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Home , Grey gull, Guanay cormorant, List of birds of Peru, Peruvian booby, Peruvian diving petrel, Peruvian pelican

THE FORAGING ECOLOGY OF PERUVIAN

DAVID CAMERON DUFFY PercyFitzPatrick Institute of AfricanOrnithology, University of CapeTown, Rondebosch7700, South Africa

ABSTRACT.--Mostfeeding by seabirdsin the Peruvian CoastalCurrent, an upwelling of high productivityoff the west coastof SouthAmerica, takes place in groups.The majorprey is an anchovy (Engraulisringens), which occursin large shoalsand is exploited mainly by three :the Peruvian (Sula variegata),Peruvian Brown (Pelecanusocci- dentalisthagus), and GuanayCormorant ( bougainvillii). Other foragingsituations have different species'compositions, and these appear to be related to the size, depth, and duration of availability of prey. Dominance interactionsbetween speciesmay be important in structuringflocks that are scavengingor feeding on planktonswarms. Interspecific piracy seemsunimportant in flocks foraging on shoals.Certain speciesusually arrive first at new feeding situations.These species may be used as guidesby other speciesor merely may be faster and thus reach food sourcesfirst. Studies of foraging of seabirdsshould be a valuable addition to the study of the distribution of at sea. Received2 April 1982, resubmitted18 March 1983,accepted 8 July 1983.

SEABIRDShave some of the largest foraging tation of patches of food (e.g. Hoffman et al. ranges of any vertebrates:birds with eggs or 1981)? young may travel 1,000 km from the nest to feed (Fisher and Lockley 1954, Harris 1977, METHODS Nelson 1979, Dunnet and Ollason 1982). De- spite the fact that they searchover such large The studyarea.--I gathered most of my observa- tions on Isla Mazorca (11ø23'S, 77ø45'W), Departa- areas,they forage over very small areason local mento de Lima, . The island lies approximately concentrationsof prey (see Brown 1980 for a 15 km offshorein an areaof frequentupwelling (Zuta review). The study of these patchesand their and Urquizo 1972)and is the site of a large and long- use by birds should improve our understand- establishedcolony of guano birds, especially Peru- ing of the ecologyand distribution of seabirds vian Booby (Sulavariegata), Peruvian at sea.For example,Erwin (1977) linked differ- ( Pelecanusoccidentalis thagus), and Guanay ences in use of patchesby three larids to dif- (Phalacrocoraxbougainvillii) (Murphy 1925;Duffy 1981, ferencesin their nesting ecology. Hoffman et 1983a).Other observationswere madeon 12 boat trips al. (1981) showed that the presence of some between Isla Mazorca and the port of Huacho speciesmay affectthe foragingof others;flocks (11ø07'S,77ø44'W) and from the shore at La Puntilia, Callao Harbor (12ø05'S, 77ø44'W). are more than aggregationsof noninteracting The Peruvian Current is one of the most produc- birds attracted to a common food source. tive of marine ecosystems(Cushing 1971).It extends The structure of flocks has never been from northern to northern Peru and out to the investigated in low-altitude upwelling areas. GalapagosIslands, (Murphy 1936). The up- The present paper reportson the numbersand welling is confinedto a relatively narrow band along behaviors of seabird speciespresent in differ- the coast(Cushing 1971). The dominant fish species ent types of feeding flocksin the Humboldt or of the upwelling is the Peruvian anchovyor ancho- Peruvian Coastal Current off the west coast of veta (Engraulisringens), which makesup about 90% of South America. Three general questionswere pelagic fish stocksin the current, basedon relative investigated:(1) what percentageof birds for- abtmdancesof eggsand larvae (Santander1981). The anchoveta is eaten by a wide variety of seabirds, age in flocksover patchesof prey, (2) doesthe predatory fish, and marine mammals (Coker 1920, species'composition of flocks differ in accor- Murphy 1936,Jordan and Fuentes1966, Paulik 1971). dance with the type of feeding situation, and A commercialfishmeal industry, which beganin 1955, (3) are flocksmerely aggregationsof indepen- took catchesof up to 12 million metric tons of an- dently attractedbirds or do the speciesinteract choveta, becoming the world's largest single-species to enhanceor inhibit the discoveryor exploi- fishery before the fish stockand industry collapsed

800 The Auk 100: 800-810. October 1983 October1983] Foragingof PeruvianSeabirds 801

TABLE1. Percentageuse of differentforaging situations by Peruvianseabirds (+ = <0.1).

Percentagein foraging situation Zoo- Number Scav- Sea- plank- Species observed Shoal enging lions ton "Other" HumboldtPenguin (Spheniscus humboldti) 18 I1 - - - 88 Waved (Diomedeairrorata) 52 48 - - - 52 Wilson's Storm-(Oceanites oceanicus) 54 94 - 6 - - Elliot'sStorm-Petrel (Oceanites gracilis) 1 .... 100 Markham's Storm-Petrel (Oceanodromamarkhami) 1 .... 100 Unidentifiedstorm- 21 5 - - - 95 CapePetrel (Daption capense) 2 .... I00 SootyShearwater (Puffinus griseus) 61,234 98 - + + 2 PeruvianDiving-Petrel (Pelecanoides garnoti) 61 7 - - - 93 MagnificentFrigatebird (Fregata magnificens) 1 .... 100 NeotropicalCormorant (Phalacrocorax olivaceus) 11 .... 100 GuanayCormorant (Ph. bougainvillii) 115,542 99 - - - 1 Red-leggedCormorant (Ph. gaimardi) 114 51 - - - 49 Blue-footedBooby (Sula nebouxii) 2 50 - - - 50 PeruvianBooby (S. variegata) 402,802 95 - + - 5 (Pelecanusoccidentalis thagus) 3,341 69 + + - 30 Red-neckedPhalarope (Phalaropus 1obatus) 1 .... 100 PomarineJaeger (Stercorarius pomarinus) 11 27 - - - 72 Jaegersp. (Stercorariussp.) 7 71 - - - 28 GreyGull (Larusmodestus) 1,429 41 + 3 43 12 Band-tailedGull (L. belcheri) 554 4 49 3 16 28 Kelp (L. dominicanus) 94 3 71 12 14 - Franklin'sGull (L. pipixcan) 743 36 11 I - 51 Sabine'sGull (L. sabini) 86 - - - 21 79 "Comic" (Sternasp.) 1,328 I - + 44 55 ElegantTern (Sternaelegans) 5 60 - - - 40 (S. sandvicensis) 2 .... 100 (S. lorata) 2 .... IO0 (Larosternainca) 7,195 26 I 8 30 34 Percentageof total numberof birds (n = 561,605) 94.4 0.1 0.2 0.6 4.7 Number of observationsfor each foraging type 65 67 49 37 137 Number of speciesin each foraging type 20 6 I0 7 27

in 1972-1973(Idyll 1973;Duffy 1983b).A pilchard surface-diving.I added "terrestrial-seizing" for birds (Sardinopssagax) was thought to havereplaced the feedingon landor in theintertidal zone. For dipping anchovetaduring the 1970's(Walsh et al. ! 980),but species,I measuredduration of contactwith water, the data are equivocal. using a spring-operatedstopwatch and subtracting Observations.--Imade as many observationsof ma- 0.2 s for my reactiontime. For divingand plunging rine birds as possibleduring the courseof other species,I measured the duration of submergencefrom fieldworkbetween September 1977 and March 1978. first contact until the 's head emerged. I mea- I recordedall foragingbirds encountered. Species are suredrates of dipping or surface-seizingby follow- listed in Table I. ing individualbirds until they completedI0 at- Most seabirds in the Peruvian Coastal Current are temptsor ceasedfeeding. I recordedinterspecific relativelyeasy to identify. The exceptionsare the interactions that included association with marine white "comic" (Sternaspp.) and the jaegers mammals,aggressive displacement from potential (Stercorariusspp.). Unidentified birds are treatedsep- sourcesof food,kleptoparasitism, and of arriv- aratelybut makeup onlya minusculeproportion of al at food sources. Not all of these data could be col- birdsobserved. I determinednumbers in small groups lectedsimultaneously, so, in the results,the sample (lessthan 20-50)by directcounts of individuals.In sizesmay differ betweendifferent measurements. larger groups,I estimateda subgroupand then I assumedthat the foraging behaviorsand situa- countedthe number of such subgroups.I defined tions I encounteredwere proportional to their true feedingtechniques by followinga simplifiedversion abundances.I attempted to observeas wide a variety of Ashmole's (1971) terminology: piracy, dipping, of foragingsituations as possible by watchingfrom surface-seizing,plunging, pursuit-plunging,and both shipsand land; by attemptingobservations at 802 DAVID CAMERONDUFFY [Auk, Vol. 100

TABLE2. Species'occurrences over dense shoals of fish (+ = < 0.1).

All birds Frequency Number Number/ at shoals at shoals Species present occurrence (%) (%) 381,957 6,160 68 95 114,380 2,288 20 77 60,036 7,504 ! 1 12 Peruvian Pelican 2,320 122 0.4 29 Inca Tern 1,888 118 0.3 25 584 117 0.! 8 Franklin's Gull 270 39 + ! 1 Red-legged Cormorant 58 12 + 8 Wilson's Storm-Petrel 51 25 + 3 25 4 + 9 Band-tailed Gull 23 7 + 5 "Comic" tern 8 3 + 5 Jaegersp. 5 1.3 + 5 Peruvian Diving-Petrel 4 0.6 + 5 3 1.0 + 5 3 3 + 1.5 3 3 + 1.5 Humboldt 2 1 + 3 Blue-footedBooby i 1 + 1.5 Storm-petrel sp. ! 1 + 1.5

night, using a full moon or bioluminescence;and by seen were feeding alone. After fieldwork, I combining observationsfrom before (September-Oc- found that the records could be divided into tober) and during (November-March) the breeding five arbitrary but recognizableforaging situa- season.The 7-month period should also have been tions:shoal-foraging, scavenging, foraging over long enough to sample any seasonalvariations in sealions,feeding on zooplankton swarms,and foraging. miscellaneous other situations. These are re- ferred to as shoal, scavenging, sealion, zoo- RESULTS , and "other" foraging groups throughout this paper. This study was conductedafter the collapse Foragingover shoals of fish.--Shoalsof ancho- of the anchoveta stock (Idyll 1973). This col- veta and other fish were frequently fed upon lapse has affected the populations of guano by seabirdsin the waters around Mazorca. Bird birds (Duffy 1983b),but food did not appear to flocks were characteristicallyvery dense. I as- be in short supply around Isla Mazorca during 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 took less than 3 h seethe fish.Of all individuals,94% foraged over (Duffy 1983a).Vogt (1942) consideredtrips over shoalsof fish. Twenty speciesparticipated (Ta- 6 h to indicate food shortages.I frequently ob- ble 1), but 98% of the individuals over shoals served shoalsof fish, and birds feeding upon were of three species:Peruvian Booby,Guanay them, around the islands. After October, an- Cormorant,and SootyShearwater (Table 2). Inca chovetas were frequent in regurgitations or Terns and Brown were less numerous stomachcasts of the cormorant,booby, and pel- than shearwatersbut more consistentlypres- ican. I assumethat the foraging behaviors I ob- ent. Other speciescomprised 0.1% or lessof the served were similar to those used before the flocks. The mean flock size over shoals was collapseof the anchovetastock. 8,363.5 birds (SD = 12,629.3; n = 65). Many large groupsforaging over shoalsper- FORAGING SITUATIONS sisted for 2-3 h or more. In other cases, instead of large groups, the birds formed a mosaicof A total of 561,605 individuals of at least 28 smaller aggregations,which persistedfor only speciesoccurred in 355 observationsof birds about 15 min. Peruvian Boobies initiated 9 of foraging (Table 1). Only 48 of all individuals 10 such ephemeral groups. October1983] Foragingof PeruvianSeabirds 803

TABLE3. Species'occurrences over sealions. TABLE4. Species'occurrence at zooplanktonswarms.

All Fre- All Fre- birds quency birds quency Num-Num- with with at at ber bet/ sea- sea- Num- Num- zoo- zoo- pres- occur- lions lions bet bet/ plank- plank- Species ent fence (%) (%) preso occur- ton ton ent fence (%) (%) Inca Tern 567 13.8 80.6 84 Species Grey Gull 43 4.3 6.1 20 Inca Tern 2,191 66.4 62 89 SootyShearwater 42 6.0 6.0 17 Grey Gull 621 28.2 17.5 59 Band-tailed Gull 16 1.4 2.2 22 "Comic" tern 580 30.5 16.4 51 Kelp Gull 11 1.1 1.6 20 Band-tailed Gull 87 10.9 2.4 22 Peruvian Booby 11 2.2 1.6 10 SootyShearwater 27 5.4 0.8 13.5 Franklin's Gull 5 1.0 0.7 10 Sabine's Gull 18 9.0 0.5 5 "Comic" tern 4 2.0 0.6 4 Kelp Gull 13 2.6 0.4 13.5 Wilson's Storm-Petrel 3 3.0 0.4 2 Peruvian Pelican I 1.0 0.1 2

gull speciessat on the water while feeding. The speciesoccupied characteristicpositions around Foragingover sealions.--Thesouthern sealion the cone of hovering birds. Grey (with lOtariabyronia (fiavescens)] provided food for the Kelp and Band-tailed gulls if present) sat on birds, either by chasing fish to the surface or the surface below the cone, Inca Terns were at by thrashing large fish and cephalopods to the center of the hovering birds, and "comic" pieces. Birds usually fed only in a very small terns were at the periphery. area immediately surrounding the sealion. Ten Grey Gulls had the highest feeding rates,fol- species,but only 0.1% of all individuals, for- lowed by Inca and then "comic" terns (Table aged over sealions (Table 1). The major bene- 5). The higher rate of the Grey Gull was not ficiary of sealion activity was the Inca Tern: due entirely to the differencein foragingmeth- 80% of the birds over sealions belonged to this ods (surface-seizingvs. hovering + dipping): species (Table 3). The other nine species oc- Band-tailedand Sabine'sgulls had lower rates curred irregularly and in small numbers. Av- than the terns, even though Band-tailedGulls erage flock size over sealions was 14.3 birds foraged in the samemanner as Grey Gulls and (SD = 45.7; n = 49). Sabine's Gulls used a foraging method inter- Foragingon zooplanktonswarms.--Dipping or mediate between dipping and surface-seizing. surface-seizingof zooplankton involved seven During one observationperiod when several species and 0.6% of all individuals (Table 1). specieswere foraging over short-livedpatches Only three specieswere common: Inca Terns, of zooplankton, Inca Terns arrived before Grey "comic" (mainly Arctic) terns, and Grey Gulls Gulls at surface patches7 of 7 times (binomial, made up 96% of all neuston-feeders (Table 4). P = 0.008). The mean group size during all zoo- Sooty Shearwaters and Kelp, Band-tailed, and plankton feeding was 95.9 (SD = 83.2; n = 37). Sabine'sgulls were rare and irregular. Scavenging.--Atsea, birds scavengedfish of- The prey I observedwere 1-cm, reddish crus- fal, sealioncorpses, and nestlingsthat had fall- tacea swarming in densities of up to 1,000/m 2 en from the guanoislands. On land, they scav- at or just below the surface.Some patchesper- enged bird corpses, pellets regurgitated by sisted for hours, but most were short-lived, ,and regurgitations from nestlings. lasting no more than 5 min. Most of the neus- Seven species,but only 0.1% of all individuals ton-feeding took place in the austral spring, in this study, scavenged(Table 1). Band-tailed before anchoveta became common in stomach Gulls were the most numerous, both in num- pellets of cormorants. bers and in frequency of occurrence(Table 6). "Comic" and Inca terns hovered in "cones" Kelp Gulls were frequent, but rarely more than of birds over zooplankton patches:a few birds two birds were present. Inca Terns occurred would be close to the surface, and a much infrequently but in large numbers. greater number would be above and outside. Kelp Gulls specialized on corpses(43 of 67; Hovering was punctuated by irregular bouts of 67%), whereas only 57 of 272 (21%) Band-tailed dipping. Sabine's Gulls landed briefly on the Gulls were necrophagous.The difference is sig- water to peck at prey, whereas the three other nificant (2X2 contingency table, correctedfor 804 DAVIDCAMERON DUFFY [Auk,Vol. 100

TABLE5. Feedingrates (dips or pecksper second). TABLE6, Species'occurrences in scavengingsitua- tions. Number of All Fre- Species œ SD n birds Num- Num- birds quency ber ber/ scav- scav- Grey Gull 0.584 0.466 477 50 pres- occur- enging enging Inca Tern 0.355 0.181 452 53 Species ent rence (%) (%) 0.166 0.062 147 18 Band-tailed Gull 0.153 0.146 71 1! Band-tailed Gull 272 5.7 51 70 Sabine's Gull 0.120 -- 7 Inca Tern 97 13.9 18 10 Franklin's Gull 86 17.2 16 7.5 Kelp Gull 67 2.4 12.6 42 Grey Gull 7 1.4 1.3 7.4 Peruvian Pelican 3 1.5 0.6 3.0 continuity; X2 = 19.1; P < 0.001). The most im- portant sourcesof food for Band-tailed Gulls while scavenging were regurgitated pellets of plunge, 1; pursuit-plunge, 1; surface-dive,3 (or cormorants (101 of 272; 37%). Inca Terns and 4 if a single piracy record for Guanay Cormo- Franklin's and Grey gulls fed on small partic- rant is excluded)]. Two speciesused 2 tech- ulate offal in the water. niques, 4 speciesused 3, and 4 speciesused 4. This gradient in food size paralleled the ap- When foragingmethods are ranked according parent dominance hierarchy. Kelp Gulls in- to their mostcommon usage (Table 8), surface- variably displacedBand-tailed and Grey gulls. seizing proves to be the dominant foraging Band-tailedGulls displacedFranklin's Gulls and methodof 6 species,surface-diving of 4 species, Inca Terns, and Franklin's Gulls displacedInca dipping of 3 species,piracy of 2 species,pur- Terns. Reversals were not observed. suit-plunging of 1 species,and plunging of 1 Mean group size was 8.1 birds (SD = 19.8; species. Species that primarily used surface- n = 67). diving had the narrowest range of foraging "Other" foraging.--This group includes those methods, only 1.25 per species.Species that recordsthat did not fall into the precedingcat- primarily used terrestrial seizing (four gulls) egories. Twenty-seven speciesand 4.7% of all had the widest range, averaging four tech- individuals were involved in foraging situa- niques each. Surface-seizingspecies averaged tions lumped into this category (Table 1). 3.6 methods; dipping species, 3.5; pirating Among the different situationswere the few species,2.8; plunging species,2.4; and pursuit- inshore recordsfrom sandy bottoms,very dis- plunging species,2.0. persed feeding on what were probably small The speciesvaried greatly in the amount of anchoveta shoals(most of the Peruvian Booby, time spent on individual feeding attempts, Sooty Shearwater, and Guanay Cormorant rec- based on duration of contact with water (Table ords), solitary foraging, and looseaggregations 5, Fig. 1). Dipping by Inca Terns took only 0.25 of apparently solitary species(Humboldt Pen- s (SD = 0.325; n = 68) while Humboldt Pen- guin and Red-legged Cormorant). The most guins were submergeda mean time of 75.0 s common species were the Peruvian Booby (SD = 44.9; n = 14). Only three species had (73.6%) and Inca Tern (Table 7). The 25 other submergencedurations of over 20 s (Fig. 1): speciescomprised less than 18%of the individ- solitary Guanay Cormorants, Red-legged Cor- uals in this category.No speciesoccurred in all morants, and Humboldt . "Other" foraging situations. Even the most Dives by Guanay Cormorantsforaging at an- common by number, the Peruvian Booby, oc- choveta shoals were much shorter (9.55 s; SD = curred only 36% of the time. Fourteen of the 4.45; n = 144) than dives by Guanayselsewhere speciesoccurred in less than 5% of the obser- (32.85 s; SD = 22.15; n = 16; P < 0.001, t = 11.04; vations. Group size was not calculated because F = 24.77;correction for unequal variances). On of the artificial nature of this category. the other hand, Peruvian Boobiesplunging at shoalsshowed no significant differencesin du- ]•ORAGING BEHAVIOR rations of submergence(shoal = 3.12 s; SD = 1.29; n = 234; all other situations = 2.99 s; SD = Seven foraging techniqueswere used by the 1.17; n = 254; P > 0.05). speciesobserved in this study (Table 8). Seven The final component of foraging behavior speciesused only a single technique [piracy, 2; measured was intraspecific group size in dif- October 1983] Foragingof PeruvianSeabirds 805

T^BLE7. Species'occurrences at "Other" foraging situations(+ = < 0.1).

All birds Frequency Number Number/ at "Other" at "Other" Species present occurrence (%) (%) Peruvian Booby 20,834 425 73.6 36 Inca Tern 2,452 84 8.7 21 Guanay Cormorant 1,162 193 4.1 4 Sooty Shearwater 1,129 188 4.0 4 Peruvian Pelican 1,017 39 3.6 19 "Comic" tern 736 52 2.6 10 Franklin's Gull 382 32 1.3 9 Grey Gull 173 16 0.6 8 Band-tailed Gull 156 10 0.5 12 Sabine's Gull 68 11 0.2 4 Peruvian Diving-Petrel 57 3.8 0.2 11 56 2.5 0.2 16 Waved Albatross 27 2.7 0.1 7 Storm-petrel sp. 20 6.7 0.1 2 Red-legged Cormorant 16 2.0 + 6 Neotropical Cormorant 11 3.7 + 2 Pomarine Jaeger 8 2.0 + 3 Jaegersp. 2 1.0 + 1 2 1.0 + 1 Peruvian Tern 2 2.0 + 0.5 Sandwich Tern 2 2.0 + 0.5 Elegant Tern 2 1.0 + 1 Blue-footed Booby 1 1.0 + 0.5 Northern 1 1.0 + 0.5 Elliot's Storm-Petrel 1 1.0 + 0.5

ferent foraging situations.Variances were very gest that, even in the highly productive Peru- large, group sizesranging over four ordersof vian Coastal Current, most food for seabirds magnitude. Of 18 specieswith sufficient rec- occursin patches.Similar patterns of aggrega- ords (Fig. 2), 10 specieshad mean group sizes tion have been observedin other oceanograph- of less than 10/occurrence, and 5 had means of ic zones listed by Ashmole (1971): the tropical 10-100/occurrence. No specieshad mean group Pacific (Gould 1974, King 1974), boreal Pacific sizes of 100-1,000/occurrence, but the three (Porter and Sealey 1981, Schneider 1982), and most common species(Guanay Cormorant, Pe- BenguelaCurrent (Duffy pers. obs.). ruvian Booby,and SootyShearwater) had group Because anchoveta were the main food taken sizes of 1,000-10,000/occurrence. 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 prob- groupstending to occurin shoal-foraging,fol- ably comprisedof anchoveta.Anchoveta have lowed by "Other," zooplankton, scavenging, very patchy distributions. In one survey, 55% and sealions. of the total biomass was confined to 13% of the survey area, while, in another, 36% of the bio- masswas concentratedin only 3.4%of the area DISCUSSION (Johannessonand Vilchez 1980). Similar con- FORAGING IN GROUPS centrationshave been reported for the north- ern anchovy (Engraulismordax) off California Over 99%of all birds foraged in groups.Sol- (Mais 1974). Densitieswithin patchesmay range itary foraging was rare: only Humboldt Pen- up to 2120 metric tons/km2 in Peru (Johannes- guins (13.5% of 39 observations),Red-legged son and Vilchez 1980). Anchoveta are therefore Cormorant (12% of 73), and Peruvian Diving both patchy enough and sufficiently abundant Petrels(100% of 3; seealso Murphy 1936)for- to explainthe largeaggregations typical of birds aged alone with any frequency.These data sug- in the Peruvian coastalupwelling area. 806 DAVIDCAMERON DUFFY [Auk,Vol. 100

TABLE8. Percentageuse of foragingtechniques by Peruvianseabirds (* = dominantmethod for eachspecies).

Put- Terres- Sur- suit- Sur- Sam- trial- face- Plung- plung- face pie Species Piracy Dipping seizing seizing ing ing dive size Humboldt Penguin ...... 37 Waved Albatross 100' ..... 100' 17 SootyShearwater 4 -- -- 59* -- 36 -- 22 Diving-Petrel ..... tOO* -- 3 Peruvian Pelican 18 -- -- 63* 19 -- -- 498 Peruvian Booby 2 -- -- 7 91 * -- -- 786 Guanay Cormorant 1 ..... 99* 152 Neotropical Cormorant ...... 100' 36 Red-leggedCormorant ...... 100' 73 Pomarine and unidentified Jaeger 100' ...... 15 Grey Gull t 3 3 94* ------508 Band-tailed Gull 11 1 39 49* ------349 Kelp Gull 7 1 16 75* ------73 Franklin's Gull 15 77* t 4 ------26 Sabine's Gull ------tOO* ------24 Arctic Tern -- 85* -- -- 15 -- -- 426 Inca Tern 1 93* -- -- 5 -- -- 483 Number of species for which each technique is the dominant 2 3 0 6 1 1 4

PREY CHARACTERISTICS AND would also facilitate finding shoals (Olson FORAGING SITUATIONS 1964). Two other deeply foraging species,the Humboldt Penguin and Red-legged Cormo- There were considerable differences in the rant, shouldalso have been able to reachdepths species' compositions among foraging situa- where anchoveta are abundant, but neither tions (Tables 2-4, 6-7) and in the use of differ- specieswas common at shoals. The penguin ent types of patches by each species(Table 1). formerly fed at shoals(Paessler 1922, Murphy Are these reflections of differences in prey 1936).Its presentrarity may reflecta recentse- composition and behavior or of limitations in rious population decline because of incidental the foraging behaviors of the bird species? mortality in fishing nets and from poaching First, I consider the anchoveta. Most shoals and becauseof the collapse of the anchoveta occurwithin 40 m of the surfaceand many are stocks(Duffy et al. in press).Red-legged Cor- found at the surfaceduring the day, but most morants appeared to specialize in foraging in occurbetween 10 and 20 m depth (Jordan1976, inshore waters with rocky substrates(Coker Johannesson and Vilchez 1980). Surface-feed- 1920, Murphy 1936, Brown et al. 1975, pers. ing species,such as gulls and terns, occurred obs.). at fish shoals, so some anchoveta must occur at The zooplanktonthat I observedbeing taken the surface. Other shallowly foraging birds, as prey and in the water at zooplankton for- such as Waved Albatross, jaegers,and the pel- aging situations were small (approximately 1 ican, stole fish from seabird species that for- cm), locally very abundant, and present near aged at depths where anchoveta were most the surface for only short periods of at most 5 abundant (Duffy 1980). min. The most common birds at zooplankton The most abundant birds at shoals were three situations were small gulls and terns, which speciesthat can plunge, pursuit-plunge, or sur- foragedby dipping and surface-seizing.Larger face-dive after deeper prey if necessary:the Pe- speciesmay have found it energetically ineffi- ruvian Booby, Guanay Cormorant, and Sooty cient to eat such small prey and to make fre- Shearwater (Table 8). The tendency for these quent moves from one short-lived patch to species to forage and feed in large numbers another. Species that forage in groups would October1983] ForagingofPeruvian Seabirds 807

36t

20-

69

40-

80

•ñ S.D.

lOO -

Fig. 1. Durationsof submergenceof somemore commonPeruvian seabirds(means and standarddevia- tions; numbers= samplesizes). also have found the patchestoo small: individ- surface. Deeper foraging methods might also uals would have done better to forage alone or have made birds more vulnerable to predation in smaller groups. by sealions. Scavengingand feeding opportunities pro- vided by sealions were also short-lived and SPECIES' INTERACTIONS AND FORAGING GROUPS small, which would favor small numbers of small birds. The exceptionwould be scaveng- Are the speciesin a foraging group present ing at corpsesthat 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 exploita- would be the most useful attribute. The largest tion of prey by other species? of the gulls, the Kelp Gull, was the corpse-spe- Peruvian Boobies tended to be the first to cialist, displacing the other species. forage at anchoveta shoals,and Inca Terns were The commonspecies in both scavengingand first at zooplankton swarms. They may have sealionsituations fed by surface-seizingor dip- found the patches of prey and then attracted ping. Deeper foraging would have been of lit- other species,or the boobyand tern may mere- tle use in obtaining fish offal, corpses,or bits ly have respondedto new patchesalready ap- of fish thrashedto piecesby a sealion on the parent to other species.Cormorants and other 808 DAVIDCAMERON DUFFY [Auk,Vol. 100

Jaeger spp. 5 Pomarine Jaeger 7 Humboldt Penguin 14 Kelp Gull 39

Waved Albatross 16

Diving Petrel 19 - Neotrop. Cormorant 3 • Red-legged Cormorant 31

• Sabine's Gull 5

• Band-tailed Gull 67

• Grey Gull 49

• Franklin's Gull 22

• Comic Tern 40

• Inca Tern 122

• Brown Pelican 56 G•uanayCormorant 57 SocietyShearwater 26 • Peruviar] Booby 118 ' ' ' ' ' ' ' lO ' ' ' ' ' ' lOO i , i , i , lOOO ' ' ' ' ' ' •oooo

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 sin- kleptoparasitismis the most visible. The aver- gle booby.Like speciesin the boreal Pacificus- age number of pirates (pelicans, jaegers, and ing Black-leggedKittiwakes (Rissa tridactyIa) to )was so low at shoal and "Other" locate patches(Hoffman et al. 1981), however, foraging situations(Tables 2 and 7), relative to Peruvian seabirdsmay respond only to repeat- the numbersof potential hosts,that piracy does ed plunging or dipping by "nuclear" (Sealy not appear to be a decisive factor in flock for- 1973)or "catalyst"species (Hoffman et al. 1981). aging. Displacement from prey, particularly Feeding at a patch may be enhanced in a num- carrion, may be much more important in de- ber of ways by the presenceof other species termining which species are present at scav- (e.g.Hoffman et al. 1981).If successfulforaging enging situations.Big species,such as the Kelp requiresdisruption of a shoaland its antipreda- Gull, monopolize large carrion, while small tor defenses,mass plunging or surface-diving scrapsand offal go to smaller,more agile birds would probablysend fish fleeing from one bird suchas the Inca Tern. Size may alsoplay a part to another, destroy the fish-to-fishorientation in groupsfeeding on zooplankton. The larger, necessaryfor coordinatedevasive action (Shaw surface-seizinggulls settleover the densestpart 1978), or perhaps cause overuse of anaerobic of zooplankton swarms and have the highest muscle tissueso that fish could no longer use foraging rates, while the smaller speciesdip bursts of speed to escape(Blaxter 1969). Such their prey around the periphery, where prey anaerobicstress could conceivablyeven lead to are presumably less abundant. The smaller, death (Parker and Black 1959). All of these fasterspecies have an advantageat new patches, would appear to be more effective with in- which they can exploit before the larger birds creases in the size of the bird flock relative to arrive. the size of the shoalbeing attacked.There must Although one or two speciesare character- be, however, some upper limit at which the isticof certainforaging situations, a much larg- food per bird decreaseswith further increases er number of speciesare minor, occasionalpar- in flock size. ticipants. It is difficult to imagine how these Among the potential negative effectsof the speciescould coevolvewith others to take ad- presence of other speciesin foraging groups, vantageof the foraging situationsstudied here. October1983] ForagingofPeruvian Seabirds 809

These peripheral speciesmay themselvesbe Summer seabird distribution in Drake Passage, major participantsin other foraging situations the Chilean Fjordsand off southernSouth Amer- than those studied here. For example, Neotrop- ica. 117: 339-356. ical Cormorants, Peruvian Brown Pelicans, Pe- COKER, R. C. 1920. Habits and economic relations ruvian Boobies, Franklin's Gulls, and Black of the guanobirds of Peru. Proc.U.S. Natl. Mus. 56:449-511. Skimmers(Rynchops niger) seem to be the main CUSHING,D.H. 1971. Upwelling and production of participantsin foraginggroups in estuariesand fish. Adv. Mar. Biol. 9: 255-334. bays (pers. obs.). Brown (1981) identified a DUFFY,D.C. 1980. Patterns of piracy among Peru- group of surface-feedingstorm-petrels (Hydro- vian seabirds:a depth hypothesis.Ibis 122:521- batidae) as characteristic of warmer, offshore 535. waters. Foraging over dolphins (Delphinidae) ß 1981. Seasonalchanges in the seabirdfauna seemsto be more important in northern waters of Peru. Ardea 69: 109-113. (Brown 1981, pers. obs.) but was never seen 1983a. The ecology of tick parasitism on farther south during this study. densely nesting Peruvian seabirds.Ecology 64: 110-119. Feeding seabirdsare much rarer than birds 1983b. Environmental uncertainty and flying or sitting on the water, so distributional commercial fishing: effects on Peruvian guano studieshave concentratedon nonfeeding birds. birds. Biol. Conserv. 26: 227-238. Closer study of feeding groups may serve as a -, C. HAYS,& M. A. PLENGE.In press. The con- valuable adjunct to distributional studies, be- servation status of Peruvian seabirds. Seabird causeit is while feeding that seabirdshave their Workshop.I.C.B.P. Technical Publ. closest links to the marine environment. DUNNET,G. M., & J. C. OLLASON.1982. The feeding dispersal of Fulmarusglacialis in the

ACKNOWLEDGMENTS breedingseason. Ibis 124:359-361. ERWlN,R. M. 1977. Foraging and breeding adapta- I thank El Ministerio de Pesca and PESCA PERU tions to different food regimesin three seabirds: for permissionto work on the islands and for pro- the Sterna hirundo, viding transportation.D. Cabrera,M. Plenge,and P. Sternamaxima, and Rynchopsni- Yengle providedessential advice and supportin Peru. ger.Ecology 58: 389-397. R. G. B. Brown, J. Croxall, H. Horn, P. Prince, D. FISHER,J., & R. M. LOCKLEY.1954. Seabirds. London, Schneider, and J. Wiens all improved the manuscript Collins. with their commentsßMy wife prepared the illustra- GOULD,P. J. 1974. (Sternafuscata). Pp. tions. Field work was funded by The National Sci- 6-33 in Pelagicstudies of seabirdsin the central ence Foundation (DEB77-16077), The International and western Pacific Ocean (W. B. King, Ed.). Council for Bird Preservation (Pan American), and Smithsonian Contrib. Zool. 158. PrincetonUniversityß Data analysisand writing were HARRIS,M.P. 1977. Comparative ecology of sea- supportedby the BenguelaEcology Programme of birds in the GalapagosArchipelago. Pp. 65-76 in the South African National Committee for Oceano- Evolutionaryecology (B. Stonehouseand C. Per- graphicResearchß rins, Eds.). London, MacMillan. HOFFMAN, W., D. HEINEMANN, & J. A. WIENS. 1981. LITERATURE CITED The ecologyof seabirdfeeding flocks in Alaska. Auk 98: 437-456. ASHMOLE,N. P. 1971. Seabirdecology and the ma- IDYLL, C. P. 1973. The anchovy crisis. Sci. Amer. rine environmentßPp. 223-287 in Avian biology, 228: 22-29. vol. 1 (D. S. Farner and J. R. King, Eds.). New JOHANNESSON,K., & R. VILCHEZ. 1980. Note on hy- York, Academic Pressß droacousticobservations of changesin distribu- BLAXTER,J. H. S. 1969. Swimming speeds of fish. tion and abundanceof somecommon pelagic fish Proceedingsof the F.A.O. conferenceon fish be- speciesin the coastalwaters of Peru,with special haviour in relation to fishing techniques and tac- emphasison anchoveta.I.O.C. WorkshopRept. tics. FAO Fish. Repts. 62: 69-100. 28: 287-323. BROWN,R. G. B. 1980. Seabirds as marine . JORDAN,R. 1976. Biologiade la anchoveta.parte 1. Pp. 1-39 in Behavior of marine animals, vol. 4 (J. Resum•n de conocimiento actual. Reuni6n de Burger,B. L. Olla, and H. E. Winn, Eds.).New trabajo sobre el fenomeno conocidocomo "El York, Plenum Pressß Nifio." Guayaquil,Ecuador. ß 1981. Seabirds in northern Peruvian waters, --, & H. FUENTES.1966. Las poblacionesde aves November-December 1977. Bol. Instit. Mar. Perif- guanerasy su situaci6nactual. Inf. Instit. Mar Callao. volum•n extraordinario: 34-42ß Per•. 10: 1-31. , F. COOKE,P. K. KINNEAR,& E. L. MILLSß 1975. KING,W.B. 1974. Wedge-tailedShearwater (Puffinus 810 DAVIDCAMERON DUFFY [Auk, Vol. I00

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