Prey Delivered to Roseate and Common Tern Chicks; Composition and Temporal Variability Carl Safina, Richard H

J. Field Ornithol., 61(3):331-338

PREY DELIVERED TO ROSEATE AND COMMON TERN CHICKS; COMPOSITION AND TEMPORAL VARIABILITY CARL SAFINA, RICHARD H. WAGNER1, DAVID A. WITTING 2, AND KELLYJ. SMITH2 National Audubon Society 306 South Bay Ave Islip, New York 11751 USA Abstract.--We observedprey deliveriesto Roseate(Sterna dougallii) and Common (S. hirundo)tern chicks.Roseate Terns were highly specializedand fed their chicksmostly sandeels (Ammodytesamericanus), whereas Common Terns delivered a diversity of prey. Species compositionof deliveredprey varied annually and weekly. Of four major prey species,the proportionof deliveriescontaining anchovies, juvenile bluefish, and herring varied with the time of morning, whereasthe proportionmade up of sandeelsremained generally constant.

ENTREGA DE ALIMENTO A POLLUELOS DE STERNA DOUGALLH Y S. HIRUNDO: COMPOSICION Y VARIABILIDAD TEMPORAL Sinopsis.--Obscrvamosla cntregade alimentoa polluelosde Sternadougallii y S. hirundo. Los adultosdc S. dougalliialimcntaron a suspolluclos muy particularmentecon individuos dc Ammodytesamericanus, micntras quc la otra cspccicdc gaviotaalimcnt6 a suspichoncs con una gran divcrsidaddc prcsas.La composici6ndcl alimcntocntrcgado a los pichoncs, result6variable a travis de1cstudio. Dc las cuatrocspccics dc pcccsutilizadas principalmcntc comoalimcnto para lospichoncs, la proporci6ncntrcgada quc contcnlaanchoas, pcz azulado y arcncavari6 a travfisdc lashoras dc la mafiana,micntras quc la quc contcnlaA. americanus pcrmancci6gcncralmcntc constantc. Ever since Volterra (1931) and Gause (1934) formulated what has becomeknown as the competitiveexclusion principle (Hardin 1960), therehas been interest in resourcepartitioning by closelyrelated sympatric species.The Common (S. hitundo) and endangered(Federal Register 52 FR 42064) Roseate(Sterna dougallii) terns often breed and forage together in the northeasternUnited States,and occasionallyhybridize (Hays 1975). But their nest site microhabitatdiffers (Burger and Gochfeld 1988 and refs.therein), they exploit differentforaging conditions (see Nisbet 1989, Safina 1990), and they are generallyreproductively isolated. In this paper we report interspecificdifferences and temporalvariability in prey delivered to Roseate and Common tern chicks.

METHODS We observedprey deliveriesto chicksof Roseateand Commonterns at Cedar Beach,New York (40øN, 73øW). During the breedingseasons of 1984-1987, we watched4, 7, 6, and 3 RoseateTern broodsand 4, 6, 9, and 9 Common Tern broodsin each year, respectively.Dates varied

• Currentaddress: Edward Grey Instituteof Field Ornithology,South Parks Rd., OxfordOXl 3PS, England. 2 Currentaddress: Rutgers University, Marine Field Station,Box 278, Tuckerton,New Jersey 08087 USA.

331 332] C. Safinaet al. J.Field Ornithol. Summer 1990 from year to year becausethe terns bred later each year. Prior to or immediately after hatching, nestswere fenced with 0.5 m high, 2.5 cm hexagonalmesh wire to keep chicksnear the nestsite. A 30 cm high band of fine meshfiberglass cloth around the inner lower portion of the fences helpedboth to retain small chicksand preventinjury to chicks.All fenced compoundswere 2-5 m in diameterand includedadequate natural or added cover to allow chicks to hide and find shade. Prey deliverieswere observedwith binocularsfrom blinds between 0500 and 0900 E.S.T. 3-5 daysper week during the chickrearing period. We observed nests for a total of 1359 h for Roseate Terns and 2193 for CommonTerns, during which 863 fishtransfers occurred to roseatechicks and 2369 fish transfers to common chicks. We were able to record all prey deliveriesduring observationperiods. Upon transfer of a fish to a chick,we notedfish species,tern species,and hour. We are confidentthat our fish identificationsare accurate,Cezilly and Wallace's (1988) skep- ticismnotwithstanding. Observers were very familiar with the fish species in the area, many of which were quite distinctivein shapeand color,and numeroussimultaneous observations by two or more of us in the field showedvirtually completeagreement among observers, except when ob- serversagreed that positiveidentification could not be made. We avoided using judgment in identifying fish; if the prey's specificidentity was unclear, it was listed as unidentified.Observation blinds were positioned to take the best advantageof morning light in helping make prey iden- tification. Identificationwas further facilitatedby the fact that terns often circledrepeatedly before attempting to transferprey to chicks,and chicks' prey handlingtime, especiallywhen young,often allowedexcellent views of prey. Alosaand Clupeaherring couldnot be identifiedto speciesduring deliveryand were clumpedin the data. These two specieswere identified as being presentbecause uneaten specimenswere recoveredadjacent to nests. Fish size relative to terns' bill length was recordedin 1984 and 1985, but not in 1986 or 1987 becausewe feared that a changeof observersin the latter two years might introduce inconsistencyinto this subjective measure.We trappedthe adult terns and measuredtheir bill length. Data were analyzed using SAS softwareat Rutgers University.

RESULTS Inter-speciesdifferences in chickdiets.--The compositionof chickdiets (Table 1) differed between tern speciesin each year and in all years combined(X 2 = 499.29, P ( 0.0001, df = 5; prey other than sandeels, anchovies,butter fish, bluefish, and herring were clumpedas 'other'). The mostapparent difference was the preponderanceof sandeels(Ammodytes americanus)in RoseateTern dietscompared to a greater diversityof prey speciesbrought by Common Terns (Table 1). We analyzedthe proportionof each of five major prey speciescom- prisingprey fed to chicksof eachtern species(Fig. 1). Roseatesbrought a higherproportion of sandeelsto chicksthan did CommonTerns in each Vol.61, No. 3 PreyDelivered to TernChicks [333

TABLE1. Prey broughtto tern nestsunder observationat Cedar Beach;number of indi- viduals observed,percent of each species'deliveries, and niche breadth values(B = 1/Zp•2; Levins 1968).

Common Terns Roseate Terns

Per- Per- Species n cent n cent American sandeel Amrnodytesamericanus 780 35.5 751 72.6 Bay anchovy Anchoa rnitchilli 168 7.7 42 4.0 Bluefish Pornatornus saltatrix 267 12.2 137 13.4 Butterfish Peprilus triacanthus 139 6.3 5 0.4 Herring Clupea and Alosa 251 11.4 70 6.8 Commonpipefish S?2gnathusfuscus 214 9.7 0 0 Atlantic mackerel Scornher scornbrusa 108 4.9 16 1.6 Long-tinnedsquid Loligopealez 1 0.05 0 0 Round herring Etrumeus teres 17 0.8 4 0.4 Scup Ste,2otornuschrysops 1 0.05 0 0 Killirish Fw2dulusspp. 16 0.2 1 0.1 Atlantic menhaden Brevoortiatyrannus 4 0.2 0 0 Flatfish, probably Winter flounder Pseudopleuronectesamericanus or Windowpane Scophthalrnusaquosus 1 0.05 0 0 Jack Caranx spp. 1 0.05 0 0 Threespined stickleback Gasterosteus aculeatus 1 0.05 0 0 Goosefish Lophius americanus 1 0.05 0 0 Unid. hake Merluccius bilinearis? 36 1.6 0 0 Common shore shrimp Palaemonetesvulgaris 59 2.7 0 0 Moth unidentified insect 53 2.4 0 0 Isopod unidentified 12 0.6 0 0 Unidentified fish 35 1.6 9 0.9

Niche breadth B = 5.63 B = 1.81

year, and for all yearspooled (X 2 -- 387.54, df = 1, P < 0.0001). Common Terns deliveredbutterfish to chicksin higherproportion than did roseares in each year and all years pooled (X2 = 56.44, df = 1, P < 0.0001). Anchovieswere deliveredin greaterproportion by CommonTerns than by rosearesfor all years pooled(X 2 = 14.91, df = 1, P (0.0001). This differencewas most pronouncedin the first two years. Both tern species deliveredherring (Clupeaharengus and Alosaaestivalis) to observedchicks in three of the four years. In two of thesethree years there was virtually no differencein the proportionwith which eachspecies delivered herring to chicks,but in 1987 commonsdelivered a significantlyhigher proportion (X2 = 33.80, df = 1, P (0.0001), and this resulted in a significant differencebetween species for all years pooled(X 2 -- 17.09, df -- 1, P ( 0.0001). Deliveries of juvenile bluefish (Pomatomussaltatrix) were ob- servedin 1985-1987. Roseatesdelivered a significantlyhigher proportion of bluefish than commonsin 1985 and 1986 (respectively,X2 = 7.10, df = 1, P ( 0.01; X2 = 13.41, df = 1, P < 0.0001), but commonsdelivered a higher proportion of bluefish than rosearesin 1987 (X2 = 5.10, df = 1, 334] C. Safina et al. j. Field Ornithol. Summer 1990

1984-1987 80 [] Roseate Terns [] Common Terns 60

Sandeels Anchovies Butterfish Bluefish Herring Other

FIGURE1. Diet compositionof Roseateand Commonterns, 1984-1987.

P < 0.02), resultingin no interspecificdifference for pooledyears (X2 = 0.76, df = 1, P < 0.4). Temporaldifferences in chickdiets.--From year to year, diet composition showedconsiderable variability. Prey compositionof chick dietsdiffered among yearsfor RoseateTerns (X2 = 264.82, df = 15, P < 0.0001) and CommonTerns (X2 = 816.58, df = 15, P < 0.0001; Fig. 2). The proportion of dietscomposed of eachof severalprincipal prey speciesvaried among yearsfor both terns (Table 2). Prey compositionof chickdiets was highly variable among weeks during the breedingseason in each year and for all years pooled(Table 3), for both Roseate Terns (X2 = 179.06, df = 24, P < 0.0001) and Common Terns (x 2 = 1051.14, df = 32, P < 0.0001). Prey compositionof chick diets differed among hours of the morning for RoseateTerns (X2 = 47.47, df = 16, P < 0.0001) and Common Terns (x 2 = 140.49, df = 16, P < 0.0001) for all years combined.Of several major prey species,the proportion of deliveriesmade up of anchovies, juvenile bluefish, and herring showedincreasing or decreasingpatterns

TABLE2. Resultsof X2tests of inter-yearvariability in the proportionof eachof 5 important prey speciesin dietsfed to chicks(dr = 3).

Roseate Tern Common Tern Preysp. X2 P< X2 Sandeels 33.54 0.0001 179.91 0.0001 Herring 129.59 0.0001 191.95 0.0001 Bluefish 81.41 0.0001 70.10 0.0001 Anchovies 14.21 0.003 379.17 0.0001 Butterfish 6.19 0.1 22.91 0.0001 Vol.61, No. 3 PreyDelivered to TernChicks [335

[] RoseateTerns Sandeels 80 [] CommonTems

0500 0600 0700 0800 0900

Anchovies •- 20 o

0500 0600 0700 0800 0900

Bluefish

0 0500 0600 0700 0800 0900

20 Herring

0500 0600 0700 0800 0900 Time of Morning

FZGURE2. Inter-hour variability in proportionsof major prey broughtto nestsof Roseate and Common terns, 1984-1987 pooled. withtime of morning,while the proportion made up of sandeelsr•mained generallyconstant (Fig. 2). Lengthoffish delivered.--Commonsbrought longer sandeels(Kruskal- Wallis x 2 = 8.71, df = 1, P < 0.01) and anchovies(Kruskal-Wallis x 2 336] C. Safinaet al. J.Field Ornithol. Summer 1990

T^BLE 3. Inter-week variability in the percent of Roseateand Common Tern chick diets comprisedof major fish categories.

Prey species RoseateTerns Sandeels Anchovies Bluefish Herring Other 15-21 June 73 27 0 0 0 22-30 June 69 18 0 11 1 1-7 July 69 3 20 6 2 8-14 July 66 5 17 13 2 15-21 July 78 3 9 2 8 22-31 July 88 0 10 0 3 1-7 August 100 0 0 0 0

Prey species Common Terns Sandeels Achovies Bluefish Herring Other 15-21 June 5 95 0 0 0 22-30 June 37 53 3 6 2 1-7 July 42 9 22 7 21 8-14 July 45 4 19 6 26 15-21 July 30 3 5 17 46 22-31 July 22 I 3 31 31 1-7 August 12 1 4 2 82

-- 8.22, df = 1, P < 0.01) than did roseates.Although there was no statisticallysignificant difference between tern speciesin the length of bluefish,butterfish, or herring brought,the mean lengthof eachof these speciesbrought by roseatesexceeded those brought by commons.For all prey other than sandeelsand anchovies,roseates' brought prey that was longer than commons'(Kruskal-Wallis X2 = 10.92, df -- 1, P < 0.001). Length of fish brought to chicks increasedfrom time of hatching in Common Terns (Kendall's tau -- 0.10, n = 301, P < 0.02), but not in roseates(Kendall's tau = 0.05, n = 303, NS). Mean estimatedlength of fish broughtby roseateswas 1.54 bill lengths,approximately 59.3 mm. Mean length of fish broughtby commonswas 1.46 bill lengths,approximately 51.2 mm. Roseateshad longerculmens (mean = 38.5 mm _+0.54 SE) than did commons(mean = 35.1 mm _+ 0.98 SE; Kruskal-Wallis X2 = 31.02, df = 1, P < 0.0001).

DISCUSSION The niche breadth indices (Table 1), highlight the Roseate Tern's heavyreliance on relativelyfew prey species,especially Amrnodytes. Nisbet (1981, 1989) summarizesother findingsof RoseateTerns' reliance on Amrnodytesand relatively specializedforaging habits. The RoseateTern's specializationmay make it more vulnerableto environmentalperturba- tions,which may be a factorin its endangeredstatus. The higherdiversity in Common Terns' diet appears to be characteristicin at least several Vol.61, No. 3 PreyDelivered to TernChicks [337 parts of their range in North America and Europe (see Lemmetyinen 1976, Erwin 1977). A divergencein the proportionof sandeelsbrought by eachspecies in 1987 is difficult to explain. Relativelylow availabilityof severalother major speciesmay have been a factor for RoseateTerns, and increased availabilityof minor 'other' specieswhich CommonTerns were capable of exploitingmay have decreasedtheir useof sandeels.Roseates appear better able to exploit sandeelsthan are CommonTerns becauseroseates seemable to divemore deeply (Nisbet 1981;Safina, unpubl.) and sandeels tend to remain near the bottomunless pursued by predatoryfish. The conspicuousabsence of silversides(Mer•idia) deservesmention. Thoughcommon in the nearbyestuary, we havevirtually neverseen one at the colonyin a decadeof study.We wereaware of the possibilitythat ternsmight deliver them, and feel confidentthat we did not misidentify Mer•idiaas Ar•choa. The lackof clarityin the estuary'swaters may account for the low frequencyof tern foragingthere and the virtual absenceof Mer•idia in our birds' diet. Observingprey deliveriesat nestscannot address the questionof how foragingbirds select prey or foraginghabitat from the rangeof possibil- ities.However, the variability we foundshows that eitherprey availability or birds'selection criteria changes, and that prey availabilityor selection variesdifferently between the two tern species.Some prey speciesmay havetheir own consistentinternal rhythms(or influencingfactors) which make them differentiallysusceptible to tern predationon a daily time scale(Fig. 2).

ACKNOWLEDGMENTS

We thank Joanna Burger and Michael Gochfeldfor valuablediscussions. Rutgers Uni- versityprovided logistical support. Ken Feustel and the Town of Babylon'sDepartment of EnvironmentalControl has providedmuch assistanceover the years.This studywas partly funded by the South Shore Audubon Society,the Huntington Audubon Society,and the Natalie P. Webster Trust.

LITERATURE CITED

BURGER,J., ANDM. GOCHFELD.1988. Nest-siteselection and temporalpatterns in habitat use of Roseate and Common terns. Auk 105:433-438. CEZILI•¾,F., ^NDJ. W^L•^CE. 1988. The determinationof preycaptured by birdsthrough direct field observations: a test of the method. Colonial Waterbirds 11:110-112. ERWIN,R.M. 1977. Foragingand breedingadaptations to differentfood regimes in three seabirds:the Common Tern, Sternahirundo, Royal Tern, Sternamaxima, and Black Skimmer,Rynchops niger. Ecology 58:389-397. G^USE,G. F. 1934. The strugglefor existence.Williams and Wilkins, Baltimore.163 pp. HARDIN, G. 1960. The competitiveexclusion principle. Science131:1292-1297. H^¾s, H. 1975. ProbableCommon x Roseatetern hybrids.Auk 92:219-234. LEMMETYINEN,R. 1976. Feedingsegregation in the Arctic and Commonterns in southern Finland. Auk 93:636-640. LEVINS,R. 1968. Evolutionin changingenvironments. Monogr. Popul. Biol. 2 Princeton Univ. Press,Princeton. 120 pp. NISBET,I. C. T. 1981. Biologicalcharacteristics of the RoseateTerns Sternadougallii. 338] c. Safinaet al. J.Field Ornithol. Summer 1990

U.S. Fish and Wildlife ServiceOffice of EndangeredSpecies, Newton Corner, Mas- sachusetts.Purchase order 50181-0840-9. 112+ pp. 1989. Status and biology of the northeasternpopulation of the Roseate Tern. U.•.Fish and Wildlife Service, Newton Corner, Massachusetts. Purchase order 50181- 88-81085. 74 pp. SAFINA,C. 1990. Foraginghabitat partitioningin Roseateand CommonTerns. Auk 107: 351-358. VOI•TERR^,V. 1931. Le5onssur la th6orymath6matique de la lutte pur la vie. Gauthier- Villars, Paris. 214 pp. Received2 Jun. 1989; accepted1 Dec. 1989.

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