January
1993]
Short
Communications
andCommentaries
FORSTER,
J.R. 1844. DescriptionesAnimallure quae
in itinere ad marls australistetras per annos 1772,
1773 et 1774 susceptocollegit observavitet delineavit JoannesReinoldus Forster (H. Lichtenstein, Ed.). AcademiaLitterarum Regia, Berlin.
GMELIN,J.F. 1788-1789. SystemaNaturae, 13th ed.
Beer,Lipsiae.
HOARE,M.E. 1976. The tactlessphilosopherJohann
Reinhold Forster (1729-98).
Hawthorn
Press,
HO^RE,M. E. (Ed.) 1982. The Resolution
journal of
JohannReinholdForster1772-1775.Hakluyt Society, CambridgeUniv. Press,Cambridge.
IREDALE,
T. 1938. WilliamAnderson--Ornithologist.
38:60-62.
JOHNSON,
O. W. 1985. Timing of primary molt in
first-yeargolden-ploversand someevolutionary
implications.Wilson Bull. 97:237-239.
JOHNSON,
O. W., ^ND P.M. JOHNSON.1983. Plumagemolt-agerelationshipsin "over-summering"and
migratoryLesserGolden-Plovers.Condor85:406419.
JOHNSON,O. W., P.M. JOHNSON,AND P. L. BRUNER.
1981. Wintering behavior and site-faithfulness
of golden plovers on Oahu. Elepaio 41:123-130.
JOHNSON,O. W., M. L. MORTON,P. L. BRUNER,AND P.
M. JOHNSON.1989. Fat cyclicity, predicted migratory flight ranges,and featuresof wintering
behavior
in Pacific
Golden-Plovers.
Condor
91:
156-177.
LANE, B. A.
3 vols.with 2 supplements.
Leighand Sotheby,
London.
LYSAGHT,A. 1959. Some eighteenth century bird
paintingsin the library of Sir JosephBanks(17431820). Bull. Br. Mus. Nat. Hist. (Historical Ser.)
1:251-371.
MATHEWS,G.M.
1931. John Latham (1740-1837): An
early Englishornithologist.Ibis 1 (13th ser.):466475.
MEDW^Y,
D.G. 1979. Someornithologicalresultsof
Melbourne.
Emu
141
Cook's third voyage. J. Soc. Bibliog. Nat. Hist.
3:315-351.
MEDW^Y, D. G.
1981.
The contribution
Islands.
Pac. Sci. 35:105-175.
PENNANT,T. 1785. Arctic zoology. Vol. 2, Birds.
Hughs, London (reprinted by Arno Press,1974).
SHARPE,
R. B. 1906. Birds. Pages79-515 in The history of the collectionscontainedin the natural
history departmentsof the British Museum, vol.
2. Trustees of the British Museum, Longmarts,
London.
STRESEMANN,E. 1949. Birds collected in the North
Pacificareaduring Capt.JamesCook'slastvoyage
(1778 and 1779). Ibis 91:244-255.
STRESEMANN,
E. 1950. Birds collectedduring Capt.
JamesCook'slastexpedition(1776-1780).Auk 67:
66-88.
STRESEMANN,
E. 1975. Ornithology from Aristotle to
present.Harvard Univ. Press,Cambridge.
WInSON, E. 1977. Observations of Hawaiian
1987. Shorebirds in Australia. Nelson,
Melbourne.
LATHAM,J. 1781-1801. A generalsynopsisof birds.
of Cook's
third voyageto the ornithologyof the Hawaiian
avifauna
during Cook'sexpeditions.Elepaio38:13-18.
Received
2 October1991,accepted
22 February1992.
The Auk 110(1):141-145, 1993
Comparisonof Rod/Cone Ratio in Three Speciesof ShorebirdsHaving
Different Nocturnal Foraging Strategies
Luz MARINA ROJASDE AZUAJE,•'3 SUSAN T•a,' AND RAYMOND MCNEIL 2
•Institutode Investigaciones
en Biomedicina
y Ciencias
Aplicadas,Universidad
de ¸riente,
Cumand, Sucre, Venezuela; and
2Dipartementde sciences
biologiques,
Universit[de Montrial,
C. P. 6128, Succ."A", Montreal, QuebecH3C3J7, Canada
Nocturnality, the habit of being activeduring darkness,is a characteristicof some aquatic birds, particularly those in the shorebird families (McNeil and
Robert 1988, Robert and McNeil
1989, Robert et al.
1989; for detailed review concerning aquatic birds,
3 Present address:D6partement de sciencesbiologiques,Universit• de Montr6al,C. P. 6128,Succ."A",
Montr6al, Quebec H3C 3J7, Canada.
see McNeil 1991, McNeil et al. 1992, 1993). Two basic
types of foraging techniquesare usedby shorebirds:
visual searchingfor prey or indicationsof their presence, on or near the surface (e.g. Pluvialisand Charadriusplovers);and probingwith the bill for buried
prey that are detectedby tactile and tastecues(e.g.
Short-billed Dowitcher, Limnodromus
griseus).Some
speciesfeed exclusivelywith the sameforagingtechnique both by night and by day (e.g.visualsearching
by Pluvialisand Charadrius
plovers, or tactile probing
142
Short
Communications
andCommentaries
[Auk,Vol. 110
Milsom1984,Milsometal. 1990),andtheBlack-winged
Stilt (McNeil and Robert 1988, Robert and McNeil
1989) take advantageof the moonlight to forage at
night (see also McNeil et al. 1992). According to
Pienkowski (1982), Grey Plovers (Pluvialissquatarola)
have pecking rates lower on very dark moonless
nights, comparedwith daylight, but not on moonlit
nights.However,ploverstrategists,
suchasthe Ringed
Plover (Charadrius
hiaticula),apparentlyuse sight as
the mainmeansof preydetection,evenon dark nights
(Pienkowski1983a).Spencer(1953) and Hale (1980)
reported that visibility of the moon is not required;
Northern Lapwings (except under dense clouds in
winter; see Milsom et al. 1990) and Eurasian Curlews
1989).Somespecies,suchasthe SemipalmatedSand-
(Numenius
arquata)forageon overcastfull-moon nights
exactlythe sameason completelyclear nights.Consequently,an importantquestionis:What allowsplover strategiststo foragevisually during darkness?
The relatively large eye in relation to head size of
plovers,comparedto that of Calidrisspecies,can be
regardedasan advantagefor feeding at night (Dugan
1981,Pienkowski1983a,b). Crab-plovers(Dromas)and
stone-curlews(Burhinus),which feed at night, and
woodcocks(Scolopax),
which perform acrobaticnocturnal display flights (see McNeil 1991), also have
large eyes. According to Pienkowski (1983b), it is
thought that ploversare mainly a low-latitude family
piper (Calidrispusilla;Evans 1979), are visual feeders
that evolved
•'
IXXX•XX
X7•XXXXX•XXX•XX
I
I
I
•11 Ill
III
I•
III
ill
Fig. 1. Schematicrepresentation of sampling
methodologyfor countingrodsand cones.
by Short-billed Dowitchers; Evans 1979, Pienkowski
1983a, McNeil and Robert 1988, Robert and McNeil
under
some conditions
and tactile feeders
under
oth-
under arid semidesert
conditions
where
most prey are active only by night.
ers (Schneider 1983). Moreover, some shorebirds
The retinal visual receptorsof birds, as of all vermodify their foraging strategiesbetween night and tebrates,are rods and cones(Meyer 1977,Tansley and
day.Thus, oystercatchers
(Haernatopus;
Hulscher ! 976, Erichsen1985).Nocturnal birds have a great prepon1982,Sutherland1982)and Tringaspecies(Goss-Cus- derance of rods in their retinas, while up to 80% of
tard 1969, 1970, Evans 1979, McNeil and Robert 1988,
photoreceptorsin diurnal birds are cones (Tansley
Robert and McNeil 1989) are normally sight feeders and Erichsen1985).If ploversare really sightfeeders
duringdaylight,but switchto tactileforagingat night. at night, we would expectthem to have proportionDuring daylight and on bright moonlitnights,Black- ately more rods than Haematopus,
Hirnantopus,
and
winged Stilts (Hirnantopus
himantopus)
usually are viTringa--daylight sight feeders that switch to tactile
sual peckers,but usescythelikesweepsof the bill (a foraging at night. The only referenceconcerningthe
tactile technique)on moonlessnights or under low rod/cone ratio in shorebirds is that of Rochon-Dumoonlight conditions(McNeil and Robert 1988,Rob- vigneaud (1943). He claimed that rod numbers vary
ert and McNeil 1989).
with the speciesin diurnal birds, but are high in
Comparedto visual"plover strategists,"
shorebirds Charadrius
hiaticulaand Calidrisalpina;both speciesforthat feed by touch (e.g. Limnodrornus)
should be relageat night (Pienkowski1983a,Batty1991).The puratively unaffectedby darkness(Dugan 1981, Pien- poseof our studywas to comparethe rod/cone ratio
kowski 1981,Goss-Custard
1983).The presenceof nuof the Grey Plover, the Greater Yellowlegs (Tringa
merous touch-sensitivenerve endings (e.g. Herbst's rnelanoleuca),
and the Short-billed Dowitcher, species
corpuscles)at the bill tip (von Bolze 1968,Schwartz- that have different foragingstrategies.
kopff 1973,Pienkowski 1983b;seealso Martin 1990),
One adult bird of each specieswas collectedin
in combinationwith a trigeminal expansionof the coastallagoons(Chacopataand Laguna de Patos)in
the state of Sucre, northeastern Venezuela. In the
forebrain (Pettigrew and Frost, 1985, Boire 1989), favors touch feeding of many scolopacidspecies(Lirn- field, within a few minutes of collection, the eyes
nodrornus,Gallinago,Calidris,etc.). In addition, taste were injected with 2.5% glutaraldehyde in 0.! M
(presenceof tastebudsat tip of beak) may play a role phosphatebuffer (pH = 7.2). In order to enhancethe
in locating areasrich in prey (Gerritsen et al. 1983, fixation, the eyeswere then punctured at the cornea
Van Heezik et al. 1983; see also Martin 1990).
and placed in the samefixative for 30 min, the time
Predominantly sight feeders such as Pluvialisand neededfor their transportationto the laboratory.FolCharadriusplovers (Pienkowski 1982, 1983a), the
lowing immediate enucleation, the retina, still atNorthern Lapwing (Vanellusvanellus;Spencer 1953, tached to the choroidal layer, was cut into nine sec-
January
1993]
Short
Communications
andCommentaries
tors, using the pecten as a landmark (Fig. 1A),
accordingto the procedureof Meyer and May (1973).
Each sectorwas subdivided into four portions (Fig.
lB) of which only two were retainedfor analysis(Fig.
1C). After 3 h in the fixative, the retinal portions were
washedwith phosphatebufferfor 10 min. The total
fixation time was lessthan 4 h. Tissueswere postfixed
in 1% OsO4in 0.1 M phosphatebuffer for I h, rinsed
in phosphatebuffer followed by distilled water, for
10 min each,and dehydrated in grade alcohol series
and propylene oxide. The tissueswere successively
infiltrated with a 1:1mixture of propylene oxide-epon
medium (LX-112) for 12 h, and pure epon medium
for another 2 h. Finally, they were embeddedin sil-
iconerubbermoldsfilled with epoxiteresin(Fig. 1D)
and polymerized in an oven (60øC)for 48 h.
TABLE1. Mean rod and cone densities (œ/100 ttm+
SE, n = 45) and rod/cone ratios corresponding to
different
Retinal
sectors
retinal
and stained with toluidin blue. For each retinal portion, 12 sections (one every 30-40 sections) were
mounted on glassslides(Fig. 1E),resulting in 24 sections
for each of the nine
sectors.
Sections
were
ex-
aminedwith a Zeissphotomicroscope.
Rodsand cones
were countedin one or two fields,238 ttm wide (Fig.
1F), for a total of 45 countsper sector,or 405 per eye.
1975).
The mean rod and cone densities and rod/cone
ratios correspondingto each different retinal sector
are given in Table 1. Rod and cone densities differ
significantly between species(rods, F, = 11.031,df =
2 and 24, P < 0.001; cones, F, = 7.90, df = 2 and 24,
P < 0.01). As indicated by the Duncan's a posteriori
multiple-range test (P = 0.05), the greatestdensityof
rods is found in the Grey Plover, followed by the
Short-billedDowitcher,while the greatestdensityof
conesis in the GreaterYellowlegs,followed by the
Grey Plover. Thus, the Grey Plover has the greatest
rod/cone ratio, and the Greater Yellowlegshas the
lowest. The density of rods and cones tends to be
greaterin someretinal sectorsthan in others,but our
Cones
Rods: cones
Grey Plover
1
2
3
4
5
6
16.9
17.2
18.5
17.1
19.3
17.8
7
8
9
17.0 ñ 1.4
16.3 ñ_ 1.0
16.8 +_ 0.5
1
2
3
4
5
6
7
8
9
12.3
13.2
13.4
13.8
14.1
18.4
11.6
12.2
11.5
+
+
+
ñ
ñ
ñ
1.3
0.7
0.8
1.1
1.3
1.4
1
2
3
4
5
6
7
8
9
11.3
12.3
13.0
21.9
17.2
15.7
14.1
14.0
14.5
12.5
14.9
18.6
13.2
17.1
17.4
+
+
ñ
ñ
ñ
ñ
1.5
0.8
0.7
2.2
1.9
1.7
1.4:1.0
1.2:1.0
1.0:1.0
1.3:1.0
1.1:1.0
1.0:1.0
17.0 ñ 1.7
1.0:1.0
17.0 + 1.4
17.1 +_ 0.5
1.0:1.0
1.0:1.0
Greater Yellowlegs
Mean rod and cone densities (•/100 ttm+ SE) were
calculatedfor each sector.Resultswere analyzed using a one-way analysis of variance (ANOVA) and
Duncan's a posteriorimultiple-range test (Nie et al.
sectors.
Rods
Semithin sections of 0.7 ttm thick were obtained
with an ultramicrotome(Reitcher-Jung,
Ultracut-E)
143
ñ 1.3
ñ 1.3
ñ 1.4
ñ 1.3
_+ 1.6
+ 2.2
+ 2.6
ñ 2.7
ñ 0.8
Short-billed
ñ
+
+
+
ñ
ñ
ñ
ñ
+
1.0
0.9
1.0
1.0
1.!
1.7
1.1
1.1
1.0
19.6
24.0
22.5
17.3
22.2
18.8
13.4
17.3
15.8
ñ
ñ
ñ
ñ
ñ
ñ
ñ
ñ
ñ
4.6
1.8
1.4
1.8
1.5
2.3
1.8
1.3
1.5
0.6:1.0
0.6:1.0
0.6:1.0
0.8:1.0
0.6:1.0
1.0:1.0
0.9:1.0
0.7:1.0
0.7:1.0
Dowitcher
11.6
14.0
14.4
15.9
16.0
15.5
13.9
14.1
14.5
ñ
ñ
ñ
ñ
ñ
ñ
ñ
ñ
ñ
1.4
1.4
1.4
1.2
1.2
1.7
1.0
1.4
1.0
1.0:1.0
0.9:1.0
0.9:1.0
1.4:1.0
1.1:1.0
1.0:1.0
1.0:1.0
1.0:1.0
1.0:1.0
(equivalentto sectors1 to 6 in our study;seeFig. 1)
of the Grey Plover (Rojasde Azuaje 1991).According
to Meyer (1977),"improvedvisual acuityin birdsmay
be correlatedwith the presence"in the retina of areas
"housingan extremelydensepopulationof conesand
rods."Theseso-calledareasof acutevision "represent
circumscribedthickeningsof the retina broughtabout
presentobjectivewasnot to analyzethe significance by an increasein the number of visual cells (predomof such a difference.
Our startinghypothesiswasverified; the Grey Plo-
ver, a diurnaland nocturnalsightfeederwith larger
eyes,hasmorerodsand a greaterrod/cone ratio than
the GreaterYellowlegs,a daylight sight feeder that
switchesto tactileforagingat night. The Short-billed
Dowitcher,a tactileforagerbothduringdayandnight,
is intermediate.
The electron microscope revealed that the outer
segmentof rodswas longer in the Grey Plover than
in the GreaterYellowlegswith the Short-billedDowitcherbeing intermediate(Rojasde Azuaje1991).Furthermore,theserods,with longeroutersegments,are
particularly abundant in some areas of the retina
inantly cones)" characteristicallylonger than elsewhere in the retina (see also Walls 1942). The outer
segments of the photoreceptors contain the visual
pigments that are responsiblefor the absorption of
light incident upon the retina (Meyer 1977). If areas
of longerconesfavorgoodvisualacuityat high light
levels(Meyer 1977),it seemslikely that areasof longer rods would be associatedwith better low-light
sensitivity.
From these results, it appearsthat the Greater Yellowlegs is lesswell adapted for nocturnal vision than
either the Grey Plover or the Short-billed Dowitcher.
For this reason,the GreaterYellowlegsmay need to
abandonits daytimesight-foragingstrategyfor a tac-
144
ShortCommunications
andCommentaries
[Auk, Vol. 110
availability of their intertidal invertebrate prey.
tile one at night, which may still be quite profitable
Pages357-366 in Cyclic phenomena in marine
since prey availability may be up to 10 times higher
plantsand animals(E. Naylor and R. G. Artnoll,
at night (Robertand McNeil 1989,McNeil et al. 1992).
Eds.). Pergamon Press,Oxford.
The Greater Yellowlegs, thus, uses a tactile sidesweepingstrategythat differsfrom the tactileprobing GERRITSEN, A. F. C., Y. M. VAN HEEZIK, AND C.
of the Short-billed Dowitcher but, as for the latter, it
SwENIqEN.1983. Chemoreceptionin two further
Calidrisspecies(C. maritimaand C. canutus).Neth.
does not need to see its prey.
J. Zool. 33:485-496.
Cone density is highest in the Greater Yellowlegs,
J. D. 1969. The winter feeding ecolfollowed by the Grey Plover and the Short-billed GOss-CusTARD,
ogy of the RedshankTringatotanus.Ibis 111:338Dowitcher, indicating particularly good visual ad356.
aptation in the Greater Yellowlegs, but for daylight
J.D. 1970. Feedingdispersionin some
only. Both the Greater Yellowlegs and the Grey Plo- Goss-CusTARD,
overwintering wading birds. Pages3-35 in Social
ver forage by sight during daylight. However, the
behaviour in birds and mammals (J. H. Crook,
Grey Plover feeds on slow-moving or sessileorganisms (in coastalhabitats on marine worms, small mollusks, crustacea, insects, etc.; in the interior on earthworms, seeds, berries, insects; Bent 1929), while the
Ed.). Academic Press, London.
GOss-CUSTARD,
J.D. 1983. Spatialand seasonalvariations in the food supply of waders Charadrii
wintering in the British Isles. Proc. 3rd Nordic
Congr. Ornithol. 1981:85-96.
Greater Yellowlegs forages on fast-swimming prey
on most occasions(water insects, small fishes, crustacea; Bent 1927). Consequently, it appears that a HALE, W. G. 1980. Waders. Collins, London.
higher cone density would give the Greater Yellow- HULSCHER,J.B. 1976. Location of cockles (Cardium
edule L.) by the Oystercatcher (Haematopusoslegsa goodvisual acuity for foraging on fast-moving
tralegusL.) in darknessand daylight. Ardea 64:
prey during daylight.
292-310.
This study was financed by the Universidad de OrJ.B. 1982. The OystercatcherHaematopus
iente, the Fundaci0nGran Mariscalde Ayacucho,and HULSCHER,
ostralegus
as a predator of the bivalve Macoma
the grant no. F-60of CONICIT (ConsejoNacionalde
balthica in the dutch Waddensea.
Ardea 70:89InvestigacionesCientificasy Tecnologicas,
Venezue152.
la). The participationof McNeil in this study was
financed by the Natural Sciencesand Engineering MARTIN,G. 1990. Birds by night. Poyser,London.
Research Council of Canada, the Universit• de MonMcNEIL, R. 1991. Nocturnality in shorebirds.Pages
1098-1104 in Acta XX CongressusInternationalis
treal, and the Universidad de Oriente through the
collaboration agreement between that university in
Venezuela
and the Universit•
de Montreal.
We thank
Ornithologici. Christchurch, New Zealand Ornithol. Congr. Trust Board,Wellington.
Th•r•se Cabanafor helpful commentson the manu- McNEII•, R., P. DRAPEAU, AND J. D. GOss-CUSTARD.
1992. The occurrenceand adaptive significance
script.
of nocturnal
habits in waterfowl.
Biol. Rev. Camb.
Philos. Soc.In press.
LITERATURE CITED
McNEIL,
R., P. DRAPEAU, AND R. PIEROTTI. 1993.
Nocturnality in colonialwaterbirds:Occurrence,
specialadaptations,and suspectedbenefits. Current Ornithol. 10: In press.
BATTY,L. 1991. Aspectsof the phenologyof waders
(Charadrii) on the Ria Formosa,Portugal.Ph.M.
McNEIL, R., AND M. ROBERT. 1988. Nocturnal feedthesis,Univ. Wales, Cardiff, United Kingdom.
BENT, A.C.
1927. Life histories of North American
ing strategiesof someshorebirdspeciesin a tropshore birds, part 1. U.S. Natl. Mus. Bull. 142.
ical environment. Pages 2328-2336 in Acta XIX
BENt, A.C.
1929. Life histories of North American
Congressus Internationalis Ornithologici (H.
shore birds, part 2. U.S. Natl. Mus. Bull. 146.
Ouellet, Ed.). Ottawa, Ontario, 1986. Univ. Ottawa Press, Ottawa.
Boire, D. 1989. Comparaisonquantitative de l'enc•phale, de sesgrandessubdivisionset de relais MEYER,D.B. 1977. The avian eye and its adaptations.
visuels,trijumeauxet acoustiques
chez28 esp•ces
Pages549-611 in The visual systemin vertebrates,
d'oiseaux. Th•se de Ph.D., Univ. Montreal, Monvol. VII/5 (F. Crescitelli, Ed.). Springer Verlag,
treal.
Berlin.
DUGAN,P.J. 1981. The importanceof nocturnalfor- MEYER,D. B., AND H. C. MAY. 1973. The topographical distribution
of rods and cones in the adult
aging in shorebirds:A consequenceof increased
invertebrate prey activity. Pages251-260 in Feedchicken retina. Exp. Eye Res. 17:347-355.
ing and survivalstrategiesof estuarineorganisms MILSOM,T.P. 1984. Diurnal behaviourof Lapwings
(N. V. Jonesand W. J. Wolff, Eds.). Plenum Press,
in relation to moon phase during winter. Bird
New York.
Study 31:117-120.
EvANs,P. R. 1979. Adaptations shown by foraging MILSOM,T. P., J. B. A. ROCHARD,AND S. J. POOLE. 1990.
shorebirdsto cyclicvariationsin the activityand
Activity patternsof Lapwings Vanellusvanellusin
January
1993]
ShortCommunications
andCommentaries
relation to the lunar cycle.Ornis Scand.21:147156.
NIE, N. H., C. H. HULL, J. G. JENKINS,K. STEINBRENNER,
AND D. H. BENT. 1975. SPSSstatistical package
for the social sciences. McGraw-Hill,
New York.
PETrIGREW,
J. D., ANDB. J. FROST.1985. A tactile fovea
in the Scolopacidae?Brain Behav. Evol. 26:185195.
PIENKOWSKI,
M.W. 1981. How foragingploverscope
with
environmental
effects on invertebrate
be-
haviour and availability. Pages179-182in Feeding and survivalstrategiesof estuarineorganisms
(N. V. Jonesand W. J. Wolff, Eds.). Plenum Press,
New
145
ROJAS
DEAZUAJE,L.M. 1991. Proporci6n de conos
y bastonesen la retina de tres especiesde aves
limlcolasy la relaci6nentre visi6n y estrategia
alimenticia.
Tesis de M.Sc., Instituto
de Inves-
tigacionesen Biomedicina y Ciencias Aplicadas,
Univ. Oriente, Cuman•, Venezuela.
SCHNEIDER,
D.C. 1983. The food and feeding of
migratory shorebirds.Oceanus26:38-43.
SCHWARTZKOPFF,
J. 1973. Mechanoreception.Pages
417-477 in Avian biology,vol. 3 (D. S. Farner and
J. R. King, Eds.).AcademicPress,New York.
SPENCER,
K. G. 1953. The Lapwing in Britain. A.
Brown & Sons, London.
SUTHERLAND,
E.J. 1982. Do oystercatchers
selectthe
York.
most profitable cockles? Anita. Behav. 30:857PIENKOWSKI,
M.W. 1982. Diet and energy intake of
861.
Grey and Ringedplovers,Pluvialissquatarola
and
K., ANDJ. T. ERICHSEN.1985. Vision. Pages
Charadriushiaticula,in the non-breeding season. TANSLEY,
623-629 in A dictionaryof birds (B.Campbelland
J. Zool. (Lond.) 197:511-549.
E. Lack, Eds.).Poyser,Calton, United Kingdom.
PIENKOWSKI,
M.W. 1983a. Changesin the foraging
VAN HEEZIK, Y. M., A. F. C. GERRITSEN, AND C.
pattern of plovers in relation to environmental
factors. Anim. Behav. 31:244-264.
SWENNEN.1983. The influence of chemoreception on the foraging behaviour of two speciesof
PIENKOWSKI,
M.W. 1983b. Surfaceactivity of some
sandpiper, Calidrisalbaand Calidrisalpina.Neth.
intertidal invertebratesin relation to temperaJ. Sea Res. 17:47-56.
ture and foraging behaviour of their shorebird
YON BOLZE,G. 1968. Anordnung und Bau der
predators.Mar. Ecol. Prog. Ser. 11:141-150.
herbstschen K6perchen in Limicolenschn•ibeln
ROBERT,
M., ANDR. MCNEIL. 1989. Comparativeday
im Zusammenhangmit der Nahrungsfindung.
and night feedingstrategiesof shorebirdspecies
Zool.
in a tropical environment. Ibis 131:69-79.
ROBERT,M., R. MCNEIL, AND A. LEDUC. 1989. Con-
ditions and significanceof night feeding in
shorebirdsand other water birds in a tropical
lagoon. Auk 101:94-101.
ROCHON-DuVlGNEAUD,
A. 1943. Lesyeux et la vision
Anz.
181:313-343.
WALLS,
G. L. 1942. The vertebrateeyeand its adaptive radiation. Cranbrook Institute of Science,
Bloomfield Hills, Michigan.
Received
2 December
1991,accepted
6 September
1992.
des vertbbrbs. Masson et Cie, Paris.
The Auk 110(1):145-148, 1993
ExtendedParent-Offspring Relationshipsin Greenland White-fronted Geese
(Anser alb iœrons ltla virostris)
STEPHANIEM. WARREN,1 A.D.
FOX,' ALYN WALSH,2 AND PADDY O'SULLIVAN2
•TheWildfowlandWetlandsTrust,Slimbridge,
Gloucester
GL27BT,UnitedKingdom;
and
2National
ParksandWildlifeService,WexfordWildfowlReserve,
NorthSlob,Wexford,Ireland
Continuing associations between parents and
fledged offspring are uncommon among most bird
species.They are, however, especiallyprevalent in
territorial species with cooperative breeding (see
Brown 1987).Although cooperativebreeding hasnot
been recorded in wildfowl, it has long been recognized that juvenile geeseremain with their parents
for at leastpart of their firstyear (Phillips 1916,Eider
and Eider 1949,Hochbaum1955).Guiding offspring
on migrationto traditionalstagingand winteringsites
and teachingoffspringvaluableforagingtechniques
and social skills, as well as the locations of safe and
productive feeding and roosting sites, are common
explanationsfor the prolongedparent-offspringrelationshipsin migratorygeeseand swans.
GreenlandWhite-frontedGeese(Anseralbifrons
fiavirostris;
Dalgetyand Scott1948)breedin WestGreenland between64ø and 72øN,and winter exclusively