pens

is1

414.

03,

900

2,88

7.70

749.

530.

1922

0.25

96T

his

stud

y (U

SNM

4313

65)

Stri

gifo

rmes

Stri

gida

eA

egol

ius

acad

icus

186

.02,

857

2,00

9.90

743.

750.

2603

0.37

00T

his

stud

y (d

onat

ed b

y B

.J. F

rost

)A

then

e cu

nicu

lari

a1

167.

05,

878

4,81

3.80

1,70

7.67

0.29

050.

3547

Alm

a an

d B

ee

de S

pero

ni (

1995

)N

inox

boo

book

223

1.4

5,62

63,

920.

441,

503.

680.

2673

0.38

35T

his

stud

yT

yton

idae

Tyt

o al

ba2

450.

06,

149

4,10

8.53

1,60

5.41

0.26

110.

3908

Alm

a an

d B

ee d

e Sp

eron

i (19

95)

and

Thi

s st

udy

J Comp Physiol A (2006) 192:1313–1326 1317

For measurements of the telencephalon andWulst, data was collected from seven caprimulgi-forms and three owls (Table 2). In addition, data fornumerous other species was gleaned from the litera-ture (Table 3). For the museum specimens, shrink-age was estimated by comparing the brain volumesof the specimens measured with known brain vol-umes of the species (see Table 1 and Iwaniuk andNelson 2003). This enabled volumes to be recon-structed that could be compared with body masses.The only species that we could not calculate ashrinkage factor for was the Feline Owlet-nightjar.For this specimen, we related the size of the telen-cephalon and Wulst only to the brain volume of thespecimen that we examined.

Digital photographs were taken throughout thebrain for every second or fourth section, dependingupon the size of the brain such that 60–80 sectionswere measured for each brain. It should be noted thatvarying the sampling interval in this fashion does notsigniWcantly aVect volumetric measurements (Iwan-iuk et al. 2006). The volumes of the telencephalonand Wulst were measured with the public domainNIH Image program (http://www.rsb.info.nih.gov/nih-image/). All hyperpallial structures were included in

the Wulst measurements: the apical hyperpallium(HA), interstitial part of the hyperpallium (HI), inter-calated part of the apical hyperpallium (IHA), anddensocellular part of the hyperpallium (HD) (Shimizuand Karten 1993; Reiner et al. 2005). It was not possi-ble to calculate the volumetric fractions of each ofthese Wulst subdivisions because they could not bereliably delineated throughout the extent of the Wulstfor all specimens. Borders were delineated by: the val-lecula laterally, the superior frontal lamina ventrallyand the ventricle medially. We deWned the caudal poleas the point at which the vallecula could no longer berecognized and the hippocampal formation was pres-ent. The border between the HA and the hippocampalformation was identiWed by a marked increase in celldensity within the hippocampal formation, as shown inprevious cytoarchitectonic studies (e.g., Sherry et al.1989). Due to diYculties in identifying the transitionbetween the parahippocampal area and HA, however,it is possible that some of the hippocampal formationwas included as part of the Wulst and vice versa.Although this is potentially a source of error, theborders we drew were replicable and the diVerencesbetween groups so large (see below), that it is unlikelythat this error would signiWcantly aVect our conclusions.

Table 3 A list of the other species used to calculate the least-squares regression lines and 95% conWdence intervals for the scatterplotsshown in Fig. 3

Data for these species was derived from Ebinger (1995), Ebinger and Röhrs (1995), Boire (1989), Carezzano and Bee de Speroni (1995),Ebinger and Löhmer (1984, 1987), Rehkamper et al. (1991), Fernandez et al. (1997) and Iwaniuk and Hurd (2005)

Order Species

Anseriformes Anas platyrhynchos, Anser anser, Dendrocygna eytoniApodiformes Chaetura pelagicaCharadriiformes Calidris minutilla, Charadrius vociferus, Limnodromus griseus, Sterna hirundo, Vanellus milesCiconiiformes Ardea cinerea, Egretta thula, Nycticorax caledonicusColumbiformes Columba leucomela, Columba livia, Phaps elegans, Streptopelia risoriaCoraciiformes Dacelo novaeguineae, Todiramphus sanctusFalconiformes Accipiter fasciatus, Falco cenchroides, Falco longipennisGalliformes Alectoris chukar, Chrysolophus pictus, Colinus virginianus, Gallus domesticus, Meleagris gallopavo,

Numida meleagris, Ortalis canicollis, Pavo meleagris, Perdix perdix, Phasianus colchicusGruiformes Fulica armillataPasseriformes Corvus corone, Entomyzon cyanotis, Garrulus glandarius, Passer domesticus, Strepera versicolor,

Taeniopygia guttataPelecaniformes Phalacrocorax auritusPodicipediformes Rollandia rollandProcellariiformes PuVinus tenuirostrisPsittaciformes Agapornis personata, Agapornis roseicollis, Alisterus scapularis, Amazona aestiva, Aratinga

acuticaudata, Cacatua roseicapilla, Calyptorhynchus funereus, Eclectus roratus, Glossopsitta concinna, Melopsittacus undulatus, Myiopsitta monachus, Neopsephotus bourkii, Nymphicushollandicus, Pionus menstruus, Platycercus elegans, Platycercus eximius, Polytelis swainsonii, Psephotus haematonotus, Psittacula eupatria, Psittacula krameri, Psittacus erithacus, Pyrrhuramolinae, Trichoglossus haematodus

Sphenisciformes Spheniscus magellanicusStruthioniformes Rhea americanaTinamiformes Rhynchotus rufescensTrochiliformes Chlorostilbon mellisugus

123

1318 J Comp Physiol A (2006) 192:1313–1326

Furthermore, these borders are the same as thoseused in previous volumetric studies (Ebinger andLöhmer 1984, 1987; Boire 1989; Rehkämper et al.1991; Ebinger 1995; Ebinger and Röhrs 1995) fromwhich we gleaned Wulst volumes for several addi-tional species (Table 3).

Statistical analysis

We performed multiple comparisons of both telence-phalic and Wulst volumes (Deacon 1990; Deaneret al. 2000; Iwaniuk et al. 2005). Telencephalic vol-umes were scaled relative to body mass and thevolume of the brain minus that of the telencephalon.Wulst volumes were scaled relative to body mass,volume of the brain minus the Wulst and volume ofthe telencephalon minus the Wulst. Using species asindependent data points, we calculated least-squaresregression lines and 95% conWdence intervals. Toaccount for possible phylogenetic eVects, we also cal-culated regression lines and 95% conWdence inter-vals using the independent contrasts approach asshown in Garland and Ives (2000). Phylogenetic rela-tionships among the additional species used to calcu-late the 95% conWdence intervals (Table 3) weretaken primarily from Sibley and Ahlquist (1990),with additional resolution provided by Christidiset al. (1991), Sheldon et al. (2000), DimcheV et al.(2002) and Wink et al. (2004). Given the uncertainrelationships among the caprimulgiform families (seeSibley and Ahlquist 1990; Mayr 2002; Cracraft et al.2004), we did test alternative topologies of the phylo-genetic tree, but the results were qualitatively identi-cal to those presented here. That is, there were nochanges in the signiWcance of the results among thediVerent branching patterns. The tree was enteredinto the PDTREE module of the Phenotypic Diver-sity Analysis Programs (PDAP) software package(available from T. Garland). Because we relied uponmultiple sources for the phylogenetic tree, we testedseveral arbitrary branch length models. Only equalbranch lengths adequately standardized the data(Garland et al. 1992) and were therefore used in allphylogenetically based statistics. Independent con-trasts were then calculated and the 95% conWdenceinterval around a least-squares linear regression line(as calculated in PDTREE) was plotted onto theoriginal plot of species as independent data points(Garland and Ives 2000). This provides a means ofdetermining whether individual species fall outsideof the 95% conWdence interval of the data withoutthe diYculties that can be associated with interpret-ing independent contrasts plots.

Results

Relative brain volume

Figure 1 is a plot of brain volume against body mass forcaprimulgiforms and owls. The owls and nightjars clus-ter into two completely distinct groups: the owls possessrelatively large brains, whereas the nightjars possessrelatively small brains. In fact, there is a signiWcantgrade shift present between the nightjar and owl clus-ters as shown by a signiWcant diVerence in intercepts(F = 5.33, df = 1, 57, P = 0.02), but not slopes (F = 0.32,df = 1, 57, P = 0.58) between the two groups. Most ofthe species from the other caprimulgiform families fallinto one of these groups. For example, the potoo isclearly within the nightjar cluster whereas the frog-mouth and owlet-nightjar are within the owl cluster.The relative brain volume of the Oilbird is more similarto the owls than the nightjars, but falls outside of the95% conWdence interval calculated for both groups.These diVerences among the caprimulgiforms remainedonce phylogeny was accounted for, except for the Oil-bird, which was within the phylogeny-corrected 95%conWdence interval calculated for the owls. Thus, thereis a signiWcant grade shift in relative brain size between

Fig. 1 A scatterplot of log-transformed brain volumes (mm3)against log-transformed body masses (g) for all caprimulgiformand owl species measured (see Table 1). The symbols refer to thefollowing: black diamond Aegothelidae (Australian Owlet-night-jar, Aegotheles cristatus); grey squares Caprimulgidae (nightjars);black square Nyctibiidae (Grey Potoo, Nyctibius griseus); blackcircle Podargidae (Tawny Frogmouth, Podargus strigoides); blacktriangle Steatornithidae (Oilbird, Steatornis caripensis); and greycircles Strigiformes (owls). The solid lines indicate the 95% conW-dence intervals for the nightjars and owls. The two other sets oflines refer to the phylogeny-corrected 95% conWdence intervalsfor the nightjars (dashed lines) and owls (dotted lines)

123

J Comp Physiol A (2006) 192:1313–1326 1319

owls and nightjars and the remaining caprimulgiformsare found within the owls (owlet-nightjar, frogmouthand possibly the Oilbird) or the nightjars (potoo).

Macromorphology

Figure 2 shows photos taken from dorsal, lateral andventral aspects of owl and caprimulgiform brains.Although only one nightjar brain (Eurostopodusargus) is shown, the nightjars and the Grey Potoo areall characterized by a prominent cerebellum andoptic lobes in both dorsal and lateral aspects, pro-nounced olfactory bulbs and a narrow, long andmedially oriented Wulst (Fig. 2). This is similar tothe photographs of the European Nightjar (Capri-mulgus europaeus) in Stingelin (1958). The remain-ing caprimulgiforms, however, vary considerably inoverall brain shape. The Oilbird has large olfactorybulbs and large cerebral hemispheres with a promi-nent and wide Wulst clearly visible on the dorsal sur-face (Fig. 2). Both the frogmouth and owlet-nightjarpossess cerebral hemispheres that are rounded attheir rostral pole (Fig. 2). In fact, the curvature of theanterior hemispheres is so rounded that the olfactorybulbs can only be viewed on the ventral surface. Thevallecula is prominent on the dorsal surface of thehemispheres and outlines a relatively large Wulst anda greater proportion of the cerebellum is obscured bythe cerebral hemispheres than in the nightjar. Thesemorphological features are shared with the Barn Owl(Fig. 2, Stingelin 1958). The Boobook Owl, on theother hand, also possesses a brain that is dominatedby the cerebral hemispheres and has a prominentvallecula (Fig. 2). The anterior hemispheres are not,however, as rounded as the Tawny Frogmouth,Feline Owlet-nightjar or Barn Owl. Instead, theycome to an acute angle and the olfactory bulbs arelocated at the rostral tip of the hemispheres, in a sim-ilar fashion to the Northern Saw-whet Owl that weexamined and photographs of other strigid owlbrains in Stingelin (1958). The Wulst also appears toextend more laterally, relative to the length of thebrain than in the Barn Owl and Tawny Frogmouth.All of these features underlie signiWcant diVerencesin telencephalon and Wulst volume that are outlinedbelow.

Relative telencephalon volume

Figure 3 shows scatterplots of telencephalic volumeagainst body mass (Fig. 3a) and overall brainvolume (Fig. 3b). In both instances, the owls, Oilbird,owlet-nightjar and frogmouth all had relatively large

telencephala compared to the nightjars and potoo. The95% conWdence intervals (both conventional and phy-logeny-corrected) were all relatively broad, however,such that none of the owls or caprimulgiforms wereactually outside of them. Thus, any expansion of theWulst that may be present does not manifest itself as asigniWcant increase in relative telencephalic volume.

Wulst size and morphology

As a proportion of the entire volume of the brain andtelencephalon, the owls possess much larger Wulstvolumes than any other species (Table 2). This is alsoreXected in scatter plots of Wulst volume againstbody mass, brain volume minus Wulst volume and tel-encephalic volume minus Wulst volume (Fig. 4).Regardless of what scaling measure is used orwhether phylogenetic information is included in thecalculation of the interval or not, the owls are allabove the 95% conWdence interval. Two of the capri-mulgiforms, the frogmouth and the owlet-nightjar,also possess large Wulsts that are above the upperlimits of the 95% conWdence intervals (Fig. 4b, c), butthey are slightly smaller than that of the owls. Thenightjars and potoo, on the other hand, possess rela-tively smaller Wulst volumes and are more similar tothe other birds included in our analysis (see Table 3).Interestingly, the Oilbird has an enlarged Wulst rela-tive to both brain volume (Fig. 4b) and telencephalicvolume (Fig. 4c). In relation to the other species, theOilbird is generally situated between the owls, frog-mouth and owlet-nightjar on one hand and the night-jar and potoo on the other hand.

The morphology of the Wulst also varies betweenthe nightjars and owls. The lamination of the Wulstlayers in the owls is distinct and each layer can bereadily identiWed cytoarchitectonically, as shown inthe Boobook Owl (Fig. 5a). The HA is quite thick,the IHA appears as a dark band with both the dorsaland ventral subregions clearly visible. The HI is dis-cernible in between IHA and HD and the HD can bereadily distinguished from the underlying mesopal-lium (M) by a thick superior frontal lamina. This isalmost identical to the Wulst architecture describedby Karten et al. (1973) and Stingelin (1958) for otherstrigid owls. The morphology of the nightjar Wulst,however, is quite diVerent (Fig. 5b). Unlike the owls,HI and IHA are diYcult to deWne cytoarchitectoni-cally and the lamina separating HD from M is not asnoticeable. Furthermore, we had diYculty in Wndingany discernible division of the internal and externalparts of the IHA. In the case of the Oilbird, whichwas a museum specimen stored in ethanol for an

123

1320 J Comp Physiol A (2006) 192:1313–1326

extended period of time (45 years), the quality ofstaining throughout the telencephalon was relativelypoor. As such, although we were able to obtain thevolume of the Wulst, we were unable to accuratelydeWne the borders of structures within the Wulst ofthe Oilbird.

As with the volumetric comparisons already dis-cussed, the other caprimulgiforms vary as to whetherthey are owl-like or nightjar-like. The frogmouth

Wulst is strikingly similar to the owl (Fig. 5c). Again,each of the layers can be readily distinguished fromone another and the morphology of each layer isconsistent with that of the owl. That is, the IHA isdarkly stained relative to HA and the dorsal and ven-tral parts can be distinguished from one another, HI isdistinct and HD is separated from M by a discretesuperior frontal lamina. The same is also true of theowlet-nightjar (Fig. 5d). The owlet-nightjar Wulst also

Fig. 2 Photographs taken from ventral, dorsal and later-al views are shown for (from top to bottom): Spotted Nightjar (Eurostopodus argus); Feline Owlet-nightjar (Aegothelis insignis) (BBM-NG101365); Tawny Frogmouth (Podargus strigoides); Barn Owl (Tyto alba); Boobook Owl (Ninox boobook); and Oilbird (Steatornis caripensis) (USNM431365). Shown on each view are vallecula (arrow); olfactory bulbs (OB); and Wulst (W) (scale bar = 5 mm). Note that the discoloration of the owlet-nightjar and oilbird are the result of long-term storage in 70% ethanol

123

J Comp Physiol A (2006) 192:1313–1326 1321

possesses a darkly stained IHA with both dorsal andventral divisions visible, HI is reasonably distinct andthe superior frontal lamina is clearly visible. The shape

of the owlet-nightjar Wulst does, however, diVer fromthe frogmouth and owls in that it extends far less later-ally. This is also evident in the pictures of overall brainshape for the owlet-nightjar (Fig. 2). Lastly, althoughnot shown, the potoo is almost identical to the nightj-ars. The layers of the Wulst are visible, but are diYcultto discern from one another in Nissl stained sections.

Discussion

Nightjars and owls clearly possess markedly diVerentbrains. They diVer not only in relative size and macro-morphology, but also in the relative size of the telen-cephalon and Wulst and in Wulst morphology. Two ofthe other caprimulgiform families surveyed, the frog-mouths and owlet-nightjars, shared similar relativebrain size, macromorphology, telencephalon andWulst size and Wulst morphology with the owls. Thepotoo, however, was almost identical to the nightjarsin all these features. Lastly, the Oilbird was interme-diate between the owls and nightjars, although it didhave a moderately expanded telencephalon andWulst.

Caveats

Although the comparisons presented herein reliedupon relatively few species within each family, thediVerences between owls and nightjars is so large thatthe eVects of sampling only a single species withineach family are limited because there is little behav-ioral and/or ecological variability in three of the fam-ilies surveyed. For example, the behavior and lifehistory of owlet-nightjars, nightjars and potoos arehighly conserved within their respective families(Cleere 1998; del Hoyo et al. 1999). The Podargidaeis the only exception. Within this family, the genusBatrachostomus feeds almost exclusively on arthro-pods that are caught by pouncing from a perch orgleaning from branches and other surfaces (Cleere1998; del Hoyo et al. 1999). However, Podargus spe-cies, such as the Tawny Frogmouth, feed on smallvertebrates in addition to arthropods, all of whichare caught by swooping down onto prey from a perchin a similar fashion to owls (Cleere 1998; del Hoyoet al. 1999; Higgins 1999). In addition to these behav-ioral diVerences between frogmouth genera, thereare marked molecular and morphological diVerencesthat have led some authors to suggest that theyshould be placed in separate families (Sibley andAhlquist 1990; Mariaux and Braun 1996). BecauseBatrachostomus specimens are extremely rare in

Fig. 3 A scatterplot of log-transformed telencephalic volumes(mm3) against: a log-transformed body masses (g); and b logtransformed brain volume minus Wulst volume (mm3; seeTable 2). The symbols refer to the following: black diamondAegothelidae (Feline Owlet-nightjar, Aegotheles insignis); greysquares Caprimulgidae (nightjars); black square Nyctibiidae(Grey Potoo, Nyctibius griseus); black circle Podargidae (TawnyFrogmouth, Podargus strigoides); black triangle Steatornithidae(Oilbird, Steatornis caripensis); grey circles Strigiformes (owls);and open circles all other birds. Two sets of 95% conWdenceintervals are shown based upon least-squares linear regressionlines calculated for all other species of birds (see Table 3):conventional statistics (solid lines) and statistics that includephylogenetic information (dotted lines). Note that the FelineOwlet-nightjar is not included in the comparison of Wulst vol-ume and body mass because body mass was not available for thespecimen examined nor could an average body mass for this spe-cies be found in the literature

123

1322 J Comp Physiol A (2006) 192:1313–1326

museum collections, we were unable to examine one,so this study only reXects the condition present inPodargus frogmouths.

Another potential source of error is the sampling ofonly a single individual of each species. It should benoted, however, that variation within species is gener-ally far lower than that between species (Stephan andPirlot 1970; Pirlot and Bee de Speroni 1987; A. N. Iwa-niuk, unpublished data). Furthermore, the volumetricdiVerences reported herein between the owl-like andnightjar-like birds are substantial and it is unlikely thateven with the inclusion of additional specimens thatour conclusions would be signiWcantly altered.

Stereopsis and Wulst size

The combination of an enlarged Wulst and global stere-opsis in owls suggests that Wulst size and stereopsis arecorrelated. This is supported by the presence of a simi-larly enlarged Wulst in owlet-nightjars and frogmouths,which are thought to have stereoscopic vision (Pettigrew1986). Wulst expansion can, however, occur indepen-dently of stereopsis and vice versa. Diurnal raptors, forexample, have stereoscopic vision (Fox et al. 1977) andlarge numbers of binocular neurons in the visual Wulst(Pettigrew 1978), but do not have an enlarged Wulst(Iwaniuk and Hurd 2005, this study). Perhaps part of thereason for this seemingly inconsistent relationshipbetween stereopsis and Wulst size is that the Wulst is notan exclusively visual structure (Funke 1989; Wild 1997;Medina and Reiner 2000; Manger et al. 2002). Indeed,the rostral Wulst receives somatosensory projections(Wild 1997; Manger et al. 2002), has cells that areresponsive to tactile stimulation of the body, limbs, headand neck (Funke 1989) and in species that forage usingtactile information from the beak, the rostral Wulst isgreatly expanded (Pettigrew and Frost 1985). Given thata large Wulst is not essential to stereopsis per se, why isthe owl’s Wulst enlarged?

Fig. 4 A scatterplot of log-transformed Wulst volumes (mm3)against a log-transformed body masses (g); b log-transformedbrain volume minus Wulst volume (mm3); and c log-transformedtelencephalic volume minus Wulst volume (mm3) for all capri-mulgiform and owl species measured (Table 2). The symbolsrefer to the following: black diamond Aegothelidae (FelineOwlet-nightjar, Aegotheles insignis); grey squares Caprimulgidae(nightjars); black square Nyctibiidae (Grey Potoo, Nyctibius gri-seus); black circle Podargidae (Tawny Frogmouth, Podargusstrigoides); black triangle Steatornithidae (Oilbird, Steatornis car-ipensis); grey circles Strigiformes (owls); and open circles all otherbirds. Two sets of 95% conWdence intervals are shown basedupon least-squares linear regression lines calculated for all otherspecies of birds (see Table 3): conventional statistics (solid lines)and statistics that include phylogenetic information (dotted lines).As with Fig. 3, the Feline Owlet-nightjar is not included in thecomparison of Wulst volume and body mass because body masswas not available for the specimen examined nor could an aver-age body mass for this species be found in the literature

123

J Comp Physiol A (2006) 192:1313–1326 1323

One feature of the visual system that does set owlsapart from other birds is the amount of binocularoverlap in their visual Weld. As mentioned previouslyowls have a much larger area of horizontal Weld binoc-ular overlap (44–50°; Martin 1984; Pettigrew andKonishi 1984; Wylie et al. 1994) than other birds (hori-zontal mean = 20°; data from Martin and Katzir 1999).The visual Weld of owls is so unique that in their cate-gorization of avian visual Welds, Martin and Coetzee(2004) placed owls in a category all their own becauseof the broad frontal binocular Weld and extensive blindareas above and behind the head. Other birds havebinocular visual Welds (Martin and Katzir 1999; Martinand Coetzee 2004) and are capable of stereopsiswithin this Weld (e.g., McFadden and Wild 1986), butthis occupies only a small part of the entire visual Weld.For example, raptors have some degree of binocularoverlap in their visual Weld, but the area of binocular

overlap is much smaller than in owls (20–24° horizon-tally and 80° vertically) and as such, it is localized toonly a portion of the entire visual Weld (Wallman andPettigrew 1985; Martin and Katzir 1999). Despite thewidth of this Weld and the size of the Wulst, binocularneurons appear to far outnumber monocular neuronsin the American Kestrel’s (Falco sparverius) visualWulst (Pettigrew 1978) and they too are capable ofstereopsis (Fox et al. 1977). Perhaps the Wulstenlargement of owls reXects their wider stereoscopicWeld compared to diurnal raptors and other birds.Frogmouths do have a large binocular Weld similar tothat of owls and convergent eye movements (Wallmanand Pettigrew 1985), which suggests the presence ofglobal stereopsis (Pettigrew 1986). Based upon Wulstsize and morphology, it follows that owlet-nightjarsmight possess stereopsis as well, but this has yet to bedemonstrated behaviorally or physiologically.

Fig. 5 Shown here are sche-matic drawings of the Wulst architecture of: a Boobook Owl (Ninox boobook); b Spotted Nightjar (Eurostopo-dus argus); c Tawny Frog-mouth (Podargus strigoides); and d Feline Owlet-nightjar (Aegotheles insignis) (scale bar = 1 mm). Each layer of the Wulst is indicated as fol-lows: apical hyperpallium (HA), internal (IHAi) and external (IHAe) layers of the intercalated part of the apical hyperpallium, interstitial part of the hyperpallium (HI); densocellular part of the hy-perpallium (HD) (following nomenclature in Reiner et al. 2004). Additional structures indicated on the drawings in-clude: vallecula (V); medial striatum (MSt); mesopallium (M) and nidopallium (N)

123

1324 J Comp Physiol A (2006) 192:1313–1326

Curiously, the Oilbird has a moderately large degreeof binocular overlap (38–50°; Pettigrew and Konishi1984; Martin et al. 2004a, b) and a moderately enlargedWulst (Table 2; Fig. 4), but an electrophysiologicalstudy failed to Wnd binocular neurons in the OilbirdWulst (Pettigrew and Konishi 1984). Given that thedevelopment of the owl visual Wulst is sensitive tovisual input (Pettigrew and Konishi 1976), it is possiblethat binocular vision has been lost in the Oilbird as aconsequence of roosting deep within caves. The mod-erately enlarged Wulst could therefore be a “carry-over” from a stereoscopic ancestor, like a frogmouth,that has since been co-opted for another purpose, suchas somatosensory input to the rostral Wulst from therictal bristles (see above).

Wulst lamination

In addition to variation in Wulst size, there was alsosigniWcant variation in the degree of laminationobserved in the Wulst. Although, the gradation inWulst lamination could be an artifact of an enlargedWulst, it is equally probable that it reXects functionaldiVerences related to stereoscopic vision. The con-struction of neuronal sheets (or lamina) appears topermit the construction of complex topographicalmaps that are functionally segregated in a variety ofneural structures (Striedter 2005). In mammals, thelamination pattern of the neocortex varies signiW-cantly among mammalian taxa, such that some speciespossess more lamina than others (Preuss 2001) andthis variation is at least partially related to speciesdiVerences in connectivity (LaChica et al. 1993). Therelatively poorly laminated Wulst in some birds (e.g.,nightjar, potoo) compared to the relatively well-lami-nated Wulst of other birds (e.g., owls, frogmouth,owlet-nightjar) might also reXect functional diVer-ences. The darker staining of IHA and the promi-nence of the internal and external layers in thefrogmouth, owlet-nightjar and owls compared to thenightjars and potoo probably reXects a higher densityand/or number of cells and therefore a heavier inputinto the HA. While the IHA projects to telencephalicregions outside of the Wulst (e.g. frontolateral nid-opallium), the bulk of the IHA aVerents project dor-sally to the HA (Shimizu et al. 1995). Because most ofthe binocular, disparity sensitive neurons are foundwithin the HA (Pettigrew 1979; Nieder and Wagner2000, 2001) an increase in the amount of input to theHA, such as that provided by a larger or more denselypacked IHA, could reXect an increase in the numberof binocular neurons. This, however, remains to beveriWed.

Acknowledgments We wish to thank Carla Kishinami (BishopMuseum, Honolulu, HI, USA) and the staV of the National Muse-um of Natural History (Washington, DC, USA) for loaning speci-mens to us, Peter Holz and David Middleton of HealesvilleSanctuary for collecting frogmouths, owls and other species on ourbehalf, Barrie Frost for donating a saw-whet owl brain, the curato-rial staV of the Queensland Museum, Provincial Museum of Alber-ta, National Museum of Natural History, South AustralianMuseum, Australian National Wildlife Collection and Museum ofVictoria for access to their collections, Karen Dean, Sue Swann,Angela Nguyen, Kim Krueger and Erin Kelcher for technical assis-tance, Ted Garland for the PDAP software, Jack Pettigrew forhelpful discussions on Wulst physiology and two anonymousreviewers for their comments. Funding for this study was providedby the Natural Sciences and Engineering Research Council of Can-ada, Alberta Ingenuity Fund and Canada Research Chairs Pro-gram to ANI and DRWW. All of the research reported herein wasperformed in accordance with the “Principles of animal care”, pub-lication No. 86–23, revised 1985 of the National Institute of Healthand with the Canadian Council for Animal Care regulations.

References

Alma S, Bee de Speroni N (1992) Indices cerebrales y composi-cion cuantitativa encefalica en Athene cunicularia y Tyto alba(Strigiformes: Strigidae y Tytonidae). Facena 9:19–37

Boire D (1989) Comparaison quantitative de l’encephale de sesgrades subdivisions et de relais visuals, trijumaux et acous-tiques chez 28 especes. PhD Thesis, Universite de Montreal

Carezzano FJ, Bee de Speroni N (1995) Composicion volumetri-ca encefalica e indices cerebrales en tres aves de ambienteacuatico (Ardeidae, Podicipedidae, Rallidae). Facena 11:75–83

Christidis L, Schodde R, Shaw DD, Maynes SF (1991) Relation-ships among the Australo-Papuan parrots, lorikeets andcockatoos (Aves: Psittaciformes). Condor 93:302–317

Cleere N (1998) Nightjars: a guide to the nightjars, nighthawks,and their relatives. Yale University Press, New Haven

Cracraft J, Barker FK, Braun M, Harshman J, Dyke GJ, FeinsteinJ, Stanley S, Cibois A, Schikler P, Beresford P, Garcia-Moreno J, Sorenson MD, Yuri T, Mindell DP (2004) Phylo-genetic relationships among modern birds (Neornithes). In:Cracraft J, Donoghue MJ (eds) Assembling the tree of life.Oxford University Press, New York pp 468–489

Deacon TW (1990) Fallacies of progression in theories of brain-size evolution. Int J Primatol 11:193–236

Deaner RO, Nunn CL, van Schaik CP (2000) Comparative testsof primate cognition: diVerent scaling methods producediVerent results. Brain Behav Evol 55:44–52

del Hoyo J, Elliott A, Sargatal J (1999) Handbook of the birds ofthe world, vol 5. Barn owls to hummingbirds. Lynx Edicions,Barcelona

Denton CJ (1981) Topography of the hyperstriatal visual projec-tion area in the young domestic chicken. Exp Neurol 74:482–498

DimcheV DE. Drovetski SV, Mindell DP (2002) Phylogeny ofTetraoninae and other galliform birds using mitochondrial12S and ND2 genes. Mol Phylogenet Evol 24:203–215

Ebinger P (1995) Domestication and plasticity of brain organiza-tion in mallards (Anas platyrhynchos). Brain Behav Evol45:286–300

Ebinger P, Löhmer R (1984) Comparative quantitative investiga-tions on brains of rock doves, domestic and urban pigeons(Columba L. livia). Z Zool Syst Evol Forsch 22:136–145

123

J Comp Physiol A (2006) 192:1313–1326 1325

Ebinger P, Löhmer R (1987) A volumetric comparison of brainsbetween greylag geese (Anser anser L.) and domestic geese.J Hirnforsch 3:291–299

Ebinger P, Röhrs M (1995) Volumetric analysis of brain struc-tures, especially of the visual system in wild and domesticturkeys (Meleagris gallopavo). J Brain Res 36:219–228

Fernandez P, Carezzano F, Bee de Speroni N (1997) Análisis cu-antitativo encefálico e índices cerebrales en Aratinga acuti-caudata y Myiopsitta monachus de Argentina (Aves:Psittacidae). Rev Chil Hist Nat 70:269–275

Fox R, Lehmkuhle SW, Bush RC (1977) Stereopsis in the falcon.Science 197:79–81

Funke K (1989) Somatosensory areas in the telencephalon of thepigeon. I. Response characteristics. Exp Brain Res 76:603–619

Garland T Jr, Harvey PH, Ives AR (1992) Procedures for theanalysis of comparative data using phylogenetically indepen-dent contrasts. Syst Biol 41:18–32

Garland T Jr, Ives AR (2000) Using the past to predict the pres-ent: conWdence intervals for regression equations in phyloge-netic comparative methods. Am Nat 155:346–364

Higgins PJ (1999) Handbook of Australian, New Zealand andAntarctic birds, vol 4: parrots to dollarbird. Oxford Univer-sity Press, Melbourne

Iwaniuk AN, Dean KM, Nelson JE (2005) InterspeciWc allometryand the brain and brain regions in parrots (Psittaciformes):comparisons with other birds and primates. Brain BehavEvol 65:40–59

Iwaniuk AN, Hurd PL (2005) The evolution of cerebrotypes inbirds. Brain Behav Evol 65:215–230

Iwaniuk AN, Hurd PL, Wylie DRW (2006) Comparative mor-phology of the avian cerebellum: I. Degree of foliation. BrainBehav Evol 68:45–62

Iwaniuk AN, Nelson JE (2003) Developmental diVerences arecorrelated with relative brain size in birds: a comparativeanalysis. Can J Zool 81:1913–1928

Iwaniuk AN, Nelson JE (2002) Can endocranial volume be usedas an estimate of brain size in birds? Can J Zool 80:16–23

Karten HJ, Hodos W, Nauta WJH, Revzin AM (1973) Neuralconnections of the ‘visual Wulst’ of the avian telencephalon:Experimental studies in the pigeon (Columba livia) and owl(Speotyto cunicularia). J Comp Neurol 150:253–278

LaChica EA, Beck PD, Casagrande VA (1993) Intrinsic connec-tions of layer III of striate cortex in squirrel monkey andbush baby: correlations with patterns of cytochrome oxidase.J Comp Neurol 329:163–187

Livezey BC, Zusi RL (2001) Higher-order phylogenetics of mod-ern Aves based on comparative anatomy. Neth J Zool51:179–205

Manger PR, Elston GN, Pettigrew JD (2002) Multiple maps andactivity-dependent representational plasticity in the anteriorWulst of the adult barn owl (Tyto alba). Eur J Neurosci16:743–750

Mariaux J, Braun MJ (1996) A molecular phylogenetic survey of thenightjars and allies (Caprimulgiformes) with special emphasison the potoos (Nyctibiidae). Mol Phylogenet Evol 6:228–244

Martin GR (1984) The visual Welds of the tawny owl, Strix alucoL. Vision Res 24:1739–1751

Martin GR, Coetzee HC (2004) Visual Welds in hornbills: preci-sion-grasping and sunshades. Ibis 146:18–26

Martin GR, Katzir G (1999) Visual Welds in short-toed eagles,Circaetus gallicus (Accipitridae), and the function of binocu-larity in birds. Brain Behav Evol 53:55–66

Martin G, Rojas LM, Figueroa YMR, McNeil R (2004a) Binocularvision and nocturnal activity in oilbirds (Steatornis caripensis)and pauraques (Nyctidromus albicollis): Caprimulgiformes.Orn Neo 15:233–242

Martin G, Rojas LM, Ramirez Y, McNeil R (2004b) The eyes ofoilbirds (Steatornis caripensis): pushing at the limits of sensi-tivity. Naturwiss 91:26–29

Mayr G (2002) Osteological evidence for paraphyly of the avianorder Caprimulgiformes (nightjars and allies). J Ornithol143:82–97

McFadden SA, Wild JM (1986) Binocular depth perception in thepigeon. J Exp Anal Behav 45:149–160

Medina L, Reiner A (2000) Do birds possess homologues ofmammalian primary visual, somatosensory and motor cortic-es? Trends Neurosci 23:1–12

Nieder A, Wagner H (2001) Encoding of both vertical and hori-zontal disparity in random-dot stereograms by Wulst neu-rons of awake barn owls. Vis Neurosci 18:541–547

Nieder A, Wagner H (2000) Horizontal-disparity tuning of neu-rons in the visual forebrain of the behaving barn owl. J Neu-rophysiol 83:2967–2979

Perisic M, Mihailovic J, Cuenod M (1971) Electrophysiology ofcontralateral and ipsilateral visual projections to the Wulst inpigeon (Columba livia). Int J Neurosci 2:7–14

Pettigrew JD (1978) Comparison of the retinotopic organizationof the visual wulst in nocturnal and diurnal raptors, with anote on the evolution of frontal vision. In: Cool SJ, Smith EL(eds) Frontiers in visual science. Springer, Berlin HeidelbergNew York, pp 328–335

Pettigrew JD (1979) Binocular visual processing in the owl’s tel-encephalon. Proc R Soc Lond B 204:435–454

Pettigrew JD (1986) The evolution of binocular vision. In: Petti-grew JD, Sanderson KJ, Levick WR (eds) Visual neurosci-ence. Cambridge University Press, Cambridge, pp 208–222

Pettigrew JD, Frost BJ (1985) A tactile fovea in the Scolopaci-dae? Brain Behav Evol 26:95–105

Pettigrew JD, Konishi M (1976) Neurons selective for orientationand binocular disparity in the visual Wulst of the barn owl(Tyto alba). Science 193:675–678

Pettigrew JD, Konishi M (1984) Some observations on the visualsystem of the oilbird, Steatornis caripensis. Nat Geo Soc ResRep 16:439–450

Pirlot P, Bee de Speroni N (1987) Encephalization and braincomposition in South American rodents (Caviidae, Criceti-dae, Dasyproctidae). Mammalia 51:305–320

Porciatti V, Fontanesi G, RaVaelli A, Bagnoli P (1990) Binocular-ity in the little owl, Athena noctua II. Properties of visuallyevoked potentials from the Wulst in response to monocularand binocular stimulation with sine wave gratings. BrainBehav Evol 35:40–48

Preuss TM (2001) The discovery of cerebral diversity: an unwel-come scientiWc revolution. In: Falk D, Gibson K (eds) Evo-lutionary anatomy of the primate cerebral cortex. Afeitschrift for Harry Jerison. Cambridge University Press,Cambridge, pp 138–164

Rehkämper G, Frahm HD, Zilles K (1991) Quantitative develop-ment of brain and brain structures in birds (Galliformes andPasseriformes) compared to that in mammals (insectivoresand primates). Brain Behav Evol 37:125–143

Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, KuenzelW, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M,Ball GF, Durand S, Güntürkun O, Lee DW, MelloCV, Powers A, White SA, Hough G, Kubikova L, SmuldersTV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J,Siang C, Jarvis ED (2004) Revised nomenclature for aviantelencephalon and some related brainstem nuclei. J CompNeurol 473:377–414

Reiner A, Yamamoto K, Karten HJ (2005) Organization andevolution of the avian forebrain. Anat Rec 287A:1080–1102

123

1326 J Comp Physiol A (2006) 192:1313–1326

Sheldon FH, Jones CE, McCracken KG (2000) Relative patternsand rates of evolution in heron nuclear and mitochondrialDNA. Mol Biol Evol 17:437–450

Sherry DF, Vaccarino AL, Buckenham K, Herz HS (1989) Thehippocampal complex of food-storing birds. Brain BehavEvol 34:308–317

Shimizu T, Karten HJ 1993 The avian visual system and the evo-lution of the neocortex. In: Zeigler HP, Bischof HJ (eds) Vi-sion, brain and behavior in birds. MIT Press, Cambridge, pp103–114

Shimizu T, Cox K, Karten HJ (1995) Intratelencephalic projec-tions of the visual wulst in pigeons (Columba livia). J CompNeurol 359:551–572

Sibley CG, Ahlquist JE (1990) Phylogeny and classiWcation ofbirds. Yale University Press, New Haven

Stephan H, Pirlot P (1970) Volumetric comparisons of brainstructures in bats. Z Zool Syst Evol Forsch 8:200–236

Stingelin W (1958) Vergleichend morphologische Untersuchungenam Vorderhirn der Vögel auf cytologischer und cytoarchitek-tonischer Grundlage. Verlag Helbing & Lichtenhahn, Basel

Striedter GF (2005) Principles of brain evolution. Sinauer,Sunderland

van der Willigen RF, Frost BF, Wagner H (1998) Stereoscopicdepth perception in the owl. NeuroReport 9:1233–1237

Wagner H, Frost B (1993) Disparity-sensitive cells in the owlhave a characteristic disparity. Nature 364:796–798

Wallman J, Pettigrew JD (1985) Conjugate and disjunctive sac-cades in two avian species with contrasting oculomotor strat-egies. J Neurosci 5:1418–1428

Wild JM (1997) The avian somatosensory system: the pathwayfrom wing to Wulst in a passerine (Chloris chloris). BrainRes 759:122–134

Wilson P (1980) The organization of the visual hyperstriatum inthe domestic chick. I. Topology and topography of the visualprojection. Brain Res 188:319–332

Wink M, Sauer-Gürth H, Fuchs M (2004) Phylogenetic relation-ship in owls based on nucleotide sequences of mitochondrialand nuclear marker genes. In: Chancelor RD, Meyburg B-U(eds) Raptors worldwide. WWGBP, Berlin, pp 517–526

Wylie DR, Shaver SW, Frost BJ (1994) The visual response prop-erties of neurons in the nucleus of the basal optic root of thenorthern saw-whet owl (Aegolius acadicus). Brain BehavEvol 43:15–25

123