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Birds Attracted To A Common Food Source. The Structure of Seabird Flocks Has Never Been
Birds Attracted To A Common Food Source. The Structure of Seabird Flocks Has Never Been
FORAGING
ECOLOGY
DAVID
OF PERUVIAN
DUFFY
SEABIRDS
CAMERON
ABSTRACT.--Most feeding by seabirdsin the Peruvian CoastalCurrent, an upwelling of high productivityoff the west coast SouthAmerica,takesplacein groups.The majorprey of is an anchovy(Engraulis ringens), which occursin large shoalsand is exploitedmainly by three species: the Peruvian Booby (Sulavariegata), Peruvian Brown Pelican (Pelecanus occidentalis thagus), GuanayCormorant(Phalacrocorax and bougainvillii). Other foragingsituations have different species' compositions, and these appear to be related to the size, depth, and duration of availability of prey. Dominanceinteractionsbetween species may be important in structuringflocksthat are scavenging feedingon planktonswarms. or Interspecific piracy seemsunimportant in flocks foraging on fish shoals.Certain speciesusually arrive first at new feeding situations.Thesespecies may be usedas guidesby other species merely may or be faster and thus reach food sourcesfirst. Studies of foraging of seabirdsshould be a valuable addition to the study of the distribution of birds at sea. Received April 1982, 2 resubmitted March 1983,accepted July 1983. 18 8
SEABIRDS have some of the largest foraging ranges of any vertebrates:birds with eggs or young may travel 1,000 km from the nest to feed (Fisher and Lockley 1954, Harris 1977,
Nelson 1979, Dunnet and Ollason 1982). De-
spite the fact that they searchover such large areas,they forage over very small areason local concentrations prey (see Brown 1980 for a of review). The study of thesepatchesand their use by birds should improve our understanding of the ecologyand distribution of seabirds at sea.For example,Erwin (1977) linked differencesin use of patchesby three larids to differencesin their nesting ecology. Hoffman et al. (1981) showed that the presenceof some species may affectthe foragingof others;flocks are more than aggregationsof noninteracting
birds attracted The structure to a common food source. of seabird flocks has never been
The studyarea.--I gathered most of my observations on Isla Mazorca (1123'S, 7745'W), Departamento de Lima, Peru. The island lies approximately
15 km offshore an areaof frequentupwelling(Zuta in and Urquizo 1972)and is the siteof a largeand longestablishedcolony of guano birds, especiallyPeruvian Booby(Sulavariegata), Peruvian Brown Pelican (Pelecanus occidentalis thagus), and GuanayCormorant (Phalacrocorax bougainvillii) (Murphy 1925;Duffy 1981, 1983a). Other observations were madeon 12 boattrips
between Isla Mazorca and the port of Huacho (1107'S,7744'W) and from the shore at La Puntilia,
Callao Harbor (1205'S, 7744'W).
The Peruvian Current is one of the most productive of marine ecosystems (Cushing 1971).It extends
from northern Chile to northern Peru and out to the
investigated in low-altitude upwelling areas. The presentpaper reportson the numbersand behaviorsof seabirdspeciespresent in different types of feeding flocksin the Humboldt or
Peruvian Coastal Current off the west coast of
South America. Three general questionswere investigated: what percentage birds for(1) of age in flocksover patchesof prey, (2) doesthe species'compositionof flocks differ in accordance with the type of feeding situation, and (3) are flocksmerely aggregations indepenof dently attractedbirds or do the species interact to enhanceor inhibit the discoveryor exploi800
Galapagos Islands, Ecuador(Murphy 1936). The upwelling is confinedto a relativelynarrowbandalong the coast(Cushing 1971). The dominant fish species of the upwelling is the Peruvian anchovyor anchoveta (Engraulis ringens), which makesup about90%of pelagicfish stocksin the current, basedon relative abtmdances eggsand larvae (Santander1981).The of anchoveta is eaten by a wide variety of seabirds, predatory fish, and marine mammals (Coker 1920, Murphy 1936,Jordan and Fuentes1966,Paulik 1971). A commercial fishmealindustry,which beganin 1955, took catchesof up to 12 million metric tons of anchoveta, becoming the world's largest single-species fishery before the fish stockand industry collapsed
October1983]
801
Number
ScavI1 48 94
.... ....
Sea- plank"Other"
Species
HumboldtPenguin(Spheniscus humboldti)
Waved Albatross(Diomedea irrorata) Wilson's Storm-Petrel(Oceanites oceanicus)
88 52 100 100
1
1
Unidentifiedstorm-petrels CapePetrel(Daption capense) Sooty Shearwater (Puffinus griseus) PeruvianDiving-Petrel(Pelecanoides garnoti) Magnificent Frigatebird (Fregata magnificens) NeotropicalCormorant(Phalacrocorax olivaceus) Guanay Cormorant bougainvillii) (Ph. Red-legged Cormorant gaimardi) (Ph. Blue-footed Booby (Sula nebouxii) Peruvian Booby variegata) (S.
Peruvian Pelican (Pelecanus occidentalis thagus) Red-neckedPhalarope(Phalaropus 1obatus) PomarineJaeger(Stercorarius pomarinus)
5
....
+ -
+ -
95
I00
98 7 ....
.... 99 51
2 93 100
100
50
95 69 .... 27
+ +
1 49 50 5 30
100
72
7 1,429
554
71
41
43
28
12
4
3 36 I 60 .... .... 26 94.4 65 20
49
71 11 -
3
12 I + -
16
14 21 44 -
28
51 79 55 40 100 IO0 34 4.7 137 27
94 743
86 1,328
5
2 2 7,195
I 0.1 67 6
8 0.2 49 I0
30 0.6 37 7
I "terrestrial-seizing" birds for in 1972-1973 (Idyll 1973;Duffy 1983b). pilchard surface-diving.added A on zone.Fordipping (Sardinops wasthought havereplaced sagax) to the feeding landorin theintertidal I duration contact of with water, anchoveta duringthe 1970's (Walshet al. ! 980),but species, measured usinga spring-operated stopwatch and subtracting the data are equivocal. time.Fordivingand plunging Observations.--I madeasmanyobservations ma- 0.2 s for my reaction of I measured duration submergence the of from rine birds as possibleduring the courseof other species,
fieldworkbetweenSeptember 1977and March 1978. I recorded foraging all birdsencountered. Species are
listed in Table I.
ing individualbirdsuntil they completed atI0 tempts ceased or feeding. recorded I interspecific
interactions that included association with marine
mammals, aggressive displacement from potential sources food,kleptoparasitism, orderof arrivof and
al at food sources. Not all of these data could be col-
(less than20-50)by directcounts individuals. of In larger groups,I estimated subgroup a and then
countedthe number of such subgroups. defined I
lected simultaneously, in the results, sample so, the sizes maydifferbetween differentmeasurements.
I assumed that the foraging behaviorsand situations I encounteredwere proportional to their true
I to as feeding techniques following simplified by a version abundances.attempted observe wide a variety situations possible watching as by from of Ashmole's(1971) terminology: piracy, dipping, of foraging observations at surface-seizing, plunging, pursuit-plunging, and both shipsand land;by attempting
802
All birds
Number Number/ at shoals
Frequency
at shoals
(%) 68 20 !1
0.4 0.3
(%) 95 77 12
29 25
Grey Gull
Franklin's Gull
584
270
117
39
0.!
+
8
!1
Red-legged Cormorant
Wilson's Storm-Petrel Waved Albatross Band-tailed Gull "Comic" tern
58
51 25 23 8
12
25 4 7 3
+
+ + + +
8
3 9 5 5
Jaegersp. Peruvian Diving-Petrel Pomarine Jaeger Elegant Tern Kelp Gull Humboldt Penguin Blue-footedBooby Storm-petrel sp.
5 4 3 3 3 2 i !
+ + + + + + + +
night, using a full moon or bioluminescence; by and combining observations from before (September-October) and during (November-March) the breeding season.The 7-month period should also have been long enough to sample any seasonalvariations in foraging.
RESULTS
five arbitrary but recognizableforaging situations:shoal-foraging, scavenging, foragingover sealions,feeding on zooplankton swarms,and
miscellaneous other situations. These are re-
ferred to as shoal, scavenging, sealion, zooplankton, and "other" foraging groups throughout this paper. This study was conductedafter the collapse Foraging overshoals fish.--Shoalsof anchoof of the anchoveta stock (Idyll 1973). This col- veta and other fish were frequently fed upon lapse has affected the populations of guano by seabirds the watersaround Mazorca.Bird in birds (Duffy 1983b),but food did not appear to flockswere characteristically very dense. I asbe in short supply around Isla Mazorcaduring sumed other such dense bird flocks were also my study. Foraging trips by Guanay Cormo- feeding on fish shoals,even when I could not
rants and Peruvian Boobies took less than 3 h
(Duffy 1983a).Vogt (1942) considered trips over 6 h to indicate food shortages. frequently obI served shoalsof fish, and birds feeding upon
them, around the islands. After October, an-
seethe fish.Of all individuals,94%foragedover shoalsof fish. Twenty species participated(Table 1), but 98% of the individuals over shoals
chovetas were frequent in regurgitations or stomach casts the cormorant,booby,and pelof ican. I assumethat the foraging behaviors I observed were similar to those used before the
were of three species: Peruvian Booby,Guanay Cormorant, and SootyShearwater (Table2). Inca
Terns and Brown Pelicans were less numerous
Many large groupsforaging over shoalspersisted for 2-3 h or more. In other cases, instead of at least 28
of large groups, the birds formed a mosaicof smaller aggregations, which persistedfor only
about 15 min. Peruvian Boobies initiated 9 of
speciesoccurred in 355 observationsof birds foraging (Table 1). Only 48 of all individuals
October1983]
803
Freat
birds quency
ber bet/ seaseaNumNum-
birds quency
zoozoo-
bet
Species
Inca Tern
Species
Inca Tern
ent
567
fence
13.8
(%)
80.6
(%)
84
preso ent
2,191
ton (%)
62
ton (%)
89
Grey Gull
43
4.3
6.1
20
SootyShearwater
Band-tailed Gull
42
16
6.0
1.4
6.0
2.2
17
22
Grey Gull
"Comic" tern
621
580
28.2
30.5
17.5
16.4
59
51 22
11 11
5 4 3 I
1.1 2.2
1.0 2.0 3.0 1.0
1.6 1.6
0.7 0.6 0.4 0.1
20 10
10 4 2 2
Band-tailed
Sabine's
Gull
87
10.9
2.4
SootyShearwater
Gull
27
18
5.4
9.0
0.8
0.5
13.5
5
Kelp Gull
13
2.6
0.4
13.5
the cone of hovering birds. Grey Gulls (with Kelp and Band-tailed gulls if present) sat on
the surface below the cone, Inca Terns were at
curred irregularly and in small numbers. Average flock size over sealions was 14.3 birds
(SD = 45.7; n = 49).
Foragingon zooplankton swarms.--Dipping or surface-seizingof zooplankton involved seven species and 0.6% of all individuals (Table 1). Only three specieswere common: Inca Terns, "comic" (mainly Arctic) terns, and Grey Gulls made up 96% of all neuston-feeders (Table 4). Sooty Shearwatersand Kelp, Band-tailed, and Sabine'sgulls were rare and irregular. The prey I observedwere 1-cm, reddish crustacea swarming in densities of up to 1,000/m 2 at or just below the surface.Some patchespersisted for hours, but most were short-lived,
lasting no more than 5 min. Most of the neuston-feeding took place in the austral spring,
before anchoveta became terns common hovered in stomach in "cones"
the center of the hovering birds, and "comic" terns were at the periphery. Grey Gulls had the highest feeding rates,followed by Inca and then "comic" terns (Table 5). The higher rate of the Grey Gull was not due entirely to the differencein foragingmethods (surface-seizingvs. hovering + dipping): Band-tailedand Sabine'sgulls had lower rates than the terns, even though Band-tailedGulls foraged in the samemanner as Grey Gulls and Sabine'sGulls used a foraging method intermediate between dipping and surface-seizing. During one observationperiod when several species were foragingover short-livedpatches of zooplankton, Inca Terns arrived before Grey Gulls at surfacepatches7 of 7 times (binomial, P = 0.008). The mean group size during all zooplankton feeding was 95.9 (SD = 83.2; n = 37). Scavenging.--At sea,birds scavengedfish offal, sealioncorpses, and nestlingsthat had fallen from the guanoislands.On land, they scavenged bird corpses, pellets regurgitated by cormorants,and regurgitations from nestlings. Seven species,but only 0.1% of all individuals in this study, scavenged(Table 1). Band-tailed
Gulls were the most numerous, both in num-
pellets of cormorants.
"Comic" and Inca
greater number would be above and outside. Hovering was punctuated by irregular bouts of dipping. Sabine's Gulls landed briefly on the water to peck at prey, whereas the three other
bers and in frequency of occurrence(Table 6). Kelp Gulls were frequent, but rarely more than two birds were present. Inca Terns occurred infrequently but in large numbers. Kelp Gulls specialized on corpses(43 of 67; 67%), whereas only 57 of 272 (21%) Band-tailed Gulls were necrophagous. The difference is significant (2X2 contingency table, correctedfor
804
[Auk,Vol. 100
All
Fre-
Species
SD
0.181 0.062 0.146 --
birds
Grey Gull
Inca Tern Arctic Tern Band-tailed Gull Sabine's Gull
0.584 0.466
477
452 147 71 7
50
53 18 1!
Species
Band-tailed Inca Tern Gull
Franklin's
Gull
86
16
7.5
67 7
3
2.4 1.4
1.5
12.6 1.3
0.6
42 7.4
3.0
continuity; X2 = 19.1; P < 0.001). The most important sourcesof food for Band-tailed Gulls while scavengingwere regurgitated pellets of
cormorants (101 of 272; 37%). Inca Terns and
Franklin's and Grey gulls fed on small particulate offal in the water.
plunge, 1; pursuit-plunge, 1; surface-dive,3 (or 4 if a single piracy record for Guanay Cormorant is excluded)]. Two speciesused 2 techniques, 4 speciesused 3, and 4 speciesused 4.
This gradient in food size paralleled the apparent dominance hierarchy. Kelp Gulls invariably displacedBand-tailedand Grey gulls. Band-tailedGulls displacedFranklin's Gulls and Inca Terns, and Franklin's Gulls displacedInca
Terns. Reversals were not observed.
When foragingmethods rankedaccording are to their mostcommonusage(Table 8), surfaceseizing proves to be the dominant foraging methodof 6 species, surface-diving 4 species, of
dipping of 3 species,piracy of 2 species,pursuit-plungingof 1 species, and plunging of 1
species. Species that primarily used surface-
"Other" foraging.--This group includes those recordsthat did not fall into the precedingcategories. Twenty-seven speciesand 4.7% of all individuals were involved in foraging situations lumped into this category (Table 1). Among the different situationswere the few inshore recordsfrom sandy bottoms,very dispersed feeding on what were probably small anchoveta shoals(most of the Peruvian Booby, Sooty Shearwater, and Guanay Cormorant records),solitary foraging, and looseaggregations of apparently solitary species(Humboldt Penguin and Red-legged Cormorant). The most common species were the Peruvian Booby
(73.6%) and Inca Tern (Table 7). The 25 other speciescomprisedlessthan 18%of the individuals in this category.No species occurredin all
diving had the narrowest range of foraging methods, only 1.25 per species.Species that primarily used terrestrial seizing (four gulls) had the widest range, averaging four techniques each. Surface-seizingspeciesaveraged 3.6 methods; dipping species, 3.5; pirating species, 2.8; plunging species, 2.4; and pursuitplunging species,2.0. The speciesvaried greatly in the amount of time spent on individual feeding attempts, based on duration of contact with water (Table 5, Fig. 1). Dipping by Inca Terns took only 0.25
s (SD = 0.325; n = 68) while Humboldt Pen-
"Other" foraging situations. Even the most common by number, the Peruvian Booby, occurred only 36% of the time. Fourteen of the speciesoccurred in less than 5% of the observations. Group size was not calculated because of the artificial nature of this category.
]ORAGING BEHAVIOR
guins were submergeda mean time of 75.0 s (SD = 44.9; n = 14). Only three species had submergence durations of over 20 s (Fig. 1): solitary Guanay Cormorants,Red-legged Cormorants, and Humboldt Penguins. Dives by GuanayCormorantsforaging at anchoveta shoals were much shorter (9.55 s; SD =
Seven foraging techniqueswere used by the species observedin this study (Table 8). Seven species usedonly a single technique[piracy, 2;
The final component of foraging behavior measured was intraspecific group size in dif-
October 1983]
Foraging PeruvianSeabirds of
805
Frequency
at "Other"
present 20,834
2,452
occurrence 425
84
(%) 73.6
8.7
(%) 36
21
1,162 1,129
1,017
736
193 188
39
52
4.1 4.0
3.6
2.6
4 4
19
10
Franklin's
Gull
382
32
1.3
Grey Gull
Band-tailed Gull Sabine's Gull
173
156 68
16
10 11
0.6
0.5 0.2
8
12 4
57 56
27
3.8 2.5
2.7
0.2 0.2
0.1
11 16
7
Storm-petrel sp. Red-legged Cormorant NeotropicalCormorant Pomarine Jaeger Jaegersp. Cape Petrel
Peruvian Sandwich Tern
20 16 11 8 2 2
2 2
0.1 + + + + +
+
2 6 2 3 1 1
0.5 0.5
Tern
2 1 1
1
+ + +
+
1 0.5 0.5
0.5
ferent foraging situations.Varianceswere very large, group sizesranging over four ordersof magnitude. Of 18 specieswith sufficientrecords (Fig. 2), 10 specieshad mean group sizes
of less than 10/occurrence, and 5 had means of
gest that, even in the highly productive Peruvian Coastal Current, most food for seabirds
occursin patches.Similar patterns of aggregation have been observedin other oceanographic zones listed by Ashmole (1971): the tropical Pacific(Gould 1974, King 1974), boreal Pacific (Porter and Sealey 1981, Schneider 1982), and BenguelaCurrent (Duffy pers. obs.).
Because anchoveta were the main food taken
by birds during the study period and because Group size varied between foraging situa- anchovetatypically occurin shoals(Vogt 1942), tions (Tables2-4, 6-7), the largestintraspecific most shoalsexploited by the birds were probgroupstending to occurin shoal-foraging, fol- ably comprisedof anchoveta.Anchoveta have lowed by "Other," zooplankton, scavenging, very patchy distributions. In one survey, 55%
and sealions.
DISCUSSION
survey area, while, in another, 36%of the biomasswas concentrated only 3.4%of the area in
(Johannessonand Vilchez 1980). Similar con-
FORAGING IN GROUPS
centrationshave been reported for the northern anchovy (Engraulis mordax) California off
(Mais 1974).Densitieswithin patchesmay range up to 2120 metric tons/km2 in Peru (Johannesson and Vilchez 1980). Anchoveta are therefore both patchy enough and sufficientlyabundant
Over 99%of all birds foragedin groups.Solitary foraging was rare: only Humboldt Penguins (13.5% of 39 observations),Red-legged Cormorant (12% of 73), and Peruvian Diving
806
TABLE Percentage of foraging 8. use techniques Peruvian by seabirds = dominant (* method eachspecies). for
Put-
Terres-
Sur-
suit-
Sur-
Sam-
Species
Humboldt Penguin
Waved Albatross
face dive
100'
pie size
37
17
SootyShearwater Diving-Petrel
Peruvian Pelican
4 .....
18
---
---
59*
63*
-19
36 tOO*
--
----
22 3
498
-.....
--
91*
--
...... 3
1
3
39
94*
49*
---
---
11
Kelp Gull
Franklin's Gull Sabine's Gull Arctic Tern Inca Tern
7
15 --1
1
77* -85* 93*
16
t ----
75*
4 tOO* ---
---15 5
------
------
73
26 24 426 483
Number of species
would also facilitate finding shoals (Olson 1964).Two other deeply foraging species, the Humboldt Penguin and Red-legged Cormorant, shouldalsohavebeen able to reachdepths
where anchoveta are abundant, but neither
species' compositions among foraging situations (Tables 2-4, 6-7) and in the use of different types of patchesby each species(Table 1). Are these reflections of differences in prey composition and behavior or of limitations in the foraging behaviors of the bird species?
First, I consider the anchoveta. Most shoals
specieswas common at shoals. The penguin formerly fed at shoals(Paessler1922, Murphy 1936).Its presentrarity may reflecta recentserious population decline becauseof incidental
occurwithin 40 m of the surfaceand many are found at the surfaceduring the day, but most occurbetween 10 and 20 m depth (Jordan1976,
Johannesson and Vilchez 1980). Surface-feed-
stocks(Duffy et al. in press).Red-leggedCormorants appeared to specialize in foraging in inshore waters with rocky substrates(Coker
the surface. Other shallowly foraging birds, such as Waved Albatross,jaegers,and the pelican, stole fish from seabird species that foraged at depths where anchoveta were most abundant (Duffy 1980).
The most abundant birds at shoals were three
species that can plunge, pursuit-plunge, or surface-dive after deeper prey if necessary: Pethe ruvian Booby, Guanay Cormorant, and Sooty Shearwater (Table 8). The tendency for these species to forage and feed in large numbers
October 1983]
ForagingPeruvian of Seabirds
807
36t
20-
69
40-
80
lOO -
S.D.
also have found the patchestoo small: individuals would have done better to forage alone or in smaller groups. Scavengingand feeding opportunities provided by sealions were also short-lived and
small, which would favor small numbers of
surface. Deeper foraging methods might also have made birds more vulnerable to predation by sealions.
SPECIES' INTERACTIONS AND FORAGING GROUPS
Are the speciesin a foraging group present small birds. The exceptionwould be scavenging at corpses that were rich and relatively per- becauseeach has respondedindependently to sistent food sources. In this case, dominance in a common stimulus or doesthe presenceof one interspecific interactions rather than agility speciesaffect either the discoveryor exploitawould be the most useful attribute. The largest tion of prey by other species? Peruvian Boobies tended to be the first to of the gulls, the Kelp Gull, was the corpse-speforage at anchoveta shoals,and Inca Terns were cialist, displacing the other species. The commonspecies both scavenging in and first at zooplankton swarms. They may have sealionsituationsfed by surface-seizing dip- found the patchesof prey and then attracted or ping. Deeper foraging would have been of lit- other species, the boobyand tern may mereor tle use in obtaining fish offal, corpses, bits ly have respondedto new patchesalready apor of fish thrashedto piecesby a sealionon the parent to other species. Cormorantsand other
808
Jaeger spp. 5
Pomarine Jaeger 7
Humboldt Penguin 14
Kelp Gull 39
16
Waved Albatross
Diving Petrel
-
19
3
Neotrop. Cormorant
Red-legged Cormorant 31
Sabine's Gull 5
Band-tailed
Gull
67
Grey Gull
Franklin's Comic Tern
49
Gull 22 40 Inca Tern
Brown
122
56
Pelican
Guanay Cormorant 57
Society Shearwater 26
' ' ' ' ' ' ' lO ' ' ' ' ' ' lOO i , i , i , lOOO
Fig. 2. Intraspecific group sizes combined from all feeding situations (mean and standard deviation; numbers = sample sizes;x-axis = log-scale).
speciesfrequently ignored plunging by a single booby.Like species the boreal Pacificusin ing Black-legged Kittiwakes(Rissa tridactyIa) to locate patches(Hoffman et al. 1981), however, Peruvian seabirdsmay respondonly to repeated plunging or dipping by "nuclear" (Sealy 1973)or "catalyst" species (Hoffman et al. 1981). Feeding at a patch may be enhanced in a number of ways by the presenceof other species (e.g.Hoffmanet al. 1981).If successful foraging requiresdisruptionof a shoaland its antipredator defenses,massplunging or surface-diving would probablysend fish fleeing from one bird to another, destroy the fish-to-fishorientation necessary coordinatedevasiveaction(Shaw for 1978), or perhaps cause overuse of anaerobic muscletissueso that fish could no longer use bursts of speed to escape(Blaxter 1969). Such anaerobicstress could conceivablyeven lead to
death (Parker and Black 1959). All of these would appear to be more effective with increases in the size of the bird flock relative to
kleptoparasitismis the most visible. The average number of pirates (pelicans, jaegers, and
albatrosses)was so low at shoal and "Other"
foraging situations(Tables2 and 7), relative to the numbersof potential hosts,that piracy does not appear to be a decisive factor in flock foraging. Displacement from prey, particularly carrion, may be much more important in determining which species are present at scavenging situations.Big species, suchas the Kelp Gull, monopolize large carrion, while small scraps and offal go to smaller,more agile birds suchas the Inca Tern. Size may alsoplay a part in groupsfeeding on zooplankton. The larger, surface-seizing gulls settleover the densest part of zooplankton swarms and have the highest foraging rates, while the smaller speciesdip their prey around the periphery, where prey are presumably less abundant. The smaller, fasterspecies have an advantage new patches, at which they can exploit before the larger birds
arrive.
the sizeof the shoalbeing attacked. There must Although one or two speciesare characterbe, however, some upper limit at which the isticof certainforagingsituations, muchlarga food per bird decreases with further increases er number of species minor, occasional are parin flock size. ticipants. It is difficult to imagine how these Among the potential negative effectsof the speciescould coevolvewith others to take adpresence of other speciesin foraging groups, vantageof the foraging situationsstudiedhere.
October 1983]
ForagingPeruvian of Seabirds
809
Summer seabird distribution in Drake Passage, the Chilean Fjordsand off southernSouthAmerica. Ibis 117: 339-356.
COKER,R. C.
56:449-511.
DUFFY, D.C. 1980. Patterns of piracy among Peruvian seabirds: depth hypothesis. a Ibis 122:521535.
1983a. The ecology of tick parasitism on densely nesting Peruvian seabirds.Ecology 64:
110-119.
ACKNOWLEDGMENTS
I thank
El Ministerio
PERU
for permissionto work on the islands and for providing transportation. Cabrera,M. Plenge,and P. D. Yengle providedessential adviceand supportin Peru.
R. G. B. Brown, J. Croxall, H. Horn, P. Prince, D. Schneider,and J. Wiens all improved the manuscript
Workshop.I.C.B.P. Technical Publ. DUNNET, M., & J. C. OLLASON. G. 1982. The feeding dispersal of Fulmars Fulmarusglacialisin the breedingseason. Ibis 124:359-361. ERWlN, M. 1977. Foraging and breeding adaptaR. tions to different food regimesin three seabirds: the Common Tern Sterna hirundo, Royal Tern Sternamaxima,and Black Skimmer Rynchops niger.Ecology58: 389-397.
FISHER, & R. M. LOCKLEY.1954. Seabirds.London, J.,
Collins.
GOULD, J. 1974. Sooty Tern (Sternafuscata). P. Pp. 6-33 in Pelagicstudiesof seabirds the central in
and western Pacific Ocean (W. B. King, Ed.).
Smithsonian Contrib. Zool. 158.
HARRIS, M.P. 1977. Comparative ecology of seabirdsin the Galapagos Archipelago.Pp. 65-76 in
graphicResearch
LITERATURE CITED
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