BINOCULAR VISION AND NOCTURNAL ACTIVITY IN OILBIRDS ... · BINOCULAR VISION AND NOCTURNAL ACTIVITY...

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233 ORNITOLOGIA NEOTROPICAL 15 (Suppl.): 233–242, 2004 © The Neotropical Ornithological Society BINOCULAR VISION AND NOCTURNAL ACTIVITY IN OILBIRDS (STEATORNIS CARIPENSIS) AND PAURAQUES (NYCTIDROMUS ALBICOLLIS): CAPRIMULGIFORMES Graham R. Martin 1 , Luz Marina Rojas 2 , Yleana Maria Ramirez Figueroa 2 , & Raymond McNeil 3 1 School of Biosciences, The University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK. E-mail: [email protected] 2 IIBCA, Universidad de Oriente, Avenida Universidad, Cerro del Medio. Apartado de correos 094, Cumaná, Sucre, Venezuela. 3 Département de sciences biologiques, Université de Montréal, C.P. 6128, Succ. “Centre- ville”, Montréal, Quebec H3C 3J7, Canada. Resumen. – Visión binocular y actividad nocturna en el Guácharo (Steatornis caripensis) y el Chota- cabras Pauraque (Nyctidromus albicollis). – Las características del campo visual fueron medidas en el Guácharo (Steatornis caripensis) y el Chotacabras pauraque (Nyctidromus albicollis) utilizando una técnica de reflejo oftalmoscópico. Aunque los ojos de estas aves dan la apariencia de estar desplazados frontalmente, en la práctica, sus campos binoculares funcionales son relativamente estrechos, con un máximo de 38° de anchura y un alcance vertical de 100° para el Guácharo, y 25° x 110° para el Chotacabras pauraque. La anchura máxima se ubico en 10° arriba del eje horizontal en ambas especies. En el Chotacabras pauraque, el área ciega detrás de la cabeza es igual a 89°, mientras que el campo retiniano monocular es de 148°. El campo binocular aparente (óptico) es de 65° de ancho, en comparación con el campo funcional (retiniano) de 25° aproximadamente. Los campos binoculares de estas aves preponderantemente nocturnas son similares a los de especies de aves primordialmente diurnas. Esto sustenta la hipótesis de que la binocularidad en aves tiene que ver más con la proyección contra-lateral de cada ojo que con la habilidad de lograr imágenes dispares del mismo objeto desde los dos ojos. Tales proyecciones contra-laterales terminan en una sección del campo de cada ojo que proporciona un campo óptico de flujo simétricamente ampliado, en vez de funcionar como una base para la extracción de una información de orden más elevado a partir de imágenes dispares. Abstract. – Visual field characteristics were measured using an ophthalmoscopic reflex technique in Oil- birds (Steatornis caripensis) and Pauraques (Nyctidromus albicollis). Despite these birds’ apparent frontal-eyed appearance, their functional binocular fields are relatively small with a maximum width of 38º and vertical extent of 100º in Oilbirds, and 25º x 110º in Pauraques. Maximum width occurred 10º above the horizontal in both species. In Pauraques, the blind area behind the head equals 89º and the monocular retinal field equals 148º. The apparent (optical) binocular field is 65º wide, compared with the functional (retinal) field approx. 25º. The binocular fields in these highly nocturnal birds are similar to those of strongly diurnal species. This supports the hypothesis that binocularity in birds is concerned with the contra lateral projec- tion of each eye rather than achieving disparate images of the same object from two eyes. These contra lat- eral projections result in a section of the field in each eye that provides a symmetrically expanding optic flow field, rather than a basis for the extraction of higher order information from disparate images. Accepted 30 September 2003. Key words: Oilbird, Pauraques, Steatornis caripensis, Nyctidromus albicollis, vision, birds, binocular, visual fields, binocularity.

Transcript of BINOCULAR VISION AND NOCTURNAL ACTIVITY IN OILBIRDS ... · BINOCULAR VISION AND NOCTURNAL ACTIVITY...

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ORNITOLOGIA NEOTROPICAL 15 (Suppl.): 233–242, 2004© The Neotropical Ornithological Society

BINOCULAR VISION AND NOCTURNAL ACTIVITY IN OILBIRDS (STEATORNIS CARIPENSIS) AND PAURAQUES (NYCTIDROMUS

ALBICOLLIS): CAPRIMULGIFORMES

Graham R. Martin1, Luz Marina Rojas2, Yleana Maria Ramirez Figueroa2, & Raymond McNeil3

1School of Biosciences, The University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK. E-mail: [email protected]

2IIBCA, Universidad de Oriente, Avenida Universidad, Cerro del Medio. Apartado de correos 094, Cumaná, Sucre, Venezuela.

3Département de sciences biologiques, Université de Montréal, C.P. 6128, Succ. “Centre-ville”, Montréal, Quebec H3C 3J7, Canada.

Resumen. – Visión binocular y actividad nocturna en el Guácharo (Steatornis caripensis) y el Chota-cabras Pauraque (Nyctidromus albicollis). – Las características del campo visual fueron medidas en elGuácharo (Steatornis caripensis) y el Chotacabras pauraque (Nyctidromus albicollis) utilizando una técnica dereflejo oftalmoscópico. Aunque los ojos de estas aves dan la apariencia de estar desplazados frontalmente,en la práctica, sus campos binoculares funcionales son relativamente estrechos, con un máximo de 38° deanchura y un alcance vertical de 100° para el Guácharo, y 25° x 110° para el Chotacabras pauraque. Laanchura máxima se ubico en 10° arriba del eje horizontal en ambas especies. En el Chotacabras pauraque,el área ciega detrás de la cabeza es igual a 89°, mientras que el campo retiniano monocular es de 148°. Elcampo binocular aparente (óptico) es de 65° de ancho, en comparación con el campo funcional (retiniano)de 25° aproximadamente. Los campos binoculares de estas aves preponderantemente nocturnas sonsimilares a los de especies de aves primordialmente diurnas. Esto sustenta la hipótesis de que labinocularidad en aves tiene que ver más con la proyección contra-lateral de cada ojo que con la habilidadde lograr imágenes dispares del mismo objeto desde los dos ojos. Tales proyecciones contra-lateralesterminan en una sección del campo de cada ojo que proporciona un campo óptico de flujo simétricamenteampliado, en vez de funcionar como una base para la extracción de una información de orden más elevadoa partir de imágenes dispares.

Abstract. – Visual field characteristics were measured using an ophthalmoscopic reflex technique in Oil-birds (Steatornis caripensis) and Pauraques (Nyctidromus albicollis). Despite these birds’ apparent frontal-eyedappearance, their functional binocular fields are relatively small with a maximum width of 38º and verticalextent of 100º in Oilbirds, and 25º x 110º in Pauraques. Maximum width occurred 10º above the horizontalin both species. In Pauraques, the blind area behind the head equals 89º and the monocular retinal fieldequals 148º. The apparent (optical) binocular field is 65º wide, compared with the functional (retinal) fieldapprox. 25º. The binocular fields in these highly nocturnal birds are similar to those of strongly diurnalspecies. This supports the hypothesis that binocularity in birds is concerned with the contra lateral projec-tion of each eye rather than achieving disparate images of the same object from two eyes. These contra lat-eral projections result in a section of the field in each eye that provides a symmetrically expanding opticflow field, rather than a basis for the extraction of higher order information from disparate images.Accepted 30 September 2003.

Key words: Oilbird, Pauraques, Steatornis caripensis, Nyctidromus albicollis, vision, birds, binocular, visualfields, binocularity.

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INTRODUCTION

In all eye types visual performance is a com-promise between the conflicting fundamentalcapacities of sensitivity and resolution (Land& Nilsson 2002). The balance of these capac-ities in any one eye is achieved through adap-tations of both optical and retinal structures,and this balance of sensitivity and resolutionis assumed to reflect both the behavior andthe ecology of the species (Archer et al. 1999).In most birds, flight is considered to be con-trolled primarily by vision which requires ahigh degree of spatial resolution (Davies &Green 1994) and that this outweighs therequirements for high sensitivity. However, asmall number of birds are active in naturallylow light-levels, where high sensitivity isrequired (Martin 1990). The majority of suchnocturnally active species are found amongthe owls (Strigiformes) and the nightjars andtheir allies (Caprimulgiformes). It is amongbirds from these orders that adaptations ofoptical and retinal structures that haveevolved to maximize sensitivity are likely tobe found. Some owls live an almost exclu-sively nocturnal lifestyle under the cover ofclosed canopy woodlands and must experi-ence some of the lowest naturally occurringnatural light levels (Martin 1990). Nightjars,although mainly nocturnal, tend to fly in theopen airspace above tree canopies or insparsely vegetated habitats and hence experi-ence higher night time light levels. However,the most extreme example of a low light-levellifestyle among flying birds is provided by thecave dwelling Oilbirds (Steatornis caripensis, Ste-atornithidae, Caprimulgiformes) (Thomas1999). Recent investigation of the adaptationsof Oilbird and nightjar eyes to these noctur-nal conditions (Rojas et al. 2004) have shownthat the retina of Oilbirds exhibits extremeadaptations for sensitivity. Rod photorecep-tors occur at a very high density that isachieved by the receptors being arranged

irregularly in a various-tiered structure of akind hitherto described only among deep-seafish (Locket 1977). However, compared withowl eyes, the overall eye size and entrancepupil diameter of Oilbird eyes are not excep-tional.

It has been assumed that large binocularfields are also associated with the nocturnalhabit and that this feature of visual topogra-phy is typically combined with adaptationsof optics and retinal structures to constitutea syndrome of adaptations associated withthe nocturnal habit, e.g., Walls 1942, Tansley1965, Welty & Baptista 1988, Voous 1988).However, investigation of visual fields inTawny Owls (Strix aluco, Strigidae) has alreadyshown the binocular region to be consider-ably smaller than appears from anecdotalobservation with a maximum width of 47º(Martin, 1984). It is also clear than binocularfield size is not maximized within constraintsimposed by the eye’s optics. For example,it has been shown that if full use weremade of the optical field of each eye thenmaximum binocular field width wouldequal 111º in Tawny Owls. Never-the-less,interspecific comparison has shown thatthe binocular field of owls are the broadestrecorded in birds with the majority ofspecies having a maximum binocularfield width between 20º and 30º, and insome species binocular fields are only 10º inmaximum width (Martin & Katzir 1999).These interspecific comparisons havelead to the hypothesis that binocularityin birds is not primarily concerned withhaving two eyes looking at the same scenein order to extract higher order informationfrom their disparate images, but is simply aconsequence of placing each eye so as tohave a portion of its field facing forward forthe extraction of information from anexpanding optical flow field (Martin & Katzir1999). Within this framework, the width ofthe binocular field of any particular species is

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viewed as determined by the need for anexpanding flow field for the control offlight or of head movements. This is balancedagainst requirements for lateral vision,with the balance moderated by the degreeto which other senses are involved inforaging tasks (Martin & Katzir 1999).To test the wider generality of the associationof a wider frontal binocular field andnocturnality, and the above hypothesisconcerning the general function of binocu-larity in birds, we have determined the

binocular field characteristics of Oilbirdsand Pauraques (Nyctidromus albicollis,Caprimulgidae).

Oilbirds (Fig. 1) breed and roost in cavesoften at sufficient depth that no daylight canpenetrate, and this must result in the majorityof individuals never experiencing throughouttheir life-time natural light levels above thoseof maximum moonlight (maximum recordedlife-span 12 years) (Thomas 1999). Withincaves, Oilbirds employ echolocation usingaudible click vocalizations which provides low

FIG. 1. Oilbird (Steatornis caripensis) and Pauraques (Nyctidromus albicollis): Top, three quarter views of theheads showing the prominent eyes and long rictal bristles. Bottom, frontal views of the heads taken fromthe horizontal plane (as defined in Figures 2 and 3).

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spatial resolution to avoid in-flight collisions(Konishi & Knudsen 1979) although, due to alow wing loading, flight speeds are low (Tho-mas 1999). However their nocturnal foragingfor fruits is thought to be guided primarily byvision, with olfaction playing a secondary role(Snow 1961).

Pauraques (Fig. 1) inhabit more open hab-itats where they forage on the wing betweendusk and dawn for insects flying in the openairspace above vegetation (Cleere 1999). Atnight they are likely to experience similar lightregimes to the Oilbirds, but since they are notcave dwelling they are more likely to beexposed to crepuscular light levels when for-aging and may be exposed to high daytimelight levels when roosting.

METHODS

Oilbirds and Pauraques were obtained underlicense from the Instituto de Parques ofVenezuela. Oilbirds were obtained from thebreeding colony, Cueva del Guácharo, in theParque Nacional El Guácharo near Caripe,northeastern Venezuela. Pauraques wereobtained in the Mapire region (State ofAnzoátegui) in farmland situated within theVenezuelan llanos habitat type. Birds werecaught after dusk by the use of spotlights andthrow-nets.

Visual field parameters were determinedin live birds (three birds of each species) usingan ophthalmoscopic reflex technique as usedpreviously with a range of bird species (Mar-tin & Katzir 1995). Each bird was restrainedwith the body immobilized and the head posi-tion fixed by holding the bill. In Oilbirds thebill was held in a specially built metal holdercoated with cured silicone sealant to producea non-slip surface and the bill held in positionby tape (Micropore®). In Pauraques, becauseof the small bill size, the head was held manu-ally in position within a specially designedholder but it was not taped in position. The

body was held in a cradle of foam rubber andsecured by straps (Velcro®). The bill holderwas mounted on an adjustable mechanismand the head positioned so that the mid-pointof a line joining the corneal vertices was at theapproximate centre of the visual perimeterapparatus. The perimeter's co-ordinate systemfollowed conventional latitude and longitudewith the equator aligned vertically in the birds'median sagittal plane and this co-ordinatesystem is used for the presentation of thevisual field data (Fig. 2). Each bird’s head waspositioned with the plane through the eyesand bill tip pointing at an angle of approxi-mately 20° below the horizontal. Heads inthis position are depicted in Figure 2. Theprojection of the bill tip when measurementswere made was determined accurately fromphotographs and the visual field data cor-rected for this.

The eyes were examined using an ophthal-moscope mounted on the perimeter arm. Thevisual projections of the limits of the frontalretinal visual field at elevations above andbelow the bill for each eye were determined asa function of elevation (10° intervals) in themedian sagittal plane. The retinal visual fieldis the functional visual field. It is defined asthat portion of the optical visual field that isserved by retina. The optical visual field is thelimit of visual field determined by the eye’soptical system. It is this optical field that isseen in casual observations of the eye and itslimit is defined by the positions from which itis possible to look through the pupil andobserve the black pigmentation of the fundus.The retinal field is always smaller than theoptical field. In birds, this gives rise to theimpression that visual fields, including frontalbinocular fields, are more extensive than theyfunctionally are.

In the Pauraques, we were able to deter-mine the limit of the optical field at elevationsabout the horizontal as well as the limits ofthe retinal field at all elevations in the frontal

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sector. We also determined the limit of theretinal and optical fields in the horizontalplane directly behind the head in both Oil-birds and Pauraques. By combining thesemeasures with those for the frontal field limitin the same horizontal, plane we were able todetermine the total width of each monocularretinal field and the extent of the blind area inthe horizontal plane.

Procedures, which in other bird species,e.g., herons (Martin & Katzir 1994), have

readily elicited eye movements when birds arepositioned in this apparatus (such as light tap-ping sounds and flashes of light in the periph-ery of the visual field) were employed todetermine whether spontaneous eye move-ments were present and, if present, to mea-sure their maximum amplitude. This can beachieved by determining the extreme posi-tions at which the limit of the retinal fieldprojects at different elevations. For a detaileddescription of the apparatus and methods, see

FIG. 2. Perspective views of the projection of the binocular fields in Oilbirds and Pauraques. For co-ordi-nates the diagram uses the conventional latitude and longitude system but with the equator aligned verti-cally in the median sagittal plane of the head. Grids are at 20º intervals. It should be imagined that eachbird’s head lies at the centre of a transparent sphere with the features of the field projected onto its sur-face. The birds’ heads are pointing to the left of the observer in a position similar to the view shown inFigure 1 but at a more acute angle. The sketch (taken from a photograph) shows each head in the correctvertical orientation for the co-ordinate system. This was also the approximate head-bill angle employedwhen measurements were made.

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(Martin & Katzir (1994). From these data, topographical maps

of the frontal visual fields (corrected forviewing from an hypothetical viewing pointplaced at infinity) were constructed for eachspecies.

RESULTS

Despite these birds’ apparent frontal-eyedappearance (Fig. 1), their functional binocularfields are relatively small with a maximumwidth of 38º and a vertical extent of 100º in

FIG. 3. Horizontal section through the visual field of the Pauraques. The plane of the section is the hori-zontal of Figure 2. The area of overlap of the optical fields is defined by the positions of the optical fieldmargins. The apparent binocular field equals 65º, compared with the functional (retinal) field of 25º. Eachmonocular retinal field extends to 148º. The blind sector behind the head equals 89º.

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Oilbirds, and a maximum width of 25º andvertical extent of 110º in Pauraques (Fig. 2).Maximum width occurred 10º above the hori-zontal in our coordinate system in both spe-cies. We did not record spontaneous eyemovements in either species. A sectionthrough the complete visual field in the hori-zontal plane of Pauraques (Fig. 3) shows thatthe blind area behind the head is 89º with themonocular retinal field equaling 148º and themonocular optical field equaling 168º. Thisproduces an optical binocular field of 65º,compared with the retinal (functional) field ofapproximately 25º. Thus although Pauraquesappear (Fig. 1) to have a broad binocular field,the functional field has a maximum with ofapproximately only 40% that of the apparentfield (Fig. 3).

DISCUSSION

Binocularity and nocturnality. The overallbinocular field shape of Oilbirds (38ºmaximum width x 100º height) is broaderbut shorter than that of Pauraques (25º x110º). The binocular fields of these speciesare both narrower and longer than thatof Tawny Owls in which binocular fieldsmeasure 47º (maximum width) x 80º (verticalextent). Since all three species have incommon a highly nocturnal lifestyle, thisresult does not support the hypothesisthat the nocturnal habit in birds results in aconvergence upon common visual fieldtopography. Rather it supports the hypothesisthat visual field topography is associated withforaging behavior and the extent to whichsensory cues other than vision are employedin the location and taking of food items ratherthan the general level of ambient illuminationat which birds are active (Martin & Katzir1999).

The 20º wide sector at the periphery ofthe frontal fields that is not served by retinawhich we found in Pauraques is found also

in owls. However, this feature is not associ-ated with the nocturnal habit since it is alsofound in a wide range of diurnally active spe-cies. This suggests that in no bird species isfrontal binocular field width maximizedwithin the constraints imposed by the eye’soptical system. In all species examined todate, including the Pauraques (Fig. 3), theextent of the retinal visual fields to the rear ofthe head are maximized within the opticalfield and there is no blind optical margin tothe visual field.

The generally long and narrow natureof the binocular field in the two species ofthis investigation is similar to the binocularfields of a wide range of mainly diurnallyactive birds that differ markedly in bothphylogeny and behavioral ecology. Thesespecies have binocular fields that range intheir maximum width of between 20º and30º, coupled with a vertical extent of between100º and 180º. Among the diurnally activespecies showing this topography are RockDoves (Columba livia), various species ofherons, albatrosses, penguins, hornbills,and Short-toed Eagles (Circaetus gallicus)(Katzir & Martin 1994, 1998; Martin 1998,1999; Martin & Katzir 1999, Martin &Coetzee in press).

Projection of the bill tips in relation to the binocularfield. In all of the species discussed immedi-ately above, the projection of the bill tip fallsclose to the locus of maximum binocular fieldwidth, and is located approximately centrallyor slightly below centre. However, in Oilbirdsand Pauraques, the projection of the bill tipfalls towards the lower periphery of the binoc-ular field in a manner similar to that foundamong owls, ducks and long-billed shorebirds(Martin 1984, 1986b; Martin 1994, Guille-maine et al. 2002). These are species that relymainly upon non-visual cues to locate preyitems. The long-billed shorebirds and ducksprimarily employ tactile and chemical cues

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from the bill to locate prey items while theowls employ auditory cues (Martin 1986a).This suggests that, when Oilbirds are forag-ing, visual cues may play only a general orien-tation role with the prominent rictal bristles(Fig. 1a) providing close range tactile cues andolfaction providing more distant cues to foodsources. The principal sensory cues used byPauraques when feeding for insects is notknown but the anatomical structures associ-ated with feeding among Caprimulgidaeincludes a wide gape produced by adaptationof the lower jaw (Buhler 1970) and long rictalbristles, and both anatomical features arefound in Pauraques. Together these producean extensive area for trawling small insectsfrom the air space, although it is possible thatsome Caprimulgiform birds take some itemsfrom the ground or through the pursuit oflarger individual items that are typically takenin flight from below, e.g. foraging behaviorsdescribed in European Nightjars (Caprimulguseuropaeus) (Schlegel 1967, Cramp 1985, Cleere1999).

The high degree of specialization of theOilbirds’ and Pauraques’ retinal structures forthe maximization of sensitivity at the expenseof resolution (high densities of rod receptorsin both species, which in Oilbirds arearranged in a various banked structure, andthe presence of a tapetum in Pauraques)(Rojas et al. 2004), also suggests that visionin both of these species is employed primarilyfor general orientation, rather than pursuit ofindividual food items which would requirehigh acuity. However, more detailed observa-tions of feeding behavior are clearly required.The positioning of the bill towards the loweredge of the visual field may be indicativethat these birds approach larger individualitems from below (as reported in EuropeanNightjars), when they would be more easilyseen in silhouette against the night sky(Martin, 1990). The eyes appear to be ori-ented slightly upwards (Fig. 1) but we were

unable to determine the projections of theoptic axes that would have verified this obser-vation.The function of binocularity in Oilbirds and Pau-raques. It has been hypothesized that binocu-larity in birds is not concerned primarily withthe extraction of higher order cues fromdisparate views of the same scene (Martin& Katzir 1999), although it may play thisrole in certain granivorous birds whenforaging on the ground (McFadden 1994).The presence of a relatively narrow frontalbinocular field in both of the stronglynocturnal forms investigated here, coupledwith the high sensitivity-low resolution retinalstructures, suggests that cues for the detec-tion of the small disparities between theimages of the two eyes in these species arelikely to be minimal. This supports thehypothesis that binocularity is primarily theresult of the contra lateral projection of eacheye’s visual field in order to achieve a symmet-rically expanding optical flow field in eacheye, rather than with achieving two views ofthe same object. The slightly broader binocu-lar fields of these nocturnal species, comparedwith diurnally active species, may be inter-preted as a compensation for a reduced num-ber of optical elements that provide the cuesfor the optical flow field at reduced spatialresolution associated with lower light levels(Martin & Katzir 1999).

ACKNOWLEDGMENTS

This work was supported by grants from theRoyal Society of London, the Natural Sci-ences and Engineering Research Council ofCanada, Consejo Nacional de InvestigacionesCientíficas y Tecnológicas de Venezuela, andthe Consejo de Investogación de la Univer-sidad de Oriente. The investigations were inaccordance with guidelines established by theUniversidad de Oriente and the CanadianCouncil on Animal Care.

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REFERENCES

Archer, S. N., M. B. A. Djamgoz, E. Loew, J. C.Partridge, & S. Vallerga. 1999. Adaptive mech-anisms in the ecology of vision. Kluwer, Dor-drecht, Netherlands.

Buhler, P. 1970. Schademorphologie und Kiefer-mechanik der Caprimulgidae (Aves). Z. Morph.Tiere 66: 337-399.

Cleere, N. 1999. Family Caprimulgidae (Nightjars).Pp 302-386 in del Hoyo J., A. Elliott, & J. Sar-gatal (eds.). Handbook of the birds of theworld. Volume 5: Barn-owls to hummingbirds.Lynx Edicions, Barcelona, Spain.

Cramp, S. 1985. Handbook of the birds of Europe,the Middle East and North Africa. Volume 4:Terns to woodpeckers. Oxford UniversityPress, Oxford, UK.

Davies, M. N. O., & P. R. Green, 1994. Perceptionand motor control in birds: an ecologicalapproach. Springer-Verlag, Berlin, Germany.

Guillemaine, M., G. R. Martin, & H. Fritz. 2002.Feeding methods, visual fields and vigilance indabbling ducks (Anatidae). Funct. Ecol. 16:522-529.

Katzir, G., & G. R. Martin. 1994. Visual fields inherons (Ardeidae) - panoramic vision beneaththe bill. Naturwissenschaften 81: 182-184.

Katzir, G., & G. R. Martin. 1998. Visual fields inthe Black-crowned Night Heron Nycticorax nycti-corax: nocturnality does not result in owl-likefeatures. Ibis 140: 157-162.

Konishi, M., & E. I. Knudsen. 1979. The Oilbird:hearing and echolocation. Science 204: 425-427.

Land, M. F., & D.-E. Nilsson. 2002. Animal eyes.Oxford Univ. Press, Oxford, UK.

Locket, N. A. 1977. Adaptations to the deep-seaenvironment. Pp 67-192 in Crescitelli, F. (ed.).Handbook of sensory physiology. Volume VII/5. Springer-Verlag, Berlin, Germany.

Martin, G. R. 1984. The visual fields of the tawnyowl, Strix aluco L. Vision Res. 24: 1739-1751.

Martin, G. R. 1986a. Sensory capacities and thenocturnal habit of owls (Strigiformes). Ibis 128:266-277.

Martin, G. R. 1986b. Total panoramic vision in theMallard Duck, Anas platyrhynchos. Vision Res.26: 1303-1306.

Martin, G. R. 1990. Birds by night. T & A D Poy-ser, London, UK.

Martin, G. R. 1994. Visual fields in woodcocksScolopax rusticola (Scolopacidae; Charadrii-formes). J. Comp. Physiol. A 174: 787-793.

Martin, G. R. 1998. Eye structure and amphibiousforaging in albatrosses. Proc. R. Soc. Lond. BBiol. Sci. 265: 1-7.

Martin, G. R. 1999. Eye structure and foraging inKing Penguins Aptenodytes patagonicus. Ibis 141:444-450.

Martin, G. R., & H. C. Coetzee in press. Visualfields in hornbills: precision-grasping and sun-shades. Ibis.

Martin, G. R., & G. Katzir. 1994. Visual fields andeye movements in herons (Ardeidae). BrainBehav. Evol. 44: 74-85.

Martin, G. R., & G. Katzir. 1995. Visual fields inostriches. Nature 374: 19-20.

Martin, G. R., & G. Katzir. 1999. Visual field inShort-toed eagles Circaetus gallicus and the func-tion of binocularity in birds. Brain Behav. Evol.53: 55-66.

McFadden, S. A. 1994. Binocular depth perception.Pp 54-73 in Davies M. N. O., & P. R. Green.Perception and motor control in birds: an eco-logical approach. Springer-Verlag, Berlin, Ger-many.

Rojas, L. M., Y. Ramirez, R. McNeil, M. Mitchell, &G. Marin. 2004. Retinal morphology and elec-trophysiology of two Caprimulgiform birds:The cave-dwelling and nocturnal Oilbird(Steatornis caripensis), and the crepuscularly andnocturnally foraging Common Pauraque (Nyc-tidromus albicollis). Brain Behav. Evol. 64: 233–242.

Schlegel, R. 1969. Der Ziegenmelker. Wittenberg,Lutherstadt.

Snow, D. W. 1961. The natural history of the Oil-bird, Steatornis caripensis, in Trinidad. 1. Generalbehaviour and breeding habits. Zoologica 46:27-48.

Tansley, K. 1965. Vision in vertebrates. ChapmanHall, London, UK.

Thomas, B. T. 1999. Family Steatornithidae (Oil-bird). Pp 244-251 in del Hoyo J., A. Elliott, &J. Sargatal (eds.). Handbook of the birds of theworld. Volume 5. Barn-owls to hummingbirds.Lynx Edicions, Barcelona, Spain.

241

Page 10: BINOCULAR VISION AND NOCTURNAL ACTIVITY IN OILBIRDS ... · BINOCULAR VISION AND NOCTURNAL ACTIVITY IN OILBIRDS (STEATORNIS CARIPENSIS) AND PAURAQUES (NYCTIDROMUS ALBICOLLIS): CAPRIMULGIFORMES

MARTIN ET AL.

Voous, K. H. 1988. Owls of the northern hemi-sphere. Collins, London, UK.

Walls, G. L. 1942. The vertebrate eye and its adap-tive radiation. Cranbrook Institute of Science,

Blomfield Hills, Michigan.Welty, J. C., & L. F. Baptista, 1988. The life of

birds. 4th ed. W. B. Saunders, New York, NewYork.

242