0042-6989190 $3.00 + 0.00 Copyright Q 1990 Pergamon Press plc
Yirion Res, Vol. 30, No. 9, pp. 12774289, 1990 Printed in Great Britain. All rights reserved
RETINAL GANGLION CELL DISTRIBUTION AND BEHAVIOUR IN PROCELLARIIFORM SEABIRDS B.P. HAYES’+
and M.
DE
L. BROOKE*
Science, Institute of Ophthalmology, Judd Street, London WCIH 9QS and 2Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, U.K. and Percy Fitzpatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7700, South Africa ‘Department
of Visual
(Received 20 November 1989; in reaifed form 5 February 1990) Abstract-Retinal ganglion cell distribution in nine species of proceliariiform seabirds was studied by Nissl staining of retinal whole-mounts and the construction of density contour maps. Most species showed a horizontal linear area of high cell density, but concentric distributions with dorsal and central cell concentrations were found in two species. These results are discussed in relation to the birds’ foraging behaviour. Retina
Ganglion cell distribution
Procellariiform seabirds
INTRODUCTION
Tube-nosed seabirds of the order Procellariiformes (albatrosses, petrels and their allies) are
highly pelagic birds which feed in various ways, for example many gadfly petrels (Pterodroma spp.) seize squid on the sea surface at night, prions (Pachyptila spp.) skim surface crustacea from the surface of the sea (Harper, Croxali & Cooper, 1985; Harper, 1987) while many shearwaters (Pu@zus spp.) dive by day to catch their food (Broon, Bourne & Wahl, 1978). These different feeding methods will impose subtly different demands on the birds’ visual systems. We would therefore expect these variations in feeding behaviour to be reflected in interspecific retinal differences. Reinforcing this expectation is the knowledge that procellariiforms are structurally homogeneous, which makes it more likely that retinal differences represent adaptive rather than phylogenetic differences. Although the feeding habits of proceliariiforms are known in general terms, there are many individual species that have virtually never been seen feeding. They may feed at night hundreds of kilometres from land. The retinae of such species may yield hints concerning their precise foraging habits. Our retinal study aims to explore how the ganglion cell distribution of several species *To whom all correspondence
should be addressed at: Department of Research Services, Glaxo Group Research Ltd, Greenford Road, Greenford, Middlesex WB6 ONE, U.K. 1277
Visual streak
Area dorsalis
relates to feeding habits, and to use that relation to suggest how some little-known proceiiariiforms may feed. Previous macroscopic studies of the retina in other proceiiariiforms have shown a linear area or visual streak, usually with a central fovea (Wood, 1917; O’Day, 1940; Lockie, 1952; Meyer, 1977). Such a linear area of high cell density may aid detection of movement on the horizon or orientation with respect to the horizon (Meyer, 1977). This contrasts with the retinal organisation of ground feeding birds, where one or more areas or foveas are found, in the posterior, dorsal or lateral retina (Meyer, 1977). To study ganglion cell distribution in a number of retinae we have developed a special image analysis system (Hayes & Fitzke, 1988) which automates the production of density contour maps. Our study shows a spectrum of ganglion cell distributions within the proceliariiforms, from the visual streak to a concentric organisation like that found in the pigeon retina (Hayes, 1982). MATERIALS
AND METHODS
Eleven eyes from eight species of procellariiforms were collected post mortem from Gough Island (40”2i’S, 9”53’W) South Atlantic. These eight species were the Sooty Albatross (Phoebetriu jh.wx, 1 eye), Kergueien Petrel (Pterodroma brevirostris, 2 eyes), Soft-plumaged Petrel (P. mollis, 1 eye), Atlantic Petrel (P.
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B. P. HAYFSand M. DE l_. BROOIU:
incerta, 2 eyes), Broad-billed Prion (Pac~ypr~~a cirtata, I eye), Common Diving Petrel (Pelecanoides urinatrix, 2 eyes), Great Shearwater (Pu$inus grab, I eye) and Little Shearwater (Pu@ws assimilis, 1 eye). In addition, two Manx Shearwater eyes (Pt.&us pufinus) were collected from birds terminally ill with the disease puffinosis (from Skomer Island, Wales). Eyes were fixed and stored in formal saline for up to I yr. They were then dissected in normal saline to isolate the retina from the underlying pigment epithelium. The retina was stained in 0.5% cresyl violet for ZOmin, dehydrated in ascending alcohols, flattened and wholemounted in XAM. Retinal shrinkage during processing was measured in 2 retinae of the Manx Shearwater. At 4%, area1 shrinkage was negligible, and has not been corrected for in the ganglion cell size measurements or contour maps. The size distribution of ganglion cells was studied in single retinae from the Common Diving Petrel, Little Shearwater, Manx Shearwater, Soft-plumaged Petrel and Sooty Albatross. These species were chosen to encompass a wide range of eye sizes. Two samples of 30-70 cells were taken from each retina, in the central retina approx. 1 mm nasal to the tip of the pecten (central retinal sample), and in the temporal retina approx. 1 mm from the ora terminalis (peripheral retinal sample). Ganglion cells were identified as ceils that stain strongly for Nissl substance, by the criteria given by Ehrlich (1981) for the avian retina. The mean soma caliper diameter of each ganglion cell was found at 400 x magnification with the DIGIT image analysis system (Hayes & Fitzke, 1988). Size distribution of the cells was plotted as percentage frequency distribution histograms. To map the density distribution of ganglion cells a low magnification map was drawn of the retina and ganglion cells were counted per microscope field at 400 x magnification (Hayes & Holden, 1983). The counts were made with the aid of the image analysis system, which superimposes dots on each counted cell seen in the microscope. Samples (area 0.026 mm’) were taken every millimetre and the positions of the samples and the counts were marked on the map of the retina. The DISMAP computer software (Hayes & Fitzke, 1988) was used to map the cell densities as follows: the outline and cell counts from the low magnification retinal map were recorded on floppy disc with the aid of a high resolution digit& tablet and BBC B or Acorn
Archimedes computer (Acorn. Cambridge. U.K.). The DISMAP software then calculated the sample densities and interpolated densities at regular density intervals by linear interpolation. These interpolated densities were plotted on a computer map of the retina (Fig. I )_ They were used to locate contour lines drawn with a computer art program. The total number of cells was calculated by the software from the retinal area x average cell density. In order to orientate the maps correctly the o~entation of the retina was found by measuring the angle of the pecten to the bill in dissections of the eye in situ in the head (Hayes & Holden, 1983). This angle averaged 40 deg for seven eyes of the Broad-billed Prion, Soft-plumaged and Common Diving Petrels. Published (Harrison, 1987) and unpublished photographs of procellariiforms in flight show that the bill is held at an average angle of 25 deg to the horizontal (19 photographs of 9 species). The angle of the pecten to the horizontal is therefore approx. 65 deg, and this angle was used to orientate the maps of ganglion cell distribution. RESULTS Structure of the ganglion cell layer
In the central retina, cell bodies were closely packed (Fig. 2). Ganglion cell bodies were rounded, with large pale nuclei. Differential focusing was used to identify the dark angular nuclei of glia and the small pale stained cell bodies of displaced amacrine c&s, which lie next to the inner plexiform layer. Differential focusing was also necessary to find the greatest diameter of each ganglion cell for measurement. After the ganglion cells were identified by their staining and relative size, they were counted and marked with white dots (Fig. 2) with the aid of the image analyser and camera lucida attachment (Hayes & Fitzke, 1988). Mean ganglion cell diameter for the central retina varied between 6.6 rt I.1 pm (n = 57) (mean f SD) for the Manx Shearwater (Fig. 4) and 11.9 f 2.3 pm (n = 67) for the Soft-plumaged Petrel (Fig. 5). In the peripheral retina ganglion cell bodies were elliptical in shape, and had large pale stained nuclei and densely stained abundant Nissl substance in the cytoplasm. They were widely spaced, often with bands of thick nerve fibres between them (Fig. 3). Mean ganglion cell diameter varied between 14.6 + 4.4 ,um (n = 71)
Fig. 2. Nissl stained ganglion cells in the central retina of the Broad-billed F’rion. 327 ganglion cells are present (marked with faint white dots). g: ganglion cell. Scale line 100pm.
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Fig. 3. Nissl stained ganglion cells in the dorsal periphery of the retina of the Broad-billed Won. 48 ganglion cells (g) are present. and these show marked Nissl substance. The densely stained nuclei of glial cells (gl) and palely stained displaced amacrine cells (a) are also shown. Bundles of ganglion cell axons (b) are found between the cells. Scale line IOOpm.
1280
Retinal
1281
ganglion cell distribution
Imm
u
Fig. 1.Computer map of a whole-mount of the Common Diving Petrel retina (right retina). The numbers are cell densities (x 1000cells/mm2) interpolated by the computer. N: nasal, T: temporal, D: dorsal, V: ventral retina, shaded area: pecten.
for the Manx Shear-water and 23.1 + 7.1 pm for the Soft-plumaged Petrel (n = 32) (Fig. 5).
Percentage frequency distribution histograms of ganglion cell diameter show the much greater variation in cell diameter in the peripheral retina than the central retina (Fig. 4).
50
Ganglion cell density distribution
40
Retinal area and total number of ganglion cells for each eye is shown in Table 1. A wide spectrum of distributions was found. We have classified the distributions according to the pattern of contours and the ganglion cell density level throughout the retina as follows.
30 20
2 lo
F” B
(B)
20
t
IO
0
r
I 10
20
30
Mean soma diameter (pm)
Fig. 4. Percentage frequency distributions of mean soma diameter of ganglion cells in the central (a) and peripheral (b) Manx Shearwater retina. The central cells show a narrow size distribution with a mean diameter of 6.6 f 1.1 pm (mean f SD, n = 61). Peripheral cells show a wide size distribution from 6 to 28 pm, mean 14.6 & 4.4 pm (n = 71).
P
c A
CP B
CP C
CP
c D
P E
Fig. 5. Histogram of mean ganglion cell soma diameter for five species of procellariiforms (A: Common Diving Petrel, B: Manx Shearwater, C: Little Shearwater, D: Softplumaged Petrel and E: Sooty Albatross). c: central retinal samples. p: peripheral retinal samples. Bars: &SD. The number of cells per sample was 28-7 I.
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B. P. HAYESand M.
Table 1. Retinal area and estimated total number of ganglion ceils for each of the eya examined Retinal area 0nm’~
Species
Total number of ganglion cells
Sooty Albatross Manx Sheatwater Manx Shearwater Soft-plumaged Petrel Common Diving Petrel Common Diving Petrel Broad-billed Priori Atlantic Petrel Atlantic Petrel Great Shearwater Kergueien Petrel Kerguelen Petrel Little Shearwater
734 150 158 354 97 134 173 415 423 378 477 479 279
1,185,OOO 3,848,OOO 2,169,OOO 993,000
Mean values
327
1.320,000
1,165,000 807,000 733,008 1,107,000 629.000 568,000 859,000 I ,875,OOO
1,220,000
(I) Well defined hear area/low cell densities. The Sooty Albatross showed a well defined horizontal linear area displaced towards the retinal temporal pole, and containing a peak cell density of 8900cells/mm2 in the mid temporal retina (Fig. 6). (A well defined linear area is a concentration of ganglion cells with a steep rise
DE
L. B~oo~t
in ganglion cell density at its edges.) This was the largest of the eyes examined (retinal area 734 mm’) and it showed the lowest ganglion cell densities. However the total numbr of ganglion cells was about average at 1,165,OOO(average for the nine species examined = 1,320,000 cells, see Table 1). (2) Well defined linear area /high ceN densiries. The Manx Shearwater showed a well defined horizontal linear area containing a peak cell density in the central retina (Fig. 7). The eye was small (average retinal area 154 mm’) and ganglion cell densities were high, reaching a peak value of 21,500 cells/mm2. The total number of ganglion cells was low at 770,000 (average of 2 retinae). (3) Well defined hear area/moderate ceil ahsiries. The Soft-plurn~~ Petrel retina also showed a well defined horizontal linear area, but this area was displaced towards the nasal pole in this species (Fig. 8). The eye was of medium size (retinal area 354mm2) with moderate ganglion cell densities, reaching a peak of 14,2OOcells/
Fig. 6. Contour m.sp of ganglion cell density dimibutim in the retin8 of the Sooty Albatross fteft retinn). Ihecontow:iinsranIiaerofequidenrirywithdarrityiatennlrof20g0~*.Numbanan:~icj x ma/mm’. l: pmk of all dlmnity in the mid-tc!apolnI retina, 8!wb&/mln’. sbbed arm: p-m. N: nasal, T: tem~l, D: dorsal, V: VmtraJ. Part of the vcntro-tmpo ml retina WM lost during preparation
of the retinal whole mount.
Retinal ganglion cell dist~bution
t283
Fig. 7. Contour map of ganglion cell density distribution in the Manx Sheatwater retina (right retina). Note the high cell densities in the horizontal linear area, reaching a peak of 21,500 cells/mm2 in the nasal central retina (*).
mm2 in the central retina. The total number of ganglion cells was close to average at I ,107,OOO. (4) Well defined linear area plus a concentric distribution in she retinal periphery. This distribution was found in the retina of the Common Diving Petrel, where there was a prominent horizontal linear area containing high densities of ganglion cells (Fig. 9). Peak density in the central retina, in the centre of the linear area, was 17,000 cells/mm* (average of 2 retinae). The more peripheral parts of the cell distribution showed contour lines parallel to the ora terminalis, which we have called a concentric distribution This was the smallest of the eyes examined, with a retinal area of 116 mm2, and the total number of ganglion cells was 599,000; the lowest found (averages for 2 retinae). (5) Poorly dejined linear area/moderate cell densities. This type of distribution was found in the Broad-billed Prion, Atlantic Petrel and Great Shearwater retinae (Fig. 10). A peak of cell density was found in the posterior retina, at 13,800--14,900 cells/mm2. Moderate cell densities were present throughout the retina. The retinal area and total number of ganglion cells
varied between 173 mm2 and 859,O~ cells for the small retina of the Prion, to 419 mm2 and 1,598,OOO cells for the Atlantic Petrel retina (values for the Great Shear-water were retinal area = 378 mm’, total number of ganglion cells = 1,186,OOO). (6) Concentric distribution /high cell densities, with posterior and dorsal concentrations of ganglion cells. The Kerguelen Petrel showed
very high ganglion cell densities over the central half of the retina (Fig. 11). Density contour lines were mainly concentric to the ora terminalis and 2 peaks of ganglion cell density were found at 19,000 cells/mm*. These concentrations of ganglion cells were in the posterior retina and the mid dorsal retina (Fig. 11). Although this was not the largest retina examined (retinal area was 478 mm2, n = 2) the total number of ganglion cells was the highest at 3,009,OOO(average of 2 retinae). (7) Concentric distribution]low cell densities and two concentrations of ganglion cells. The retina of the Little Shearwater showed a concentric dist~bution of density contours with low ganglion cell densities (Fig. 12) throughout the
1284
B. P. Ham and M.
DE
L. BROOU
D
Fig. 8. Ganglion cell density distribution of the Soft-plumagaJ Petrel (left retina). The linear area of high density is displaced towards tbc nasal pok (N) and peak density is found in the central retina (14,200 ails/mm’).
retina. These densities were comparable to those found in the retina of the Sooty Albatross. There was some suggestion of a weak horizontal bias to the distribution in the posterior retina. The peak densities of 10,500 were found in the posterior and mid dorsal retina, in similar positions to those of the Kerguelen Petrel. The retina1 area was 279 mm2 and the total number of ganglion cells !393,000;these values were close to the averages for all the species examined (see Table 1).
distribution may reflect the presence of a number of morphological cell types (Hayes, 19%2; Ikushima et al., 1986). We have recently described one of these morphoiogical types; a special population of large g&ion ails ia the retina of proceliariiforms dorso-temporal (Hayes, Martin & Brooke, 1989). In the 9 species which we examined retinal area varied between 134 and 734 mm’. The maps we have presented provide a graphical representation of the variations in gangjion cell density across the retina, which may reflect variations in visual acuity (Hushes, 1977). This DiSCUSSN)N is the first time that seabird retinae have been studied in this way. Previous studies of procelThe microscopic structure of the ganglion cell layer of the seabird retinae that we observed by lariiform retinae have been made by macroor by Nissl staining of retinal whole-mounts is similar scopic observation of the f&us to that found in other avian retinae, e.g. by Nissl microscopic sectioning of the posmrior retina. staining of the chicken retina (Ehriich, 1981) Thus Wood (1917) deacribal a darkly outlined and the quail retina (Ikushima, Watanabe & Ito, horizontal macroscopic band across the retina 19g6), or by axonal transport of horseradish of the Sooty Sbeanvater (Ps@u8 ptireus), conperoxidase in the pigeon retina (Hayes, 1982). taining a lighter centre, which he be&ad to be Small ganglion cells of uniform sixe are tightly a central linear fovea. O’Day (1940) described a packed in the central retina but a much wider central strip with a singk oval fovea in the retina size distribution is seen in the periphery, includ- of the Shy Albatross (Diomedea caura) and ing small and large cell bodies. This wider Giant Petrel (Macronectes spp.). Macroscopic
1285
Retinal ganglion cell distribution
lmm -
V Fig. 9. Ganglion cell density distribution of the Common Diving Petrel (right retina). The linear area is separated into islands of high density with a peak in the posterior retina (17,000cells/mm2). Peripheral density contours are curved parallel to the ora (concentric organisation).
and microscopic study of the retinae of the Manx Shear-water and Fulmar Petrel (Fulmaris glaci&) by Lockie (1952) revealed a linear area centralis without a fovea. Our study shows that the majority of procellariiform retinae studied contains a linear area of high ganglion cell density, as would be expected from macroscopic observations of a visual streak. In macroscopic studies of the retina it was assumed that this streak was horizontally orientated and we have confirmed this in three species by measurement of the angles of the bill and pecten to the horizontal. Such measurements assume that the post mortem eye retains its normal position in the head. The horizontal projection of the visual streak in visual space has also been shown by superimposing retinal and visual field maps of the Manx Shearwater (Hayes, Martin & Brooke, 1990). The possible functions of the linear area of the avian retina were reviewed by Meyer (1977). One function often attributed to the visual streak is movement detection, however the small ganglion cells of the streak are poorly adapted
for this function, which is usually ascribed to large, fast responding and conducting ganglion cells (Perry, 1982). Alternatively, in a review of the occurrence and function of the visual streak in mammalian and non-mammalian retinae, Hughes (1977) concluded that it is common to species that live in an open terrain environment, where “the majority of objects of interest are represented in a horizontal strip of the retinal image”. This would certainly be true for procellariiform seabirds, which spend most of the day and night flying over the open sea, except during breeding. According to this idea the high density of small ganglion cells in the visual streak of seabirds is an adaptation to high visual acuity along the horizon. The prominence of the visual streak, which we have assessed by the distribution of density contour lines, varies in different species. The streak is well defined in the retinae of the Sooty Albatross, Manx Shear-water, Soft-plumaged Petrel and Common Diving Petrel, poorly defined in the Broad-billed Prion, Atlantic Petrel and Great Shear-water, and absent in the retinae of the Kerguelen Petrel and Little Shear-
1286
B. P. HAYES and M.
DE
L. BROOKE
Fig. IO. Ganglion cell density distribution of the Broad-billed Frion (kft retina). The distribution a horizontal bias and a density peak in the amtral retina (i3,8OO~&/uun~.
water. The Kerguelen Petrel and Little Shearwater show concentric distributions of ganglion cell density contours. Concentric distributions have been described in the retinae of ground feeding birds such as the pigeon (Binggeii & Paule, 1969; Galifret, 1968, Hayes & Holden, 1983), chicken (Ehrlich, 1981) and quail (Ikushima et al., 1986). Dorsal concentrations of ganglion cells are found in the retinae of the Kerguelen Petrel and Little Shearwater. A dorsal concentration of ganglion cells is well known in the pigeon retina (Binggeli & Paule, 1969; Galifret, 1968; Hayes & Holden, 1983), where it is believed to be a myopic region of the retina used for ground feeding (Holden, Hodos, Hayes 8i Fit&e, 1988). We did not anticipate finding this adaptation of the retina in seabirds. Can these differences in g&ion cell distribution be explained by the different foraging behaviour of procellarliform species? For now, let us exclude the gadfly petrels from the discussion. The species with the best-defined linear streak feed in two ways. Manx Shearwaters and Common Diving Petrels mostly feed underwater at shallow depth, where potential prey will be at roughly the same level as the bird (Cramp dc
show
Simmons, 1977). Sooty Albatrosses eat large squid (Berruthi, 1979; Thomas, 1982) seized on the surface and presumably de&c&d from afar. In both feeding modes, potential pray is likdy to be spotted in roughly the same horizontal plane as the bird, which may render a horizontal streak advantageous. Possibly the low overall cell density in the Sooty Alktross retina is associated with%thespecies large prey, and consequently limited need for high visual acuity. The Broad-billed Priori and Great Shcarwater, with pooriy detined streaks, both faad in two principal styles. The prioa feeds by filtering planktonic organisms from the water while floating or by hydroplaning when its head is immenrcd and wings OU~SW~&~. Less spcciW mo~hol~y for underwater swimming than the Maax Sbearwater), the Great Sheatwater faedr, either by pIut&ng from a small height into the water and pursuing prey underwater or by seizing prey below the SW&CC wbik mknming (Harper et al., 1985). Although that part of the retina which views the horizontal may be important, the birds may aiso benefit from a moderately acute view of the scene below, using the dorsal
Fig. 1I. Ganglion cell density distribution in the Kerguelen Petrel (right retina). Contour lines are mainly orientated parallel to the ora in a concentric organisation. There is a horizontal extension in the nasal periphery. Two islands of high cell density are found in the mid-dorsal retina (peak density 18,600 cells/mm*) and the central retina (peak density 19,300 cells/mm*).
retina. The ideal retina for these birds might then have a poorly-defined streak. Finally, Little Shearwaters, although feeding in the manner of the two other shearwaters, often seize food at the surface without immersing themselves beyond the head and neck (Cramp & Simmons, 1977; Harper et al., 1985). With prey at various levels relative to the eyes (depending on feeding method) there may be no advantage in a horizontal streak. Instead a concentric pattern is found. Although most gadfly petrels are believed to obtain food by seizing it on the surface (Harper et al., 1985), obse~ations are scarce, not least because many species feed at night (e.g. Imber, 1973). Our ganglion cell density maps allow us to suggest that the Soft-plumaged Petrel may indeed mostly surface-seize while the larger more robust Atlantic Petrel may be able to submerge somewhat more, take prey at greater depth and benefit from more acute vision in the dorsal field. The retinal maps make us think that the Kerguelen Petrel feeds in a quite difIerent manner to its two congeners. Harper (1987) records how Kerguelen Petrels he observed were dip-
ping, whereby the flying bird picks prey from the surface or just below. Such a style of feeding might require good vision in all parts of the visual field; hence the concentric ganglion cell distribution. The species feeds entirely at night (Harper, 1987). Judging by the bill which is delicate for a gadfly petrel, the prey are small. This was partly confirmed by Schramm (1983) who found that Kerguelen Petrels feed their chicks on more crustacea and fewer squid than Soft-plumaged and Great-winged Petrels (P. mucropteru). Both factors, i.e. small prey size and nocturnal feeding, would increase the advantage of highly-~nsitive eyes of high all-round acuity, which might be why the Kerguelen Petrel has over twice as many ganglion cells as the other species we studied. It is interesting that the eye of the Kerguelen Petrel should be so different from that of the Soft-plumaged and Atlantic Petrels when, on independent morphological grounds, Imber (1985) has suggested that the Kerguelen Petrel belongs in a monospecific genus Lugensa. We would conclude by mentioning that the average total number of ganglion cells in the pro~lla~ifo~s was 1.3 million; this is half of
1288
B.
P. HAYESand M.
DE
L. BROOKX
Fig. 12. Ganglion cell density distribution of the Little Shearwater (right retina). Contour lines are organ&u-l concentricaBy in the periphery. CeD densities are low, reaching peaks of 10,500 aUs/mm* in the central retina (*) and 7~~11~~~~ in the dorsal retina.
the total number of optic nerve fibres found in graminivorous birds (Bin&i & Pauie, 1969; Duff& Scott, 1979; Ikushima et al., 1986), and must represent a generally lower visual acuity across the seabird retina. As seabirds take generally larger prey, this lower acuity may be no disadvantage. AcknawIe&~nr.r-Scicntigc research on Gough Island is carried out with the perm&sion of the Island Councii and Administrator of Tristan da Ctmha. M .de L. Brook& visit to Gough bland was made poasibk by the logistic support of the South African Deportment of the Environment Affairs and the co-opemtion of the South African Committee for Antamtic Reacarch. He is very grateful for awards from the Foundation for Research Development, the Council for scientifkc and Industrial Raearch, the British Ecological Society and the Frank M. Chapman Memorial Fund, and to the Tristan In vestments vcssehs. Tristania Xl and Hehla, for removing him from Gough IsJand. Stud& of ganglion ceJJ distribution by 9. P. Hayes were funded from c0mmed like to thank J. Cooper for his comments on the
would
~ploitati~n 0fimrocanal+8s0nw=.WC
rn8nuacript. IWWtRENCES
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Meyer, D. B. (1977). The avian eye and its adaptations (Chap. 10). In Crescitelli, F. (Ed.), Handbook ofsensory physiology VII/S, The visual system in vertebrates (pp. 549412). Berlin: Sponger-Verlag. O’Day, K. (1940). The fundus and fovea centralis of the albatross (Diomedea Cauta Cauta-Gould). British Journal of Ophthalmology, 24, 201-207.
Perry, V. H. (1982). The ganglion cell layer of the mammalian retina. Progress in Retinal Research I, 53-80.
Schramm, M. (1983). The breeding biologies of the petrels Pterodroma macroprera, P. brevirostris and P. mollis at Marion Island. Emu, 83, 75-81. Thomas, G. (1982). The food and feeding ecology of the Light-mantled Sooty Albatross at South Georgia. Emu, 82, 92-100. Wood, C. A. (1917). The jimdus ocuti of bird especia#y as viewed by the ophthalmoscope. Lakeside Press: Chicago.
Yirion Res, Vol. 30, No. 9, pp. 12774289, 1990 Printed in Great Britain. All rights reserved
RETINAL GANGLION CELL DISTRIBUTION AND BEHAVIOUR IN PROCELLARIIFORM SEABIRDS B.P. HAYES’+
and M.
DE
L. BROOKE*
Science, Institute of Ophthalmology, Judd Street, London WCIH 9QS and 2Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, U.K. and Percy Fitzpatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7700, South Africa ‘Department
of Visual
(Received 20 November 1989; in reaifed form 5 February 1990) Abstract-Retinal ganglion cell distribution in nine species of proceliariiform seabirds was studied by Nissl staining of retinal whole-mounts and the construction of density contour maps. Most species showed a horizontal linear area of high cell density, but concentric distributions with dorsal and central cell concentrations were found in two species. These results are discussed in relation to the birds’ foraging behaviour. Retina
Ganglion cell distribution
Procellariiform seabirds
INTRODUCTION
Tube-nosed seabirds of the order Procellariiformes (albatrosses, petrels and their allies) are
highly pelagic birds which feed in various ways, for example many gadfly petrels (Pterodroma spp.) seize squid on the sea surface at night, prions (Pachyptila spp.) skim surface crustacea from the surface of the sea (Harper, Croxali & Cooper, 1985; Harper, 1987) while many shearwaters (Pu@zus spp.) dive by day to catch their food (Broon, Bourne & Wahl, 1978). These different feeding methods will impose subtly different demands on the birds’ visual systems. We would therefore expect these variations in feeding behaviour to be reflected in interspecific retinal differences. Reinforcing this expectation is the knowledge that procellariiforms are structurally homogeneous, which makes it more likely that retinal differences represent adaptive rather than phylogenetic differences. Although the feeding habits of proceliariiforms are known in general terms, there are many individual species that have virtually never been seen feeding. They may feed at night hundreds of kilometres from land. The retinae of such species may yield hints concerning their precise foraging habits. Our retinal study aims to explore how the ganglion cell distribution of several species *To whom all correspondence
should be addressed at: Department of Research Services, Glaxo Group Research Ltd, Greenford Road, Greenford, Middlesex WB6 ONE, U.K. 1277
Visual streak
Area dorsalis
relates to feeding habits, and to use that relation to suggest how some little-known proceiiariiforms may feed. Previous macroscopic studies of the retina in other proceiiariiforms have shown a linear area or visual streak, usually with a central fovea (Wood, 1917; O’Day, 1940; Lockie, 1952; Meyer, 1977). Such a linear area of high cell density may aid detection of movement on the horizon or orientation with respect to the horizon (Meyer, 1977). This contrasts with the retinal organisation of ground feeding birds, where one or more areas or foveas are found, in the posterior, dorsal or lateral retina (Meyer, 1977). To study ganglion cell distribution in a number of retinae we have developed a special image analysis system (Hayes & Fitzke, 1988) which automates the production of density contour maps. Our study shows a spectrum of ganglion cell distributions within the proceliariiforms, from the visual streak to a concentric organisation like that found in the pigeon retina (Hayes, 1982). MATERIALS
AND METHODS
Eleven eyes from eight species of procellariiforms were collected post mortem from Gough Island (40”2i’S, 9”53’W) South Atlantic. These eight species were the Sooty Albatross (Phoebetriu jh.wx, 1 eye), Kergueien Petrel (Pterodroma brevirostris, 2 eyes), Soft-plumaged Petrel (P. mollis, 1 eye), Atlantic Petrel (P.
1278
B. P. HAYFSand M. DE l_. BROOIU:
incerta, 2 eyes), Broad-billed Prion (Pac~ypr~~a cirtata, I eye), Common Diving Petrel (Pelecanoides urinatrix, 2 eyes), Great Shearwater (Pu$inus grab, I eye) and Little Shearwater (Pu@ws assimilis, 1 eye). In addition, two Manx Shearwater eyes (Pt.&us pufinus) were collected from birds terminally ill with the disease puffinosis (from Skomer Island, Wales). Eyes were fixed and stored in formal saline for up to I yr. They were then dissected in normal saline to isolate the retina from the underlying pigment epithelium. The retina was stained in 0.5% cresyl violet for ZOmin, dehydrated in ascending alcohols, flattened and wholemounted in XAM. Retinal shrinkage during processing was measured in 2 retinae of the Manx Shearwater. At 4%, area1 shrinkage was negligible, and has not been corrected for in the ganglion cell size measurements or contour maps. The size distribution of ganglion cells was studied in single retinae from the Common Diving Petrel, Little Shearwater, Manx Shearwater, Soft-plumaged Petrel and Sooty Albatross. These species were chosen to encompass a wide range of eye sizes. Two samples of 30-70 cells were taken from each retina, in the central retina approx. 1 mm nasal to the tip of the pecten (central retinal sample), and in the temporal retina approx. 1 mm from the ora terminalis (peripheral retinal sample). Ganglion cells were identified as ceils that stain strongly for Nissl substance, by the criteria given by Ehrlich (1981) for the avian retina. The mean soma caliper diameter of each ganglion cell was found at 400 x magnification with the DIGIT image analysis system (Hayes & Fitzke, 1988). Size distribution of the cells was plotted as percentage frequency distribution histograms. To map the density distribution of ganglion cells a low magnification map was drawn of the retina and ganglion cells were counted per microscope field at 400 x magnification (Hayes & Holden, 1983). The counts were made with the aid of the image analysis system, which superimposes dots on each counted cell seen in the microscope. Samples (area 0.026 mm’) were taken every millimetre and the positions of the samples and the counts were marked on the map of the retina. The DISMAP computer software (Hayes & Fitzke, 1988) was used to map the cell densities as follows: the outline and cell counts from the low magnification retinal map were recorded on floppy disc with the aid of a high resolution digit& tablet and BBC B or Acorn
Archimedes computer (Acorn. Cambridge. U.K.). The DISMAP software then calculated the sample densities and interpolated densities at regular density intervals by linear interpolation. These interpolated densities were plotted on a computer map of the retina (Fig. I )_ They were used to locate contour lines drawn with a computer art program. The total number of cells was calculated by the software from the retinal area x average cell density. In order to orientate the maps correctly the o~entation of the retina was found by measuring the angle of the pecten to the bill in dissections of the eye in situ in the head (Hayes & Holden, 1983). This angle averaged 40 deg for seven eyes of the Broad-billed Prion, Soft-plumaged and Common Diving Petrels. Published (Harrison, 1987) and unpublished photographs of procellariiforms in flight show that the bill is held at an average angle of 25 deg to the horizontal (19 photographs of 9 species). The angle of the pecten to the horizontal is therefore approx. 65 deg, and this angle was used to orientate the maps of ganglion cell distribution. RESULTS Structure of the ganglion cell layer
In the central retina, cell bodies were closely packed (Fig. 2). Ganglion cell bodies were rounded, with large pale nuclei. Differential focusing was used to identify the dark angular nuclei of glia and the small pale stained cell bodies of displaced amacrine c&s, which lie next to the inner plexiform layer. Differential focusing was also necessary to find the greatest diameter of each ganglion cell for measurement. After the ganglion cells were identified by their staining and relative size, they were counted and marked with white dots (Fig. 2) with the aid of the image analyser and camera lucida attachment (Hayes & Fitzke, 1988). Mean ganglion cell diameter for the central retina varied between 6.6 rt I.1 pm (n = 57) (mean f SD) for the Manx Shearwater (Fig. 4) and 11.9 f 2.3 pm (n = 67) for the Soft-plumaged Petrel (Fig. 5). In the peripheral retina ganglion cell bodies were elliptical in shape, and had large pale stained nuclei and densely stained abundant Nissl substance in the cytoplasm. They were widely spaced, often with bands of thick nerve fibres between them (Fig. 3). Mean ganglion cell diameter varied between 14.6 + 4.4 ,um (n = 71)
Fig. 2. Nissl stained ganglion cells in the central retina of the Broad-billed F’rion. 327 ganglion cells are present (marked with faint white dots). g: ganglion cell. Scale line 100pm.
1279
Fig. 3. Nissl stained ganglion cells in the dorsal periphery of the retina of the Broad-billed Won. 48 ganglion cells (g) are present. and these show marked Nissl substance. The densely stained nuclei of glial cells (gl) and palely stained displaced amacrine cells (a) are also shown. Bundles of ganglion cell axons (b) are found between the cells. Scale line IOOpm.
1280
Retinal
1281
ganglion cell distribution
Imm
u
Fig. 1.Computer map of a whole-mount of the Common Diving Petrel retina (right retina). The numbers are cell densities (x 1000cells/mm2) interpolated by the computer. N: nasal, T: temporal, D: dorsal, V: ventral retina, shaded area: pecten.
for the Manx Shear-water and 23.1 + 7.1 pm for the Soft-plumaged Petrel (n = 32) (Fig. 5).
Percentage frequency distribution histograms of ganglion cell diameter show the much greater variation in cell diameter in the peripheral retina than the central retina (Fig. 4).
50
Ganglion cell density distribution
40
Retinal area and total number of ganglion cells for each eye is shown in Table 1. A wide spectrum of distributions was found. We have classified the distributions according to the pattern of contours and the ganglion cell density level throughout the retina as follows.
30 20
2 lo
F” B
(B)
20
t
IO
0
r
I 10
20
30
Mean soma diameter (pm)
Fig. 4. Percentage frequency distributions of mean soma diameter of ganglion cells in the central (a) and peripheral (b) Manx Shearwater retina. The central cells show a narrow size distribution with a mean diameter of 6.6 f 1.1 pm (mean f SD, n = 61). Peripheral cells show a wide size distribution from 6 to 28 pm, mean 14.6 & 4.4 pm (n = 71).
P
c A
CP B
CP C
CP
c D
P E
Fig. 5. Histogram of mean ganglion cell soma diameter for five species of procellariiforms (A: Common Diving Petrel, B: Manx Shearwater, C: Little Shearwater, D: Softplumaged Petrel and E: Sooty Albatross). c: central retinal samples. p: peripheral retinal samples. Bars: &SD. The number of cells per sample was 28-7 I.
1282
B. P. HAYESand M.
Table 1. Retinal area and estimated total number of ganglion ceils for each of the eya examined Retinal area 0nm’~
Species
Total number of ganglion cells
Sooty Albatross Manx Sheatwater Manx Shearwater Soft-plumaged Petrel Common Diving Petrel Common Diving Petrel Broad-billed Priori Atlantic Petrel Atlantic Petrel Great Shearwater Kergueien Petrel Kerguelen Petrel Little Shearwater
734 150 158 354 97 134 173 415 423 378 477 479 279
1,185,OOO 3,848,OOO 2,169,OOO 993,000
Mean values
327
1.320,000
1,165,000 807,000 733,008 1,107,000 629.000 568,000 859,000 I ,875,OOO
1,220,000
(I) Well defined hear area/low cell densities. The Sooty Albatross showed a well defined horizontal linear area displaced towards the retinal temporal pole, and containing a peak cell density of 8900cells/mm2 in the mid temporal retina (Fig. 6). (A well defined linear area is a concentration of ganglion cells with a steep rise
DE
L. B~oo~t
in ganglion cell density at its edges.) This was the largest of the eyes examined (retinal area 734 mm’) and it showed the lowest ganglion cell densities. However the total numbr of ganglion cells was about average at 1,165,OOO(average for the nine species examined = 1,320,000 cells, see Table 1). (2) Well defined linear area /high ceN densiries. The Manx Shearwater showed a well defined horizontal linear area containing a peak cell density in the central retina (Fig. 7). The eye was small (average retinal area 154 mm’) and ganglion cell densities were high, reaching a peak value of 21,500 cells/mm2. The total number of ganglion cells was low at 770,000 (average of 2 retinae). (3) Well defined hear area/moderate ceil ahsiries. The Soft-plurn~~ Petrel retina also showed a well defined horizontal linear area, but this area was displaced towards the nasal pole in this species (Fig. 8). The eye was of medium size (retinal area 354mm2) with moderate ganglion cell densities, reaching a peak of 14,2OOcells/
Fig. 6. Contour m.sp of ganglion cell density dimibutim in the retin8 of the Sooty Albatross fteft retinn). Ihecontow:iinsranIiaerofequidenrirywithdarrityiatennlrof20g0~*.Numbanan:~icj x ma/mm’. l: pmk of all dlmnity in the mid-tc!apolnI retina, 8!wb&/mln’. sbbed arm: p-m. N: nasal, T: tem~l, D: dorsal, V: VmtraJ. Part of the vcntro-tmpo ml retina WM lost during preparation
of the retinal whole mount.
Retinal ganglion cell dist~bution
t283
Fig. 7. Contour map of ganglion cell density distribution in the Manx Sheatwater retina (right retina). Note the high cell densities in the horizontal linear area, reaching a peak of 21,500 cells/mm2 in the nasal central retina (*).
mm2 in the central retina. The total number of ganglion cells was close to average at I ,107,OOO. (4) Well defined linear area plus a concentric distribution in she retinal periphery. This distribution was found in the retina of the Common Diving Petrel, where there was a prominent horizontal linear area containing high densities of ganglion cells (Fig. 9). Peak density in the central retina, in the centre of the linear area, was 17,000 cells/mm* (average of 2 retinae). The more peripheral parts of the cell distribution showed contour lines parallel to the ora terminalis, which we have called a concentric distribution This was the smallest of the eyes examined, with a retinal area of 116 mm2, and the total number of ganglion cells was 599,000; the lowest found (averages for 2 retinae). (5) Poorly dejined linear area/moderate cell densities. This type of distribution was found in the Broad-billed Prion, Atlantic Petrel and Great Shearwater retinae (Fig. 10). A peak of cell density was found in the posterior retina, at 13,800--14,900 cells/mm2. Moderate cell densities were present throughout the retina. The retinal area and total number of ganglion cells
varied between 173 mm2 and 859,O~ cells for the small retina of the Prion, to 419 mm2 and 1,598,OOO cells for the Atlantic Petrel retina (values for the Great Shear-water were retinal area = 378 mm’, total number of ganglion cells = 1,186,OOO). (6) Concentric distribution /high cell densities, with posterior and dorsal concentrations of ganglion cells. The Kerguelen Petrel showed
very high ganglion cell densities over the central half of the retina (Fig. 11). Density contour lines were mainly concentric to the ora terminalis and 2 peaks of ganglion cell density were found at 19,000 cells/mm*. These concentrations of ganglion cells were in the posterior retina and the mid dorsal retina (Fig. 11). Although this was not the largest retina examined (retinal area was 478 mm2, n = 2) the total number of ganglion cells was the highest at 3,009,OOO(average of 2 retinae). (7) Concentric distribution]low cell densities and two concentrations of ganglion cells. The retina of the Little Shearwater showed a concentric dist~bution of density contours with low ganglion cell densities (Fig. 12) throughout the
1284
B. P. Ham and M.
DE
L. BROOU
D
Fig. 8. Ganglion cell density distribution of the Soft-plumagaJ Petrel (left retina). The linear area of high density is displaced towards tbc nasal pok (N) and peak density is found in the central retina (14,200 ails/mm’).
retina. These densities were comparable to those found in the retina of the Sooty Albatross. There was some suggestion of a weak horizontal bias to the distribution in the posterior retina. The peak densities of 10,500 were found in the posterior and mid dorsal retina, in similar positions to those of the Kerguelen Petrel. The retina1 area was 279 mm2 and the total number of ganglion cells !393,000;these values were close to the averages for all the species examined (see Table 1).
distribution may reflect the presence of a number of morphological cell types (Hayes, 19%2; Ikushima et al., 1986). We have recently described one of these morphoiogical types; a special population of large g&ion ails ia the retina of proceliariiforms dorso-temporal (Hayes, Martin & Brooke, 1989). In the 9 species which we examined retinal area varied between 134 and 734 mm’. The maps we have presented provide a graphical representation of the variations in gangjion cell density across the retina, which may reflect variations in visual acuity (Hushes, 1977). This DiSCUSSN)N is the first time that seabird retinae have been studied in this way. Previous studies of procelThe microscopic structure of the ganglion cell layer of the seabird retinae that we observed by lariiform retinae have been made by macroor by Nissl staining of retinal whole-mounts is similar scopic observation of the f&us to that found in other avian retinae, e.g. by Nissl microscopic sectioning of the posmrior retina. staining of the chicken retina (Ehriich, 1981) Thus Wood (1917) deacribal a darkly outlined and the quail retina (Ikushima, Watanabe & Ito, horizontal macroscopic band across the retina 19g6), or by axonal transport of horseradish of the Sooty Sbeanvater (Ps@u8 ptireus), conperoxidase in the pigeon retina (Hayes, 1982). taining a lighter centre, which he be&ad to be Small ganglion cells of uniform sixe are tightly a central linear fovea. O’Day (1940) described a packed in the central retina but a much wider central strip with a singk oval fovea in the retina size distribution is seen in the periphery, includ- of the Shy Albatross (Diomedea caura) and ing small and large cell bodies. This wider Giant Petrel (Macronectes spp.). Macroscopic
1285
Retinal ganglion cell distribution
lmm -
V Fig. 9. Ganglion cell density distribution of the Common Diving Petrel (right retina). The linear area is separated into islands of high density with a peak in the posterior retina (17,000cells/mm2). Peripheral density contours are curved parallel to the ora (concentric organisation).
and microscopic study of the retinae of the Manx Shear-water and Fulmar Petrel (Fulmaris glaci&) by Lockie (1952) revealed a linear area centralis without a fovea. Our study shows that the majority of procellariiform retinae studied contains a linear area of high ganglion cell density, as would be expected from macroscopic observations of a visual streak. In macroscopic studies of the retina it was assumed that this streak was horizontally orientated and we have confirmed this in three species by measurement of the angles of the bill and pecten to the horizontal. Such measurements assume that the post mortem eye retains its normal position in the head. The horizontal projection of the visual streak in visual space has also been shown by superimposing retinal and visual field maps of the Manx Shearwater (Hayes, Martin & Brooke, 1990). The possible functions of the linear area of the avian retina were reviewed by Meyer (1977). One function often attributed to the visual streak is movement detection, however the small ganglion cells of the streak are poorly adapted
for this function, which is usually ascribed to large, fast responding and conducting ganglion cells (Perry, 1982). Alternatively, in a review of the occurrence and function of the visual streak in mammalian and non-mammalian retinae, Hughes (1977) concluded that it is common to species that live in an open terrain environment, where “the majority of objects of interest are represented in a horizontal strip of the retinal image”. This would certainly be true for procellariiform seabirds, which spend most of the day and night flying over the open sea, except during breeding. According to this idea the high density of small ganglion cells in the visual streak of seabirds is an adaptation to high visual acuity along the horizon. The prominence of the visual streak, which we have assessed by the distribution of density contour lines, varies in different species. The streak is well defined in the retinae of the Sooty Albatross, Manx Shear-water, Soft-plumaged Petrel and Common Diving Petrel, poorly defined in the Broad-billed Prion, Atlantic Petrel and Great Shear-water, and absent in the retinae of the Kerguelen Petrel and Little Shear-
1286
B. P. HAYES and M.
DE
L. BROOKE
Fig. IO. Ganglion cell density distribution of the Broad-billed Frion (kft retina). The distribution a horizontal bias and a density peak in the amtral retina (i3,8OO~&/uun~.
water. The Kerguelen Petrel and Little Shearwater show concentric distributions of ganglion cell density contours. Concentric distributions have been described in the retinae of ground feeding birds such as the pigeon (Binggeii & Paule, 1969; Galifret, 1968, Hayes & Holden, 1983), chicken (Ehrlich, 1981) and quail (Ikushima et al., 1986). Dorsal concentrations of ganglion cells are found in the retinae of the Kerguelen Petrel and Little Shearwater. A dorsal concentration of ganglion cells is well known in the pigeon retina (Binggeli & Paule, 1969; Galifret, 1968; Hayes & Holden, 1983), where it is believed to be a myopic region of the retina used for ground feeding (Holden, Hodos, Hayes 8i Fit&e, 1988). We did not anticipate finding this adaptation of the retina in seabirds. Can these differences in g&ion cell distribution be explained by the different foraging behaviour of procellarliform species? For now, let us exclude the gadfly petrels from the discussion. The species with the best-defined linear streak feed in two ways. Manx Shearwaters and Common Diving Petrels mostly feed underwater at shallow depth, where potential prey will be at roughly the same level as the bird (Cramp dc
show
Simmons, 1977). Sooty Albatrosses eat large squid (Berruthi, 1979; Thomas, 1982) seized on the surface and presumably de&c&d from afar. In both feeding modes, potential pray is likdy to be spotted in roughly the same horizontal plane as the bird, which may render a horizontal streak advantageous. Possibly the low overall cell density in the Sooty Alktross retina is associated with%thespecies large prey, and consequently limited need for high visual acuity. The Broad-billed Priori and Great Shcarwater, with pooriy detined streaks, both faad in two principal styles. The prioa feeds by filtering planktonic organisms from the water while floating or by hydroplaning when its head is immenrcd and wings OU~SW~&~. Less spcciW mo~hol~y for underwater swimming than the Maax Sbearwater), the Great Sheatwater faedr, either by pIut&ng from a small height into the water and pursuing prey underwater or by seizing prey below the SW&CC wbik mknming (Harper et al., 1985). Although that part of the retina which views the horizontal may be important, the birds may aiso benefit from a moderately acute view of the scene below, using the dorsal
Fig. 1I. Ganglion cell density distribution in the Kerguelen Petrel (right retina). Contour lines are mainly orientated parallel to the ora in a concentric organisation. There is a horizontal extension in the nasal periphery. Two islands of high cell density are found in the mid-dorsal retina (peak density 18,600 cells/mm*) and the central retina (peak density 19,300 cells/mm*).
retina. The ideal retina for these birds might then have a poorly-defined streak. Finally, Little Shearwaters, although feeding in the manner of the two other shearwaters, often seize food at the surface without immersing themselves beyond the head and neck (Cramp & Simmons, 1977; Harper et al., 1985). With prey at various levels relative to the eyes (depending on feeding method) there may be no advantage in a horizontal streak. Instead a concentric pattern is found. Although most gadfly petrels are believed to obtain food by seizing it on the surface (Harper et al., 1985), obse~ations are scarce, not least because many species feed at night (e.g. Imber, 1973). Our ganglion cell density maps allow us to suggest that the Soft-plumaged Petrel may indeed mostly surface-seize while the larger more robust Atlantic Petrel may be able to submerge somewhat more, take prey at greater depth and benefit from more acute vision in the dorsal field. The retinal maps make us think that the Kerguelen Petrel feeds in a quite difIerent manner to its two congeners. Harper (1987) records how Kerguelen Petrels he observed were dip-
ping, whereby the flying bird picks prey from the surface or just below. Such a style of feeding might require good vision in all parts of the visual field; hence the concentric ganglion cell distribution. The species feeds entirely at night (Harper, 1987). Judging by the bill which is delicate for a gadfly petrel, the prey are small. This was partly confirmed by Schramm (1983) who found that Kerguelen Petrels feed their chicks on more crustacea and fewer squid than Soft-plumaged and Great-winged Petrels (P. mucropteru). Both factors, i.e. small prey size and nocturnal feeding, would increase the advantage of highly-~nsitive eyes of high all-round acuity, which might be why the Kerguelen Petrel has over twice as many ganglion cells as the other species we studied. It is interesting that the eye of the Kerguelen Petrel should be so different from that of the Soft-plumaged and Atlantic Petrels when, on independent morphological grounds, Imber (1985) has suggested that the Kerguelen Petrel belongs in a monospecific genus Lugensa. We would conclude by mentioning that the average total number of ganglion cells in the pro~lla~ifo~s was 1.3 million; this is half of
1288
B.
P. HAYESand M.
DE
L. BROOKX
Fig. 12. Ganglion cell density distribution of the Little Shearwater (right retina). Contour lines are organ&u-l concentricaBy in the periphery. CeD densities are low, reaching peaks of 10,500 aUs/mm* in the central retina (*) and 7~~11~~~~ in the dorsal retina.
the total number of optic nerve fibres found in graminivorous birds (Bin&i & Pauie, 1969; Duff& Scott, 1979; Ikushima et al., 1986), and must represent a generally lower visual acuity across the seabird retina. As seabirds take generally larger prey, this lower acuity may be no disadvantage. AcknawIe&~nr.r-Scicntigc research on Gough Island is carried out with the perm&sion of the Island Councii and Administrator of Tristan da Ctmha. M .de L. Brook& visit to Gough bland was made poasibk by the logistic support of the South African Deportment of the Environment Affairs and the co-opemtion of the South African Committee for Antamtic Reacarch. He is very grateful for awards from the Foundation for Research Development, the Council for scientifkc and Industrial Raearch, the British Ecological Society and the Frank M. Chapman Memorial Fund, and to the Tristan In vestments vcssehs. Tristania Xl and Hehla, for removing him from Gough IsJand. Stud& of ganglion ceJJ distribution by 9. P. Hayes were funded from c0mmed like to thank J. Cooper for his comments on the
would
~ploitati~n 0fimrocanal+8s0nw=.WC
rn8nuacript. IWWtRENCES
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Biqtgeli, R. L. & Pat&, W. J. (1969). The pigeon retina: Quantitative aspects of the optic nerve and ganglion ceg layer. Jwmoi of Cmpwotiw Near&gy 13?, l-18. Broon, R. 0. B., Boume, W. R. P. & Wahi, T. R. (1978). Diving by shearwaters. Condor, So, 123-125. Cramp, S. & Simmons. K. E. L. (1977). i%e bids o/ tk western Poleorctic (VoI. I). Oxf’ordz Oxford University Press. Duff, T. A. & Scott, G. (1979). EUron micmacnpjc evidence of a ventronasal to dotaotempoti variation in f&c size in pigeon optic nerve. Joww/ of Comqoeatjce Newvkgy 183, 679488. Ehrhch, D. (1981). Regional -on of the chick retinaasreveakdbythesiaeanddenaityofncuronainthe ganglion all layer. Jmmnd o~Compomtk Neurohgy 195, 643457.
GaSfret, Y. (1968). Les dhsa~ aircs foncdonch de la ntine du pigeon. Zeit.wbtft j3r ii%?i@c~ und fnikraakopi#kc.4nutomdr,sa, 535-545. Harper, P. C. (1987). Feeding bahaviour and other notes on 20 species of prouBariiformes at sea. Noromir, 34, 169-192. Harper, P. C., Croxall, J. P. & Cooper, J. (19ff5). A guide muinebirdainarc&and tof~gmethodsuaedby subntuctic ees3.lEamuss3-i-, 2% 22. Harrison, P. (1987). Se&ra!r of the world. A ~togro#tic gut&. London: Helm. Hayes, B. P. (1982). The structural organiaation of the pigeon retina. Prosrry k &t&tat Rereur& I. 193-221. Hayes, 9. P. & Fit&, F. W. (1988). The study of c&J and particle distributions with a simple image analysis system. Microscopy and ,iMlJ’SiS, 4, 21-23.
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