The Evolution of Stereopsis and the Wulst in Caprimulgiform Birds: a Comparative Analysis
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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 to stereopsis and the Wulst both within the order and perceive depth from retinal disparity cues), but its dis- birds in general. tribution amongst other birds has remained largely unexplored. Here, we present data on species variation Keywords Wulst · Caprimulgiformes · Evolution · in brain and telencephalon size and features of the Stereopsis · Strigiformes Wulst, the neuroanatomical substrate that subserves stereopsis, in a putative sister-group to owls, the order Caprimulgiformes. The caprimulgiforms we examined Introduction included nightjars (Caprimulgidae), owlet-nightjars (Aegothelidae), potoos (Nyctibiidae), frogmouths A series of neurophysiological, neuroanatomical and (Podargidae) and the Oilbird (Steatornithidae). The behavioral experiments has demonstrated that owls owlet-nightjars and frogmouths shared almost identical possess a visual system that is very similar to primates relative brain, telencephalic and Wulst volumes as well (van der Willigen et al. 1998) and cats insofar as it is as overall brain morphology and Wulst morphology designed to subserve stereopsis. At least two features with owls. SpeciWcally, the owls, frogmouths and owlet- of the owl visual system sets them apart from most nightjars possess relatively large brains and telence- other birds. First, owl eyes are positioned frontally, phalic and Wulst volumes, had a characteristic brain such that they have a large area of binocular visual Weld shape and displayed prominent laminae in the Wulst. overlap [44 to >50° horizontally; Barn Owl (Tyto alba), In contrast, potoos and nightjars both had relatively Pettigrew and Konishi 1984; Tawny Owl (Strix aluco), small brains and telencephala, and Wulst volumes that Martin 1984; Northern Saw-whet Owl (Aegolius acadi- are typical for similarly sized birds from other orders. cus), Wylie et al. 1994]. Although all birds have some The Oilbird had a large brain, telencephalon and degree of binocular overlap (Martin and Katzir 1999), Wulst, although these measures were not quite as large the magnitude pales in comparison to that of owls as those of the owls. This gradation of owl-like versus (Martin and Coetzee 2004). Second, compared to other nightjar-like brains within caprimulgiforms has signiW- species, owls have a grossly hypertrophied visual Wulst cant implications for understanding the evolution of (Stingelin 1958; Karten et al. 1973; Pettigrew 1979; Iwaniuk and Hurd 2005), the putative homolog of mammalian primary visual cortex (V1) (e.g., Shimizu and Karten 1993; Medina and Reiner 2000; Reiner A. N. Iwaniuk (&) · D. R. W. Wylie Department of Psychology, University of Alberta, et al. 2005). Recordings from the owl Wulst reveal that Edmonton, AB, Canada T6G 2E9 it is functionally like V1; Wulst neurons are selective e-mail: [email protected] for orientation, movement direction, spatial frequency and binocular disparity (Pettigrew and Konishi 1976; D. R. W. Wylie Centre for Neuroscience, University of Alberta, Pettigrew 1979; Porciatti et al. 1990; Wagner and Frost Edmonton, AB, Canada T6G 2E9 1993; Nieder and Wagner 2000, 2001). Critically, the 123 1314 J Comp Physiol A (2006) 192:1313–1326 vast majority (86%) of neurons are binocular and documented a large amount of variation in Wulst size tuned to a particular disparity (Pettigrew 1979). Binoc- and structure in birds, but did not provide any ular neurons are present in the Wulst of other species, detailed volumetric data for the Wulst or its constitu- but they are not as numerous as they are in owls (e.g., ent regions and only included a single caprimulgiform Perisic et al. 1971; Pettigrew 1978; Wilson 1980; Den- (Caprimulgus europaeus). If claims of stereopsis in ton 1981). Although the role of the Wulst in stereopsis the owlet-nightjar and frogmouth are correct (Petti- has yet to be deWnitively proven, the available neural grew 1986), then we would expect to see an enlarge- evidence from owls suggests that the Wulst mediates ment of the Wulst in both families such that they are stereopsis. similar to owls. Similarly, the relative size of the While it is clear that the owls have evolved global Wulst could indicate whether potoos have stereo- stereopsis (i.e., depth perception throughout all or scopic vision or not. Enlargement of the Wulst can most of the visual Weld) independently from mammals also result in an increase in overall brain and telence- (Pettigrew 1986), its evolution and phylogenetic distribu- phalic volumes (Iwaniuk et al. 2005; Iwaniuk and tion within birds has not been investigated. Owls are Hurd 2005) and changes in Wulst morphology (Sting- considered by some to be closely related to the order elin 1958). We therefore surveyed the Wve currently Caprimulgiformes (Sibley and Ahlquist 1990; Livezey recognized caprimulgiform families and examined the and Zusi 2001), which is a diverse assemblage of noc- following features: brain size and morphology, telen- turnal birds. Three families within the Caprimulgiformes cephalic size and Wulst size and morphology. possess frontal eye position comparable to owls: frog- mouths (Podargidae; binocular overlap = 50° horizon- tally; Wallman and Pettigrew 1985), owlet-nightjars Methods (Aegothelidae) and Oilbird (Steatornis caripensis, Steatornithidae; binocular overlap = 38–50°, Pettigrew Specimens and Konishi 1984; Martin et al. 2004a, b). Nightjars (Caprimulgidae), on the other hand, have a narrower Brain volumes were measured from Wxed brains as binocular visual Weld (25°; Martin et al. 2004b). Lastly, well as endocranial volumes (Iwaniuk and Nelson nothing is known about the visual Weld or abilities of 2002) of skeletal specimens (Table 1). These data the Wfth family: the potoos (Nyctibiidae). included measurements from over 200 individuals Stereopsis is thought to be present in both owlet- representing 18 caprimulgiform and 40 owl (Strigifor- nightjars and frogmouths (Pettigrew 1986) because of mes) species. Fixed brains of a Spotted Nightjar their frontal eye position and an area of binocular (Eurostopodus argus), Barn Owl (Tyto alba) Boo- visual overlap comparable to that of owls (Wallman book Owls (Ninox boobook, n = 2) and Tawny Frog- and Pettigrew 1985; Pettigrew 1986). However, there mouths (Podargus strigoides, n = 3) were extracted are no behavioral studies that demonstrate stereopsis from carcasses obtained as roadkills and from Heales- and no reports of electrophysiogical investigations of ville Sanctuary (Healesville, VIC, Australia). Grey the Wulst for either family. With respect to the Oilbird, Potoo (Nyctibius griseus), Oilbird, Pauraque (Nycti- electrophysiological investigations failed to Wnd any dromus albicollis) and Feline Owlet-nightjar (Aegoth- binocular neurons in the Wulst (Pettigrew and Konishi eles insignis) specimens were loaned to us from the 1984), despite the presence of a broad area of binocu- National Museum of Natural History (Washington, lar visual Weld overlap (Pettigrew and Konishi 1984; DC, USA) and the Bishop Museum (Honolulu, HI, Martin et al. 2004a, b). Finally, Pettigrew (1986) USA) and a Northern Saw-whet Owl was donated by reported that there was no evidence of binocular neu- B.J. Frost (see Table 2). The brains of all of the rons in the Wulst of nightjars based on both electro- museum specimens, which were all stored in 70% eth- physiological and anatomical investigations, but details anol for up to 45 years, were extracted and placed are lacking. into buVered 4% paraformaldehyde. They were sub- Given that both the owls and frogmouths possess a sequently placed into 30% sucrose in 0.1 M phos- grossly enlarged Wulst (Pettigrew 1986; Iwaniuk and phate buVered saline until they sank. The brains were Hurd 2005) and owls, and possibly frogmouths, pos- then embedded in gelatin and serially sectioned in the sess stereopsis (Pettigrew 1986), it is conceivable that transverse plane on a freezing stage microtome at Wulst enlargement underlies functional global stere- 40 m. The sections were collected in 0.1 M phos- opsis. Currently, little is known about how the rela- phate buVered saline, mounted onto gelatinized tive size of the Wulst varies among birds and this is slides, stained for Nissl substance with thionin and especially true of caprimulgiforms. Stingelin (1958) coverslipped 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 Body volume mass (g) (mm3) Caprimulgiformes Aegothelidae Australian owlet-nightjar Aegotheles cristatus 81,42041.0 Caprimulgidae Chuck-will’s-widow Caprimulgus carolinensis 9 1,360 109.5 European nightjar Caprimulgus europaeus 10 880 67.0 Large-tailed nightjar Caprimulgus macrurus 91,01078.0 Whip-poor-will Caprimulgus vociferus 10 820 50.8 Common nighthawk Chordeiles minor 10 850 57.1 Spotted nightjar Eurostopodus argus 21,24072.0 Great eared-nightjar Eurostopodus macrotis 5 1,460 168.8 White-throated nightjar Eurostopodus mystacialis 2 1,330 170.0 Pennant-winged nightjar Macrodipteryx vexillarius 687066.1 Pauraque Nyctidromus albicollis 891056.6 Ocellated poorwill Nyctiphrynus