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Peabody Museum of Natural History
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MUS. COMP 7
Bulletin 24 COMP, ZOOL.
me s
LISGRARY
FEB 2 1969
teatiact
Comparative Feeding Ecolo ooy
: of Sea Birds of a
Tropical Oceanic Island
by
N. Philip Ashmole
and
Myrtle J. Ashmole
New Haven, Connecticut
1967
PEABODY MUSEUM OF NATURAL HISTORY
YALE UNIVERSITY
BULLETIN 24
Comparative Feeding Ecology of Sea Birds
of a Tropical Oceanic Island
BY
N. PHILIP ASHMOLE AND MYRTLE J. ASHMOLE
Peabody Museum of Natural History and Department of Biology,
Yale University
NEW HAVEN, CONNECTICUT
30 November 1967
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EpiTtor: Jeanne E. Remington
Asst. Epiror: Nancy A. Ahlstrom
Communications concerning purchase or exchange of publications should
be addressed to the Publications Office, Peabody Museum of Natural History,
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MUS. COMP. ZOOL.
LIBRARY
FEB 2 1968
HARVARD
UNIVERSITY.
Printed in the United States of America
CONTENTS
PISCE MO IGURES: eee ceri, ROR Neat re NM OEE oat. ES ahetis vote vetanels te hivvee
LIDSTE AS TST BT PA AO Cone OU ee ee ee Rene eee Ra ae Te
1. INTRODUCTION
CP CaDTS COE CNS AVES ENE APT ONN pas ilev eich oiey saj\o cach cieyp) euaqouoh >. «)/0/ 80) s\ususyvei
Christmas Island and its sea bird populations ....................
2. ‘TECHNIQUES
Collection of samples’... .-, .jrssanissae Borwobyare smite spars © arcs rere
[Le eue lg Madera) MOS Wn ee A Bre O oo Rane er C oN COCmaroOoS se ore
BIE EI OCS KO ANALYSIS, 5.2010 5) -\ 2) s.6/ere ssh o crcyosshsiaioue oie epeaale aroun aaan ie. She hab atecare
3. SpEcIEs ACCOUNTS
Phaethon rubricauda Red-tailed Tropic-bird .............+++.....
Puffinus natvttatis Christmas Island Shearwater ........0:0.3..4%
EL CLOOLONIO OIG Me MOCHEX PVCELED | oi). scacestagd o: 2) -Jajtolensie coker picasa
BU Clits Pu UESCALA SOOGY METI: « /a.ayshs: &<2¥o avon /hs;~ sy seep e ies tiv cielo pei aiaiete oat
UANUOLES SLO LEGS *ESCOWI NOGGY 00) 5 os isyeie ie 6 ois 8 ole east e =e ual oteleton aay eke
Giese Oa. WVNGe MOT ae6.e. 6 yocoiss tayo a+ Wem inilais Sieiaps <is'eis.s aieccre a) nase
EIMOUSHUCTEUETOSET USB 1ACK INOOGY: Nai cfepe1s c.ciepe 01 21- cxolaya fein 9210 one ae) sia) el
Pnoceisterna cerulea Blue-prey Noddy s.ci\-..<cecscs «0c dase e erste
4. COMPARISON AND SUMMARY OF THE DIETS OF THE BIRDS
Ereporiionus of fish, squid. amd (Other 1€CMIS" ./5..../...,- 120 0 evens oles sire
SIZ ENO LE FOOL TCEMIS co 2) ses iice re eee ta ae eta dis aed SON ALD he
6. THe Birps In THEIR MARINE ENVIRONMENT
he environment, andthe availability of food 2.2.2.2... 26660622.
Feeding zones, and adaptations for feeding far from the colony ....
Feeding methods, and associated structural adaptations ............
7. SEASONAL CONSIDERATIONS
Seasonal wariationeis THE SeEMVITONMENE .<,. eae s bape mice aysccheesioms ae
Seasoital vatiationvin the food. of the Birds ve i s/s %.< 2, 4s.0,0¢ seers ee oc
Seasonal variation Im breeding ACLIVILIES << 2.6416, o:0, 6:0, 315109) ayo ccm om me
PPMP FES UISSEOIN 5c. < \o/'¢,ciscise MANN Tn RAP APRs Sy hn, GRU a alae Bigraanaetaid ote. pee
ROCIPERE HO ey. Ste Ae yk Nant a ih tra ala claiced a: lytic Sinn dineiqv aiaisians Heuy Memon aun
ne RIM CROPARE TRON BIEN EG: 1. te RnaeaRya ts cet SA Wack cs sxatula: ett lmbw’> sbatbeve stele soporarthae
OUR ONE TOC MDEED I td) 0S estar Bram cl (ttre eva nto ie) aia: tajaeria woos ere Wea folrandeaves bet rae nies
lv
iv
LIST OF FIGURES
. Breeding activity among eight species of sea birds on Cook Island and
Motu Tabu (both in the lagoon of Christmas Island), based on obser-
vations made during the series of visits by N. P. A. in 1963 and 1964,
Whose timing is shown at the top,...:-..:.---.--..--s¢eeeeee eee
2. Major features of the Central Equatorial Pacific Ocean ............
3. Percentage composition of samples from eight species of sea birds and
from: surface-caught Yellowfin Tuna) .:2.... 22... 4255. .).0 seeeeee
4. Size-frequency distribution of fish and squid in the diets of the birds. . .
5; Important ‘fish families in the diets of the birds\:).<. 2 \.jc.-ciee eee
6. Bills of the sea birds studied on Christmas Island: natural size photo-
sraphs of specimens ‘preserved in alcohol. 3... 7.221. 22 sere
7. Feeding methods employed by the sea birds studied ................
8. Seasonal variation in the proportions (by volume) of the major food
Glasses|im’ the diets of the birds)... cya .te wis « «<6 se eileen
9. Seasonal variation in the size of the fish and squid in the diets of four
IbIGG FSPEGIES |» a)saje.2 n- Velen ice ele nveaiom stelere oie 2 y<icl tic! ele ice ee
10. Seasonal variation in the representation (by number) of some important
fish families in the diets of Sterna fuscata, Gygis alba, and Anous
ECTUULETOSUTOS) cine atele nic cle slave) siavela ene sieve! sia) allelic) olay aa ate olielle! eiyehe al ol ee
11. Two views of a dense flock of Anous tenuirostris feeding over a tuna
school’ close to the western end of Christmas Island’... .... .- ee
LIST OF TABLES
1. The sea bird populations Gf Ghristmas (Island icici idic kes crcieh 3 s.5 ocr
2. Food samples from sea birds on Christmas Island: general information
and. condition Of salmiples) sommecasn iss. 2c es ee ween lee eee
. Percentage composition of food samples from the bird species ........
. Volumes of food items in samples from the bird species ..............
Qa of oo
. Length of fish and squid in the diets of the birds: cumulative percentages
. Invertebrates other than cephalopods in the diets of Pterodroma alba
and. Procelsterna Cerulea isc ys so. wievsie nies 2.4. wd ee be Sisk a ere are a oe
. Length of incubation shifts of some sea birds on Christmas Island, and
percentages of identified fish in their diets belonging to primarily reef-
originating, families”. o 22 52- Fess we ote bee wee eee nine cee oe eee
. Mean dimensions of some Christmas Island sea birds ...............-
9. Frequency of occurrence of fish and squid obtained from Gygis alba
adults at different: times: ofidaye ea. 424 nac6 312 208s siedinds ites aetae
85
86
98
2a.
2b.
LIST OF APPENDICES
Composition, 6f food samples: basic datas i..)0/G so sles a sla hone ene ea Ui
pedcoial data} OR BSW len OEMS. is snc ai <avelalt spies elaie wie a ne wicls comes eee 121
seasonal data on squid, mantle Jenoths: os aj. ics! s ant sete sinisyeloe do = @ 125
Fish families in the diets of the birds: number of fish identified in each
EMRE Ed 5 ASN cated Aare Oh ede Eh Sa Be nla SEVIS A caitlin Saath rence ae Ss 128
Pepialopods:im: the dicts of the binds) i 9242) o2ie sso echo eer cde cae eos 130
Details of the stomach contents of 191 Yellowfin Tuna (Neothunnus
macropterus), caught by surface-trolling within 10 miles of Christmas,
Jarvis, Washington and Fanning Islands (Line Islands) ............. 131
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YALE UNIVERSITY, PEABODY MUSEUM OF NATURAL HiIsToRY BULLETIN 24
131 p., 11 Fics., 1967
Comparative feeding ecology of sea birds of a tropical oceanic island
by N. Puitip ASHMOLE AND MyrTLeE J. ASHMOLE
ABSTRACT
In 1963 and 1964, 800 food samples, regurgitated or dropped by captured
birds, were collected on Christmas Island (Pacific Ocean) from Phaethon
rubricauda, Puffinus nativitatis, Pterodroma alba, Sterna fuscata, Anous stolidus,
Gygis alba, Anous tenuirostris and Procelsterna cerulea. Food items were
counted, measured, and identified as far as possible. The diets are analysed by
number, by volume, and by frequency of occurrence of the different food
classes, and the size of the prey taken by the different birds is compared. Fish
(from many families, but especially Exocoetidae) and squid (mainly Ommas-
trephidae) formed the bulk of the food; fish were especially important in A.
tenuirostris and Pr. cerulea, and squid in Pt. alba and P. nativitatis. Pt. alba
and Pr. cerulea took many invertebrates other than squid, including insects
(Halobates) and crustaceans. Although the large birds in general took much
larger prey than the small ones, the petrels P. nativitatis and Pt. alba took
fewer large fish than the smaller terns S. fuscata and A. stolidus. The diet of sur-
face-caught Yellowfin Tuna (Neothunnus macropterus) differed from that of
the birds in that fewer squid but more other invertebrates were eaten, while the
representation of the various fish families was very different.
The oceanography of the Central Equatorial Pacific is considered in relation
to the distribution of surface-feeding tunas, which drive their prey to the surface
and so make it available to birds. Concentrations of plankton and nekton at
“fronts” may have important effects on the distribution of tunas and of birds.
Seasonal variation in the environment is slight, and only A. tenuzrostris showed
striking differences in its diet at different seasons. Some of the birds feed close
inshore, but others range far from land even when breeding, and have various
adaptations for this, including long incubation shifts, infrequent feeding of the
young, and in Pt. alba, secretion of stomach oil. Only Ph. rubricauda and P.
nativitatis can catch prey appreciably below the surface; all the other species
feed mainly by “Dipping” or “Plunging to surface,” but their feeding methods
differ in detail.
Numbers of most of the species were probably limited originally by compe-
tition for available food. Among the birds which are not closely related, reduc-
tion of interspecific competition to the level permitting coexistence depends
mainly on differences in feeding methods, feeding zones and feeding times.
Among the closely related species it depends more on differences in body size
and in the other morphological characteristics determining the size of the prey.
Vergleichende Nahrungs-Oekologie bei Seevégeln einer
tropischen Ozeaninsel
von N. Philip Ashmole und Myrtle J. Ashmole
ZUSAMMENFASSUNG
1963 und 1964 wurden 800 Nahrungsproben, von gefangenen Végeln entwe-
der fallengelassen oder wiederausgestossen, von Phaethon rubricauda, Puffinus
nativitatis, Pterodroma alba, Sterna fuscata, Anous stolidus, Gygis alba, Anous
tenuirostris und Procelsterna cerulea auf Christmas Island (Pazifik) gesam-
melt. Die einzelnen Bestandteile der Nahrungsproben wurden so weit als m6-
glich gezahlt, gemessen und identifiziert. Die Art der aufgenommenen Nahrung
wird zahlen- und volumenmissig und nach der Haufigkeit des Auftretens der
verschiedenen Nahrungs-Klassen analysiert und die Grésse der Beute bei den
verschiedenen Végeln wird verglichen. Fisch (von vielen Familien, aber haup-
tsichlich Exocoetidae) und ‘Tintenfisch (hauptsdschlich Ommastrephidae)
machten den Hauptanteil der Nahrung aus. Fische waren besonders wichtig
fiir A. tenuirostris und Pr. cerulea, und Tintenfische fiir Pt. alba und P.
nativitatis. Pt. alba und Pr. cerulea nahmen viele Wirbellose ausser Tinten-
fisch an, einschliesslich Insekten (Halobates) und Krustentiere. Obwohl die
grossen Végel im allgemeinen eine viel gréssere Beute brachten als die kleinen,
nahmen die Sturmvégel P. nativitatis und Pt. alba weniger grosse Fische an als
die kleineren Seeschwalben S. fuscata und A. stolidus. Die Nahrung der an der
Oberflache gefangenen Gelbfinnigen Tuna (Neothunnus macropterus) unter-
schied sich von der der Végel darin, dass weniger Tintenfische aber mehr andere
Wirbellose aufgenommen wurden, wahrend die verschiedenen Fischfamilien
sehr unterschiedlich vertreten waren.
Die Ozeanographie des zentralen aquatorialen Pazifik wird in Hinblick auf
die Verteilung der Tuna betrachtet, die an der Oberflache Nahrung aufnehmen,
ihre Beute an die Oberflaiche treiben und so fiir die V6gel erreichbar machen.
Konzentration von Plankton und Nekton bei “fronts” kann von grosser Wir-
kung auf die Verteilung von Tuna und von Végeln sein. Jahreszeitliche Varia-
tion in der Umwelt ist gering und nur A. tenuirostris zeigte zu verschiedenen
Jahreszeiten auffallige Unterschiede in den Nahrungsgewohnheiten. Einige der
Voégel nehmen Nahrung nahe der Kiiste auf, andere dagegen weit vom festen
Land entfernt, sogar wahrend des Briitens, und haben dafiir verschiedene
Anpassungsméglichkeiten, einschliesslich langer Schichtwechsel beim Briiten,
seltene Fiitterung der Jungen, und, bei Pt. alba, Absonderung von Magenol. Nur
Ph. rubricauda und P. nativitatis k6nnen Beute merklich unter der Oberflache
fangen. Alle die anderen Arten nehmen Nahrung hauptsadchlich auf, indem sie
nur bis zur Oberflaiche niederstossen (“Dipping”) oder sich fallen lassen
(“Plunging to surface”), aber ihre Methoden differieren untereinander in Ein-
zelheiten.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 3
Der Zahlen-Bestand dur meisten der Arten war wahrscheinlich urspriing-
lich beschrinkt durch den Wettbewerb fiir erreichbare Nahrung. Unter den
Vogeln, die nicht eng verwandt sind, hingt der Ausgleich des Nahrungs-Kamp-
fes zwischen den Arten zur Koexistenz hauptsachlich ab von den Unterschieden
beziiglich der Art, der Zone und der Zeit der Nahrungsaufnahme. Bei den eng
miteinander verwandten Arten hangt der Ausgleich eher ab von Unterschieden
in Korpergrésse und anderen morphologischen Eigentiimlichkeiten, die die
Grosse der Beute bestimmen.
CpasunteibHad OKOIOruA UWatranna Mopcxax Itan wa Tponmaeckom
Oxeauckom OcTpoBe
H. ®aimm Ammor uw Mopta x. Aumox
ABCTPART
800 o6pasioB NHMH, UspHTaHHol uin OpomeHnHol noliMaHHEIMA WTuNAMH, OnII0
coOpaHo B 1963 u 1964 rogax Ha PomyectBeHckom OcTpoBe B THxoM OkeaHe OT
Phaethon rubricauda, Puffinus nativitatis, Pterodroma alba, Sterna fuscata, Anous
stolidus, Gygis alba, Anous tenuirostris, Procelsterna cerulea. EXMHUIbI IMI OBI
COCUHTAHE, CMePeHEI, H 10 BOSMOMKHOCTH ON03HAHEI. OOpas IMTAaHHA usyyaeTcCA 10
WHCAIY, KOIMYeECTBY, H YACTOTe IOBTOPCHUA pasHEIX COPTOB NMMH. CpaBHUBaeTcA Be-
IWUHHA JOOMUH, B3ATAA PasHEIMM UTHWaMu. PHOa (MHOTHX PO0B, HO OcOOeHHO
Exocoetidae) WH kKapakaTuuBl (TiaBubiM oOpas0om Ommastrephidae) cocTaBialn
OorbMy10 wacTs num. PHO6a Oba OcobOeHHO BaxHOl Waa A. tenuirostris m Pr. cerulea
@ KapakaTuup fia Pt. alba un P. nativitatis. Pt. alba wu Pr. cerulea 6paau MHOTUX
OeclO3BOHOUHEIX NOMHMO kapakaTul, BkUOGad HacekoMBIXx (Halobates) u pakooOpas-
HBIX. XOTA OOIbINME ITH OOMIKHOBeEHHO Opasu FOOHUY OdabIMeTO pasMepa, UeM Ma-
JeHbKue, BUIOXBOCTHe KauypKH P. nativitatis uw Pt. alba Opaam MeHbINee KOIMGECTBO
OOIbIIMX PHO YemM MeHbINNe 10 pasMepy KpayEn S. fuscata uy A. stolidus. Inma Kel-
TOULABHUKOBOTO TyHIa (Neothunnus macropterus) oOTAMYaeTCA OT IMUM ITH TeM,
YTO NOKUPAeCTCA MeHbIMe KapakaTHy u OOAbMe APyrux Oesl03BOHOUHEIX KHBOTHELX,
@ TAaKKe TEM, UTO POJEI WOMKUPAeMBIX PHIO COBepMeHHO Apyrue.
OkeaHorpadua DWeHTpasbHOTO skBaTOpHaIbHOrO Tuxoro okeaHa Oplla yaTeHa B
OTHOIMEHUH K pactipeseleHni TYHUa, UMTaMeroca y WOBepXHOcTH BOE. TyHel TOHUT
ROOMY K MOBEPXHOCTH BOAE U TAKUM OOpas0M UpesocTaBAseT ee UTHNaM. Konnex-
Tpallun WIAaHKTOHA WH HeEKTOHA Ha «@POHTAaX» MOKET CHAbHO NOBIMATS Ha pacipee-
JeHve TYHIa H ITH. Ces0HHble H3MCHCHUA He3HauUTeIbHL, U TOKO A. tenuirostris
CyIMeCcTBeHHO MeHAeT OOPas IMTAHHA C Ce30Ha Ha ce30H. HekorTophe NTHUE UMTAWTCA
y Oepera, Apyruve OTIeTAawT Aateko OT BeMIM, GyAYYH UpucMocoOIeHHEIMM K YTOMY:
JAMHHEIC CMCHBL BLICHKUBAHHA, PeAKM KOPM MTeHNOB, H BbIeeHHe meTyAOUHOTO
macia (y Pt. alba), Toapxo Ph. rubricauda u P. nativitatis ,oOpmawT mMMy Ha 3Ha-
WHTeIbHO TIyOMHE Of WOBepXHOCTHIO BOAH; Boe Apyrue MOpOAL KOPMATCA ORy-
HaACh WIM Walaa Ha MOBEPXHOCTb, XOTA METOAE KOPMACHHA OTAMUAITCA B eTAIAX.
YucieHHOcTh OObIMMHCTBA DOpok BepoATHO ObIla OrpanuyeHa copeBHOBaHHeM
B 7o0nye nnmn. Cpequ ITH, He cOCTOAMIMX B OAMSKOM poscTBe, NOHMKeHHe MexK-
BUAOBOM KOHKYPeHUAH JO YPOBHA, WOBBOTAIOMETO COBMeCTHOe CYMeCTBOBAHHe, 3aBH-
CHT T1aBHEIM 00Pa3s0M OT PasHHUE B ciocoOax, paeHax, H BpeMeHax NMTaHHA. Cpeqn
Oolee pOAcTBeHHEIX NOpos, Oomee cyMecTBeHHYW pPO‘b UTpaeT pasHua B BeAMUHHE
a H Te Apyrue MOpotormyeckue OcOOeHHOCTH, KOTOphIe OUpesedAWT BeAMYHAY
yo0nran.
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COMPARATIVE FEEDING ECOLOGY OF SEA BIRDS
OF A TROPICAL OCEANIC ISLAND?
by N. PHILIP ASHMOLE and MYRTLE J. ASHMOLE
1. INTRODUCTION
OUTLINE OF THE INVESTIGATION
This analysis of the food of sea birds on Christmas Island forms part of a
study whose object was to describe and compare the sexual and molt cycles of
various species of sea birds and to try to relate them to the feeding ecology of
the different species.
In the course of routine work, several thousand birds were handled, and
some individuals of all the species regurgitated (or dropped) food, which was
collected and preserved. In addition, some catching was carried out with the
prime objective of obtaining food samples. It is the analysis of the 800 food
samples obtained which forms the basis of this paper.
Samples were collected on eight fairly evenly spaced visits to the island be-
tween March 1963 and February 1964, with a single later visit in June 1964 (Fig.
1: the short visit at the end of November 1963 was treated as part of the pre-
ceding visit, while the January 1964 visit was interrupted for a few days in the
middle of the month). It is thus possible to compare food obtained at different
seasons, an obviously necessary preliminary to understanding the breeding re-
gimes of the different species. It was unfortunately not practicable to sample
directly the availability of food organisms in the area of Christmas Island during
the course of the study. However, some relevant information is provided by the
publications of the Pacific Oceanic Fishery Investigations (now the Biological
Laboratory, Honolulu) of the Bureau of Commercial Fisheries, U.S. Fish and
Wildlife Service.
Since samples were obtained from eight species, including all the most
abundant of the smaller sea birds breeding on the island, the analysis repre-
sents an attempt to determine the degree of difference to be found in the food
and feeding habits of the various members of a sea bird community typical of
tropical oceanic islands. All the species feed in the surface layers of the sea,
and it is clear that there are considerable possibilities for competition for food,
both within and between species. Furthermore, in contrast with some other
oceanic islands, Christmas Island appears to offer, for nearly all the species con-
1 Published with the aid of a National Science Foundation Publication Grant No. GN-528.
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TaySe[eD :4ajsvsoIna] vjng “xavuns ur AyUTeUL Inq “AIeaX JO saw} [[e 3 SuIpaaiq Puno} aq ULI :yNs YING *F9-gg6I 10} LILP asieds Ino WIM
yOIyUOD JOU s2op Asnsny-sun[ ur (Surdv] Jo ATqvumnsoid) yead ev YIM Inq ‘Aeak ay) [Te Surpseiq autos seM aiayI IVY) JUdUIAILIs s,19ySeTTeD
:Diyv]AjIvp VYING “UOSeas SUIPIIIG JOIUIM asnyIp & st a1ay3 ATqeqoad ‘ggg] 1saquiaidag ur MorInq ¥ UT [JeYyss8a UayoIq YsoaJ & PUNO; “y'g'N
ayiym ‘Avyy 0} Arenuef{ wos pue JaqWwiaaoN Ul sisou paps1OdaI JIYsETTeD Inq ‘eiep aienbapeut :s2uyjnsiqjv vjJaSasfosaN ‘ajnpayIs Surpseciq
IL]IUIIS V paIIIpuUl F9-E9Gl UL suONvAIasqo ‘Avy ut ATUTeUT SuLArT YIIM UOsvas Surpssiq AUIUINS payIeUI-[[IM v pap10Ia1 ((Q96T) JOYySETTeED
:snayiovdg snuy[ng ‘SMO|[OF SV I[QLIIVAL st PULIS] SPWSIIYD UO spirq vas Jo sa1dads JayI0 aYI Jo sa[NpayIs Surpaciq ay} UO UONLULIOJUT
‘slaquinu [eNURIsqns dU, paysep sy} pue syDTYyD Maz
e jo aouasaid ay} Sunvorpur auly payop ay3 ‘padojdura are sat108a322 omy ATUO syDTYD Og ‘aUePUNQe WHUTXeUT IIaYy) 0} asopD a1aM 83a
yey ysoyIyI ay pue ‘sssa pey uoneindod ay Jo uonszodoid [enuejsqns v yey) 1x9U ay) ‘s88a pey sprq May ve ATUO IeYp sayeorpuT dur]
JSQUUTY) dy) ‘S589 OJ ‘syIYy paspayun jo aduasaid ayi duT] JaMOT JY) ‘s83a Jo aduasaad oy) saqvorpur oui, soddn arp ‘sardads yoea 104
‘doy ay 3e UMOYs st Suu asoYyM ‘FOG pu FOBT UT “W'd'N Aq S}ISIA JO Satias ay} Sulinp apeur suonvasasqo uo
paseq ‘(purysy seunstzyD JO uoose] ay) Ur YIOG) Nqvy, NIopy pue purjsy YooD uo sparq vas Jo sarseds yyS19 Suowe AWANIe Surpssig *[ aunora
8 PEABODY MUSEUM BULLETIN 24
cerned, a much larger number of suitable breeding sites than are actually oc-
cupied. It is thus highly probable that the populations of the various species are
ultimately limited by the availability of food (Ashmole 1963a), although cer-
tain species may have recently been adversely affected by man’s activities.
CHRISTMAS ISLAND AND ITS SEA BIRD POPULATIONS
Christmas Island, the largest member of the Line Island group in the central
Pacific, lies about 1,200 miles south of Hawaii at 02° N., 157° W. (Fig. 2). The
170° W 160° W 150° W 140° W
e sen '] i] |
F os W A t i e
/ ° °
4 N 2° a
° ‘s = 20°N
sea’, © hei ts N.E. TRADES +
o
eJOHNSTON xi PREDOMINATE
—— nS - ae
10°N¢ — NORTH EQUATORIAL CURRENT <——~ -+10°N
—»> EQUATORIAL COUNTERCURRENT >» —___» ___»
. YA
WASHINGTON» 4
FANNINGe ¢
<-SOUTH EQUATORIAL CURRENT ——-—————- _ <—_—_—_——_—_——_- <—_—_—_——_———
‘4 | pe CHRISTMASS h ‘ Me 4
o° Pee N \N EQUATORIAL 7“ UPWELLING \ NS \ 0°
JARVIS
Me
° ®o . y
° eo Zz
PHOENIX ISLANDS e a Si Ee TRADES
= : “PREDOMINATE
10° S+ “+ + + + 410° s
170° W 160° W 150° W 140° W
FIGURE 2. Major features of the Central Equatorial Pacific Ocean.
closest other island is Fanning Island, about 165 miles to the northwest, while
to the southwest Jarvis Island is about 220 miles away. The Line Islands as a
group are one of the most distant from continental land, North America
being over 3,000 miles to the northeast.
Christmas Island is a coral atoll with a total length of 32 miles and a breadth
of 15 miles at its western end. The eastern part of the island is solid land with
various landlocked lagoons, the central part is a maze of small islets and la-
goons, while at the western end is an enormous shallow lagoon which has
two connections with the sea. This lagoon contains a number of islets, of which
three have large colonies of sea birds, and birds also nest in several parts of the
main island. The total land area of Christmas Island is about 330 square miles,
while the main lagoon has an area of 142 square miles. The maximum depth of
the lagoon is only about 15 feet, but the seaward slopes of the island are steep,
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 9
TABLE 1. The sea bird populations of Christmas Island®
SPECIES ESTIM. NO. OF ADULTS
Puffinus pacificus (Gmelin), Wedge-tailed Shearwater............... 2,500
*Puffinus nativitatis Streets, Christmas Island Shearwater............. 7,000
*Pierodroma alba (Gmelin), Phoenix Petrelcz 250i foc weds cece 6,100
Nesofregetta albigularis (Finsch)’, White-throated Storm Petrel....... 100
*Phaethon rubricauda Boddaert, Red-tailed Tropic-bird............... 1,300
pueawoertyaira Lesson, 1 Masked: Booby. .<.«.... <0 <:2:0% «jst «asa she aieie vs.0'e 100
Sane sue (innaeus), Red-footed Booby... 6... iiiis<i.die adsjeic ofemieictelae os 600°
Sula leucogaster (Boddaert), Brown Booby.................cccecece 100
Fregata minor (Gmelin), Great Frigate-bird..................0.0000- 600¢
Fregaia ariel (G. R. Gray), Lesser Frigate-bird.................000. 2, 0004
Sierna una Peale) Grey-backed’ Terns «.).)...\0.52 56.0 dee 2 acd sa snwee s 1,000
Earermnyuscaia Linnaeus, Sooty “Vert... sjs « «<i. aise #14 soe ib. lselh @ sledge 1,000, 000°
Phalasseus bergiz (Lichtenstein), Crested Tern.......5....0.cs0s0+e0 200
*Procelsterna cerulea (F. D. Bennett), Blue-grey Noddy............... 3,300
Anous sioldus (Linnaeus), Brown: Noddy-*s.2..22 214.4. oi. 4s 622 ac ken 1,900
*Anous tenuirostris (Temminck), Black or Lesser Noddyt............. 15,000
SGyats alba (Sparrman), White or Fairy Term®...-< 5. .... 6... 62200.%- 1,800
EXPLANATION. All sea birds known to breed regularly on the island are included. The figures
quoted are based on estimates made by personnel of the Pacific Ocean Biological Survey
Program of the Smithsonian Institution during three visits to the island in March, June and
November 1964. For each species the estimates of the numbers of adults present on the main
island and the three islets Motu Tabu, Motu Upua and Cook Island were summated for
each visit, and the highest of the three totals was used, rounded to the nearest 100. The figures
do not represent the total breeding populations, but do give an idea of the relative abundance
of the various species.
* Species whose food was studied are marked with an asterisk.
NOTES FOR TABLE 1:
a. Nomenclature is from Peters (1931, 1934), except that Anous minutus is considered as
conspecific with A. tenuirostris (following Mayr 1945), and diareses are omitted from
Phaethon and Anous in accordance with the International Code of Zoological Nomen-
clature (1961) Article 27. Trinomials are not used since they are unnecessary for present
purposes: furthermore, several of the species are so badly in need of revision that sub-
specific assignment would be misleading.
b. This should probably be considered a form of Fregetta fuliginosa (Gmelin): see Bourne
(1957).
c. These figures are probably underestimates, since not all the mainland colonies were
visited consistently.
d. This figure is the estimate made by N. P. A. during a visit in 1964 to the colony recorded
by Gallagher (1960).
. It is particularly difficult to make a realistic estimate of the numbers of this species.
For the sake of uniformity we recommend the adoption of the English names Brown
Noddy and Black Noddy respectively for A. stolidus and A. tenutrostris, as recommended
by Robertson, Paulson and Mason (1961).
g. As pointed out by Eisenmann (1955), ‘“‘White Tern”’ is the least confusing English name
for this species, since ‘‘Fairy Tern’’ is applied to Sterna nerets.
™m Oo
10 PEABODY MUSEUM BULLETIN 24
the 100 fathom line being generally less than a mile from the shore. A fuller
description of the island is available in Gallagher (1960), and its history has
been briefly described by King (1955).
The sea bird community of Christmas Island is both large in terms of num-
bers of individuals and unusually rich in species. General accounts of the birds
have been given by various authors, especially King (1955) and Gallagher
(1960). Recently the island has been visited regularly by personnel of the
Pacific Ocean Biological Survey Program of the Smithsonian Institution, who
have made estimates of the numbers of birds present on each visit. These esti-
mates, kindly made available by the Smithsonian Institution, form the basis of
Table 1, which gives an indication of the relative numbers of the 17 species of
sea birds which are known to breed regularly on the island. The Procellari-
iformes are represented by two shearwaters, one gadfly petrel (Pterodroma)
and one storm petrel; the Pelecaniformes by one tropic-bird, three species of
boobies and two frigate-birds; and the Laridae by no less than seven species of
terns.
It can be seen from Table 1 that among the larger species the numbers of
Sula dactylatra and S. leucogaster are small, while S. sula is much more abun-
dant. The two shearwaters and the gadfly petrel are present in roughly equal
numbers, while the population of Nesofregetta albigularis is very small. Among
the terns Sterna fuscata is by far the most abundant, but the population of
Anous tenuirostris is also very large, and there are substantial numbers of all
the other terns. The population of Thalasseus bergii, though absolutely small, is
relatively dense since this species apparently feeds entirely within the lagoon
and along the coastal beaches, whereas the other terns feed almost entirely at sea.
In the present study it was necessary to concentrate attention on the species
which bred on two islets (Cook Island and Motu Tabu) in the main lagoon.
This meant that among the Pelecaniformes only Phaethon rubricauda could
be studied, but all three larger species of Procellariiformes and six of the
seven species of tern were available. In practice, however, Puffinus pacificus and
Thalasseus bergit could not conveniently be investigated in any detail. Islets
in the lagoon (Cook Island, Motu Tabu and Motu Upua) are the main breed-
ing places for all the birds studied except Sterna fuscata. This species has
enormous colonies in various parts of the main island (Gallagher 1960), but the
relatively small colony on Cook Island was the most convenient for investigation.
To facilitate comparisons, the eight bird species studied are treated here-
after in order of decreasing weight (Table 2; but see also Table 8, which gives
other dimensions of the birds).
24> TECHINIOUES
COLLECTION OF SAMPLES
All the food samples were collected from Cook Island or Motu Tabu, with
the exception of one batch of samples (March 1963) from a mainland colony of
S. fuscata. However, in the analysis and discussion all samples are considered as
representing the food of the species on Christmas Island as a whole.
In addition to the collection of regurgitations produced by adults and
chicks during routine handling, special efforts were made to catch individuals of
certain species at times when they were likely to provide samples. For in-
stance, adult Puffinus nativitatis and Pterodroma alba were always caught when
seen with chicks at night, since they often regurgitated under these circum-
stances. Most samples from Anous stolidus and A. tenuirostris were obtained
from roosting birds, while Procelsterna cerulea often regurgitated if caught
as they returned to the island in the evening. A few regurgitations were ob-
tained from roosting Gygis alba, but this species, alone among those studied,
carries food for the young in its bill, and most samples were obtained by sys-
tematic attempts to catch (with a large long-handled net) all individuals seen
carrying food.
Regurgitations (and items dropped by G. alba) were carefully collected off
the ground, often with the help of a spoon; however, on occasions some food
was inevitably lost. All samples were labeled with the species, date, and locality,
and were preserved in formalin in individual containers for later analysis.
LABORATORY [TREATMENT
Typical regurgitations contained fish and squid in various stages of digestion
(the squid often with the head separated from the mantle), and also fragments
of largely digested fish and squid. In addition, according to the bird species,
there might be squid eye-lenses, squid beaks, severed squid arms, oil or other in-
vertebrates.
Each sample was cleaned of sand and plant debris, and the contents were
sorted initially into fish, squid, and other invertebrates. Subsequently the fish in
sufficiently good condition were identified to the family level; some generic and
specific identifications were made, and these are given in Appendix 3. The 869
squid collected during the first half of the study (from March to September
1963) were identified by Dr. Malcolm R. Clarke (Appendix 4); since these
proved to be almost entirely of one family—and in fact largely of one species
—the squid were not identified during the remainder of the study. Inverte-
brates other than squid occurred in significant quantity in samples from only
two of the bird species: they were identified as far as possible.
The items in each food class in each sample were counted. When the food
was in an advanced stage of digestion, it was often difficult to determine exactly
how many items were represented, and certain arbitrary rules were followed.
If the only fish materials in a sample were vertebrae, one fish was recorded as
11
12 PEABODY MUSEUM BULLETIN 24
present. If the only squid materials were beaks, one squid was counted, re-
gardless of the number of beaks that were present, since it is likely that beaks
are retained for long periods in the stomachs of certain species, and thus do
not represent only the most recent meal. Also, if 5 squid mantles and 6 heads
were present 6 squids were recorded.
Two additional small points should be mentioned here. First, crustacean
ectoparasites of fish were considered as food items when they occurred in the
samples, even though they were probably not eaten intentionally. Second, it is
possible that in some of the more digested samples, food items from the stomachs
of fish and squid subsequently eaten by birds may have been considered as
separate items in the diet of the birds. However, we are of the opinion that this
was a very infrequent occurrence.
Volumes of all the food items were measured by displacement. These meas-
urements were of course frequently of partially digested objects, and thus do
not always represent the size of the objects at the time of capture, although
they are probably reasonably proportional to the latter. In addition, lengths of
all fish and squid were measured individually. For fish the measurement used
was from the most anterior point to the base of the tail: this was easier than us-
ing either total length or ‘fork length,’ since the tails were frequently damaged.
For squid, the maximum (dorsal) mantle length was used, rather than the
total length of the animal, because the heads were frequently not attached. Each
fish, or squid mantle, was recorded as Grade 1, Grade 2 or Grade 3 according
to its condition. Grade 1 items were those in good condition, whose length
could be measured accurately; Grade 2 items were slightly broken or digested,
but fairly accurate measurements could be obtained; Grade 3 items were largely
digested but were assigned to length classes spanning 1, 2, 4 or occasionally 8
cm by estimating their original length. This system made it possible to use all
the data in parts of the analysis, but to restrict the treatment to the best data
where appropriate. Volumetric measurements were also made of the fragments
of fish and squid which could not be considered as separate food items.
MetTHops oF ANALYSIS
In any study of the food of an animal species, it is clearly necessary to
identify, at least approximately, the various food items. However, since many
animals take a wide variety of foods, including some which occur only rarely
and are of negligible importance in the diet, a simple list of the food items
obtained from a given species is of little value, and it is essential also to utilize
quantitative methods. Hartley (1948) discussed various quantitative methods
employed in the analysis of bird foods, while Reintjes and King (1953), in a
paper on the food of tunas, included a discussion of methods of analysis which
is largely relevant also to birds.
For both birds and fish, there are three principal methods of basic analysis,
which can be applied to stomach contents or to regurgitations. Each of the meth-
ods requires initial sorting of the food into food classes or groups, which may be
individual food species or appropriate higher categories if precise identifica-
tion is not practicable. After this, the first method involves recording the total
numbers of items in each food class, the second uses the volumes or weights of
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 13
the different food classes in each sample, while the third—frequency-of-occur-
rence analysis—is based on the proportion of samples in which each food class
is present, regardless of quantity. Any of the three basic methods may be sup-
plemented by additional techniques, of which the most important are measure-
ment of the nutritive values of the different food classes (Gibb and Betts 1963,
Kahl 1964), and determination of the size-frequency distributions of the items in
each food class (as in Bowman 1961). The latter is especially important in
comparing the feeding ecology of species taking generally similar foods in the
same area, as in the present study. One additional technique is that of estimating
the original weight of the food items (Madsen and Sparck 1950, Bowmaker
1963, Skokova 1963). Use of this technique—which requires considerable knowl-
edge of the food items concerned—can add considerably to the information
gained from partly digested food.
The three basic methods of analysis provide indications of rather different
aspects of the feeding ecology of the species. A food class which is present in
very high numbers must clearly be abundant, and the bird must be well adapted
to catching it. However, a numerical analysis alone gives little indication of the
importance of each food in the diet of the bird, since it ignores the size of the
food items. One serious consequence is that one or a few atypical samples can
exert a disproportionate effect. To take a case from our own experience, one
sample from G. alba contained, in addition to one fish with a volume of 0.5 ml,
19 fish larvae with an aggregate volume of 0.2 ml; a more typical sample ob-
tained on the same day contained two squid with a total volume of 2.1 ml. In a
solely numerical analysis the second sample would exert only one tenth of the
effect of the first, although it was three times as large. This problem is overcome
by measurement of the volume (or weight) of the various foods in each sample,
to obtain indications of the relative general importance of the various food
classes in the diet of the bird. However, neither numerical nor volumetric anal-
ysis indicate the frequency with which the different foods are available; for in-
stance, an extremely abundant food might be eaten exclusively for a time, but
be available only for a short period. Frequency-of-occurrence analysis provides
the necessary information as to whether a food is consistently available (and
attractive) to the bird, and so is a reliable food source.
The very different impressions which may sometimes be conveyed by the
three different types of analysis are well demonstrated by the top two species in
Fig. 3. Comparing the diets of the two species by number alone, fish would ap-
pear to be much more important in P. nativitatis than in Ph. rubricauda, but
reference to the volumes shows that in terms of bulk, the reverse is the case.
Furthermore, the frequency-of-occurrence figures show that in P. nativitatis,
although fish are present in much greater numbers than squid, they occur with
slightly less regularity.
Both Hartley (1948) and Reintjes and King (1953) concluded that it is
essential to apply more than one method of analysis in order to obtain a valid
picture of the diet of the animal concerned; this is especially true when it is
necessary to compare the feeding ecology of different species, or of a single
species at different seasons. However, analysis by volume (or weight) is perhaps
the most important method, and some workers have concentrated on it; one
14 PEABODY MUSEUM BULLETIN 24
NUMBER VOLUME FREQUENCY OF OCCURRENCE
FISH SQUID OTHER
INVERTEBRATES
PHAETHON
RUBRICAUDA
80samples
PUFFINUS
NATIVITATIS
49
PTERODROMA
ALBA
95
WS
STERNA
FUSCATA
243
ANOUS
STOLIDUS
38
GYGIS
ALBA
152
ANOUS
TENUIROSTRIS
110
SS66GbG
PROCELSTERNA
CERULEA
34
BOGOOOCGCOGB
YELLOWFIN
TUNA
191
G €€¢6¢66¢666
aw agaGG@GQG
FIGURE 3. Percentage composition of samples from eight species of sea birds and from
surface-caught Yellowfin Tuna.
Each complete circle represents 100%. Solid black is used for fish, diagonal lines
for squid, and dots for other invertebrate food. Figures below the names indicate
the number of samples obtained from each species. The Frequency of Occurrence
diagrams indicate the percentage of samples in which each food class was represented.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 15
example is Frith’s (1959) fine study of the ecology of ducks in New South
Wales. On the other hand Carrick (1959), in his work on the feeding of two
species of ibis, Threskiornis spinicollis (Jameson) and T. molucca (Cuvier),
used only analysis by number and frequency of occurrence, since he was investi-
gating primarily the effect of ibis predation on locust numbers. Furthermore, it
must be remembered that analysis by all three methods is extremely time-con-
suming, and may be impossible or uneconomic if the samples are in poor con-
dition. Sometimes under these circumstances the most useful procedure is to
examine a large series of samples but to use mainly frequency-of-occurrence
analysis. Valuable results have been obtained in this way by Madsen (1957)
in his work on the food of fish-eating birds in Denmark, by Belopol’skii (1957)
in his study of the stomach contents of an enormous series of arctic birds, and by
Tickell (1964), in a comparison of the diets of Diomedea melanophris Tem-
minck and Diomedea chrysostoma Forster.
However, even if all the available methods of analysis are employed (as, for
instance, in Madsen and Sparck 1950, and Olney 1964 and earlier papers),
the relative importance of the different food classes can be fully understood
only in the light of knowledge of the whole biology of the species concerned. For
example, a prey which is not normally eaten in quantity, but which can be uti-
lized when other food is scarce, may be of critical importance in permitting a
species to survive in a particular environment; this is apparently so in the case
of snails in the diet of the Song Thrush Turdus philomelos Brehm in Britain
(Davies and Snow 1965).
The use of several different types of analysis enables comparisons between
species or between seasons to be made with greater confidence. However, as
pointed out by King and Ikehara (1956:64) “Regardless of the method or
methods of analysis used, there are many uncontrollable variables inherent in
food studies which detract from the precision of the results.” Furthermore, for
the reasons discussed by the same authors, it is generally impractical to apply
Statistical tests of significance to the data. Under these circumstances, it is clear
that one must be very cautious when drawing conclusions from the results, and
it is for this reason that we have presented much of our data in detail in the
appendices.
In the present study we decided to use all the three basic methods described
above: analysis by number, by volume, and by frequency of occurrence. Al-
though we based these primary analyses on the division of the food into broad
classes (fish, squid, and other invertebrates), identification of a high propor-
tion of the less digested fish to the family level made it possible also to com-
pare the representation of different fish families in the diets of the different
birds. Furthermore, our data on the lengths and volumes of the fish and squid
in the samples provide a basis for comparison of the sizes of prey which the
various species are able to exploit.
In presenting information on the overall composition of the diets of the dif-
ferent birds, the numbers of items in each class of food are presented as per-
16 PEABODY MUSEUM BULLETIN 24
centages of the total numbers of items in all food classes. ‘The volumes of all the
items in each of the different food classes are summated for each food class,
and expressed as percentages of the total volume of the food in all classes. ‘This
is the ‘aggregate-total-volume’ method (Reintjes and King 1953:96), in which
samples of different sizes exert effects proportional to their volumes. Frequency
of occurrence of each food class is presented as the percentage of samples in
which the class was represented. Because nearly all the samples contained more
than one class of food, these percentages when summated far exceed 100.
Hartley (1948), in representing the percentage occurrence of different foods,
used a method is which the total number of occurrences of all food classes is
called 100, and the percentage of the total provided by each food class is cal-
culated. It is apparently this method which is used in the majority of the
tables in Belopol’skii’s (1957) work on sea birds. However, it is not used here
(although the figures for the calculations are available in Appendix 1) be-
cause it obscures the important information on the proportion of the samples
which contain a particular food class.
Where only a small number of food classes is involved (for instance the
fish, squid and other invertebrates of our primary analysis) it is useful and
practicable to bear in mind continually the results of the three different types
of analysis, representing numbers, volume, and frequency of occurrence. How-
ever, when it is necessary to compare the representation of larger numbers of
food classes, for instance the various fish families in the present study, it is cum-
bersome always to use, in discussion, the results of all three methods. ‘Trautman
(1952), facing this problem in his study of pheasant food habits, recorded
numbers of items, weights, and frequency of occurrence, but in his discussion
relied mainly on comparison of weights. Welsh (1949, quoted by Reintjes
and King 1953), in a study of the food of various Hawaiian fishes, obtained per-
centages for each food by number, volume, and frequency of occurrence, and
then averaged these to obtain a single index of importance. Rather than com-
bining percentages representing different types of information, we have pre-
ferred to use, in discussion of the importance of the various fish families in the
diets of different birds, a composite ranking system derived from the results of
the three methods of analysis. For each bird species, the fish families were
ranked separately in order of overall numbers, in order of total volume, and
in order of frequency of occurrence: the three rankings were summated for each
fish family, so that the families could then be arranged in a single sequence for
that bird. The resulting rankings avoid the implication of precision conveyed
by averaged-percentage figures, and are considered to give a good indication
of the relative importance of the different families in the diets of the birds.
(We find that an identical ranking system has been described by Waldron and
King [1962] in comparing the importance of fish families in the food of tunas.)
There are various complications in attempting to compare quantitatively
the food of the different sea birds on Christmas Island, and these need to be
borne in mind when considering the results. First, since the samples were either
regurgitations, or food carried in the bill by G. alba, they cannot be considered
as complete stomach contents. However, regurgitations probably give a better
indication than stomach contents of the composition of recently taken food,
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 17
since organisms with very durable parts are less likely to be over-represented.
There remains the difficulty that food tended to be consistently less di-
gested in some species than in others. The extreme examples are G. alba,
in which much of the food—being carried in the bill—was in perfect condition,
and Pt. alba, in which the food was very largely digested (see Table 2), so that
it was often hard to judge how many fish and squid were represented in a sam-
ple. These differences in condition should not in themselves seriously affect
the comparison of the overall proportions by volume of fish and squid in the
different bird species, since fish and squid flesh are nearly always easy to tell
apart, even at very late stages of digestion. However, if the soft parts of fish
and squid were digested at very different rates, the reliability of the compari-
sons would be reduced; although no relevant measurements are available, the
data in Table 2 do not suggest that there are great differences. On the other
hand, the comparison of the representation of the different fish families in the
diet of the different birds must be affected to some extent by general differences
in the condition of the samples from different bird species. This is because
some fish families are easy to recognize, with practice, even in late stages of diges-
tion, while others are much more difficult. For instance the very diagnostic
spines of Exocoetidae are relatively resistant to digestion, Gempylus serpens
Cuvier and Valenciennes (Gempylidae) have a very distinctive body form, and
Scombridae can be recognized, with practice, at a much later stage of digestion
than many other fish. In contrast, larval fish are frequently not identifiable even
when in relatively good condition.
Regurgitations were obtained from both adults and nestlings. The two types
of samples are considered together in the analysis, since it was generally not
known which of the samples from adults were of food about to be fed to young.
For instance the vast majority of the samples carried in the bill by G. alba, and
of the regurgitations obtained from S. fuscata during the breeding season, were
clearly of food intended for the young, but many of the samples from the two
Anous species and from Pr. cerulea (and also the regurgitations from G. alba)
were obtained from roosting birds and were not of food intended for nestlings.
Another problem is that the number of samples obtained was very different
in the different species, as was the distribution of the samples around the year
(Table 2 and Appendix 1). Clearly, only striking differences should be ac-
cepted with confidence in cases where the number of samples is small.
In comparing the size of regurgitations (or of individual food items) from
the different bird species, we have expressed volumes measured in milliliters by
displacement, as percentages of body size measured in grams. This procedure
seems justified for comparative purposes since the specific gravities of the food
of the different species must be extremely similar (and also close to one).
PEABODY MUSEUM BULLETIN 24
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3. SPECIES ACCOUNTS
(The species are treated in order of decreasing body weight—see ‘Table 2)
PHAETHON RUBRICAUDA Boddaert—Red-tailed Tropic-bird
STATUS
This tropic-bird, which is the only member of its family found on Christ-
mas Island, breeds on both Cook Island and Motu Tabu, as well as on other
islets and the main island; over two hundred nests were investigated on Motu
Tabu during the study, while more than a thousand birds breed on Christmas
Island as a whole (Table 1). Since the three resident species of boobies (Sula
spp.) and the two species of frigate-birds (Fregata spp.) were not available on
the islets, Ph. rubricauda was easily the largest species studied; it is over twice
the weight of the next species, P. nativitatis (Table 2).
GENERAL DESCRIPTION AND CONDITION OF SAMPLES (T’ABLE 2)
Tropic-bird chicks regurgitate readily when they have recently been fed,
and nearly three-quarters of the food samples were collected from nestlings.
The 49 regurgitations contained on average 3.8 items each, a number lower
than in regurgitations from any of the other species. The average volume of the
three largest regurgitations (133.4 ml) expressed as a percentage of the average
weight of adults (in grams), gives a figure of 20%, which is high in compari-
son with most of the other species. The largest regurgitation obtained (175.7
ml) was more than three times the volume of the largest from any of the other
species.
In comparison with the other seven species, the food items were in moderate
condition; however, a few were very largely digested. In samples from adults
5% of the fish were Grade 1, and 55% of all the fish were identified to family.
The squid in samples from adults included 5% which were Grade 1, and all
the squid examined were identified to family. A fairly high proportion of the
samples contained separate squid beaks and lenses. Although the highest num-
ber of lenses in a sample was only three, the number of beaks was often very
high, and one sample contained 192; evidently in such cases the birds regurgi-
tated their gizzard contents.
QUANTITATIVE COMPOSITION OF SAMPLES (FIG. 3 AND TABLE 3)
One third of the food items were fish, but these made up more than half of
the food by volume. This relationship implies that the fish were generally
bulkier than the squid, in contrast with the situation in all the other species
studied (except Pr. cerulea), in which the fish were generally smaller than the
squid. Squid had a slightly higher frequency of occurrence than fish, but 71%
of the samples contained both squid and fish; this proportion is higher than in
any other species studied, although each sample from Ph. rubricauda con-
19
PEABODY MUSEUM BULLETIN 24
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ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS pa!
tained, on average, fewer items than those from any of the other species (Table
2). A few invertebrates other than squid were found, but these clearly form a
negligible part of the diet.
S1zE OF Foop Items (Fic. 4, ‘TABLES 4 AND 5, AND APPENDIX 2)
The fish taken by Ph. rubricauda ranged in length from the 2-4 cm class to
the 26-28 cm class, with one much larger halfbeak. This was the only bird
species which took no fish in the 0-2 cm class, while only two fish longer
than 16 cm were found in samples from other species. Although even in the
present species only 8 of the 60 fish were more than 16 cm long (four of them
Coryphaenidae), the volume data confirm the generally large size of the fish
which it ate. The mean volume of the fish in good condition was 21.8 ml, a figure
more than five times that for any other species. Furthermore, this mean volume,
when expressed as a percentage of the body weight in grams, gives a figure of
3.3%, much higher than that for any of the other species. The bulkiest fish ob-
tained from Ph. rubricauda had a volume of 84.0 ml when partly digested, and
both this and a number of other fish were enormously bulkier than any fish
from the other bird species. It is also of interest that this volume of the largest
fish represents more than 12.6% of body weight, which is higher than the equiv-
alent figures in the other species.
The squid taken by Ph. rubricauda ranged in mantle length from the 2-4
cm class to the 10-12 cm class. None of the other species took any squid more
than 10 cm in mantle length and all took some less than 2 cm. The frequency
distribution within the range also contrasted with the other species, showing a
peak of 36% in the 6-8 cm class and 22 in the 8-10 cm class (Fig. 4). Corre-
spondingly, the mean volume of the squid in good condition collected from Ph.
rubricauda was 20.7 ml, while among the other species the highest value was
about 7.1 ml.
Although there was thus a large difference in the size of squid taken by Ph.
rubricauda and by the other species, it was not as large as might have been ex-
pected from the fish data. In Ph. rubricauda the mean volumes of the squid and
of the fish in good condition were about equal (20.7 and 21.8 ml respectively),
but in all the other species (except Pr. cerulea) the squid were much larger in
volume than the fish (Table 4). Considering only the largest items rather than
the means, it is noteworthy that while the largest squid recorded in this study
(43.7 ml) came from Ph. rubricauda, it represented only 6.6% of the bird’s
weight, and several other species took squid much larger in proportion to their
size. Correspondingly, the difference in absolute terms between the largest
squid from Ph. rubricauda (43.7 ml) and the largest from another species
(25.3 ml in Pt. alba) is much less impressive than the equivalent difference in
the fish (>84.0 ml and >16.9 ml).
IDENTIFICATIONS OF Foop ITEMs (Fic. 5 AND APPENDICES 3 AND 4)
Fish from only four families were identified; this was fewer than for any of
the other bird species except Pt. alba, in which only one fish was identified.
Exocoetidae easily rank highest, followed by Coryphaenidae, Diodontidae and
Tetraodontidae. Except for Exocoetidae, these are families which do not rank
29) PEABODY MUSEUM BULLETIN 24
FISH BODY LENGTH (cm) SQUID MANTLE LENGTH (cm)
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 40 42 0 24 6 8) 1602
ee wt ee ial aie f |
% 40
PHAETHON
RUBRICAUDA 7°
EP Hitt ty == (0)
60
PUFFINUS
NATIVITATIS 7°
60 60
a0 PTERODROMA 2°
2 ALBA ae
10) —— c0)
5 STERNA 4°
: FUSCATA 7°
(¢) (0)
a ANOuUS %*
a) STOLIDUS ”°
10) 10)
ADULTS
GYGIS 60
ALBA 40
ANOUS ze
TENUIROSTRIS 7°
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100
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ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 23
high in the diets of any of the other birds studied. (The ranking of the fish
families takes into account their relative numbers, volume and frequency of oc-
currence: see section on Methods of Analysis for details.)
It is of special interest to find that Diodontidae (porcupine fishes) are eaten
in appreciable numbers by Ph. rubricauda (and to some extent also by S. fus-
cata), since members of this family can inflate themselves when alarmed, and
their numerous sharp spines might be expected to provide an extremely effec-
tive defense against predators. That Ph. rubricauda is affected by the spines
under certain circumstances was shown on an occasion when an adult was
caught, and regurgitated—after terrific efforts and obviously acute discomfort
—a porcupine fish about 9 cm long, and the partially digested remains of
another. Although the adult was with a chick at the time, it seems unlikely
that these fish would have been regurgitated for it.
As in the other birds, nearly all the squid identified were Ommastrephidae,
but one individual was probably a member of the Histioteuthidae—the only one
found during the study. All the Ommastrephidae identified were members of
the genus Symplectoteuthis—as were nearly all the squid taken by all the
species of birds—but Ph. rubricauda was unusual in providing almost as
many individuals of species B as of species A. Clarke (1965) has shown that
both Ommastrephes pteropus in the North Atlantic and Symplectoteuthis oua-
laniensis in the Indo-Pacific occur in two forms, one with and one without a
large dorsal light organ. Since the nomenclature of the forms of the ‘species’
Symplectoteuthis oualaniensis has not yet been resolved, we refer to the form
without the light organ as Symplectoteuthis species A and to the form with the
light organ as Symplectoteuthis species B.
The few other invertebrates comprised three isopods, a parasitic copepod
(Penella sp.), one egg cluster and one unidentified object. Two of the isopods
were fish lice, and together with the parasitic copepod may be considered as
accidental food.
Stonehouse (1962b) found that on Ascension Island Phaethon aethereus
and Ph. lepturus fed mainly on Exocoetidae. As well as some other fish he re-
corded one species of squid, Hyaloteuthis pelagicus, but it is clear that squid
were far less important in the diet of these Ascension Island birds than they
were in that of Ph. rubricauda on Christmas Island. Gibson-Hill (1947) in-
vestigated the food of the tropic-birds Ph. rubricauda and Ph. lepturus on the
Cocos-Keeling Islands and Christmas Island, Indian Ocean. His combined data
show that in these populations the diet was about 35-50% squid (presumably by
number) and the remainder fish; hence squid were less important than in our
Christmas Island (Pacific) samples.
FIGURE 4. Size-frequency distribution of fish and squid in the diets of the birds.
For details of measuring techniques see text (Techniques: Laboratory Treatment).
The diagram includes both items which could be measured accurately and those whose
lengths were estimated. When items could be estimated only to be in one of two ad-
jacent 2 cm classes, they were allotted alternately. Items represented only by frag-
ments were not included. Figures at the right of each histogram indicate the number
of items on which it is based.
PEABODY MUSEUM BULLETIN 24
24
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ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS
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ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS pag
PUFFINUS NATIVITATIS Streets—Christmas Island Shearwater
STATUS
Two species of shearwater are abundant on Christmas Island, but the larger
of the two, Puffinus pacificus, nests in burrows in very soft ground, and could
not conveniently be studied. The present species, P. nativitatis, nests on the sur-
face, and records were kept for over one hundred nests in a study area on Motu
Tabu and for a few nests on Cook Island. There are also colonies on several
other islets in the lagoon, and the total population must be close to 10,000
birds (Table 1). The diet of this species can usefully be compared with that
of Pt. alba, the third member of the Procellariiformes which breeds commonly
on Christmas Island. Pt. alba has slightly longer wings than P. nativitatis, but is
distinctly lighter (Table 8).
GENERAL DESCRIPTION AND CONDITION OF SAMPLES (TABLE 2)
Although a few regurgitations were obtained from nestlings, most were
from adults caught at night, either when they were about to feed chicks or while
they were courting. The 80 regurgitations contained on average 10.5 items
each; this figure is easily the highest among the larger species studied. The
average volume of the three largest regurgitations was 36.0 ml, or 11% of the
body weight of the bird; this percentage is lower than in any of the other species
(except Pr. cerulea), which is of interest in view of the high number of items
per sample.
The food items were generally largely digested. Only 1% of the fish in sam-
ples from adults were Grade 1, and only 20% of the fish were identified to
family; 3% of the squid obtained from adults were Grade 1, and 62% of the
squid were definitely identified to the family level. Separate squid beaks and eye
lenses were each present in about one quarter of the samples, the highest num-
ber of beaks in a single sample being 14, and that of lenses 13. However, one
FIGURE 5. Important fish families in the diets of the birds.
Within each bird species, the representation of each fish family is shown by three
columns, indicating respectively number, volume, and frequency of occurrence. The
number and volume of members of each fish family are given as percentages of the
totals of all fish identified in samples from that bird species; to obtain the frequency
of occurrence the number of samples which contained members of the family is
expressed as a percentage of the total number of samples. The rankings (see Tech-
niques: Methods of Analysis) of the various fish families in each bird species are
indicated by the numbers below the columns: where two families share a ranking, it is
preceded by an = sign. The diagram includes all families which rank seventh or
higher in the diet of any bird species. At the right of the diagram are given the total
numbers of items obtained from each bird species, while in the circles are shown the
proportions of these items which were fish identified to family, fish not identified,
and other items (including squid, Crustacea and insects). Type X were a distinct
group of small fish whose identity has still not been determined. The family Mullidae—
accidentally omitted from the diagram—ranked =6th in S. fuscata, providing 1%
by number, 2% by volume and 2% frequency of occurrence; this family ranked 9th
in A. tenuirostris and also in G. alba.
PEABODY MUSEUM BULLETIN 24
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ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 29
P. nativitatis was dissected and the gizzard contained 230 squid beaks, indicat-
ing that they must be retained over a considerable period. In contrast to the
situation in Pt. alba, these beaks and lenses were apparently all from squid simi-
lar in size to those found only partly digested in the regurgitations.
QUANTITATIVE COMPOSITION OF SAMPLES (Fic. 3 AND ‘TABLE 3)
Nearly two thirds of the food items were fish, but these made up less than
one third of the food by volume. Squid, on the other hand, were present in
smaller numbers but much larger volume, showing that the individual squid
were on average bulkier than the individual fish. In spite of the large number
of fish taken, squid had a higher frequency of occurrence (90%) than fish
(75%). This relationship, which was also found in some other species, is
discussed in the comparative section. Only two items other than fish and squid
were recorded, in separate samples—both were small crustaceans. In contrast
to Pt. alba, none of the samples were noted to contain large quantities of
stomach oil.
SIZE OF Foon ITEMs (Fic. 4, TABLEs 4 AND 5, AND APPENDIX 2)
The fish taken by P. nativitatis ranged in total length from the 0-2 cm class
to the 12-14 cm class, but of the 531 fish obtained only 17 were longer than 8
cm. The length-frequency distribution shows a strong peak in the 2-4 cm class
(55% of the total), as in several of the other species studied; the distribution
for the present species is especially similar to that for Pt. alba. The mean volume
of the fish in good condition was 3.7 ml, very different from the figure of 0.7
ml which was the average volume of all the fish regardless of their condition
(Table 4). Looking at the details of the samples it was clear that in this species
the small fish which were an important part of the diet were very rarely
Grade 1 or 2. The length-frequency distributions (Fig. 4) confirm that P. natiwvi-
tatis took a much lower proportion of large fish than did S. fuscata and A.
stolidus. Furthermore, the bulkiest fish obtained had a volume of only 11.5 ml,
or 3.6% of the body weight, a figure much lower than those for any of the
other species except Pr. cerulea.
The squid taken by P. nativitatis ranged in mantle length from the 0-2
cm class to the 8-10 cm class, but 98% were between 2 and 8 cm, with a peak in
the 4-6 cm class. The mean volume of the squid in good condition was 6.6 ml
and the volume of the largest squid was 19.8 ml. Both these figures are similar
to those for S. fuscata and A. stolidus, but are lower relative to body weight.
IDENTIFICATIONS OF Foop ITEMs (Fic. 5 AND APPENDICES 3 AND 4).
Fish from ten families were recorded among the 107 fish which were iden-
tified to the family level. Exocoetidae were by far the most important, compris-
ing 36% of the identified fish by number and 59%, by volume. However, it
must be remembered that Exocoetidae were among the easiest fish to identify
in largely digested samples, so their pre-eminence in the diet of P. nativitatis
may be somewhat exaggerated. Scombridae, then Gonostomatidae, Emmelich-
thyidae and Myctophidae were next in importance.
All the cephalopods identified were Ommastrephidae; the only genus re-
30 PEABODY MUSEUM BULLETIN 24
corded was Symplectoteuthis, and 19 individuals were determined as species A,
one as species B. One of the two Crustacea recorded was an isopod and the
other either a mysid or euphausiid.
We know of no published information on the food of this species of shear-
water, but it is clear from accounts of stomach contents of other members of the
genus Puffinus that Crustacea, as well as fish and squid, are an important food
of some members of the group (see, for instance, Murphy 1936 and Palmer
1962).
PTERODROMA ALBA (Gmelin)—Phoenix Petrel
STATUS
Pterodroma alba is the only gadfly petrel which breeds on Christmas Island;
it is most abundant on the islets Motu Tabu and Motu Upua, but also breeds
in small numbers on Cook Island. The total population is probably between
7,000 and 10,000 birds, of which perhaps 2,000 breed on Motu Tabu. A study
area on the latter island was chosen in March 1963 and contained over 500
marked nests by the end of the study. Most of the food samples were obtained
from Motu Tabu, but a few were from Cook Island.
GENERAL DESCRIPTION AND CONDITION OF SAMPLES (TABLE 2)
Almost half of the regurgitations were obtained from nestlings, while the
other half were produced by adults, usually when they had arrived to feed
chicks. Regurgitations from this species presented special problems in collec-
tion and analysis, mainly because many of them consisted largely of oil
(whose significance is discussed in the section on Feeding Zones) which it was
impossible to collect quantitatively from the ground. Because of this, no at-
tempt was made to measure the amount of oil in each sample, although notes
were kept of its presence; neither was oil in a sample considered as a “food
item.” It must therefore be remembered throughout the discussion of this
species that only the discrete food organisms, or identifiable remains, were con-
sidered. A related problem is the large number of samples containing only
squid beaks and/or lenses. As mentioned in the section on Laboratory Treat-
ment, such remains were arbitrarily considered as only one food item, irrespec-
tive of how many were present, because they do not necessarily represent re-
cently collected food.
The 95 samples collected from Pt. alba contained on average 4.4 items each,
one of the lowest figures among the species studied. The average volume of the
three largest regurgitations (disregarding oil) was 36.7 ml, very similar to
that for P. nativitatis (Table 2); this figure represents 14% of the body weight.
In Pt. alba, even more than in P. nativitatis, the food items were generally
largely digested—almost none of the fish or squid were Grade 1. Only one fish
was identified to the family level, and only 24% of the squid examined
could be definitely assigned to family; both these figures are lower than in any
of the other bird species. An interesting feature of the samples was that sev-
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 31
eral contained pieces of very large squid, especially arms, eye lenses and beaks.
Beaks and lenses were found in over half the samples, and in more than one
third of the samples they provided the only evidence of the presence of squid.
The highest number of beaks found in a single sample was 22, and of lenses
was 24. One Pt. alba was dissected and 172 squid beaks were found in the giz-
zard, indicating, as in the case of P. nativitatis, that beaks must be retained
there over a considerable period.
QUANTITATIVE CoMPOSITION OF SAMPLES (Fic. 3 AND TABLE 3)
One quarter of the food items were fish, but they made up only 14% of the
volume of the food because they were, on average, much smaller than the
squid. This percentage of fish, both by number and by volume, is much lower
than in the other species studied. About half of the food items were squid, and
they made up over three quarters of the total volume, a proportion higher than
in any of the other species. The remainder of the food consisted of other in-
vertebrates, which were far more important in the diet of this species than in
any of the others except Pr. cerulea. These invertebrates were mainly marine
water striders (Gerridae) and Crustacea (see Table 6); together, they com-
prised one quarter of the total food items, although only 8% of the total vol-
ume. The frequency-of-occurrence figures show that virtually all the samples
contained squid (or squid beaks), while fish were present in nearly half, and
other invertebrates in rather less. As already mentioned, many samples from
this species contained oil, but the presence of oil was not correlated with the
presence of any one class of food.
SIZE OF Foop Items (Fic. 4, ‘TABLEs 4 AND 5, AND APPENDIX 2)
The fish taken by Pt. alba ranged in length from the 0-2 cm class to the
8-10 cm class, plus two longer individuals, of which one was a Gempylus sp. in
the 20-22 cm class. The length-frequency distribution indicates a great prepon-
derance of small fish, as in P. nativitatis. However, the largest fish taken was
about as bulky as any obtained from other species except Ph. rubricauda, al-
though it was not exceptionally large in relation to body weight.
The squid taken ranged in mantle length up to 10 cm, but there were a
negligible number in the 0-2 cm class. The length-frequency distribution has a
peak in the 4-6 cm class, and except for a higher proportion in the 8-10 cm
class, is similar to those for the birds of similar size. The volume data also show
TABLE 6. Invertebrates other than cephalopods in the diets of Pterodroma alba
and Procelsterna cerulea
Pterodroma alba Procelsterna cerulea
% of total Frequency of % of total Frequency of
number volume _ occurrence number volume _ occurrence
Gerridae (Hemiptera) ie <O025 11 16 7 68
Crustacea 6 2 23 24 5 47
Other 7 6 19 1 5 26
TOTALS 26 8 38 42 16 82
a2 PEABODY MUSEUM BULLETIN 24
this resemblance, although the bulkiest squid taken (25.3 ml) was larger than
those obtained from any other species except Ph. rubricauda.
The other invertebrates taken by this species were mostly extremely small.
Halobates micans, a marine water strider, was the commonest item; it has a
body length of about 0.6 cm, and about 13 are needed to contribute a volume of
0.1 ml. However, a few of the Crustacea and some unidentified objects were
several centimeters long and had volumes of a few milliliters.
It is thus clear that there is a very large range in the size of the food items
taken by this species; it catches insects less than 1 cm long, while one took a fish
over 20 cm long, and the volumes range from less than .01 ml to 25 ml. In addi-
tion, Pt. alba was apparently unique among the species studied in that it evi-
dently regularly ate pieces of squid much larger than any of the ones which it
swallowed whole. For example, several samples contained arms of very large
squid—probably some over 30 cm in overall length. Furthermore, many of the
isolated eye lenses in the samples were clearly from squid far larger than any
of those encountered whole. Thus ten of the larger lenses from the samples had
diameters between 1.0 cm and 1.76 cm, while some of the larger squid obtained
whole during the study, with mantle lengths between 6 cm and 9.5 cm, had
lens diameters between 0.3 and 0.5 cm.
The largest squid obtained were unfortunately not available for measure-
ment of the lenses. However, a personal observation by N.P.A. of a stranding
of large squid on the beach of North Chincha Island, Peru, is relevant in that
of the nine dead individuals observed, two lacked heads entirely, two lacked
most of the arms, while the other five were more or less intact; however, all
lacked both eyes. The missing parts may have been eaten by gulls after the
stranding occurred, but the fact that it was the eyes and arms which were at-
tacked throws some light on the occurrence of large lenses and arms in regur-
gitations of Pt. alba. A similar, but moribund and still intact squid (Doszdicus
gigas), was found on the beach at Paracas, Peru. This had a mantle length of
55.5 cm and weighed six kilograms. Its eye lenses had a diameter of 1.7 cm,
which is almost the same as the largest lens obtained from Pt. alba regurgita-
tions, showing clearly the very large size of some of the squid on which this
species feeds.
IDENTIFICATIONS OF Foon ITEMs (Fic. 5 AND APPENDICES 3 AND 4)
Only one fish was identified to family, and was a member of the Gempy-
lidae. All the whole squid which were identified to family were Ommas-
trephidae, but families other than Ommastrephidae were well represented
among the cephalopod fragments which were frequently present in samples
from Pt. alba. Regurgitations obtained in the first five sampling periods yielded:
5 arms (in four samples) of either Onychoteuthidae or Enoploteuthidae, 3
beaks (in one sample) of Onychoteuthidae, one beak probably of Chiroteuthi-
dae, one beak of a pelagic octopus, and a few other beaks and pens from
cephalopods other than Ommastrephidae.
Of the 111 food items classed as “other invertebrates” (Table 6) the most
interesting were marine Gerridae (Insecta: Hemiptera), of which 51 were
present in eight samples; those identified were Halobates micans. The other
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 33
invertebrates comprised: 6 Stomatopoda, 1 decapod shrimp, 3 Euphausiidae, 9
other Crustacea; 5 Nematoda; 8 spermatophores, possibly of squid; and 27 un-
identified objects, in one sample looking much like faecal matter.
We know of no published information on the food of this species, but other
members of the genus clearly feed largely on squid (Falla 1934, Murphy 1936).
However, Crustacea have also been recorded as important in the diet of young
Pterodroma neglecta (Oliver 1930), and remains of pteropods and coelen-
terates have been found in the stomachs of Pt. phaeopygia (Loomis 1918).
STERNA FUSCATA Linnaeus—Sooty Tern
STATUS
Sterna fuscata is by far the most abundant breeding bird of Christmas Is-
land, as of many other tropical oceanic islands. Vast numbers can be found
breeding twice each year in various parts of the main island, and there is also
a colony on Cook Island in which breeding is more or less synchronous with
the mainland colonies. The total population of Christmas Island is probably
well over one million birds. The Cook Island colony was chosen for study of the
breeding cycles of individuals (Ashmole 1965), and most of the food samples
were obtained from there. However, all of the samples collected in March 1963
were from a colony on the main island. S. fuscata is very similar in size to A.
stolidus, a species much less common on the island but from which samples
were also obtained. A close relative, S. lunata, breeds in one part of Christmas
Island, but there was unfortunately no opportunity to study its food.
GENERAL DESCRIPTION AND CONDITION OF SAMPLES (TABLE 2)
Virtually all the samples were regurgitations from adult birds, and three-
quarters, collected in March, August and September 1963, were obtained from
birds which were about to feed chicks, or were in the process of feeding them. A
high proportion of the samples thus represent food intended for chicks. The
242 samples contained on average 5.6 items each. The average volume of the
three largest regurgitations was 48.0 ml, a figure much higher than in P.
nativitatis and Pt. alba, which were both considerably heavier birds, and sur-
passed only by Ph. rubricauda. Expressed as a percentage of body weight, this
gives a figure of 28%, which is higher than in any of the other species.
The food items were not in an advanced stage of digestion in comparison
with those from the other bird species. Of the fish, 16% were Grade 1, and
79% were identified to family. Of the squid 12% were Grade 1, and 88% of
those examined were definitely identified to family.
QUANTITATIVE CoMPosITION OF SAMPLES (Fic. 3 AND TABLE 3)
By number, fish comprised 60% of the food items, but by volume the figure
was only 38%. Conversely, squid were present in smaller numbers but larger
volume. In spite of the higher numbers of fish, squid had a slightly higher
frequency of occurrence; this relationship is discussed under Comparison and
Summary of the Diets of the Birds. Apart from fish and squid, only one other
item—a small crustacean—was found.
34 PEABODY MUSEUM BULLETIN 24
SIZE OF Foon ITEMs (Fic. 4, TABLEs 4 AND 5, AND APPENDIX 2)
The fish taken by S. fuscata ranged in length from the 0-2 cm class to the
16-18 cm class. However, 85% were between 2 and 8 cm, and S. fuscata was
unique among the birds studied in that the three classes 2-4 cm, 4-6 cm and
6-8 cm were about equally important; all the other species of similar size had
strong peaks in the 2-4 cm class. The volume data also show the large size of fish
taken; the mean volume of the fish in good condition was 2.5 ml, while the
bulkiest single fish had a volume of >15.8 ml, or >9.1% of the body weight, a
figure among the highest obtained.
The squid ranged in mantle length from the 0-2 cm class to the 8-10 cm
class, but as in nearly all the other species the vast majority (98%) were be-
tween 2 and 8 cm. In contrast to the situation in the fish, the length distribution
of the squid, and the average volume of those in good condition, are similar to
those for P. nativitatis and Pt. alba.
IDENTIFICATIONS OF Foop ITEMs (Fic. 5 AND APPENDICES 3 AND 4)
The 633 fish identified to the family level provided representatives of 21
families, a figure exceeded only by G. alba. Although the number of families
is high, over 80% of the identified fish belonged to the four commonest fam-
ilies. Exocoetidae ranked first, very closely followed by Scombridae, while
Gempylidae and Emmelichthyidae were also important. Of the 77 Scombrids ex-
amined in detail, 69 proved to be Yellowfin Neothunnus macropterus (Tem-
minck and Schlegel).
Of the 380 cephalopods identified to family, 1 was a small Argonauta sp.
(Octopoda), while all the rest were Ommastrephidae. 300 specimens were
identified as members of the genus Symplectoteuthis, and of these 186 could be
assigned definitely to species A and 16 to species B. A single euphausiid crusta-
cean was found.
Available published information on the food of S. fuscata was summarized
by Ashmole (1963b). The diet of this species on Ascension Island was similar
to that on Christmas Island in that it consisted of fish and squid. The small
number of samples obtained there yielded representatives of only five fish
families, all of them also found in the samples from Christmas Island. In
addition, Bruyns and Voous (1965) recorded about six Vinciguerria cf. lucetia
(Garman) (Gonostomatidae) regurgitated at night by an individual in the
Pacific.
ANOUS STOLIDUS (Linnaeus)—Brown Noddy
STATUS
Anous stolidus is not present in large numbers on Christmas Island, but some
hundreds breed on Cook Island, Motu Tabu and especially Motu Upua, the
total population being of the order of 2,000 birds. The species was not studied
intensively, but food samples were obtained whenever there was an opportunity:
most were collected on Motu ‘Tabu. This species invites comparison with S.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 35
fuscata, which is almost exactly the same size and nests on many of the same
islands in the tropical oceans, and with its small congener, A. tenuirostris.
GENERAL DESCRIPTION AND CONDITION OF SAMPLES (TABLE 2)
Nearly all the regurgitations were obtained from adult birds, mostly while
they were roosting at night. The 38 samples contained on average 5.1 objects
each. The average volume of the three largest regurgitations was 26.3 ml, which
is 15% of the body weight. This is much lower than in S. fuscata, but it must be
remembered that a relatively small number of regurgitations were obtained
from the present species and that most were from roosting birds.
Few of the fish were in Grade 1 condition, but two-thirds were identified
to family. More squid were in Grade 1 condition and all of the ten examined
were identified.
QUANTITATIVE COMPOSITION OF SAMPLES (Fic. 3 AND TABLE 3)
By number, 71% of the food items were fish, but by volume fish and squid
were of equal importance, and the frequency of occurrence of squid was slightly
higher than that of fish. No other invertebrates were found.
SIZE OF Foop Items (Fic. 4, TABLEs 4 AND 5, AND APPENDIX 2)
The fish taken by A. stolidus ranged in length from the 0-2 cm class to
the 14-16 cm class; there was a definite peak in the 2-4 cm class, but as in S.
fuscata fish larger than this made up more than half the total (56%). The mean
volume of the fish in good condition was 3.7 ml, or 2.1% of the body weight,
and the bulkiest individual fish had a volume of >16.9 ml, or >9.8 of the
body weight. All these figures are higher than in any of the other species except
Ph, rubricauda.
The length-frequency distribution for the squid is similar to those in the
birds of similar size, virtually all squid being in the range 2-8 cm mantle length.
However, in the small sample available both the mean volume of the squid
in good condition and the volume of the largest individual squid were slightly
lower than in the comparable species.
IDENTIFICATIONS OF Foop ITEms (Fic. 5 AND APPENDICES 3 AND 4)
The 93 fish identified to the family level provided representatives of 9 fam-
ilies. Exocoetidae were by far the most important and occurred in 40% of all
the samples. They were followed by Scombridae, Gempylidae, Engraulidae and
Holocentridae. However, the high ranking of Engraulidae was produced by a
single sample with 18 individuals.
All of the ten cephalopods identified to family were Ommastrephidae; of
the four identified to species, three were Symplectoteuthis species A and one
Symplectoteuthis species B.
On Ascension Island Dorward and Ashmole (1963) found that the food
of A. stolidus consisted largely of fish. They also summarized most of the pub-
lished reports on the food of the species, but in addition it should be noted
that Anderson (1954) mentioned it taking fish and squid up to about four
36 PEABODY MUSEUM BULLETIN 24
inches long, while Baker (1948) recorded the presence of small fish and crusta-
ceans in the stomachs of birds collected in Micronesia.
GYGIS ALBA (Sparrman)—White Tern
STATUS
Gygis alba is common on Christmas Island, with a total population of two or
three thousand individuals. However, there are far more S. fuscata and A.
tenutrostris, while A. stolidus and Pr. cerulea are about equal to G. alba in
abundance (Table 1). The species breeds all the year round on islets in the
main lagoon, with probably the most important concentration on Cook Is-
land, where most of the samples were obtained: the rest came from Motu Tabu.
G. alba is very similar in size to A. tenuirostris, but is very different in plumage,
the form of the bill and legs, and in many aspects of its biology.
GENERAL DESCRIPTION AND CONDITION OF SAMPLES (TABLE 2)
A total of 152 food samples were obtained, of which all but 19 were from
adults. The majority of the samples were of food carried in the bill, since food
for the chick is normally carried in this way, and whenever a bird was seen
carrying food an attempt was made to catch it. However, 54 regurgitations
were also obtained, of which 35 were from adults. Dorward, in his study of the
species on Ascension Island, only once saw an adult regurgitate; this was at night
during handling (pers. comm.). Most of our regurgitations from adults were
obtained from roosting birds in the early part of the night. On one occasion,
however, an adult was caught near its large chick while carrying one fish, but
readily regurgitated 19 larval fish, which it clearly could not have carried all
at once in its bill. It seems very possible that these would have been fed to the
chick, by regurgitation, if it had not been caught. The fact that the samples
include regurgitations as well as food carried in the bill complicates the analy-
sis, and various figures in Table 2 are given separately for the two different
categories of samples.
The 152 samples contained 379 food items. The samples carried in the bill
contained, on average, only 1.3 items, but the regurgitations contained 4.3
items each, which is comparable to the number in regurgitations of most of
the other species. The greatest number of objects carried in the bill of a single
bird was four. The average volume of the three largest samples carried in the
bill was 11.3 ml and of the three largest regurgitations 19.0 ml. Expressed as per-
centages of body weight these volumes are comparable to those from the other
species.
Food items from G. alba were generally in excellent condition. Of the fish
from samples carried in the bill 90% were Grade 1, and in regurgitated sam-
ples 31% were Grade 1. For squid the figures are 92% and 43% respectively.
These proportions are far higher than for any of the other species, both for
the samples carried in the bill and for the regurgitations. The good condition
of the regurgitations probably reflects a tendency for the birds to feed at dusk,
only a few hours before the majority of the regurgitations were obtained (see
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 37
section on Feeding Methods). Of the fish, 879% were identified to the family
level, and of the squid examined, all could be assigned to families. No separate
squid beaks or lenses were recorded.
QUANTITATIVE COMPOSITION OF SAMPLES (Fic. 3 AND TABLE 3)
Well over half (59%) of the food items were fish, although they made up
less than half (47%) of the volume of the food. Conversely, squid provided less
than half the number of items, but more than half the volume. More than half
of the squid were obtained in a short period in February 1964, and if this
period is excluded the percentage of fish in the diet becomes 77% by number
and 59% by volume. The frequency-of-occurrence figures are of special inter-
est: 74% of the samples contained fish, but only 34% contained squid. It can
thus be seen that there was an almost complete separation of the samples into
those containing fish alone and those containing squid alone, with only 7% con-
taining both: the latter figure is enormously lower than in any other species.
This certainly results partly from the fact that many samples carried in the
bill contained only a single item. However, the regurgitations contained on
average 4.3 items each, which is comparable to the samples from several
other species (Table 2). They contained 42% fish and 58% squid by number,
and yet only 14% of them contained both.
In one sample a single crustacean was found, but it is obvious that other
invertebrates are not a significant part of the diet of this species on Christmas
Island.
SIZE OF Foop ITEMs (Fic. 4, TABLEs 4 AND 5, AND APPENDIX 2)
The fish obtained from G. alba ranged in length from less than 1 cm to the
14-16 cm class. However, considering the samples from adults only, the size-
frequency distribution of fish carried in the bill is very different from that
from regurgitations (Fig. 4). As might be expected, small fish are under-
represented in samples carried in the bill, almost all the fish less than 2 cm long
being from regurgitations. Since a large majority of the samples were of food
carried in the bill, the distribution obtained from all the samples combined
(Fig. 4 and Table 5) is probably biased in favor of large fish. This problem is
discussed further in the section comparing the diets of the species.
An additional complication in this species is that since the food brought to
the young by the adults is usually (possibly always) carried in the bill, fish from
regurgitations of juveniles should have a size distribution similar to those car-
ried in the bill by adults and not to those from regurgitations of adults. The
small number of fish obtained from juvenile regurgitations satisfy this expecta-
tion, since they comprise 8 fish in the 2-4 cm class, 8 in the 4-6 cm class, and 4 in
the 6-8 cm class. In contrast, 48% of the fish from adult regurgitations were in
the 0-2 class (Fig. 4).
The eight fish obtained from G. alba which were over 8 cm in length were
all either halfbeaks (often separated from the Exocoetidae as the family He-
miramphidae) or Gempylus sp.; the latter have length more disproportionate
to their volume than any other fish occurring in our samples, and the long beaks
38 PEABODY MUSEUM BULLETIN 24
of the halfbeaks add much to their length and very little to their volume: thus
these long fish were not particularly bulky. The mean volume of all the fish in
good condition obtained from G. alba was 1.2 ml. This is 1.2% of the body
weight of the bird, a figure comparable to those obtained for the other species.
The largest fish was 9.2 ml, representing 9.1% of the body weight.
The squid obtained from G. alba ranged in mantle length from the 0-2 cm
class to the 6-8 cm class, but the length-frequency distribution shows an
enormous peak (of 77%) in the 2-4 cm class. However, it should be pointed
out that of the 100 squid in this class, 71 were obtained in 15 samples (of which
14 were regurgitations) during a single week in February 1964. All the squid
collected from G. alba during this period were in the 2-4 cm class, while at other
times squid in other size classes were also found commonly. Thus the apparent
tendency for G. alba to take a lower percentage of large squid than A. tenur-
rostris may not be a real one; in the other samples (excluding February) 41%
of the squid taken by G. alba were over 4 cm, while the comparable figure for
A. tenuirostris is 35% (also excluding February, although only four squid were
obtained then).
The mean volume of the squid in good condition obtained from G. alba
was 2.1 ml, which is 2.1% of the body weight of the bird. The bulkiest squid
taken was 8.5 ml, or 8.4% of the body weight. Both the mean and maximum
volumes are lower than in any of the other species except Pr. cerulea, but in re-
lation to body weight they are not exceptional. Furthermore, the mean figure is
strongly influenced by the large number of small squid obtained in February
1964.
IDENTIFICATIONS OF Foop ITEMs (Fic. 5 AND APPENDICES 3 AND 4)
A total of 195 fish obtained from G. alba were identified to the family level,
and provided representatives of 22 families, a higher number than in any of
the other bird species. By contrast, 633 fish from S. fuscata were identified, but
in only 21 families, while for A. tenuzrostris the figures are 519 fish in 17 famil-
ies. Five fish families represented in the food of G. alba were not recorded from
any of the other birds. ‘There thus seems to be a real tendency for G. alba to
take a very wide variety of fish. Furthermore, among the common families
which provide the bulk of the food, there were striking differences between G.
alba and all the other birds. Whereas in most of the other species Exocoetidae
were easily the most important family, in G. alba Blenniidae ranked highest,
although the percentage by volume of Exocoetidae was higher. Among the
Exocoetidae, halfbeaks were more important than in the diets of the other
bird species. Myctophidae and Gonostomatidae also ranked unusually high.
The Blenniidae are of special interest, since in most of the other bird
species they were unimportant, and even in A. tenutrostris, where they shared
second place, about seven other families were of comparable importance. Of
the 79 Blenniidae obtained from G. alba, 30 (in 26 samples) were Aspidontus
filamentosus, 15 (in 11 samples) were Runula tapeinosoma, 23 (in 3 samples
in November) were larval Petroscirtes mitratus and only 11 (in 4 samples, all
in November) were Cirripectus sp. By contrast, it was only Cirripectus sp.
which was eaten by other bird species, principally A. tenuirostris, but also A.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 39
stolidus, S. fuscata, Pr. cerulea and P. nativitatis. Unlike Cirripectus sp., Aspi-
dontus filamentosus and Runula tapeinosoma “are not associated with coral,
but tend to swim in open waters over reefs and elsewhere” and both have been
encountered “on the high seas, often near glass floats, etc.” Larval Petroscirtes
mitratus are “pelagic, and at times surface dwellers” (Donald W. Strasburg, pers.
comm.).
Of the 15 squid obtained from G. alba during the period March through
September 1963, all but one were Ommastrephidae (Symplectoteuthis species
A). However, the other one belonged to the genus Abralia (Enoploteuthidae),
and examination by Dr. Malcolm Clarke of a few of the regurgitations obtained
from G. alba in February 1964 (when squid were unusually important in its
diet), showed that most of the squid were Abralia sp., although Symplecto-
teuthis species A was also present.
In his study of G. alba on Ascension Island, Dorward (1963) examined 37
food samples. Eleven fish families were recorded, but the only fish which oc-
curred frequently were members of the families Blenniidae, Exocoetidae and
Trichiuridae. Only one cephalopod was found, implying that squid are much
less important than in the Christmas Island population. Gibson-Hill (1951)
recorded that in the Cocos-Keeling Islands (Indian Ocean) the fish obtained
from this species were mostly a species of Stolephorus (Engraulidae) while
Fisher (1906) mentioned that halfbeaks were among the fish taken at Laysan Is-
land. Both Murphy (1936) and Baker (1948) recorded the presence of marine
crustaceans in stomachs of this species, but Baker also mentioned insects (see
section on Feeding Methods).
ANOUS TENUIROSTRIS (Temminck)—Black Noddy
STATUS
Anous tenutrostris is by far the most abundant small tern breeding on Christ-
mas Island (Table 1). Although its numbers do not approach those of the larger
S. fuscata, it is present in much greater numbers than S. lunata, Pr. cerulea,
and G. alba; it is also far commoner than its larger relative, A. stolidus. A.
tenuirostris nests in trees, mainly on the islets in the lagoon of Christmas Is-
land; the largest colony is probably that on Cook Island, and a small section
of this was studied in some detail, but observations were also made on Motu
Tabu, and food samples were obtained from both. A tenuirostris is the smallest
of the birds studied except for Pr. cerulea, but it is very close in size to G. alba
(Table 8).
GENERAL DEscRIPTION AND CONDITION OF SAMPLES (TABLE 2)
Over three-quarters of the samples obtained from this species were from
adults, and all were regurgitations. A large proportion of those from adults
were obtained by catching roosting birds in the early part of the night. The
110 samples contained on average 18.3 items each, which is much higher than
in any of the other species except Pr. cerulea. The average volume of the
three largest regurgitations was 17.2 ml, which is 19% of the body weight.
40 PEABODY MUSEUM BULLETIN 24
The regurgitations often consisted of tightly packed masses of small fish, and
much of the food was in a fairly advanced stage of digestion. Of the fish in
samples from adults 10% were Grade 1, and 27% of all the fish were identifiable
to family. The latter low figure reflects the fact that most of the fish were very
small, and for this reason were generally hard to identify. Of the squid, 4%
were Grade | and more than two-thirds were identified to family. No separate
squid beaks or lenses were found.
QUANTITATIVE COMPOSITION OF SAMPLES (FIG. 3 AND TABLE 3)
A very high proportion of the food of this species was fish. Fish accounted
for 95% of the number of food items, while 4°% were squid. By volume, fish
made up 77% and squid 25% of the diet. Fish had a very high frequency of oc-
currence, being found in 96% of the samples. Squid, in spite of their low num-
bers, were found in 38% of the samples; this reflects the facts that they were
spread over samples from all the different periods, and that in almost every
individual sample they were heavily outnumbered by fish—no sample contained
more than five squid. Other invertebrates were unimportant in the diet of this
species. They made up only 1% by number and less by volume, and occurred
in only two samples.
SIZE OF Foop ITEMs (Fic. 4, TABLEs 4 AND 5, AND APPENDIX 2)
Fish taken by this species ranged in length from less than 1 cm to the 8-10
cm class, but over half were less than 2 cm and 90% less than 4 cm long. The
three fish in the 8-10 cm class were Gempylus sp., and were exceeded in volume
by many shorter fish. The volumetric data also demonstrate the generally small
size of the fish taken. The mean volume of the fish in good condition was 0.4
ml, which represents about 0.4% of the body weight; both these figures are far
lower than in any of the other terns except Pr. cerulea. However, the largest
fish by volume was 6.6 ml, or 7.3% of the body weight, which is not far below
the equivalent figures for the other terns.
Squid in samples from this species ranged in mantle length from the 0-2
cm class to the 6-8 cm class; 64% were less than 4 cm. The mean volume of
the six complete squid was 3.6 ml, a high figure resulting from the fact that
three unusually large individuals were included. The figure for the average vol-
ume of all the squid (1.7 ml: Table 4) indicates that A. tenuirostris took squid.
hardly larger than G. alba. The bulkiest individual squid was 10.0 ml, which is
11% of the body weight.
Thus, A. tenuirostris feeds mainly on very small fish, although it is capable
of taking much larger individuals. Squid, while taken in far smaller numbers,
are on average much larger and are thus a significant part of the diet.
IDENTIFICATIONS OF Foon ITEMs (FIG. 5 AND APPENDICES 3 AND 4)
The identified fish in the samples from A. tenuirostris belonged to 17
families, of which two were not represented in any of the other species. Looking
at the representation of the various families, the most striking feature is that
no one or a few families were of outstanding importance, but about ten made
significant contributions to the diet. Exocoetidae ranked first and were followed
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 41
by Scombridae and Blenniidae, ranking equally. Almost as important were
Gempylidae, Holocentridae, Emmelichthyidae, Gobiidae, Myctophidae, Mulli-
dae and Mugiloididae. It is worth noting that in contrast to the situation in G.
alba all the 113 Blenniidae identified were Cirripectus sp. which “lives among
coral branches on shallow reefs. It is abundant in the lithothamnion ridge area
near the outer edges of atolls’ (Strasburg, pers. comm.).
All the squid identified to family were Ommastrephidae; those identified to
genus were all Symplectoteuthis and the eight which could be determined
specifically were species A. Invertebrates other than squid were unimportant in
the diet, only 22 being recorded; of these 21 were mysids or euphausiids in a
single sample and the other was a stomatopod larva.
On Ascension Island, as on Christmas Island, fish formed the main part of
the diet, squid being present in only three out of 25 regurgitations examined
(Ashmole 1961). Representatives of eight fish families were identified, Blenni-
idae, Holocentridae and Exocoetidae being most fequent.
PROCELSTERNA CERULEA (F. D. Bennett)—Blue-grey Noddy
STATUS
Procelsterna cerulea nests in loose colonies of a hundred or so on a number
of the islets on Christmas Island, both in the main lagoon and in some of the
smaller lagoons. The total population must number three or four thousand
birds, which is roughly equal to that of G. alba; it is however much smaller than
that of its close relative A. tenuirostris. The species was studied, and food samples
collected, on both Motu Tabu and Cook Island. Pr. cerulea is by far the smallest
of the species studied, averaging half the weight of A. tenwirostris, the next
smallest, and only 7% of the weight of Ph. rwbricauda, the largest.
GENERAL DESCRIPTION AND CONDITION OF SAMPLES (TABLE 2)
No samples were collected from this species before August 1963, so the data
do not quite span a year. All of the 34 samples were regurgitations from adults
and most were obtained by catching the birds in flight, with a hand net, shortly
after they returned to the islets in the evening; the rest were from roosting birds
in the early part of the night. The samples contained an average of 41.8 food
items each, a figure far higher than in any of the other species; even A. tenut-
rostris had less than half as many items per sample. The average volume of the
three largest regurgitations (3.4 ml) represents only 7.5% of the body weight
of the bird, a figure much lower than for any other species, and less than half
that for A. tenutrostris.
Many of the food items were in good condition, although their minute size
made analysis difficult. Of the fish, 8% were Grade 1, and 38% could be
identified to the family level. Of the squid, 189% were Grade 1, and 74% of those
examined were identified to family.
QUANTITATIVE COMPOSITION OF SAMPLES (Fic. 3, TABLEs 3 AND 6,
AND APPENDIX 1)
Half of the food items obtained from Pr. cerulea were fish, but they made up
42 PEABODY MUSEUM BULLETIN 24
three-quarters of the diet by volume; squid comprised 9% of the food by num-
ber? and 10% by volume. Fish had a very high frequency of occurrence (97%),
while squid occurred in just half of the samples.
Invertebrates other than squid were much more important in the diet of this
species than in any of the other birds studied. They comprised 42% of the
total number of food items, but even in this small species they were small in
relation to the fish and squid eaten and so contributed only 16% to the volume
of the diet. Considered together, other invertebrates had a frequency of occur-
rence of 82%, more than double that for any other species. These invertebrates
fall into three groups: Crustacea, insects and other invertebrate items (Table 6).
The Crustacea were all extremely small and, although they comprised 24% of
the total food items, they contributed only 5% of the volume. The insects were
all marine water striders, which provided 16% of the total numbers and 7% of
the volume; their frequency of occurrence (68%) was higher than that of the
Crustacea (47%) in spite of the higher numbers of the latter. Finally there is a
group of other items, mostly unidentified, which comprised only 1% of the total
numbers but contributed 5% to the total volume and occurred in 26% of the
samples.
SIZE OF Foon ITEMs (Fic. 4, ‘TABLEs 4 AND 5, AND APPENDIX 2)
The fish taken by Pr. cerulea were small in comparison with those taken by
most of the birds and ranged in length from less than 1 cm to the 8-10 cm class.
However, nearly three-quarters of the fish were less than 2 cm long, while the
longer fish were nearly all Gempylidae, with relatively low volumes. The fish
taken by Pr. cerulea were not only small in absolute volume, but were re-
markably small in relation to the weight of the bird. Thus the mean volume
of the fish in good condition was only about 0.1 ml, or about 0.2% of the body
weight, while the largest fish represented only 1.5% of the body weight.
All but one of the 117 measurable squid had mantle lengths in the 0-2 cm
class, in strong contrast to the situation in all the other birds; however, four-
fifths of these small squid occurred in three samples. The mean volume of
the squid was 0.04 ml, and the bulkiest squid was 1.1 ml, representing 2.4% of the
body weight of the bird; this is a much lower figure than in any other species.
The various arthropods found in the samples never exceeded 1 cm in body
length, and most were much less than this. ‘The body lengths of the water striders
were about 0.6 cm, while some of the Crustacea were only 0.5 cm. The volumes
of the arthropods were extremely small; about 13 of both water striders and the
Crustacea are needed to make up 0.1 ml, and much of this is chitin.
IDENTIFICATIONS OF Foop ITEMs (Fic. 5, TABLE 6, AND
APPENDICES 3 AND 4)
Fish from seven families were identified in the diet of this bird, but mem-
bers of one family—Gempylidae—were of overwhelming importance. It is of in-
terest that this family did not form a specially large part of the diet of A.
tenuirostris, although the latter species took many fish in the same size range as
2 However, 102 out of the 123 squid were from three regurgitations in August.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 43
those caught by Pr. cerulea. Next in importance was Type X (see note to Fig.
5), which among the other birds was found only in small numbers in the diet
of A. tenuirostris. Exocoetidae, Scombridae and Blenniidae, in this order, were
also of some importance.
Of the squid identified two were Loligo (Loliginidae); all the rest (from
a single sample) were Rhynchoteuthis larvae of an ommastrephid, probably
Symplectoteuthis sp.
As already mentioned, the other invertebrates in the diet of this species
were mostly Crustacea and marine water striders (Gerridae). The Crustacea
were mostly Pontella sp. (Copepoda), while all the water striders identified were
Halobates micans.
Our general impression of the diet of Pr. cerulea is that it consists of any
small animals, with a volume between about 0.01 and 1 ml, which are available
at the surface of the ocean. In the area of Christmas Island at the time of
our study the vast majority of such animals were apparently tiny fish, but this
need not be so at all Procelsterna colonies at all times. For instance, Murphy
(1936: 1148) records that stomachs of Procelsterna albivitta from the San Ambrosio
Group were mostly filled with small shrimp-like crustaceans about 10 mm in
length. Specimens from other islands in the southeast Pacific contained small
cephalopod mandibles, remains of crustaceans, and tiny fish with silvery eyes,
resembling larval eels. Oliver (1930) also noted that small red crustaceans have
been found in the stomachs of P. albivitta on Lord Howe Island.
4, COMPARISON AND SUMMARY OF THE DIETS
OF THE BIRDS
PROPORTIONS OF FIsH, SQUID, AND OTHER ITEMS
(Fic. 3 AND TABLE 3)
The main elements in the diets of the species studied were fish and squid;
the frequency of occurrence of fish varied among the species from 45% to 97%,
and of squid from 34% to 97%. Other invertebrates were frequent in samples
from only two species and even in these they were of little volumetric impor-
tance.
A striking general result of the present study is the demonstration of the ma-
jor part played by squid in the diet of the species investigated. In three out of
the eight species squid formed well over half of the food by volume, and in
another three it formed about half; only the two small inshore-feeding terns,
A. tenuirostris and Pr. cerulea, took much less squid than fish. Among the other
six species the diet comprised on average 60% squid and 38.5% fish by vol-
ume, or 43% squid and 52% fish by number. The squid fraction of the diet was
restricted almost entirely to one genus—Symplectoteuthis—of the family Om-
mastrephidae, only 0.4% of the identified squid belonging to other families. In
contrast, among the fish, a number of families were well represented and 12
families each contributed more than 1% of the identified fish.
These figures are based on averaged data for bird species which were sam-
pled unequally and were of widely different abundance; however, the results
are similar if S. fuscata, which is by far the most numerous species breeding on
Christmas Island, is considered alone. By volume, its diet was 62% squid to 38%
fish, while by number it was 40% squid to 60% fish. All of the identified
squid were Ommastrephidae of the genus Symplectoteuthis. Among the fish,
eight families were represented by more than 1% of the total number of identi-
fied fish, and five families by more than 5% (Appendix 3). The family Exo-
coetidae, which was the most important fish family in this and four of the other
bird species, provided nearly one third of the total number of identified fish in
the diet of S. fuscata, and 40%, by volume (Fig. 5). Thus even Exocoetidae
did not approach Ommastrephidae in their importance in the diet of this
species.
These results imply that in the open ocean in the vicinity of Christmas Is-
land, squid of the genus Symplectoteuthis are available to the birds in remark-
able quantity and may rival in available biomass the whole of the rich fish
fauna. Although at least some of the bird species feed to some extent at
night, it seems certain that Symplectoteuthis spp. must be available at the sur-
face in quantity during the day.
Another interesting aspect of the availability of squid is their remarkably
high frequency of occurrence, relative to their numbers, in the diets of a num-
ber of the species (Table 3). In Ph. rubricauda and Pt. alba, in which a greater
number of squid than fish were eaten, one would expect the frequency of oc-
44
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 45
currence of squid to be higher than that of fish, but in P. nativitatis, S. fuscata
and A. stolidus fish were far more numerous than squid, and yet the frequency of
occurrence of squid was higher. In A. tenuirostris and Pr. cerulea, in which
squid formed a tiny proportion of the diet by number, the frequency of oc-
currence of squid was nevertheless rather high. Only in G. alba is this trend re-
versed, squid occurring with relatively low frequency. This tendency for squid
to have a very high frequency of occurrence in samples from a wide variety of
species suggests that they are available at the surface of the ocean with great
regularity. However, the observational evidence on the behavior of small squid
in the open ocean is so scanty that no further discussion is profitable at present.
Ph. rubricauda, the largest of the birds studied, took about twice as many
squid as fish, but in contrast to the situation in all the other birds (except Pr.
cerulea) the squid were of smaller average volume than the fish, so that they
provided just under half of the diet by volume. In spite of the fact that the
samples contained, on average, a very low number of food items, the fre-
quency of occurrence of both fish and squid is high, resulting in an outstand-
ingly high proportion of samples (71%) containing both fish and squid. Com-
paring the figures with those for the other species (Table 3), it is clear that in
Ph. rubricauda the frequency of occurrence of fish is peculiarly high in relation
to their numbers, suggesting that this species contrasts with the others in feed-
ing more on individual, dispersed fish rather than on shoals. It obtains large
fish with great regularity, but often takes squid of much smaller volume in the
same samples.
The diet of Pt. alba contains a higher proportion of squid than those of any
of the other species, and it also differs from all but Pr. cerulea in the high in-
cidence of other invertebrates, mostly insects and Crustacea. Squid provide 48%
of the food by number, but this figure becomes 65% if the other invertebrates
are excluded. Thus Pt. alba takes nearly twice as many squid as fish, while all
the other species (except Ph. rubricauda) take greater numbers of fish. By
volume, squid form 78% of the diet, since although fish and other invertebrates
each contribute 26% of the total numbers of food items, by volume they make
up only 22% together. Pt. alba is unique among the species studied in eating
parts of large squid, but, as discussed later, it is possible that it attacks only
dead or moribund ones.
The diets of P. nativitatis, S. fuscata, and A. stolidus on Christmas Island
were very similar in overall composition; they took respectively 63%, 60% and
71% of fish by number, the remainder being squid. In all three the percentage
of fish by volume was lower (respectively 29%, 38% and 51%), but the differ-
ence was most dramatic in P. nativitatis, emphasizing the small size of the fish
taken by this species. Although in all three species the numbers of fish were
substantially greater than those of squid, the frequencies of occurrence of squid
were higher. This suggests that squid were available to these species with
greater regularity, although fish were apparently more abundant when avail-
able.
G. alba forms an interesting contrast with these three species, since although
the composition of its diet was extremely similiar (fish 59% by number,
46 PEABODY MUSEUM BULLETIN 24
47% by volume), the overall frequency of occurrence of fish was 74% and
of squid only 34%. However, during the short visit in February 1964 squid
were predominant in the diet, comprising 89% of the food items, 90% of the
volume, and having a frequency of occurrence of 75%. It thus appears that G.
alba is more dependent on fish than any of the larger species—although less
so than the two smaller noddies—but eats a high proportion of squid in certain
periods when they are easily available.
The diets of the two remaining species, A. tenuirostris and Pr. cerulea, were
similar to each other—and contrasted with those of all the other birds studied—
in the overall importance of fish in the diet; in both, fish formed three-quarters
of the food by volume and occurred in almost all the samples. In A. tenuzrostris
squid formed a tiny proportion of the food by number, but their relatively large
size and the fact that they had a fairly high frequency of occurrence made them
a significant part of the diet. In Pr. cerulea squid were of much less importance,
but other small invertebrates, mostly marine water striders and tiny Crustacea
(Table 6), were present in large numbers (42%), appreciable volume (16%)
and in a high percentage of the samples (82%). In this respect the diet of Pr.
cerulea contrasts strongly with that of the closely related A. tenuirostris, which
feeds in mixed flocks with it, but which is just twice its weight; A. tenuzrostris
takes a very small number of Crustacea and no water striders. On the other
hand one of the much larger species, Pt. alba, took 26% of invertebrates other
than squid, of which half were fairly large Crustacea and other items, but the
other half were water striders of the same species as those taken by Pr. cerulea
(Table 6). We are therefore faced with the problem of why the catching of
water striders should be impossible or uneconomic for A. tenuirostris, which
is only twice the weight of Pr. cerulea and has similar feeding adaptations, and
yet should be practicable for Pt. alba, which is more than five times the weight
of Pr. cerulea. Presumably the answer lies in the method of feeding of Pt. alba,
but as yet this is largely unknown (see section on Feeding Methods).
This discussion so far has been based on the overall composition of the
diets, but it is useful also to consider the extent of variation among the sampling
periods in the proportions of fish, squid, and other items. There is little sign of
consistent seasonal variation in the composition of the diets of any of the species
(see Fig. 8 and the section on Seasonal Variation), but it is clear that the diets
of some of the species are much more variable than of others. For instance,
the consistent dependence of A. tenuirostris on fish is noteworthy, while Pt.
alba never took more than a small proportion of fish. It is of interest to note in
this connection that Belopol’skii (1957), in studies of sea birds extending over
several years, found that birds feeding almost entirely on one type of food
(for instance fish), did so in different years, even though the species composi-
tion sometimes changed markedly. The diets of P. nativitatis and S. fuscata both
showed considerable variation, the latter being especially interesting since the
number of samples involved was large, so that the observed contrasts are un-
likely to be due to sampling errors. The most extreme variation was seen in
G. alba, where the overall diet was about half fish and half squid, but the per-
centage of fish (by volume) reached 93% in August and was only 10% in Feb-
ruary.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 47
The generally high level of variation in the composition of the diets suggests
that most of the species take fish or squid indifferently as they become avail-
able, rather than hunting specifically for either fish or squid. Even A. tenwtros-
tris and Pr. cerulea, which take very little squid, may not be exceptions, since
they are the species known to feed close to the island (see section on Feeding
Zones); it is very possible that Symplectoteuthis squid are less common in this
area than in the open ocean where the other species feed.
S1zE OF Foon ITeMs (Fic. 4, TABLEs 4 AND 5, AND APPENDIX 2)
In view of the general similarity in the composition of the diets of the vari-
ous species studied, a comparison of the size of the individual food items taken
by the different birds is clearly important in assessing the possibility of compe-
tition between them. Direct comparison of the length-frequency distributions of
the prey of the different bird species can be made from the histograms of Fig.
4. The same data are used in the cumulative treatment in Table 5, showing
more clearly how the birds fall into groups as regards the size of their prey.
The most striking differences are between Ph. rubricauda and the other birds,
as might be expected from the large difference in body weight. Of the fish
taken by Ph. rubricauda, 63% were longer than 8 cm (Table 5), while among
the other species the highest proportion of fish longer than 8 cm was 16% (in A.
stolidus). The length-frequency distribution of the fish obtained from Ph. rubri-
cauda was of interest in that it showed no strong peak, a large number of
classes being roughly equally represented. Of the squid taken by this species,
63% were more than 6 cm in mantle length, while among the other species
the highest proportion was 22%. It is noteworthy that in spite of its large size,
Ph. rubricauda produced regurgitations containing fewer items, on average,
than those of any of the other species (Table 2). Since the regurgitations were
as large relative to body size as in most of the other species, the small number
of items per sample must reflect the fact that the fish taken were exceptionally
large in relation to body size (Table 4). The squid, however, were of similar
size relative to body weight as in most of the other birds. The fact that the fish
and squid taken by Ph. rubricauda averaged about the same in volume,
whereas in all the other species except Pr. cerulea the squid were much bulkier
than the fish, suggests that Symplectoteuthis squid larger than 12 cm in mantle
length are not readily available. The large isolated eye-lenses, beaks and arms
found in samples from Pt. alba clearly came from much larger squid, but those
that were identifiable proved to belong to members of different squid families
(see Species Accounts). These squid may have been unavailable to Ph. rubri-
cauda, or they may have been too large for it to swallow whole. Since this
species lacks the adaptations of the bill which enable Pterodroma spp. and the
albatrosses to tear off pieces from objects too big to swallow, it is not surprising
to find such large squid unrepresented in its diet.
The next two species in size, P. nativitatis and Pt. alba, fed upon prey of
similar size; the length-frequency distributions for both fish and squid were
closely parallel. However P. nativitatis took rather more fish in the 0-2 cm class
and Pt. alba more squid in the 8-10 cm class. The latter difference is reflected
in the volume data (Table 4), which show that the largest squid—and also the
48 PEABODY MUSEUM BULLETIN 24
largest fish—taken by Pt. alba were considerable bulkier both absolutely and in
relation to the size of the bird than any taken by P. nativitatis.
These two Procellariiformes took unexpectedly small fish in comparison
with the two largest terns, S. fuscata and A. stolidus, which are much lighter.
P. nativitatis and Pt. alba took respectively 70% and 68% of fish less than 4 cm
long, while for the terns the figures are respectively 34% and 44% (Table 5).
This difference is not paralleled in the squid data; the length-frequency dis-
tributions for the four species are all extremely similar, although Pt. alba was
the only one to take an appreciable number of squid in the 8-10 cm class. As
might be expected from this, the mean volumes of the squid taken by these
species are fairly similar, while the volumes of the largest individual squid ob-
tained from them show only minor differences (Table 4). Both Figure 4 and
Table 4 show the similarity in the size of the prey taken by S. fuscata and A.
stolidus, and even the apparent differences in the length-frequency distributions
could be the result of inadequate sampling in A. stolidus. However, one fish
obtained from A. stolidus had a larger volume than any from S. fuscata, and
the mean volume of the fish in good condition was also considerably higher in
A. stolidus.
G. alba, though closely similar in size to A. tenuirostris, took a higher pro-
portion of large fish. The mean length of the fish obtained was close to those
for P. nativitatis and Pt. alba, but the length-frequency distribution differed in
the relative lowness of the peak in the 2-4 cm class and the larger numbers of
fish both shorter and longer than this. As mentioned in the Species Account,
regurgitations from adult G. alba (presumably of food not intended for
chicks) contained more small fish than the samples carried back in the bill for
chicks (Fig. 4, inset). It is certain that most—if not all—of the food for the
chick is carried in the bill, and this habit could not have evolved, nor be main-
tained by selection, if a high proportion of the food items captured for the
chick were very small. This is made clear by reference to A. tenutrostris, in
which both adults and juveniles frequently regurgitated 50 or more tiny fish.
If the adults carried food for their chicks in the bill, they would obviously need
to make many more trips. In spite of possible bias in the sampling, the fact
that G. alba took a substantial number of fish in the 4-6 cm and 6-8 cm classes,
while A. tenwirostris took only a tiny number in the 6-8 cm class and few in the
4-6 cm class, is sufficient to show that G. alba makes much greater use of large
fish than A. tenuirostris, at least while feeding young.
It is unlikely that the sample of squid obtained from G. alba is biased in
favor of large individuals, since the majority were obtained from regurgitations
in a short period in February, and all of these were in the 2-4 cm class, while
at other times many squid in the 4-6 cm class were also obtained. Thus all that
can be said is that neither G. alba nor A. tenutrostris took many very small
squid, and neither took any more than 8 cm long. On the other hand it is cer-
tain that both took generally smaller squid than did the two petrels and the two
larger terns (Table 4 and Fig. 4).
The size distribution of the fish taken by Pr. cerulea is very similar to that
for A. tenuirostris, but even more heavily weighted towards the 0-2 cm class.
Breaking this 0-2 cm class into two parts we find that the proportion of all the
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 49
fish which are between 1 and 2 cm long is almost the same in the two species,
but Pr. cerulea takes twice as many in the 0-1 cm group (Table 5). This dif-
ference is reflected in the volume data (Table 4), which show that the fish taken
by Pr. cerulea average only about one-quarter the size of those eaten by A.
tenuirostris. The relatively few squid taken by Pr. cerulea were almost all
smaller than those obtained from any of the other species.
REPRESENTATION OF DIFFERENT KINDS OF FISH AND SQuID (Fic. 5 AND
APPENDICES 3 AND 4)
Since the diets of a number of the bird species are similar in general com-
position and in the size of the food items taken, it is of interest to consider
whether there are important differences in the kinds of fish and squid taken.
The comparisons have necessarily been made mainly at the family level, al-
though some generic comparisons were possible in the case of the Blenniidae.
The percentage representation of important fish families by number, volume
and frequency of occurrence are shown in Figure 5, where the overall rankings
are also indicated (see Methods of Analysis for details of the ranking system).
The numbers of representatives of all the fish families obtained by each species
are given in Appendix 3, together with the few precise fish identifications. ‘The
figure and the appendix must be used with the reservation—discussed in the sec-
tion on Methods of Analysis—that in partly digested samples members of cer-
tain fish families are much easier to recognize than others. Pt. alba does not
appear in Fig. 5 because the samples from this species were so far advanced in
digestion that only one fish could be assigned to a family.
Fish from 33 families were identified, but many of these were represented
in single or very few samples, and the 15 families shown in Fig. 5 include all
those which rank high in the diet of any of the bird species. These families
make up 93% of the identified fish by number.
In the diet of five of the seven species, the family Exocoetidae ranked first;
furthermore, in G. alba, in which Blenniidae ranked first, Exocoetidae pro-
vided a higher percentage of the diet by volume. In Ph. rubricauda, P. natt-
vitatis and A. stolidus Exocoetidae were of far greater importance than any
other fish family, while in S. fuscata and A. tenuirostris other families were
almost as important. Although the distinctiveness of remains of Exocoetidae
must bias the results to some extent, there is no reason to doubt the pre-emi-
nence of this family in the diets of these birds. Furthermore, the fact that
Exocoetidae were not identified from Pt. alba may indicate that they did not
make up a large proportion of the fish which it obtained. If so, this is a distinct
difference between the diet of this species and those of all the other birds.
The main interest in the fish obtained from Ph. rubricauda is that al-
though Exocoetidae were of outstanding importance, the other three families
represented—Coryphaenidae, Diodontidae and ‘Tetraodontidae—which all pro-
vided a significant fraction of the diet, were of little importance or were absent
from the diets of the other birds. This evidence supplements the data on the
frequency of occurrence of fish and squid, in suggesting that the feeding habits
of Ph. rubricauda contrast strongly with those of the other species investigated.
50 PEABODY MUSEUM BULLETIN 24
The fish portions of the diets of P. nativitatis, S. fuscata and A. stolidus were
strikingly similar, although twice as many fish families were represented in the
diet of S. fuscata as in the other two species (undoubtedly partly due to the
fact that more samples were obtained from S. fuscata). In all three species Exo-
coetidae were important, but in S. fuscata Scombridae were almost equally im-
portant, and this feature differentiates the diet of this species from all the others
studied; Gempylidae and Emmelichthyidae were also present in quantity, but
none of the other 17 families was of great importance. In A. stolidus Exocoeti-
dae, besides being far more abundant than the members of any other family,
were on average much larger than the other fish taken. However, Scombridae
and Gempylidae ranked second and third respectively, as in S. fuscata.
G. alba, in which nearly all the fish were identifiable, fed on a very different
selection of fish. Blenniidae were the most important family, and it has already
been mentioned that most of these blennies were kinds not taken at all by the
other birds (see Species Accounts). Over half the Exocoetidae were halfbeaks,
which were relatively unimportant in the diets of the other bird species; Mycto-
phidae ranked third. In all, 22 families were represented, the highest number
for any of the bird species. Although these included five families not identi-
fied in samples from the other birds, the four families Emmelichthyidae, Cory-
phaenidae, Diodontidae and Tetraodontidae were absent.
In A. tenuirostris, whose diet was almost entirely fish, more than two
thirds were unidentifiable, but the remainder were sufficient to indicate that
a wide variety of families were important in the diet, with no one outstanding.
Exocoetidae ranked first, but nine other families were important either by virtue
of their numbers, volume, or frequency (Fig. 5), and a total of 17 families
were recorded. Pr. cerulea, which appeared to feed largely in the same places
as A. tenuirostris, had a very different diet, in that Gempylidae were enor-
mously more abundant than any other fish family. Next in importance were
Type X (see note to Fig. 5), a group represented elsewhere only by two in-
dividuals from A. tenuirostris; Exocoetidae ranked third. Only seven families
were recorded in the diet.
The cephalopods collected up to the end of September 1963 were individ-
ually examined by Dr. Malcolm Clarke, and identified as far as possible.
Because the vast majority of these proved to be squid of a single genus, and
because nearly all the squid obtained later in the study were similar, only a
few of the latter were sent for identification. A summary of the data for the
period March through September 1963 is given in Appendix 4. Of the 869
cephalopods examined 790 (91%) were definitely or provisionally identified to
the family level. Of these, 84% were definitely Ommastrephidae, while an ad-
ditional 15% were recorded as being ‘probably’ or ‘possibly’ Ommastrephidae.
‘However, fragmentary remains of cephalopods belonging to families other than
Ommastrephidae were also obtained from Pt. alba (see Species Account), and
squid obtained from G. alba in February 1964 were largely Enoploteuthidae
(see Species Account), Of the Ommastrephidae which were identified defi-
nitely to the generic level, all were Symplectoteuthis. 257 Symplectoteuthis
squid were definitely assigned to species, and another 117 were tentatively
identified; only two species were present, and of the individuals definitely
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS Sl
identified 92% were species A and 8% species B (see definition under Identifi-
cation of Food Items in Ph. rubricauda Species Account). However, the data
suggest that Ph. rubricauda takes a higher proportion of species B than the other
birds; 15 individuals (in 6 samples) were definitely or tentatively assigned to
species A, and 10 individuals (in 4 samples) to species B.
5. FOOD OF SURFACE-CAUGHT YELLOWFIN TUNA
Through the cooperation of the Biological Laboratory, Honolulu, of the
Bureau of Commercial Fisheries, U.S. Fish and Wildlife Service, we are able to
present details of the food of Yellowfin, Neothunnus macropterus (Temminck
and Schlegel), caught at the surface in the Christmas Island region. Although
other predatory fish species, in particular Skipjack, Katswwonus pelamis (Lin-
naeus), undoubtedly feed extensively in the surface layers of the sea in this
area, there are fewer data on their food. A comparison of the food of tunas
with that of tropical oceanic birds is of particular interest since there is evidence
that many species of birds depend very largely on schools of aquatic predators,
probably mainly tunas, to make their prey available at the surface of the sea. At
least close to islands, most fish schools feeding at the surface have birds as-
sociated with them (Murphy and Ikehara 1955), and one might expect to find a
close correlation between the food of the two groups.
The Yellowfin is common in the Central Pacific and frequently feeds in the
surface layers when young, especially close to islands. Large numbers were
caught in the region of the Line Islands and Phoenix Islands during 12 cruises
of Fish and Wildlife Service Vessels in 1950 and 1951. Data on the food of Yel-
lowfin obtained during these cruises were presented by Reintjes and King
(1953). However, in the present context it seemed important to limit con-
sideration to surface-caught fish, so we have re-analysed the relevant data.
Our analysis is of quantitative data and identifications—filed on punch
cards—of the stomach contents of the 191 Yellowfin caught by surface trolling
within 10 miles of Christmas Island, and also of Fanning, Washington and
Jarvis Islands, its closest neighbors. Fish caught with pole-and-line were ex-
cluded since they were almost all obtained in one month, while the troll-caught
fish were relatively well distributed by season, as follows; February (1951) 24,
April (1951) 34, May (1950) 50, May (1951) 15, June (1951) 4, September (1950)
11, November (1950) 53. A few Yellowfin were caught at the surface more than
10 miles from the islands. These fish were excluded from the analysis because of
their small numbers, although if more had been available it would have been
especially interesting to compare their food with that of the birds, since most of
the bird species feed far from land. The Yellowfin involved in the present anal-
ysis were mostly rather small, 36% being less than 1000 mm in fork length, while
only 2% were more than 1300 mm. Larger individuals are more often caught
on longline gear than at the surface.
As far as possible the tuna food data were treated in the same way as those
for the bird food, although the samples consisted of stomach contents and not
regurgitations, and were collected in different years and with different seasonal
distribution. However, it does seem reasonable to suppose that these tuna were
feeding at times in close association with some of the bird species studied. In
particular A. tenutrostris and Pr. cerulea are inshore feeders, whilst A. stolidus
and G. alba probably do a fair proportion of their feeding within 10 miles of
land.
a2
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS a4
The details of the analysis are given in Appendix 5, but the overall propor-
tions of fish, squid (with which we have included 4 small octopods) and other
invertebrates in the Yellowfin stomachs are shown in Fig. 3. The very high
proportion by number (96%) of other invertebrates is immediately evident,
being far greater than in any of the bird species. However, these items were
mostly very small and provided only 61% of the volume. Thus although Yel-
lowfin are capable of taking very large items (one carangid of 540.0 ml was ob-
tained) most of the food items were tiny (about 0.5 ml). The frequencies of
occurrence of squid and especially of fish were high, considering their low total
numbers: few stomachs contained neither fish nor squid.
The fish in the diet of the Yellowfin, although only 3% by number, formed
34% by volume. Nineteen fish families were identified in our sample of Yellow-
fin stomachs (Appendix 5), which is just under half of those recorded in
Reintjes and King’s study of their whole series of 1,097 stomachs. Of the identi-
fied fish, only 9% (both by number and by volume) were from families repre-
sented on Figure 5—i.e., families that ranked high in the diet of at least one of
the bird species studied. Furthermore, 10% of the identified fish (17% by
volume) were from families not identified at all in the diets of the birds. The
most important fish families in the diet of Yellowfin were Carangidae, Acan-
thuridae, and Ostraciontidae; of these the first and third were not found in the
food of the birds, while Acanthuridae were identified only in very small num-
bers. Together, these three families formed 84% of the identifiable fish (74% by
volume). Blenniidae and Myctophidae, two families which occurred regularly
in the diets of some of the bird species, were next in importance. The iden-
tified Blenniidae were Petroscirtes sp., the same genus as a few larval blennies
obtained from G. alba.
Three families of fast-swimming fish which ranked high in the diets of the
birds were not important in the diet of the Yellowfin included in our sample:
Exocoetidae and Scombridae each occurred in only one Yellowfin stomach
and Gempylidae in two. Yellowfin do obtain Exocoetidae (flying fish and half-
beaks) at times: for instance, in Reintjes and King’s full study 24 individual
Exocoetidae were recorded. Nevertheless, the overwhelming importance of mem-
bers of this family in the diets of the birds, and their relatively infrequent
occurrence in stomachs of surface-caught Yellowfin, suggests that the ability to
“fly” above the surface of the water is a rather effective defence against aquatic
predators, but renders the animals extremely vulnerable to predation by agile
sea birds. Scombridae and Gempylidae were also better represented in Reintjes
and King’s full study than in our samples; however, their ability to swim at high
speed might be expected to make them relatively less vulnerable to predation
by other fish than by birds, so their better representation in the samples from
the birds than in those from the tunas is reasonable.
Very few of the squid found in the stomachs of Yellowfin were identified,
even to family level. However, of the two species occurring in the study as a
whole, one was Symplectoteuthis oualaniensis, the same ‘species’ that occurred
commonly in the diets of most of the birds. Two individuals of this form were
the only identified squid in the Yellowfin stomachs now under consideration.
The other invertebrates were mostly very small, and a large number of them
54 PEABODY MUSEUM BULLETIN 24
were unidentified megalops (crab larvae). During two days in May 1950, an ex-
ceedingly dense aggregation of megalops was in the vicinity of Christmas Is-
land and the Yellowfin caught at this time contributed very largely to the high
numbers of other invertebrates. If such a concentration had been present during
1963/64, it might well have been utilized by the birds, especially Pr. cerulea.
No water striders were recorded in the tuna stomachs.
Thus, although there are many biases in this type of comparison, it does
seem that there is surprisingly little overlap in the food of Yellowfin feeding
at the surface close to land and the food of the bird species in this study. One
important consideration is that all the tunas whose stomachs were analysed were
caught within ten miles of land, while a number of the bird species probably fed
almost entirely outside this range (see Feeding Zones). This partly explains
the fact that the percentage of fish in the diet of the Yellowfin which are
members of primarily reef-originating families is far higher (95%: data in Ap-
pendix 5) than in any of the birds studied. (For details of the designation of
“reef-originating” fish families, and of the proportions of reef-originating fish in
the diets of the birds, see text under Feeding Zones, Table 7, and Appendix 3.)
However, it must also be remembered that, as described elsewhere, most of the
bird species can catch prey only when it is very close to the surface, and this
happens mainly when the prey animals are pursued from below by predatory
fish; it may well be that certain fish hardly ever come right to the surface, even
when pursued. These fish would not be available as food for most of the birds
even if they were common below the surface and were eaten extensively by
tunas. This situation might apply, for instance, to members of the family
Acanthuridae, which are common in inshore waters and were eaten in numbers
by the Yellowfin, and yet were found in very few samples obtained from the
birds.
6. THE BIRDS IN THEIR MARINE ENVIRONMENT
THE ENVIRONMENT, AND THE AVAILABILITY OF Foop
The environment of the sea birds of Christmas Island, apart from their nest
sites, is provided by the Central Equatorial Pacific, a region which has been the
subject of extensive research by the staff of the U. S. Bureau of Commercial
Fisheries Biological Laboratory in Honolulu. The following brief account is
based almost entirely on the results of this work, and especially on an able dis-
cussion by Murphy and Shomura (manuscript) of the distribution of tunas in re-
lation to environmental factors, which the authors have kindly allowed us to
see before publication.* We consider in the present paper only those aspects of
the oceanography and biology of the region which are most relevant to the feed-
ing ecology of the birds; seasonal aspects are treated in a later section.
The dominant features at the surface in the Central Equatorial Pacific are
three currents, the North Equatorial Current flowing to the west north of about
latitude 10° N., the South Equatorial Current flowing to the west south of about
latitude 5° N., and the Equatorial Countercurrent flowing to the east between
them (Fig. 2). The northeast trade winds blow over the North Equatorial Cur-
rent and the southeast trades over the South Equatorial Current. Christmas
Island, at 2° N., lies in the South Equatorial Current, about 200 miles south of
its boundary with the Countercurrent. The oceanography of the region has been
described in a series of reports (references in Austin, 1960). Recently Roden
(1963) has analysed variations in sea level, temperature and salinity of the
Central Tropical Pacific, while Wyrtki (1965) presented results of harmonic anal-
ysis of the sea surface temperatures. The climatology of the region is also dis-
cussed by Hutchinson (1950), Riehl] (1954), and Wiens (1962).
A critical feature of the oceanography of the Central Equatorial Pacific is the
upwelling of nutrient-rich water which occurs in the South Equatorial Current
at the Equator (Cromwell 1953). Ryther (1963) explained: “Briefly, the effects
of Coriolis’s force north and south of the equator on the westerly drift of the
Equatorial Current results in the poleward divergence of the surface layers,
which are replaced with water upwelling from depths within the thermocline
(150-200 m).” The equatorial upwelling is responsible for the fact that zooplank-
ton abundance is generally higher between 114° S. and 5° N. than further from
the Equator (King and Hida 1957), although it is still low in comparison with
many other regions (King and Demond 1953). Similarly, King and Iversen
(1962) found that forage organisms sampled by midwater trawls (mainly at
night) were more abundant within 5° of the Equator than further to the north
and south.
Murphy and Shomura argue that the upwelled westerly-flowing water north
of the Equator is deflected towards the northwest to an extent which varies,
spatially and temporally, according to the regularity and strength of the south-
east trade winds. The region between about 114° N. and the southern boundary
*While this paper was in press we encountered the discussion by Blackburn of the role of
fronts in concentrating food for tunas (1965, Oceanogr. Mar. Biol., Ann. Rev. 3: 299-322).
35
56 PEABODY MUSEUM BULLETIN 24
of the Countercurrent is a zone of convergence. Plankton concentrations are
highest close to the Equator, but as the water moves to the northwest it “ma-
tures”; that is to say it becomes warmer, the concentrations of phosphate and
zooplankton decline, and deep-swimming Yellowfin become more abundant,
presumably because they congregate to feed on the forage animals responsible
for the decline of the zooplankton. It appears that the Line Islands lie in a re-
gion (about longitudes 140°-160° W.) which benefits most from the equatorial
upwelling, since the upwelled water is richer in nutrients than further east, and
the wind stress is generally sufficient to cause vigorous upwelling but not so
strong as to transport the upwelled water to the convergence south of the Coun-
tercurrent before it has time to mature.
However, it must be remembered that most tropical sea birds depend partly
or entirely on schools of predatory fish (mainly tunas) to drive their prey close to
the surface and so make it available. Murphy and Shomura demonstrate that
the distribution of these surface schools of small tuna is at variance with that
of the larger deep-swimming tuna and cannot be explained in terms of the gen-
eral distribution of zooplankton.
In the Central Equatorial Pacific surface schools of tuna are on average far
more abundant close to land, where they comprise mainly small Yellowfin,
than in the open ocean, where Skipjack predominate (Murphy and Ikehara
1955). However, there are certain zones of open ocean which have relatively high
densities of surface schools. Thus the latter authors, considering oceanic areas
far from land, found that in the latitudinal zone between 0° and 5° N. (in
which Christmas Island lies), less than half as many fish schools were seen per day
as in the Countercurrent (5°-10° N.) or in the South Equatorial Current south
of the Equator (0°-10° S.). Abundance was again low in the North Equatorial
Current (north of 10° N.).
Murphy and Shomura suggest that the abundance of tuna schools in certain
zones of the open ocean may be explained by their association with “fronts,”
and also that phenomena similar to “fronts” may occur close to islands, resulting
in concentration of tuna schools there. A “front” is defined by Cromwell and
Reid (1956) as “a band along the sea surface across which the density changes
abruptly.” However, fronts are normally detected by abrupt changes in the sur-
face temperature, which may be of the order of degrees per hundredth or
tenth miles, but are often much less (Voorhis and Hersey 1964). Although it is
clear that there are many different types of fronts, many of them are associated
with convergence and sinking (Uda 1938, Cromwell and Reid 1956, Knauss
1957). The biological significance of such fronts is that they tend to concentrate
plankton species which are capable of resisting the downward currents. As
pointed out by King and Demond (1953): “When a strong convergence has per-
sisted for a sufficient length of time, an area of relatively high-plankton abun-
dance should result, providing rich pasturage for plankton-feeding animals”
(see also Ragotzkie and Bryson 1953). We do not know of published accounts of
measurements of the abundance of plankton or nekton at fronts, but Uda
(1938) noted “‘yellow-greenish water-colour due to the densely concentrated
planktons” at a “siome” (i.e., a front visible at the surface) in the North Pacific
near Japan, while the fascinating account by Beebe (1926: 41-70) of a major cur-
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS ST
rent rip (i.e. front) in the Eastern Pacific at 2° N., 86° W., demonstrated the
remarkable concentrations of organisms which are sometimes produced. Beebe
said: “. .. here was a concentration of organisms greater than I have ever seen—
the larger dotting the water and making visible its depths, the minute so abun-
dant that in places they were of the consistency of soup.” It is clear that even
slow sinking of converging water at a front must rapidly cause enormous differ-
ences between the abundance of plankton along the line of the front and in
the areas away from it. The narrowness of the rich zone was particularly noted
by Beebe (p. 50): “Again and again I was impressed with one outstanding
feature of the Current Rip, this uncharted zoGlogists’ paradise—the narrowness
of its limits and the sharpness with which these limits were defined. It was a
world, not of two, but to all intents and purposes of a single plane—length.
From first to last we followed its course along a hundred miles, and yet ten yards
on either side of the central line of foam, the water was almost barren of life.
The thread-like artery of the currents’ juncture seethed with organisms—liter-
ally billions of living creatures, clinging to its erratic angles as though magnet-
ized.” Beebe clearly recognized the convergent nature of the front, although
he did not speak in terms of sinking water. However, the narrowness of the
rich zone is a clear indication that this was the concentrating mechanism.
The overriding importance of fronts in producing local concentrations of
forage animals probably accounts for the fact that although zooplankton abun-
dance in general is higher between the Equator and 5° N. than between 5° N.
and 10° N. (King and Hida 1957), surface schools of tuna are much more
abundant in the latter zone. In the best-studied region, between 140° W. and 170°
W., Murphy and Shomura demonstrate a close correspondence between the
average rate of sighting tuna schools (generally accompanied by birds) in three
different latitudinal zones of the open ocean, and the rate of crossing fronts in
the different zones. To give an idea of the actual abundance of fronts and
birds it should be mentioned that in the area between 0° and 5° N. fronts were
crossed at an average rate of 0.34 per 114 hours, while fish schools were de-
tected at a rate of 0.34 per day. (A front was defined in this case as “‘a temperature
change of any magnitude that was completed during 15 minutes or less at a
speed of about 8 knots.’’) It thus appears that although there is a zone of con-
vergence (and often an “Equatorial Front”) between 114° N. and 5° N. (Cromwell
1953), the greater number of fronts in the area of the Countercurrent pro-
vides more rich feeding grounds for tuna and birds. Presumably the high fre-
quency of fronts in this area results partly from the complex interactions of the
westward or northwestward flowing water at the northern boundary of the South
Equatorial Current with the variable eastward flow of the Countercurrent.
Probably many of the fronts are local and transitory, but whenever they are
associated with sinking they could be important in concentrating plankton and
the forage animals on which the tunas and birds feed. Whereas the zone between
the Equator and 5° N. has much less than half as many tuna schools and fronts
than the Countercurrent, the South Equatorial Current between the Equator and
5° S. is almost as rich as the Countercurrent, both in tuna schools and fronts.
The great importance of fronts associated with convergence, as well as areas
of upwelling, in providing favorable feeding grounds for fish and whales has pre-
58 PEABODY MUSEUM BULLETIN 24
viously been recognized (Beebe 1926, Uda 1938, 1953, 1954). However, Mur-
phy and Shomura’s demonstration of the correspondence between the abun-
dance of fronts and the abundance of surface schools of tuna in different parts
of the Central Pacific may prove to be an important advance in the under-
standing of this area, and perhaps provides the explanation of its relatively high
populations of surface-feeding tunas and sea birds, in spite of the low average
abundance of zooplankton (cf. King and Demond 1953: 141).
It has long been known by ornithologists that marine birds often congregate
to feed at the boundaries between currents (for example, Beebe 1926, Brooks
1934, Murphy 1936: 88-89, Stonehouse 1962a, King and Pyle 1957, Bourne 1959:
15, 1963, 1965), but the richness of such areas has often been attributed to the
effects of upwelling or vertical mixing in making nutrients available, whereas
it now appears that concentration of organisms as a result of convergence and
sinking at fronts is frequently the critical phenomenon. Simple observations
at sea should generally permit differentiation of the two phenomena, since up-
welling of nutrient-rich waters produces a broad zone of enrichment tens or
hundreds of miles wide, while the concentration of organisms at a convergent
front may be only a few tens of yards in width, as noted by Beebe (1926). A zone
in which there are many fronts, for instance the Equatorial Countercurrent in
the Pacific (Murphy and Shomura), may give a superficial appearance of ho-
mogeneity, but the fact that fronts can easily be detected by thermograph read-
ings, even when they are not visible at the surface, provides interesting oppor-
tunities for further investigation.
While the above discussion has concerned fronts in the open ocean, Murphy
and Shomura point out that “front-like” circulation cells and eddies are found
near islands, especially on the leeward sides. They are produced by flow of a cur-
rent past the island, and involve some vertical mixing, and so can result in local
enrichment (Sette 1955, McGary 1955, Hardy 1928). While the data of King and
Hida (1957, Appendix A) did not show any great abundance of zooplankton
round Palmyra Island, it is probable that concentrations in eddies are often so
local as to be difficult to detect by routine sampling. However, the importance
of reef-dwelling fish (especially Acanthuridae) in the diet of Yellowfin caught
close to islands (Appendix 5) suggests that the availability of food close to reefs,
as well as concentrations of plankton and forage animals in eddies, may be im-
portant in maintaining the tuna populations close to islands. Both these factors
are compatible with the fact that a very high percentage of the tunas caught by
live-baiting and trolling in the vicinity of the Line Islands and Phoenix Islands
are obtained within a few miles of the islands on the leeward side (Bates 1950,
Ikehara 1953).
This discussion of the distribution of surface schools of tunas in the Central
Pacific is directly relevant to the feeding ecology of the birds of Christmas Is-
land, for two closely linked reasons. First, since tunas are highly mobile preda-
tors feeding on many of the same types of foods as the birds, their distribution
should be a fair indication of the distribution of potential food for the birds.
Second, probably all the tern species, and the other birds to a greater or lesser ex-
tent, are dependent on the presence of marine predators such as tunas to make
potential prey available at the surface. We may therefore come to the prelimi-
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 59
nary conclusion, which needs confirmation by direct systematic observations,
that for oceanic birds breeding on Christmas Island there are several widely sep-
arated areas which may provide abundant available food. First, there will be a
favorable feeding area to leeward of the island, whose size is not known but
which probably does not extend more than about twenty miles to the west.
Second, for birds which are adapted to feeding far from the colony, exceptionally
favorable feeding areas may be present in the Countercurrent a few hundred
miles to the north, and a roughly equal distance in the opposite direction, in the
South Equatorial Current south of the Equator. There is also the possibility
that there may sometimes be a fairly rich feeding zone for Christmas Island sea
birds at a distance intermediate between the inshore zone and the distant oceanic
areas to north and south; this would be associated with convergence and sinking
at the “Equatorial Front” which is sometimes present within the South Equa-
torial Current at about 2° N.
The importance of the inshore feeding area to certain bird species is apparent
from our observations, which are discussed in the next section. There are many
indications that the Countercurrent is rich in birds (see especially King and
Pyle 1957, Bruyns 1965, as well as Murphy and Ikehara 1955 and Waldron 1964).
King and Pyle’s observations suggest that the northern boundary of the Coun-
tercurrent has especially high densities of birds, but the nature of the oceano-
graphic features responsible for the richness of this zone is not yet fully under-
stood (see discussion in Austin 1960). Bates (1950) reported Captain Castle (an
experienced commercial fisherman) as having several times observed “booby
birds” [probably Red-footed Boobies] “by the thousands” working over tre-
mendous concentrations of Yellowfin in an area some 200 miles north of Christ-
mas Island, in the region of the convergence of the Equatorial Countercurrent
with a northwesterly current originating at Christmas Island. Of interest also is
Captain Castle’s opinion that in the Line Islands the local current interfaces
or “tide rips” (i.e., fronts) and not the reef areas contain the greater concentra-
tions of tuna.
It was not practicable to sample directly the food available to the sea birds
during the study on Christmas Island. However, in 1951 and 1952, U. S. Fish and
Wildlife Service research vessels sampled the forage animals in the surface layers
of the sea (down to 400 m), mainly with Isaacs-Kidd trawls, in connection with
their studies of the food of tunas (King and Iversen 1962). The results of this
work showed a good general correlation between the trawl-catch volumes and
zooplankton volumes, both being highest in the South Equatorial Current be-
tween 5° S. and 5° N., slightly lower in the Countercurrent, and yet lower
further to the north and south (King and Iversen 1962, King and Hida 1957).
The usefulness of the results of this trawling in considering the feeding ecol-
ogy of the birds is limited by the fact that nearly all the trawling was done at
night, while the few daytime hauls gave dramatically different results. For in-
stance in the Countercurrent at about 6° N., between 161° W. and 163° W., four
hauls were made two hours after sunrise and two hauls one hour after sunset, all
within 110 meters of the surface. The day hauls had an average volume of
11.4 ml., with an average of 158 organisms, while the night hauls averaged 106.4
ml., with 614 organisms. Thus, far fewer animals were obtained during the day
60 PEABODY MUSEUM BULLETIN 24
and they were on the average much smaller, nearly all the fish and squid cap-
tured being larval forms.
Although some of the stronger swimming animals may have been able to
dodge the net during the day (Pearcy and Laurs 1966), the difference between
day and night hauls must be primarily related to the nightly movement to the
surface waters of animals which are mesopelagic during the day, forming the
“deep scattering layers.” (The mesopelagic zone is that between about 200 and
1000 m—Hedgpeth 1957.) The animals in the deep scattering layers which reflect
back sound from echo-sounders are evidently mainly fish, especially Mycto-
phidae (Hersey and Backus 1962), but some Crustacea (especially Euphausiidae
and Sergestidae) apparently show similar movements. King and Iversen’s data
suggest that in the Central Pacific Myctophidae form a large proportion of the
fish which are close to the surface only at night, but that Stomiatidae, Gono-
stomatidae and Nemichthyidae are also important, and a number of other fam-
ilies probably fall into the same category (see also Marshall 1960). These groups
of fish and Crustacea are not represented to a large extent in the stomach con-
tents of Yellowfin and Skipjack caught at the surface and on longline gear in
the Central Pacific (Reintjes and King 1953, Waldron and King 1962) suggesting
that although the animals of the deep scattering layers doubtless constitute the
major part of the biomass of the forage animals of the area, their migration
during the day to depths to which light hardly penetrates is a rather effective way
of avoiding predation by tunas, which apparently feed mainly during the day.
Since the birds included in this study depend largely on tunas to make their
prey available, Myctophidae and other fishes with similar habits should not
normally be available to them. However, several of the bird species did in fact
obtain some Myctophidae and Gonostomatidae, suggesting that they some-
times feed at night, or during twilight periods when some Myctophidae and
similar fish are sometimes still present close to the surface (Pearcy 1964). It is
clear that for the animals of the deep scattering layers there must be a very criti-
cal balance of selective pressures operating to determine the light intensities at
which they should arrive at and leave the surface; individuals arriving earlier
or staying later will obtain more food, but will run a higher risk of predation.
The occurrence of some of these fish in food samples from birds is presumably a
manifestation of the latter type of selection.
The foregoing discussion of the representation in the diets of the birds of fish
which are at the surface only at night should not be allowed to obscure the fact
that a vast proportion of the food of the birds consists of fish and squid which
are epipelagic and are present in the surface layers during the day; these ani-
mals are very rarely caught by trawling. Of the fish, Exocoetidae, Scombridae and
Gempylidae are all of great importance in the diets of the birds; probably
none of these are actually available to birds feeding at the surface except when
pursued from below, but all are normally found close to the surface. Blenniidae
are also important in two of the bird species and are eaten to some extent by
Yellowfin and Skipjack. However, they are totally absent from samples obtained
by midwater trawling in the open ocean (King and Iversen 1962); they may
perhaps be commoner close to land, although some of the species concerned are
not reef dwellers.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 61
In general, squid are apparently present at the surface more commonly at
night than during the day (see, for instance, Baker 1960), but small squid are
sometimes seen at the surface in daylight. Furthermore, the importance of Om-
mastrephidae of the genus Symplectoteuthis in the diets of so many of the bird
species (including some that do not normally feed at night) strongly suggests
that these squid are regularly available at the surface during daylight, al-
though perhaps especially in the morning and evening (see data for G. alba—Ta-
ble 9). Certain squid (including a number of Ommastrephidae) are known to
be able to jump clear of the water (Arata 1954, Lane 1957, Clarke, 1966),
while Heyerdahl (1950) reported that in the South Pacific, small squid were reg-
ularly seen in daylight gliding several feet above the water. Although there are
no records of flying behavior in Symplectoteuthis spp., this may well be be-
cause of the small number of observations of flying squid in which the species
concerned has been identified, and there is already enough evidence to indicate
that some members of the family Ommastrephidae have evolved a method of
escape from marine predators similar to that used by the flying fish (Exocoetidae).
This adaptation is probably very effective in relation to predators approaching
from below, but it must render the animals especially vulnerable to predation
by those birds—such as S. fuwscata—which are specialists in catching their prey
in the air. It is doubtless more than coincidence that Exocoetidae and Om-
mastrephidae—both groups of animals noted for their flying ability—are much
more important in the diets of tropical sea birds than in those of tunas.
FEEDING ZONES, AND ADAPTATIONS FOR FEEDING
FAR FROM THE COLONY
It was argued in an earlier paper (Ashmole 1963a) that population size and
many features of the biology of tropical sea birds are profoundly influenced by
the fact that “their breeding distribution is largely governed by the distribu-
tion of islands suitable for breeding, and while breeding they must either use
only a small proportion of the total available feeding areas, or they must spend
much time flying to and from more distant feeding areas.” It is clear that some
of the birds of Christmas Island are adapted to the first of these alternatives,
feeding only close to the island, while others exploit the second, commuting
great distances between their feeding grounds and the breeding colonies.
Since direct observations were made on the feeding zones of only a few of the
species, we must use for the others negative evidence and observations from
other areas. However, for most of the species we also have information on the
lengths of incubation shifts and data on the relative proportions of reef-
originating and pelagic fish in the diets (see below).
It can be seen from Table 7 that among the species studied there was enor-
mous variation in the mean length of the incubation shifts, the extremes being
Sterna fuscata with a mean of seven days, and Anous tenuirostris with a mean of
1714 hours. In general, long incubation shifts in a population indicate that
abundant food is not available close to the nest, since short shifts are uneconomic
if the time required to fly to and from the feeding grounds is long. Shifts lasting
several days, which are found in many petrels in the temperate zones as well as
in the majority of tropical sea birds, occur when birds have to travel great
62 PEABODY MUSEUM BULLETIN 24
TABLE 7. Length of incubation shifts of some sea birds on Christmas Island, and
percentages of identified fish in their diets belonging to primarily reef-originating
families (for details see text under ‘“‘Feeding Zones ---”’, and Appendix 3)
Number of ‘bird days’ Percentage of identified
Mean length of of observations on fish designated as
Species shifts observed* incubation shifts reef-originating
Phaethon rubricauda 6 days 174 O>
Puffinus nativitatis 43 days 9 3
Pterodroma alba 5 days 36 No information
Sterna fuscata 7 days 69 4 2
Anous stolidus No information 0 33
Gygis alba 3 days 31 34°
Anous tenuirostris 17 $ hours 314 56
Procelsterna cerulea 20 hours 14 5
NOTES FOR TABLE 7:
a. Calculated by summating the periods of observations at all the nests and dividing by the
total number of change-overs recorded. Nests were inspected at 0700 hrs, 1300 hrs,
and 1900 hrs each day.
b. Diodontidae and Tetraodontidae omitted: see text.
c. Some Blenniidae omitted: see text.
distances to their feeding grounds from the nearest available breeding locality.
However, selection for shifts lasting several days will be strong, even if the
feeding grounds are only a relatively short distance away, if the food there is
patchy in distribution or sometimes unavailable (for instance during storms).
The longer a fishing trip is, the less likely it is to be unproductive as a result of
bad luck in searching for food, or of short-term fluctuation in its availability.
This factor will be important in the evolution of shifts of a particular modal
length, since the off-duty bird cannot return until it has built up sufficient re-
serves to last through the subsequent shift. If it fails to obtain enough food dur-
ing the period of the normal shift, and so does not return at the expected time,
its mate is likely to desert. This has been observed, for example, by Vogt (1942,
reprinted 1964) in Phalacrocorax bourgainvillit and by Dorward (1962) in Sula
dactylatra. In burrow-nesting petrels, eggs are sometimes left unattended for
periods of a few days during incubation, but are brooded again when an adult
returns, and eventually hatch (Davis 1957, Warham 1964). However, in sur-
face-nesting birds, unattended eggs are usually quickly predated or the embryo
is killed by extremes of temperature.
Since birds which utilize a patchy or unreliable food supply must anyhow be
capable of fasting for considerable periods, the development of long shifts prob-
ably does not present physiological problems requiring extensive special adap-
tations. However, it should be noted that in at least some of the species in-
volved (for instance, S. fuscata) incubating birds leave the egg at intervals to
drink sea water. The flexibility of the length of incubation shifts is emphasized
by the large differences sometimes found between different populations of
single species, which are evidently related to differences in the characteristics of
the food supply (this point is further treated in the discussion).
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 63
In the period when the adults are feeding a chick, the situation is rather dif-
ferent. When away from the colony fishing, the adults no longer need to build
up their reserves for a long fast, but can return to the colony as soon as they
have satisfied their immediate needs and have obtained a full load of food for
their chick. Unfortunately we have no data on the frequency of feeding of the
chicks by the adults in the species concerned; however, it is fairly certain that
the adults return to the island more frequently when they are feeding chicks
than when they are incubating. Even in the species with very long incubation
shifts, it is probable that the chick normally receives food from one of its parents
about every two or three days, and in G. alba, A. tenutrostris and Pr. cerulea
the chick is probably often fed more than once a day.
It is clear that the Christmas Island sea birds, which have such long incuba-
tion shifts, could be foraging at enormous distances from the island even
when incubating. To take the most extreme example, if it is assumed that S.
fuscata flies at 30 miles per hour, and that flight continues throughout the night,
a seven-day incubation shift would enable an offduty bird to make a one-day
flight to a feeding area 700 miles away, followed by five days searching for and
catching food, and building up reserves for the subsequent fast, and then to re-
turn in one more day. Even though the birds doubtless normally feed closer
than this, the long shifts could carry a selective advantage as an insurance policy,
as discussed above.
The use of information on the relative proportions of reef-originating and
pelagic fish in the diets, in assessing the feeding zones of the different bird
species, was suggested by the work of Nakamura (1965) on the feeding of Skipjack
in the area of the Marquesas and Tuamotu Islands. Nakamura divided the
fish families (and also the other groups of prey animals) represented in the diets
of Skipjack into a group which may be considered primarily reef-originating,
in that they spend their adult life on reefs or in other non-pelagic areas (even
though their larval or juvenile stages are often pelagic), and a group which
are pelagic as adults. Separating the Skipjack into those caught within 75 miles
of points roughly in the center of the island groups, and those caught between
75 and 150 miles and between 150 and 225 miles out, Nakamura showed that
the percentages of reef-originating forms in the stomachs were much lower in
the areas far from the islands (respectively 61.5, 39.9 and 8.8%). We have under-
taken a similar analysis of the diets of the birds, but considering only the fish
portion of the diet. The fish families designated as primarily reef-originating
are marked with an asterisk in Appendices 3 and 5. These designations are taken
mainly from Nakamura’s Table 2, while Dr. Donald Strasburg has assisted us
in assigning the families not represented there. Diodontidae and Tetraodon-
tidae have been omitted from the calculations, since those taken by Ph. rubri-
cauda and S. fuscata may well have been pelagic forms, although most members
of these families are reef-originating. Among the Blenniidae we have consid-
ered Cirripectus sp. as reef-originating, but have omitted the other species of
Blenniidae which occurred only in G. alba, as these are at least sometimes pe-
lagic (see Species Accounts).
In Table 7 are given the percentages (by number) of fish in the diets of the
various birds which belonged to reef-originating families. The low incidence of
64 PEABODY MUSEUM BULLETIN 24
reef-originating forms in Ph. rubricauda, P. nativitatis and S. fuscata is note-
worthy, while A. tenuzrostris eats largely reef-originating forms. and A. stolidus
and G. alba are intermediate. The very low percentage of reef-originating fish in
the diet of Pr. cerulea is due mainly to the large numbers of minute Gempyli-
dae in its diet: direct observations on the feeding of this species showed that it
must be obtaining them very close to the island. Although squid were not con-
sidered in this analysis, it is of interest that since Symplectoteuthis spp. are
pelagic rather than reef-originating, the low proportion of squid in the diet of
A. tenuirostris must also reflect the fact that this species feeds very largely close
to land. Finally, it may be mentioned that if the fish portion of the diet of the
Yellowfin Tuna caught within ten miles of land in the Line Islands is treated in
the same way as that of the birds (but omitting all Blenniidae) it is found that
95% of the fish are from reef-originating families. The Yellowfin stomachs in
question contained an exceptionally high proportion of the reef-originating
Acanthuridae, but even if these are omitted more than two thirds of the remain-
ing fish are from reef-originating families.
Using both the scanty direct evidence and the indirect evidence from the
length of the incubation shifts and the proportions of reef-originating and
pelagic fish in the diets, it seems worthwhile to define as far as possible the feed-
ing zones (in relation to distance from Christmas Island) utilized by the different
bird species.
We never saw Ph. rubricauda fishing close to land and suspected that they
were foraging far out to sea. Similarly, Murphy, Bailey and Niedrach (1954) say
that the feeding range of this species “is, for the most part, much farther from
shore than that of the red-footed booby.” However, Gibson-Hill (1947) several
times saw Ph. rubricauda feeding in the afternoon close to Christmas Island
(Indian Ocean). He did not obtain information on the incubation shifts, but on
Christmas Island in the Pacific they last about six days, which would clearly
permit individuals to travel great distances from the island even while breed-
ing. That they do not normally feed close to the island is also suggested by the
fact that reef-originating fish families are not represented in their diet, except by
Tetraodontidae and Diodontidae, which include some pelagic species, as al-
ready mentioned. Outside the breeding season tropic-birds in general are truly
pelagic (Jesperson 1929; Murphy 1936: 91, 799; Baker 1947), and clearly de not
need to come to land to roost. It also appears that they feed individually rather
than in flocks, and our evidence from the food of Ph. rubricauda suggests that
they feed on dispersed prey. We may therefore conclude, provisionally, that Ph.
rubricauda scatter over the ocean around Christmas Island in search of their
food, probably exploiting areas where flying fish and other surface-dwelling fish
and squid are especially abundant, but not necessarily feeding in association
with other birds or with schooling fish.
P. nativitatis and Pt. alba appear to have incubation shifts of about five days,
although we have few data for the first of these species. ‘There are no indica-
tions that they feed especially close to shore (we never saw them feeding), and
they probably travel to feeding grounds several hundred miles away. In P. na-
tivitatis, only 3% of the identified fish in the diet were from families designated
as reef-originating (Table 7). Observations by Bruyns (1965) showed that in
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 65
November 1960 both P. nativitatis and Pt. alba were common in the Countercur-
rent at about 7° N., in the area north of Christmas Island. Bruyns comments that
P. nativitatis were not seen more than 250 miles from land, whereas Pt. alba
were seen at much greater distances from the nearest breeding grounds. Although
it cannot be shown that the birds seen furthest from land are involved in
breeding, the advanced state of digestion of the samples which we obtained
from Pt. alba suggests that they travel great distances even when breeding. Other
species of Pterodroma apparently also travel considerable distances from their
breeding grounds to feed; for instance, Falla (1934) says that in northern New
Zealand Pt. macroptera is rarely seen within fifty miles of the coast during the
day, although considerable numbers breed in the area.
The two large terns, S. fuscata and A. stolidus, are so similar in size and diet
that they merit careful comparison. It seems certain that S. fuscata often feeds
very far from land, even when breeding. Its incubation shifts on Christmas Is-
land averaged seven days, which is a little longer than on Ascension Island, and
only 9% of the identified fish in its diet were from reef-originating families (Ta-
ble 7). This species was not seen feeding immediately offshore, although in-
dividuals were seen flying past feeding flocks of other species of terns. In A. sto-
lidus, more of the identified fish (33%: Table 7) were from reef-originating
families, but we unfortunately have no data on the length of the incubation
shifts on either Christmas Island or Ascension Island. The only colonies for which
information is available are Christmas Island (Indian Ocean), where Gibson-
Hill (1951) said that the shifts were normally short, the birds sometimes mak-
ing as many as five changes in the course of a day, and the Dry Tortugas, where
the shifts average less than five hours (data in Watson 1908). Although in the
Tortugas colony S. fuscata has much shorter shifts than elsewhere (a little
more than 24 hours—Watson), they are still much longer than those of A. stoli-
dus, and there is probably a difference of similar proportions elsewhere. (See
Discussion on relations between these species in the Tortugas.) A. stolidus was
not observed feeding in the area within about three miles of the coast of
Christmas Island which was favored by small noddies, but since the popula-
tion of A. stolidus is small this might have been due to chance. At Onotoa Atoll,
Gilbert Islands, Moul (1954) frequently saw this species feeding close to the
shore, alongside A. tenuirostris. Evidence from other areas shows that in gen-
eral A. stolidus feed closer to land than S. fuscata. Data from the central Pacific
obtained recently during the “at-sea” work of the Pacific Ocean Biological Sur-
vey Program, Smithsonian Institution, support this view, but show that S.
fuscata also sometimes feed close to shore (P. J. Gould, pers. comm.). In the
area of Oahu (Hawaii) where there are large colonies of both S. fuscata and
A. stolidus, N. P. A. saw none of the former species, but many of the latter, feed-
ing over fish schools within a few miles of the island during a cruise on the
“Charles H. Gilbert” during April 1963. This observation conforms to the experi-
ence of Royce and Otsu (1955) during six cruises in the area of the Hawaiian
Islands in 1953. They found that A. stolidus were more abundant near the is-
lands, while S. fuscata ranged as far as the vessel searched, which was up to
350 miles from Oahu. Similarly, Murphy (1936: 1154) quotes the notebooks of
R. H. Beck to the effect that he found A. stolidus feeding regularly as far as 50
66 PEABODY MUSEUM BULLETIN 24
km from their homes, but S. fuscata as far as 300 km. Again, Ridley and
Percy (1958) comment that in the Seychelles (Indian Ocean) A. stolidus seem to
fish much closer to land than S. fuscata, while Bailey (1965) found that in the
northern part of the Indian Ocean in March and April, S. fuscata was the com-
monest bird at sea, while noddies were very rarely recorded more than fifty
miles from their breeding islands.
It therefore seems reasonable to conclude that the Christmas Island popula-
tion of S. fuscata range up to several hundred miles from the island, doubtless
feeding mainly in the Countercurrent (cf. Bruyns 1965), but that A. stolidus
feeds closer to the island, although not commonly as close to land as A. tenutros-
tris and Pr. cerulea.
The next species, G. alba, has incubation shifts lasting on average about
three days on Christmas Island, which is about the same as on Ascension Island
(Dorward 1963). This species is thus intermediate between S. fuscata and the two
small noddies which change over about once each day. The proportion of iden-
tified fish in the diet which were from reef-originating families is also intermedi-
ate, being 34% (Table 7). An incubation shift of three days would easily permit
the off-duty bird to feed in the region of the Countercurrent. It is of interest in
this connection that although birds can be found breeding on Christmas Island at
any time of the year, banded individuals which had finished breeding were not
seen on the island for several months; during this absence they underwent a com-
plete molt (Ashmole, in press). It seems likely that after completing their breed-
ing activities they migrate away from the island to be closer to the best feeding
grounds, and they may even spend this time at sea. Although it should be men-
tioned that Baker (1951) was of the opinion that outside the breeding period,
G. alba was less pelagic in its habits than A. stolidus, Bruyns (1965) records some
individuals several hundred miles from land in the Countercurrent, and the
Pacific Ocean Biological Survey Program have comparable records (Gould, pers.
comm.). Observations on the feeding of G. alba, and the form of the legs and
feet, suggest that it does not normally rest on the water. Any opportunity should
be taken of performing experiments similar to those of Watson (in Watson and
Lashley 1915) on A stolidus and S. fuscata, to determine whether G. alba can
rest on the water without becoming waterlogged. We suspect that this species
will prove to be capable—like S. fuscata—of spending indefinite periods in the
air, Over its oceanic feeding grounds. On the other hand, individuals feeding
chicks may obtain most of their food close to the colony; as already noted, mem-
bers of this species were seen fishing within a few miles of the coast at dawn, and
the food for the young is carried back in the bill, suggesting that it is generally
caught within a few hours’ flight of the island (see also Gibson-Hill 1950). How-
ever, few G. alba were seen fishing with the two small noddies during the day,
within about three miles of Christmas Island.
A. tenuirostris and Pr. cerulea can be treated together, since they appear to
exploit very similar feeding zones. Both have incubation shifts averaging a little
less than one day, indicating that each member of the pair normally fishes for
one day, and then returns to relieve its mate. In fact, the conspicuous evening ar-
rivals of these species at the colonies, and the steady departures in the morning,
suggest that they nearly always return to the island at night. In keeping with this,
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 67
both these species are seen commonly feeding within a few miles of the island
during the day. In A. tenwirostris 56% of the identified fish were from reef-
originating families, a figure much higher than in any of the other birds (Table
7). In Pr. cerulea, however, only 5% of the identified fish were from reef-
originating families, although this species certainly feeds in roughly the same
zone as A. tenutrostris; tiny Gempylidae were of great importance in its diet,
while fair numbers of larval Scombridae and small Exocoetidae were also eaten.
This discrepancy is probably related to the very small size of the organisms
taken by Pr. cerulea: it appears that this species, with its small size, short bill, and
habit of staying very close to the surface while feeding, rather than always making
energy-consuming swoops from a height, has the ability to exploit many of the
smaller animals of the neuston (i.e., organisms floating or swimming in surface
water or inhabiting the surface film: see David 1965). All three of the major con-
stituents of the diet of Pr. cerulea—Halobates, pontellid copepods and very small
fish larvae—appear in David’s short list of the organisms most commonly oc-
curring in hauls of the “Neuston net” in the Indian Ocean. The larger birds
studied—with the partial exception of A. tenuirostris—evidently cannot economi-
cally catch the smaller animals of the neuston, and are more dependent on pred-
atory fish to drive larger prey to the surface. Storm petrels and phalaropes,
however, are examples of other avian exploiters of the neuston. It may well be
that for the two small noddies the generally calm waters in the lee of Christmas
Island at the western end are especially favorable feeding areas. It is doubtless
significant that Bruyns (1965) failed to see either of these species (or A. stolidus)
in the Countercurrent north of Christmas Island, although S. fuscata were com-
mon there. There are indications that other populations of A. tenuirostris also
feed mainly close to land. For instance, Morris (1963) found that in the Gilbert
Islands the large flocks of noddies, which consisted mainly of this species, were
usually near the reefs but sometimes as far as 50 miles from land.
Before leaving the subject of feeding zones, it is worth considering a few of
the special problems faced by birds feeding at great distances from the island. It
is clear that for such birds it will be especially important to be able to carry a
large load of food for the chick, because the length of the time required for
travelling will make it uneconomic to visit the colony frequently. It is thus of
interest to find that S. fuscata, which had the longest incubation shifts and were
probably feeding at great distances, were capable of arriving back at the colony
with a load representing about one fifth of their total weight (Table 2). The
loads brought back by S. fuscata, in addition to being relatively larger than in any
of the other species, were also in strikingly good condition (Table 2), raising the
question as to whether this and other sea birds feeding far from their breeding
colonies may have mechanisms for retarding digestion of food intended for the
young. This problem was discussed briefly by Murphy (1936: 660) and also by
Dorward (1962) in relation to tropical boobies (Sula spp.), but it does not seem
to have been directly investigated. In S. fuscata, it is possibly relevant that the
regurgitations given to the young are often accompanied by a conspicuous
68 PEABODY MUSEUM BULLETIN 24
amount of mucus, which presumably could be specialized for retarding digestion.
Since digestion of fish by birds is generally rapid’ it does appear that in the ab-
sence of some mechanism for retarding it, the foraging range of a bird collecting
food for its young might be limited by the need to get back to the colony before
too great a proportion of the load was digested.
In striking contrast with S. fuscata, the samples from Pt. alba were small in
volume relative to body weight (Table 2). However, in addition to the items
which were collected and from which the volumes of the samples were calcu-
lated, the samples from this species often contained considerable quantities of
oil, which could not all be collected. It is also relevant that the food items were
nearly all in very poor condition, and that isolated squid beaks and lenses were
often found (Table 2). The presence of oil in many of the samples indicates that
Pt. alba, like many other petrels, has the ability to secrete stomach oil. Further-
more, the advanced state of digestion of most of the food items, and the fact that
oil was obtained in quantity both from adults which had chicks, and from
chicks, suggests that the secretion of stomach oil is an adaptation connected with
foraging far from the colony.
Matthews (1949) reviewed available information on the chemical composition
of the oil, and presented circumstantial evidence that it is a secretion of the
proventriculus. He discussed in detail the various hypotheses as to the functions
of stomach oil, but came to no definite conclusion. On the other hand, Rice and
Kenyon (1962) presented evidence that in albatrosses the oil serves as a food for
the young, and suggested that this is its primary function also in petrels and
shearwaters. Previously, this possibility had sometimes been discounted on the
grounds that the oil does not contain appreciable quantities of protein (Carter
and Malcolm 1927, Murphy 1936: 473). However, Kritzler (1948) suggested that
the proteins requisite for differentiation and growth could be supplied in the
form of semidigested material regurgitated with the oil, while the oil could pro-
vide sufficient energy for growth, as well as for survival.
Since stomach oil is given by adults to chicks, it seems reasonable to suppose
that it functions as a food for the young, and its widespread occurrence in the
Procellariiformes is explicable on the basis that many members of this group
have to collect food at great distances from their breeding places. A mechanism
for retarding digestion of food to be given to the chick would be an alternative
adaptation, but it would have the disadvantage of requiring the adult to carry
back to the colony the intact food, containing a large percentage of water. On the
other hand, by digesting food as it is caught—and excreting excess water—
throughout the period until they return to feed the chick, the birds are pre-
sumably able to build up reserves which can later be secreted as stomach oil and
transferred to the chick, together with those food items which are not yet entirely
digested. Although we know of no measurements of the calorific value of petrel
stomach oil, it seems likely that it is somewhere between five and ten times that
3 F. Ward (1914, quoted by Harris 1965) found that Larus marinus had fully digested a five-
inch fish in three hours. Skokova (1963), in a study of birds feeding on fresh water fish, records
fish being three-quarters digested after 8 hours. Van Dobben (1952) found that it took 15 hours
for Phalacrocorax carbo to digest a large fish, while Bowmaker (1963) found that P. africanus
took about three hours to digest a meal early in the day and five hours for later meals.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 69
of whole fish or squid (see data in Arimoto 1962). Since there must be, for each
species, a critical limit to the weight of the load of food which can be brought
back to the chick, the ability to carry food for the chick in the form of a lipid re-
serve represents an important adaptation to foraging far from the colony while
breeding.
Since in chicks fed largely on stomach oil the rate of differentiation is likely
to be limited by the low intake of essential amino acids, the tendency for mem-
bers of the Procellariiformes to have extremely long fledging periods is an ex-
pected correlation. Similarly, the fact that petrel chicks often become enormously
fat suggests a tendency for the supply of lipids to outrun that of amino acids.
However, these lipid reserves accumulated by chicks (both in the alimentary
tract and elsewhere in the body) are themselves important safeguards against
starvation in unusually long intervals between successive feedings: the ability of
young petrels to survive for long periods without food is well documented (e.g.,
Richdale 1945). This ability probably depends on the fact that when they are
fed, the chicks are given large meals of unusually high nutritive value. It seems
inevitable that a chick given a meal of fresh fish or squid (of which about 75% by
weight will be water—Arimoto 1962), and then starved, would survive for a
much shorter period than a chick given the same quantity of stomach oil. Thus
the secretion of stomach oil by adults may probably be regarded as an important
part of the adaptation of many Procellariiformes to infrequent feeding of the
chick, and hence to exploiting food sources at great distances from the breeding
grounds.
Although it seems almost certain that the prime function of stomach oil is as a
food for the young, the ability to accumulate oil in the digestive tract may some-
times be of value to the adults themselves, as are the reserves of subcutaneous
and peritoneal fat deposited by many birds (including Procellariiformes). A
point which is relevant in this connection is that Kritzler (1948) reported that
his Fulmars (Fulmarus glacialis) accumulated “prodigious deposits of sub-
cutaneous and visceral fat” after being fed on a diet of hog tissues supplemented
with additional lard. It may be significant that the individual from which Kritz-
ler obtained his samples of stomach oil first regurgitated oil in March, about a
month after its capture, suggesting that this nonbreeding bird may not have ac-
cumulated stomach oil until after it had laid down large fat deposits in its tis-
sues.
The hypothesis that stomach oil is primarily a reserve food supply which is
fed to chicks by their parents does not conflict with the generally accepted view
that in many Procellariiformes the ‘spitting’ of foul-smelling oil (especially by
chicks) is an important adaptation for defence against predators (see, for in-
stance, Warham 1964). However, it seems most probable that this use of the
oil, and also its employment in preening and during courtship (Fisher 1952), is
evolutionarily secondary to its nutritional function.
While this paper was in press Lewis (1966) published the results of a study
showing that glyceryl ethers are major constituents of the stomach oil of Leach’s
Petrels (Oceanodroma leucorhoa). Lewis also analysed representatives of animal
groups eaten by Procellariiformes, and found that anchovies (Engraulis mor-
dax), squid (Loligo sp.), shrimp (Peneus sp.) and zooplankton all contained ap-
70 PEABODY MUSEUM BULLETIN 24
preciable quantities of phosphorylated glyceryl ethers. Lewis discussed the possi-
ble function of petrel stomach oil, and inclined to the view that it is an excretory
product. However, he recognized that a role in the nutrition of the young is the
major alternative possibility, and we see no reason to change our conclusion
that the secretion of stomach oil is primarily a nutritional adaptation.
FEEDING METHODs, AND ASSOCIATED STRUCTURAL ADAPTATIONS
Since all the bird species included in this study depend upon food at or close
to the surface of the sea, it is of interest to compare their feeding methods, and to
consider the associated structural adaptations. To aid in this comparison, various
dimensions of the species are presented in Table 8, and their bills are shown in
Fig. 6, while feeding methods are sketched in Fig. 7.
In Figure 7 we have divided feeding methods into those in which the bird re-
mains airborne and those in which it does not. The first group includes two types
of Dipping: prey actually in the air may be captured without contact of the bird
with the water surface (Air Dipping), while if the prey is at or just below the
surface there is brief contact of the bird’s bill with the water (Contact Dipping),
but forward flight does not stop. Some birds obtaining food by Contact Dipping
may push off with their feet, and this action thus grades into Pattering, in
which the feet make frequent contact with the water; this is a method used by
many avian plankton feeders which need to maintain themselves at a roughly
constant distance above the surface, even in fairly rough water. Some species (es-
pecially the noddies) also Hover, generally close to the surface; their feet may or
may not come into contact with the water, the essential features being that for-
ward motion more or less stops, and that the body weight is supported princi-
pally by the rapidly beating wings; objects are then picked from the surface or
just above it. In the second group we distinguish Plunge to Surface, in which
the bird splashes into the water but does not normally submerge fully and takes
off again immediately, from Air Dive, in which the bird disappears below the
water surface and reappears only after an appreciable interval. Air Dives may
probably be subdivided into those in which the impetus of the dive is used to
reach the prey, and those in which there is a pursuit by swimming. Surface Dives
are those made by birds which are swimming at the surface before they sub-
merge; they always involve swimming pursuit of the prey. Finally, we have the
heterogeneous category of Feeding on Surface. Although our terminology is not
intended to be exhaustive, it is hoped that it may help in describing more pre-
cisely the feeding behavior of sea birds.
We did not observe the feeding methods of Ph. rubricauda, but Gibson-Hill
(1947) said that the birds dive from a height of 20-40 feet, dropping with half
folded wings into the water (Air Dive, Fig. 7). One bird which he watched re-
mained submerged for an average of 26.6 [sic] seconds in ten consecutive dives.
Gibson-Hill commented on the shortness of these periods, but it seems that
tropic-birds often spend much less time under water. For instance, Bailey
(1966) recorded that Ph. aethereus feeding in opaque water in the Indian Ocean
remained submerged for less than a second. It is not certainly known whether
tropic-birds pursue their prey under water or whether they rely on the impetus of
the dive for capture. However, the lack of streamlining of the tarsometatarsus
Pterodroma alba“
Anous stolidus
Puffinus
nativitatis
Procelsterna
cerulea
Phaethon rubricauda
FIGURE 6. Bills of the sea birds studied on Christmas Island: natural size photographs
of specimens preserved in alcohol.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS ae
(Ph. rubricauda has min. lateral width 7.7 mm., ant.-post. 6.5 mm.)* supports the
later alternative and suggests that the webbed feet may be important mainly for
steering and for taking off from the surface; they are also of use during flight, es-
pecially in landing, when they clearly function as flaps. Stonehouse (1962b)
suggested that tropic-birds catch some of their prey—for instance Exocoetidae—
on the wing (Dipping, Fig. 7); however, there is still no direct evidence support-
ing this idea.
The great strength of the bill of Ph. rubricauda is presumably connected with
the ability of this species to catch fish which are very large, both absolutely and
relative to body weight, including, for instance, Coryphaenidae between 20 and
30 cm long. However, it is also relevant that tropic-birds frequently engage in
fighting for nest sites, in which the bills of the contestants are interlocked and
subjected to considerable stresses (Stonehouse 1962b). That the bill of Ph. rubri-
cauda is not unnecessarily strong was made evident by the discovery on Cook
Island of an adult in which the distal third of the upper mandible had been
snapped off cleanly. The injury was quite recent (still bleeding slightly) and the
bird appeared healthy, was of normal weight and was brooding its chick. It
FEEDING WHILE FLYING
DIPPING PATTERING HOVERING
Air Dipping Contact Dipping
—> — rc
FEEDING WITH CESSATION OF FLIGHT
PLUNGING TO SURFACE FEEDING ON SURFACE
NVA
SN ee
—-
DIVING
Surface Dive Air Dive
followed by pursuit followed by direct to
pursuit prey
YC NZ
<— P—>
Sree
FIGURE 7. Feeding methods employed by the sea birds studied. See text for explanation.
4 Measurements of this and the tarsometatarsi of the two Procellariiformes were made on
single spirit specimens from Christmas Island.
PEABODY MUSEUM BULLETIN 24
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74 PEABODY MUSEUM BULLETIN 24
seemed most likely that this accident occurred at sea, since nest sites were abun-
dant on Cook Island and there was little fighting for them, but other causes
cannot be excluded. Also worth mentioning is the enormous gape of this and
other tropic-birds, which is one of the adaptations which enables them to exploit
prey of very large size relative to their body weight. The large gape must also
be critical in eating Diodontidae (porcupine fish), whose protective adaptations
make them especially difficult to swallow.
There are no indications that tropic-birds feed at night, but from observations
on their diurnal rhythms, several observers have concluded that they obtain
most of their food in the period immediately after daybreak (see Murphy 1936;
Gibson-Hill 1947).
We know of no published information on the feeding habits of P. nativitatis
(it seems possible that Anderson [1954] did not distinguish P. pacificus and
P. nativitatis). However, there are a number of accounts of the feeding of other
members of the genus Puffinus. They either Feed at Surface, or make Surface
Dives, or fly low over the water (sometimes Pattering with their feet), and then
Plunge to Surface or make Air Dives with the wings partly open. While swim-
ming under water they use their wings as well as their feet. During the Pacific
Ocean Biological Survey Program of the Smithsonian Institution, P. pacificus
have also been observed to chase and catch flying fish in mid-air (Gould, pers.
comm.).
The various species of Puffinus differ in the extent of their adaptations for
swimming and diving, and P. nativitatis is among the species most highly adapted
for aquatic life (Kuroda 1954). However, all of them contrast with Pterodroma
spp., which have quite different adaptations. The bill of P. natzvitatts is a little
longer and less deep than that of Pt. alba, and the terminal hook characteristic
of all Procellariiformes is less developed. However, the bill of P. nativitatis is ac-
tually more like those of Pterodroma species than are the bills of most other
members of the genus Puffinus. The legs and feet of P. nativitatis show the
adaptations for fast swimming emphasized by Kuroda; the tarsometatarsus is
robust but well streamlined (min. lat. width 2.8 mm., ant.-post. 7.3 mm.), while
the long toes encompass a large area of webbing (Table 8), but fold into a nar-
row lateral space for the forward stroke. As in other diving shearwaters (Ku-
roda 1954), the plumage of P. nativitatis is extremely compact, helping to give
the bird the high specific gravity necessary in birds which need to be able to sub-
merge easily (Storer 1960).
Pt. alba lacks these specializations for feeding by high-speed underwater swim-
ming. Most conspicuous is the difference in the legs and feet. The tarsi are
slender and not streamlined (min. lat. width 3.3 mm., ant.-post. 4.5 mm.), while
the toes are widespread and do not fold easily into a streamlined form. How-
ever, the webs are well developed and are doubtless important in take-off, and
probably also in holding the body off the water during feeding by Hovering.
The bill is short, deep, and powerful, while the tip of the upper mandible is
sharply decurved into a massive hook. As might be expected from the form of
the bill, Pt. alba can exert considerable force at the bill tip. ‘This species thus ap-
pears to be adapted especially for cutting and tearing its food, and this may
explain the appearance in our samples of several arms and eye lenses from
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS aS
squid larger than the bird could possibly eat whole. It is conceivable—though
improbable—that the arms were cut off living squid, but the large eye lenses
were doubtless obtained from dead or moribund animals. It is worth mentioning
that Pt. alba (and other members of the genus) have exceptionally soft and
loose plumage, which could perhaps be useful in making it difficult for living
squid to get a grip on the bird.
It is clear from a number of accounts in the literature that large dead or dying
squid are sometimes available in the open ocean. For instance, Murphy (1936:
487) wrote that “Both the shearwaters and the Pterodroma petrels occasionally
‘stand’ on the water, sustained by rapidly beating wings, while they feed upon
large and heavy objects such as the bodies of squids or fish.” Similarly Collins
(1899) mentioned the occurrence of dead giant squid in the North Atlantic in
1875, and said that the tentacles were usually eaten by Great Shearwaters (Puf-
finus gravis). Voss and Voss (1962) have described a new species of squid in the
genus Calliteuthis on the basis of a series of specimens found floating on the
surface—either dead or dying—over a period of many years: all were also muti-
lated, showing signs of having been fed upon by predators. Furthermore, Mal-
colm R. Clarke informed us (pers. comm.) that he has seen dead squid floating
at the surface on a number of occasions during oceanographic cruises. The fairly
frequent occurrence of dead or dying squid on beaches (see section on food size
under Pt. alba in the Species Accounts), also suggests that they may be available
with some regularity far from land. Relevant in this context is the work on
Loligo opalescens by Fields (1965), who assembled impressive evidence that in
this species of squid both sexes die after spawning, and quotes observations of
large numbers of sea birds (Puffinus sp. and Larus sp.) in Monterey Bay feeding
on concentrations of squid debilitated by the spawning process. If a significant
number of other species of squid also die after spawning, this would largely ex-
plain the occurrence of dead or dying squid at sea, and would suggest that such
squid must provide an important food source for sea birds. Among the species
which we studied, however, only Pt. alba showed evidence of feeding on dead or
dying squid. That Pterodroma spp. also sometimes feed on large dead fish is in-
dicated both by Murphy’s statement, quoted above, and by Kuroda’s (1955) ob-
servation of two Pt. inexpectata feeding on the carcass of a dead pollack in the
North Pacific. However, we detected no evidence of this in the regurgitations
from Pt. alba, which were generally largely digested.
Nevertheless, it must not be forgotten that gadfly petrels also eat many small
fish and squid which they must catch alive, while Pt. alba also obtains substan-
tial numbers of marine water striders. There seem to be no accounts in the lit-
erature of the feeding of Pt. alba, but the staff of the Pacific Ocean Biological
Survey Program have observed the feeding of some other gadfly petrels (es-
pecially Pt. externa); Gould (pers. comm.) said that “they are much more prone
to ‘Contact Dipping’ [Fig. 7] than the shearwaters and spend much less time in
contact with the water; like the shearwaters, they have been observed to chase
and catch flying-fish in mid-air [Air Dipping] and they spend a great deal of time
in pursuit of such prey.” The available evidence (see Kuroda 1954) indicates
that the gadfly petrels are extremely efficient fliers, their high-aspect-ratio
wings making them well adapted to traveling long distances with a minimum of
76 PEABODY MUSEUM BULLETIN 24
effort (Savile 1957). This flight efficiency, together with great skill in Dipping,
probably accounts for the fact that it is evidently economic for Pt. alba to catch
such minute prey as Halobates, which are not utilized by the terns of com-
parable size. At the same time, however, their economic flight (and strong cut-
ting bills) enables Pterodroma spp. to employ another specialized kind of
foraging behavior, discussed above, searching for and eating large floating ob-
jects such as dead squid, which are very thinly scattered over the surface of the
ocean.
Although we have no direct evidence, it may well be that Pt. alba, like some
other tubinares (cf. Murphy 1936: 486) feeds to some extent at night or just be-
fore dawn. It may be relevant that the Galapagos Swallow-tailed Gull (Larus
furcatus), which feeds at night (Hailman 1964), resembles Pt. alba in feeding very
largely on squid, and—also like Pt. alba—is recorded as taking marine water
striders (Murphy 1936: 1088).
Little detailed information is available on the feeding methods of the five
tern species, but the general accounts in the literature (e.g., Murphy 1936; As-
cension Island papers in [bis 103b, 1962-63; Anderson 1954; Moul 1954), to-
gether with our own observations on some species, permit certain comparisons to
be made. As far as we are aware none of these terns normally submerge com-
pletely, so that prey animals are available only if they are within a few inches
of the sea surface. Prey may be caught when they have jumped clear of the water
in attempts to escape marine predators, or they may be taken at the surface or
just below it. It appears that the various terns under consideration use the
methods of Air Dipping, Contact Dipping, Pattering, Hovering, and Plunging
to Surface with different frequencies, although probably none of them use one
method to the exclusion of the others.
As would be predicted from the general similarity of the feeding methods of
these five terns, their bills show a number of common features (Fig. 6 and Table
8). All are slender, more or less straight, and laterally compressed, especially
near the tip, in a manner which must minimize water resistance when the bill
penetrates the surface in the process of fishing by Contact Dipping. Further-
more, the bills of four out of the five species are of very similar length; this is
considered further in the Discussion.
The literature suggests that S. fuscata most often feed by Dipping (summary
in Ashmole 1963b). Probably both Air Dipping and Contact Dipping are
used, but it is so difficult to distinguish these actions in the field that very critical
observations will be needed to determine which is the more frequent. Watson
and Lashley (1915) mentioned only one observation of Plunging to Surface by
S. fuscata, Dipping being the normal feeding method, but during the Pacific
Ocean Biological Survey Program Plunging to Surface has also often been ob-
served (Gould, pers. comm.). However, there is no evidence that this species
ever uses its feet to maintain distance from the surface; this is consistent with the
fact that the webbing on the feet has an enormously smaller area than in the
noddies, which use their feet extensively during feeding (Table 8). Also of inter-
est in this connection is Watson and Lashley’s (1915) experimental proof that
while A. stolidus can rest on the sea overnight without harm, S. fuscata become
waterlogged in as little as 25 minutes. It is unexpected to find that a sea bird
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS iy |
which is adapted to feeding in the open ocean and which can remain away from
land for months on end (Ashmole 1963b) should lack the waterproofing adapta-
tions which would enable it to rest on the sea. However, it is very possible that
the risk of predation by fish when resting on the sea is sufficient to make aerial
resting preferable for a species which can evolve the capability.
The available data thus indicate that S. fuscata feed on prey either in the air
or right at the surface, a situation which during the day is most commonly
achieved when predatory fish, especially tunas, chase small fish or squid to the
surface, where they sometimes even jump out of the water. However, S. fuscata
evidently also feed during twilight periods and sometimes even at night.
Bruyns and Voous (1965) recorded that an individual captured at sea in the
eastern Pacific regurgitated about six fresh Vinciguerria cf. lucetia (Garman)
—family Gonostomatidae—three hours after sunset. However, Gould (in press)
records what is apparently the first actual observation of S. fuscata feeding at
night. He encountered—and observed with the aid of a flood light—a feeding
flock of this species mixed with Puffinus pacificus, in the central Pacific; it was
just before midnight and there was a full moon.
A. stolidus apparently feed both by Dipping and Plunging to Surface, and
like the previous species, depend largely on the presence of predatory fish to
scare their prey to the surface. On Onotoa Atoll (Gilbert Islands) both A. stoli-
dus and A. tenuirostris were frequently seen feeding on an ebbing tide where
“They hovered low over the reef, darting about, dropping to pick their food from
the surface of the water or just below the surface, not diving and submerg-
ing... .” (Moul 1954). Off Oahu (Hawaii) N.P.A. observed A. stolidus feeding
over tuna schools in mixed flocks with A. tenuirostris and Puffinus pacificus. On
one occasion A. stolidus were fishing by Contact Dipping, attempting to catch
fish just below the surface, but on another occasion by Plunging to Surface. Wat-
son (1908) said that A. stolidus catch fish actually in the air (Air Dipping), and
they doubtless sometimes do this. Watson and Lashley (1915) also mentioned
that “The noddy [A. stolidus] steps on the water often, sometimes strikes it with
the breast, not in diving movements, but in those of pursuit.” It is thus clear
that A. stolidus uses its feet in the way A. tenuirostris and Pr. cerulea do, to
keep the body up off the surface during fishing; the extensive webbing of the feet
(Table 8) would be of value in this and also in take-off after Plunging to Sur-
face; in fact Watson (in Watson and Lashley 1915) remarked on the ease with
which A. stolidus gets off the surface. This species, apparently alone among the
terns studied, sometimes Feeds on Surface: Audubon (1835: 265) said that in
the Gulf of Mexico it “not only frequently alights on the sea, but swims about
on floating patches of the Gulf Weed, seizing on the small fry and little crabs
that are found among the branches of that plant, or immediately beneath
them.” The staff of the Pacific Ocean Biological Survey Program have also
observed this species sitting on the water and dabbling beneath the surface
(Gould, pers. comm.). The indications are that A. stolidus is primarily—if not
exclusively—a diurnal feeder; the main arrival of birds at the colony seems al-
ways to be at dusk, and we know of no observations of nocturnal fishing.
G. alba, considered at this stage because it is next in size, presents a contrast
with the following species—A. tenuirostris—since although it is very similar in
78 PEABODY MUSEUM BULLETIN 24
size, it differs in its coloration and the form of the bill and feet. Both the culmen
and the lower edge of the mandible are unusually straight, and the base of the
bill is rather deep. The feet are specialized for perching on branches and not
for swimming or pushing off from the water; they have long claws and very little
webbing, and the tarsi are very short (Table 8).
A few G. alba were sometimes seen with feeding flocks of A. tenuirostris and
Pr. cerulea just offshore from Christmas Island. Although there were no oppor-
tunities to watch their feeding behavior at close range, it was noted on one oc-
casion that while flying over a fish school they kept well above the noddies for
most of the time. Dorward (1963), describing G. alba fishing off Ascension Is-
land, said they “swooped very fast from a height of about 20 feet and seemed to
pick things from just above the surface without touching the water.” These
birds were evidently feeding by Air Dipping, which agrees with Murphy’s (1936)
statement that the species ‘feeds not by diving but by the amazingly rapid and
precise technique of catching little fishes in mid-air as they leap out.” Gibson-
Hill (1951) recorded that on the Cocos-Keeling Islands (Indian Ocean) G. alba
feeding on Stolephorus sp. (Engraulidae) obtain them “either by hovering
over still water and picking them from the surface, or by catching them when
they are driven into the air by the attacks of larger fish. I never saw the White
Tern dive properly.” Baker (1951: 181) made the statement that G. alba “al-
most certainly obtain food also on the islands as indicated by the presence of
insects in stomach contents; this is not surprising since the birds frequent wood-
land habitats.” Baker gave no identification of the insects, and they might
have been marine water striders, but it is also possible that G. alba sometimes
hawk for insects where these are abundant close to their breeding sites.
Several times during watches from the seaward side of Cook Island soon after
first light, G. alba were seen close to the limit of visibility (probably more
than one mile offshore), apparently fishing; they were not flocking closely to-
gethe~, as feeding noddies generally do, but were working as individuals or loose
groups, suggesting that they might not be feeding in association with a tuna
school. The timing of this activity is of great interest; although it was barely
light enough to read at 0700 (local time), by 0720 G. alba had already begun
flying in from the sea, some of them carrying food. S. fuscata could also be seen
coming in between 0700 and 0800, but the A. stolidus and A. tenuirostris seen dur-
ing this period were nearly all going out. The data on the occurrence of fish and
squid in samples obtained from G. alba at different times of day (Table 9) sug-
gest that early morning fishing may be largely for squid, while mid-day samples
produce mainly fish. Samples collected in the early part of the night again
show a preponderance of squid, and many of these were in excellent condition,
suggesting that they had been caught at dusk. In addition, Myctophidae and
Gonostomatidae—fish which are generally present at the surface only at night
(see section on the environment)—are more important in the diet of G. alba
than in those of the other terns. Although most were obtained from G. alba
in the early morning or at night, myctophids were also found (in good condition)
in samples collected at 1445 and 1700, and gonostomatids in one sample ob-
tained at 1145. Two other families of fish which are normally at considerable
depths during the day were represented—each by one individual—in the sam-
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 719
TABLE 9. Frequency of occurrence of fish and squid obtained from Gygis alba
adults at different times of day
LOCAL TIME
0700 0800 0900 1200 1800 2030
—0800 —0900 -—1200 -—1800 -—1930 —2400
Samples containing fish 2 4 22 6) 14 15
Samples containing squid 5 0) 3 3 3 25
NOTES FOR TABLE 9:
Samples collected before September 1963 are not included since the time of collection
was not always recorded.
Separation of the data according to whether the food was carried in the bill or regurgitated
has no appreciable effect on the relative frequency of fish and squid.
No samples were obtained between 1930 and 2030.
ples from G. alba: a member of the Astronesthidae was collected at 1830 (early
dusk) and a rather dried-up member of the Paralepididae at 2215. Similarly,
Dorward (1963) obtained a hatchet-fish (Sternoptyx, Sternoptychidae) and a
myctophid (Lampanyctus) from G. alba within about an hour of first light.
Comments by Strasburg (pers. comm.) on the habits of two members of the
Blenniidae (Aspidontus filamentosus and Runula tapeinosoma) which formed
part of the diet of G. alba but not of that of A. tenuirostris (see Species Ac-
counts) suggest that they too are more likely to be available at the surface at
night than during the day. Whereas A. filamentosus is usually and R. tapeino-
soma sometimes taken around nightlights at the surface, in the daytime the
former is generally found beneath floating objects, while the latter, although it
is a reef-dweller commonly seen by day, “does not live near the surface, but
hovers in midwater or near the bottom . . .” (Strasburg, pers. comm.). However,
some individuals of both species were obtained from G. alba during the mid-
dle of the day, although they might have been caught in the early morning.
It may thus be said that although G. alba certainly feeds during the middle of
the day, there is some evidence that it also feeds extensively in the half light of
dawn and dusk, exploiting some prey species that are not available to the nod-
dies. If fishing at this time is done without the intervention of tunas or other
predatory fish, as is suggested by the behavior of the birds, it could provide an
explanation of the difference in the color of the dark noddies and of G. alba.
G. C. Phillips (quoted by Tinbergen 1964) has obtained experimental evidence
that the white plumage of sea birds hunting fish from the air helps them to ap-
proach their prey more closely than if they were dark. It is reasonable to sup-
pose that selection for inconspicuousness from below will be more intense in a
species which sometimes hunts undisturbed prey, than in those like the noddies
which feed almost exclusively on animals which are already fleeing marine
predators, and so are in less of a position to take avoiding action when attacked
from the air. The pure white plumage of G. alba, and its extraordinarily trans-
lucent wings and tail, appear to be very efficient in rendering it inconspicuous
against the sky in dim light. An experimental comparison of the reactions of
80 PEABODY MUSEUM BULLETIN 24
fish to G. alba and to A. tenuirostris under different light conditions would be of
great interest.
In G. alba, the total absence of melanins from all parts of the remiges, which
is unusual even in species with generally white plumage, suggests that strong
selection is operating, since unpigmented feathers become abraded more rapidly
than pigmented ones. However, the unusual molt sequence of G. alba (Dor-
ward 1963, and Ashmole, in press) ensures that the old feathers in the wings are
always dispersed among the newer ones, thus minimizing the effects of abrasion.
Although we do not fully understand why the noddies have dark plumage, its
greater resistance to abrasion may well be significant, and there may also be se-
lection favoring coloration which renders an individual inconspicuous to other
sea birds—especially members of its own species—which are likely to compete
with it for available prey. Since the tropical ocean is normally very dark blue,
dark-colored birds are inconspicuous against it (Royce and Otsu 1955), though
conspicuous from it against the sky.
The evidence suggests that the fishing methods of A. tenuirostris are almost
identical to those of A. stolidus (see, for instance, Anderson 1954, Moul 1954,
Morris 1963, and sources given in Ashmole 1962). Morris gave an interesting ac-
count of the behavior of noddies in the Gilbert Islands, saying that large flocks,
mainly of A. minutus (= A. tenutrostris), were seen over shoals of fish: “When
small fish, put up by tunny or barracuda, rise thickly, the noddies pack closely
just above the water, the whole black mass pattering and dipping almost like
storm petrels.” A. tenuirostris was frequently seen off Christmas Island, where it
generally fished in company with Pr. cerulea, while off Oahu it was observed
fishing with A. stolidus. Although the flocks varied greatly in size, density, and
behavior, A. tenuirostris were sometimes seen feeding in such tight groups that
they were clearly competing for jumping or surfacing fish. The methods used
were Dipping and Plunging to Surface. When the birds were Dipping it was
generally not possible to see whether the prey was out of the water or merely at
the surface, but sometimes it seemed certain that the birds were taking prey from
the water. Sometimes the noddies would Dip almost into the splash made by a
large fish breaking the surface, and probably the two animals were often aiming
at the same prey. When Plunging to Surface, although the body is normally noth-
ing like submerged, the bird is doubtless able to catch prey further below the
surface than when Dipping. A. tenutrostris generally put down their feet when
they come very close to the surface during fishing, but do not normally remain
long enough close to the water for this to develop into Pattering, as it does in
Pr. cerulea. However, the very fully webbed feet and moderately long tarsi of A.
tenuirostris (Table 8) are clearly of great importance in maintaining distance
from the surface. Like A. stolidus, both A. tenutrostris and Pr. cerulea sometimes
rest on the water for appreciable periods. The bill of A. tenuirostris, though
long, is very slender (Fig. 6), this presumably being related to the fact that
the species catches mainly very small food items (see Discussion).
Like A. stolidus, A. tenutrostris is probably a diurnal feeder. Murphy (1936)
believes that it also feeds extensively at night, but there seems to be no direct
evidence for this. Cullen and Ashmole (1963) suspected that at Ascension Island
some A. tenuirostris might be absent from the island at night, but both there and
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 81
on Christmas Island, as in other parts of the world, it is clear that the main de-
partures from the colonies are in the early mornings and the main arrivals in the
evenings.
Pr. cerulea was regularly observed feeding—usually in mixed flocks with A.
tenutrostris—within a few miles of the shore during trips on a fishing boat near
the western end of Christmas Island. Pr. cerulea were seen Dipping and Plung-
ing to Surface in the same way as A. tenuirostris, but it was noticed that they
used their feet more often than the latter species. For instance, on one occasion a
flock were seen over a school of Yellowfin, flying into the wind between 0 and 5
feet above the water, always putting down their feet as they approached the
surface, and Pattering with them; at intervals they pecked at the surface, but it
was not possible to see if they were catching anything. Similarly, Hindwood
(1940), describing the feeding of this species on Lord Howe Island, said that
“they fluttered above the water with their feet drooping and would drop down
and pick up what appeared to be shrimps or very small fish which were being
chased to the surface by kingfish. Occasionally they would momentarily touch the
water, paddling with their webbed feet.” During the Pacific Ocean Biological
Survey Program it has been noted that this species spends more time Hovering
than any of the other species, although the two larger noddies do Hover at times
(Gould, pers. comm.).
The importance of the legs and feet in enabling Pr. cerulea to maintain the
most economic distance from the water is reflected in the fact that the tarsi are
relatively much longer than in the two Anous species, and in the very large area
of webbing on the feet (Table 8). However, Pr. cerulea has a bill absolutely and
relatively much shorter than A. tenuirostris. In all these features—long tarsi,
extensive webbing and relatively short bill, and also in its small size—Pr. cerulea
resembles some of the storm petrels (Hydrobatidae), and it is clear that there is a
similarity also in the feeding methods and in the food eaten. However, it ap-
pears that Pr. cerulea eats more active prey than most storm petrels, and is
largely dependent on the presence of predatory fish to make this part of its diet
available.
Pr. cerulea seem to leave the colony in the morning well after first light, and
they return to it in large numbers at dusk; we have no evidence that they ever
feed at night.
7. SEASONAL CONSIDERATIONS
SEASONAL VARIATION IN THE ENVIRONMENT
Seasonal changes are much less pronounced in the Central Equatorial Pacific
than in most oceanic areas. The climatology of the region has been discussed by
Hutchinson (1950), while Riehl (1954) and Barkley (1962) also gave some rele-
vant information. Murphy and Shomura (manuscript) give a fuller analysis of
the winds of the region, and also give monthly mean surface water tempera-
tures for latitudes 0°-5° N. (see also Roden 1963, Wyrtki 1965). At the longitude
of Christmas Island the monthly means range from about 79° F. to about 81.5° F.,
with lowest temperatures in December through February and highest tempera-
tures in about June. However, Murphy and Shomura point out that although
there are climatological seasons at the Equator, “‘these may frequently be altered
or obscured by short-term changes to the extent that during a given year the
‘seasons’ may not materialize.” Since oceanographic conditions are closely related
to the preceding climatological conditions (especially through the effect of winds
on the equatorial upwelling), the result of irregular variation in the equatorial
weather can be seen in both short-term changes and trends extending over
several years in the characteristics of the surface waters, especially within five de-
grees of the Equator. Some of these non-seasonal effects are shown in Barkley’s
data on surface salinities and temperatures at Christmas Island over a period of
several years. Nevertheless, the data do show a seasonal pattern, and the abun-
dance of zooplankton in the area, which is primarily controlled by upwelling at
the Equator, probably also varies in a fairly regular seasonal pattern. The
plankton sampling which has been carried out in the area (King and Demond
1953, King and Hida 1957) was limited to short periods spread over several
years, probably resulting in blurring of seasonal trends by differences between
the years, and it was not possible to demonstrate significant differences between
seasons. However, there was a suggestion that both in the South Equatorial
Current and the Countercurrent zooplankton abundance is lower in the first
quarter of the year than at other times.
For the sea birds, the important variable is the availability of forage animals
at the surface, which, as already discussed, is more directly related to the abun-
dance of surface-feeding schools of tunas (and so perhaps to the occurrence of
fronts) than to the general abundance of zooplankton. The most relevant data
are those of Murphy and Ikehara (1955), since Waldron (1964) did not separate
oceanic sightings of bird flocks and fish schools from those closer to islands.
These data show that in oceanic areas fish schools were seen at average rates of
about one per day in the period September-November, about 0.5 per day in De-
cember-February and June-August, and less than 0.2 per day in March-May.
Variation in sightings of bird flocks was similar, and may in fact have been
largely responsible for the apparent variation in the abundance of fish schools,
since most schools were detected by sighting accompanying birds. Interpretation
82
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 83
of the observed seasonal pattern is made even more difficult by the fact that the
observations were spread unequally over three different current systems, among
which there was important variation in the abundance of fish schools.
It may therefore be concluded that the data presently available do not permit
assessment of the seasonal variation in the availability of food for the sea birds.
Nevertheless, it must not be forgotten that if there were—in the area under
consideration—seasonal changes approaching in magnitude those which occur
in many other areas, they could undoubtedly be detected from the data now
available. It is therefore reasonable to assume that seasonal changes in the avail-
ability of food for the birds are relatively slight.
SEASONAL VARIATION IN THE FOopD OF THE Birpbs
Our only other information on seasonal variation in the food supply comes
from the composition of the food obtained by the various bird species at differ-
ent times. The data are not sufficient for a detailed seasonal analysis, but the
available relevant information is summarized in Figures 8-10. Fig. 8 shows that
considering the composition of the food by volume, the relative abundance of
the major food classes (fish, squid and other invertebrates) in the samples ob-
tained varies considerably in most species from month to month, but without
showing consistent seasonal trends. Furthermore, there is little tendency for the
variations that do occur to be parallel in the different species. In spite of the
small number of samples involved, striking seasonal trends in the composition
of the food would probably have been reflected in our data. However, it is very
likely that analysis of more extensive data, gathered over a period of several
years, would bring to light some subtle seasonal tendencies.
On the other hand, there is evidence that real short-term changes in the avail-
ability of the different foods do occur. For instance in S. fuscata, for which rela-
tively large numbers of samples are available, the proportion of squid in the
food given to chicks during March 1963 (in a colony on the main island) was far
higher than in August and rather higher than in September (on Cook Island).
However, the situation in February 1964 was more similar to August and Sep-
tember 1963 than to the previous March, arguing against the possibility that
the winter breeding season (with laying mainly in December) is timed in rela-
tion to a seasonal peak in the availability of squid for feeding the young.
Similarly, the importance of short-term and perhaps randomly occurring
changes in availability of different foods is well shown by the difference in the
samples obtained from G. alba in the first three weeks of January 1964 and the
first week of February 1964. In the first period food was apparently in short sup-
ply—since several large chicks were extremely light in weight—and fish made
up a large proportion of the diet (Fig. 8). But in the first week of February food
was clearly abundant (since almost every bird handled at night regurgitated) and
consisted almost entirely of squid of extremely uniform size (see later); pre-
sumably these squid had just moved into the area.
Figure 9 gives information on the seasonal variation in the size of the fish and
squid taken. Data are presented only for P. nativitatis, S. fuscata, G. alba and
A. tenuirostris, since in the other species there were few periods with adequate
sampling. Similarly, the data on squid in the diet of A. tenuirostris are not worth
84 PEABODY MUSEUM BULLETIN 24
PHAETHON RUBRICAUDA ANOUS STOLIDUS
2 AEN NU PAPts (9 Swarniliae he et'h 2 MM) IAI XS Eon
‘N \ \ \ S \ N \)
so4 |) NUN ao4 |X| | | |S N
60 ; 60 \
\
40 N fe eB 40 \
20 i R By 2 20
) “a ee )
40 BS oe vise 1 0 Diao, sume 2 14
PUFFINUS NATIVITATIS GYGIS ALBA
Fo Tony IMM Ae F
100 100 IR ~
80 80 N \
60 60 N
‘AR
40 40 N
20 20 f ? N
) ) fee
2 3 5 18 34 32 asqmonees
4 PTERODROMA ALBA >, ANOUS TENUIROSTRIS
2 MM I S UN w_ M Yi) oa No ae
1 IX STURN TINS N
i N i of NN \
60 N 60 SS
N
WN
40 = 40
20 E 20
0 Oo 0
5 4 4 8 14 8 17, 17, cee
FUSCATA ~, PROCELSTERNA CERULEA
72 S) aN 2 MMO A 1S Ns J
. ‘ ANY BS IN ~~
80 80 a :
60 60 ji
40 40
20 20 °
0 0 3
0° 0. .0) 5) 40 NO use
# FISH SQUID OTHER INVERTEBRATES
FIGURE 8. Seasonal variation in the proportions (by volume) of the major food classes in
the diets of the birds.
The figures below the columns indicate the number of samples obtained in each
period: full shading is used only when there were at least 7 samples. Details of the
sampling periods (designated here by initial letters of the months concerned) are
given in Fig. 1.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 85
FISH SQUID
PUFFINUS NATIVITATIS
M eh | eila MiuiMe Ay Ae te Sis NS | Nee es
és 100 Ak i iy :
N & 80 NN & N aN
\ 60 N S \ \ N N \
\ ol lINENSNN|| A
\ TETENT NNT] A
SSNGURSS “IGUUSUEOU
& Steel 0 el B Fy
143 29 17 6 We53) 2808250895060) 620) 21 Laz
STERNA FUSCATA
M Nave, Jer eto % MM IS SAN MIU Tee oe
: : 100 a a fs
i ) “]SIAMATIANS
60 N N N
40 N
3) 8 ee NATL
LIA J epape HE
0 16 173.20 l2 9 2 9 70 12
GYGIS ALBA
M Dh Ze. 1 iS Meee ee
100
oO co
oO o
(SS) Ea
F
Oo BEES 7/7] 2
05, [Omi sa RE P27 IS
40
20 S S
3 2Ae 2 i Oo 1 (0) i 2
ANOUS TENUIROSTRIS
6M N J
100 z
80 : N . EI FISH >4CM,SQUID >6CM
60 NN NA
" \ N N FISH 2-4 CM,SQUID 4-6 CM
20 \ N S
S BREES : FISH 0-2 CM,SQUID 0-4CM
e 1 18g 280 240 560
FIGURE 9. Seasonal variation in the size of the fish and squid in the diets of four bird
species.
The figures below the columns indicate the number of measurable fish (or squid)
which were available in each sampling period. Full shading is used only when these
numbers are 20 or higher, and at least 7 samples contained some fish (or squid).
86 PEABODY MUSEUM BULLETIN 24
%
80 EXOCOETIDAE SCOMBRIDAE %,
60 60
: 5 STERNA FUSCATA ts
204 fa mE 20
Co} i se a = as cove | [] | cece C a seco | secs | I (0)
op Ns %3 §47% % 2 *h3 Ya Yo Ns 4%3 447% % 2 Ne
60 60
x | GYGIS ALBA :
20 20
OF tree ace me = Hd = a | a seen [ ee eee Bll 0
yz Y3 V5 *he Ysa %2 As *hro 7/23 % Vy YS Ng V4 452 *hs Y20 Yaz
60 60
z | ANOUS TENUIROSTRIS i:
20 Fi a 20
ro) 30 = 7 : i aa Bg eee tenes O Pan | os MG... Lo
hha Va Sa Ye %h7 “hz Ya tho % Ns %y *he ye N7 V7 %e 0
MAR MAY J/J AUG SEP NOV JAN FEB JUN MAR MAY J/J AUG SEP NOV JAN FEB JUN
40 40
20 20
r¢) i Ors oo ial ord oe j 1 mee eces coon OD wee 6800 see sow ecce ie}
154% Ns %o3 9/37 %3 V5 A%h2 Nip %4% As %3 Mz % UW M2 Az
100 100
80 80
60 60
40 GYGIS ALBA 40
20 20
OF ae ee oe mm Ee CO ge gee -_ O 0
ln %, % Ve Ysa %2-*%hs Yoo %3 % V3 Vs %e Vs4'%s2 %s %20 %3
40 40
a i ANOUS TENUIROSTRIS i
oo: ar = = now | rr corre rye Bees eoce EE po 3d 0
4 Ya ye *he %e Nr 7% ho % Ne %y Ns %e “hz Vz Ve ho
MAR MAY J/J AUG SEP NOV JAN FEB JUN MAR MAY J/J AUG SEP NOV JAN FEB JUN
EMMELICHTHYIDAE
= a STERNA FUSCATA
Ocho secs coe seca open fey oO
%4 % Ns 3 x7 % % Y2 As
40
sit r rf ANOUS TENUIROSTRIS
0 ecco) aae Ey === eee =< enw
% As Ve Na %e Nr %r% Vo
MAR MAY J/J AUG SEP NOV JAN FEB JUN
FIGURE 10. Seasonal variation in the representation (by number) of some important fish
families in the diets of Sterna fuscata, Gygis alba, and Anous tenuirostris.
The five fish families are considered separately. Each histogram shows, for a bird
species, variation in the percentage of the identified fish which belonged to the
relevant fish family. Solid black columns (or dashed zero lines) indicate that at least
20 fish obtained from the bird species in that sampling period were identified (i.e.,
when 100% represents at least 20 fish): in the other periods open columns or dotted
zero lines are used. The figures below the columns are frequencies of occurrence:
the first figure is the number of samples in which members of the relevant fish family
were found; the second figure is the total number of samples obtained from the bird
in that sampling period.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 87
presenting, but are available in Appendix 2, together with the fish and squid data
for the other four species. The numbers of measurable fish and squid ob-
tained in each sampling period are given in the figure, while information on
the number of samples containing fish and squid in each period is available in
Appendix 1. It is thus possible to obtain an idea of the reliability of the ob-
served differences between periods, so long as it is remembered that each item
cannot be considered as necessarily being obtained independently of others in
the same sample, since the birds may fish for considerable periods over a single
school of prey.
Examining the fish data first, the only dramatic seasonal effect is found in the
diet of A. tenuirostris, which in both May 1963 and June 1964 included 79% of
fish less than 2 cm long. In none of the other periods did the proportion of
small fish approach this level, the highest being 32% in January 1964. Thus the
diet of A. tenuirostris showed an enormous swing in favor of small fish in the
early summer of both years. In 1963 the sampling period in which many small
fish were obtained was from 29 April to 9 May, while the regurgitations obtained
in the next period, between 19 June and 5 July, contained a much lower pro-
portion of small fish. In 1964 it was sampling between 30 May and 11 June which
produced a high percentage of small fish. It is thus possible that the period of
abundance of small fish was slightly later in 1964 than in 1963. The peak of
breeding occurred at about the same time in the two years, and in both the tiny
fish were used extensively in feeding chicks. However, it was clear that the high
proportion of small fish obtained at these times did not result merely from their
selection by birds which were feeding chicks, since they were regurgitated also
by birds which did not yet have eggs and by birds which were incubating. Be-
cause of this, it does not seem plausible to suggest that small fish are equally
available at all times of year but are selected by A. tenuirostris especially when
breeding. It is more probable that they become much more abundant at
roughly the same time in each year, and that this abundance has been an impor-
tant factor influencing the evolution of the observed breeding season.
In this case, one might expect to find the seasonal abundance of small fish re-
flected in the diets of the other species. The data available for comparison are
not sufficient to be sure, but it seems that neither P. nativitatis, S. fuscata, nor
G. alba took an unusually high proportion of fish less than 2 cm long at the
times when A. tenuwirostris was catching so many. However, at least P. nativitatis
and S. fuscata, and probably G. alba, feed further out to sea than A. tenuiros-
tris, while the data for G. alba are complicated by a bias in favor of large fish in
samples carried in the bill. Unfortunately, the majority of the tiny fish obtained
from A. tenuirostris could not be identified, so we do not know how many dif-
ferent kinds of fish were involved in the peak of their abundance. However, it
appeared that only a few different species were of major importance.
In S. fuscata the large young in March and September 1963 were fed mainly
on fish more than 4 cm long (Fig. 9). The food given to the slightly smaller young
in August had a similar size composition, but at a slightly earlier stage in the
following breeding season (February 1964) more fish in the 2-4 cm class were
present in the samples. The representation of this class was even greater in June/
July 1963, when many of the samples were obtained from adults which had
88 PEABODY MUSEUM BULLETIN 24
chicks a few days old. However, the number of samples from June/July is rather
small (11 containing fish), so that this difference may not be meaningful.
The available data thus suggest that there was an early summer peak in the
abundance of small fish in inshore waters, but no well-marked seasonal cycle in
the size of the fish taken by the birds feeding further from the island. The lack
of any consistent seasonal pattern, and the rather large variation from one
sampling period to the next, may be in part a reflection of the fact that most of
the species studied fed on a wide variety of fish. There are doubtless well-
marked trends in the size-frequency distribution of the separate fish species, but
in the area well away from the island it appears that these trends do not run
parallel to one another, and so do not result in conspicuous trends in the size
distributions of the taxonomically diverse samples taken by the birds.
In contrast to the fish, the squid taken by the various bird species were almost
entirely of one family and genus (Ommastrephidae—Symplectoteuthis) and
thus might be expected to show more clear-cut seasonal size variation. Large sam-
ples are available for rather few bird species and sampling periods (Fig. 9), but
in S. fuscata, where the sampling is best, there are indications of a seasonal pat-
tern. In March 1963 and in February 1964 the proportion of squid less than 4 cm
in mantle length was considerably higher than in the large samples from Au-
gust and September 1963. However, evidence from several more years would be
needed to prove that this indicated a regular annual cycle in size. The abundance
of squid less than 4 cm long in February 1964 is shown more dramatically in
G. alba, in which the 71 squid obtained in this period were all in the 2-4 cm size
class. This abundance of small squid seems to be reflected also in the small sam-
ple from P. nativitatis (Fig. 9), but Pt. alba did not take a specially high pro-
portion of small individuals at this time (Appendix 2b).
Another possibility for seasonal variation is that members of the various fish
families might be available to different extents at different times of year. Fig. 10
gives our data for some of the more abundant fish families and the bird species
from which the largest numbers of identifiable fish were available, spread
fairly evenly throughout the period of study. However, a number of biases are
involved and the data should be interpreted with care. The sampling should be
sufficient to demonstrate any drastic seasonal changes in availability, but the
situation is made complex by the large number of kinds of fish eaten by most of
the bird species, so that subtle changes would not be apparent. In fact, few con-
sistent trends emerge from the analysis, suggesting that seasonal changes are
relatively slight.
Exocoetidae, which were important in the diets of nearly all the birds, were
clearly available in all the sampling periods. One feature of interest is that in
March 1963, a period in which the diet of S. fuscata consisted largely of squid
(Fig. 8), an unusually high proportion (73%) of the identified fish were Exocoe-
tidae. This suggests that other fish were less abundant than usual at this time. In
August and September 1963, when S. fuscata were again feeding large chicks,
relatively fewer Exocoetidae, and more Scombridae, were obtained. In February
1964 Gempylidae provided a higher percentage of the fish taken by S. fuscata
than either Exocoetidae or Scombridae, but the frequencies of occurrence of the
two latter families were higher. Scombridae were eaten in small numbers by
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 89
A. tenuirostris in all sampling periods except May 1963 and June 1964, the two
periods when this species was eating many very small fish.
The occurrence of Blenniidae has already been discussed in the Species Ac-
count for G. alba, since they were the most important family in the diet of this
species. Fig. 10 shows that Blenniidae were obtained by G. alba at all times of
year. However, Cirripectus sp., which were the only blennies taken by any of the
other bird species, were obtained from G. alba only in November; even in this
period they comprised only one third of the blennies taken. A. tenuirostris took
Cirripectus sp. in six different periods, but they were most important in No-
vember and January.
Finally, members of the family Emmelichthyidae were obtained by S. fuscata
in considerable numbers, and with some regularity, in August and September
1963, but not at all at other times. This family also featured prominently in the
diet of A. tenuirostris at about the same time, while they were present in two
samples from P. nativitatis and one from A. stolidus between June/July and
September, but at no other time. It therefore seems probable that there was a
real peak in the availability of members of this family during the late summer
of 1963.
It will be clear from the above discussion of seasonal variation in the food of
the various bird species that our evidence is largely negative; that is to say, few
well-marked seasonal changes were detected in the present study. Although
this failure may partly be ascribed to the inadequacy of the data, it should be em-
phasized that if strong seasonal trends had existed, they would have been de-
tected. Our results imply either that no consistent seasonal trends exist, or—
more likely—that subtle ones are present, but are overshadowed by short-term
fluctuations in availability, and by sampling errors. It should be pointed out
that this conclusion implies that the environment is an unusual one; in the ma-
jority of oceanic areas less intensive sampling would have detected more striking
seasonal changes in the environment.
SEASONAL VARIATION IN BREEDING ACTIVITIES
Our interpretation of the oceanic environment of Christmas Island as being
one of the most nearly seasonless of any oceanic area is supported by the rela-
tively slight seasonal variation in breeding activity shown by most of the sea
birds. Even before the start of the present study, the evidence indicated that
the breeding regimes of several species did not involve the usual well-marked
peaks in breeding activity at a particular season in each year (Gallagher 1960);
this picture has been confirmed by the investigations during 1963-64 (Fig. 1).
The initial object of the work on Christmas island was to document the
breeding schedules of individual birds, especially of S. fuscata and G. alba. Indi-
vidual S. fuscata were shown to breed either at six-month or at twelve-month in-
tervals, according to their success in the previous breeding period (Ashmole
1965); breeding seasons start each year in May-June and November-December,
and there are only two or three months in the year in which members of the
species are not breeding on the island. In contrast, individual G. alba finished
their breeding activities, underwent a complete molt, and then immediately re-
turned to breed, apparently irrespective of the season (Ashmole, in press).
90 PEABODY MUSEUM BULLETIN 24
There was a peak in breeding activity during the early summer, but the reasons
for this were not determined; neither is it certain that the peak occurs at the
same time in each year. Other species, for instance A. tenutrostris and Pr.
cerulea, showed straightforward annual cycles and definite—though extended—
breeding seasons once each year.
Looking at the breeding periods in 1963-64 of all the birds whose food was in-
vestigated (Fig. 1), the most striking feature is that at any time of year a large
proportion of the species can be found at some stage of their breeding activities.
Furthermore, it is difficult even to say which are the peak breeding periods and
which have least breeding activity. Giving equal weight to all the species
studied, the modal periods for eggs in 1963-64 were May through July and De-
cember-January, and the least popular months were November and February.
For chicks the pattern is even less sharp, but more species had chicks during
January through March and June through October, than in April-May and No-
vember-December.
However, Fig. 1 shows graphically only the data for the eight species studied
in detail; information on the breeding periods of the other species which breed
on Christmas Island is given in the note to the figure. This information shows
that among the Pelecaniformes of Christmas Island (including Ph. rubricauda)
there is a tendency for breeding to occur during the northern summer, as it does
also in the Hawaiian chain (Richardson 1957). However, in Sula dactylatra
and S. sula on Christmas Island some laying may occur at any time of year, and
in the other species except Fregata ariel there is a considerable spread in laying
dates. Puffinus pacificus also has a definite summer breeding season, in contrast
with the two Procellariiformes included in the present study. It may well be
that the food of the Pelecaniformes, which consists mainly of larger prey animals
than were taken regularly by any of the non-pelecaniform species studied, does
show an annual peak of abundance which makes it advantageous for these
species to breed at roughly the same time in each year. However, the selective
pressures involved clearly do not necessitate closely synchronized breeding, except
perhaps in the case of Fregata ariel. One may speculate that in this species,
which obtains part of its food by piracy, apparently largely on terns (personal
observations), selection has favored laying at such a time that the young are be-
ing fed at the same time as the young of S. fuscata in their summer breeding
season.
S. fuscata overshadows in number and biomass all the other terns and petrels
combined; thus the times when this species is feeding large young, especially
during August-September and February-March, are perhaps those when the de-
mand on the total food supply of the area is greatest. There is no apparent gen-
eral tendency for these periods to be avoided as breeding times by the other
species. One possible exception is A. tenuirostris, the second most numerous spe-
cies on the island, whose main breeding season overlaps to only a small extent
with the time when S. fuscata have chicks. However, A. tenuirostris takes mainly
smaller prey than S. fuscata and feeds much closer to shore, and it seems more
likely that the timing of its breeding season is related to the season of abun-
dance of small fish which are not important to S. fuscata, than that it is related
directly to a need to minimize competition with the more numerous species.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 91
Of interest in this connection is the fact that many adults and apparently all
juvenile A. tenuzrostris leave the island after the breeding season; this could im-
ply that for this species Christmas Island is a particularly favorable place for
breeding (for instance, because of the abundance of nest sites), but that at
other times of year feeding conditions are better elsewhere, either because there
is less competition for food or for some other reason.
Figure 1 also demonstrates the almost total lack of overlap between the breed-
ing seasons of A. tenutrostris and Pr. cerulea, two species which both feed mainly
close inshore, often in mixed flocks, and whose diets are similar in consisting
largely of fish less than 4 cm in length (Figs. 3 and 4 and Table 5). If, as suggested
in the previous section, there is a peak in the abundance of the small fish
taken by A. tenutrostris in early summer, it is necessary to explain why Pr. cerulea
lays mainly in autumn (Fig. 1 and Gallagher 1960). It could be argued that the
breeding season is timed so as to minimize competition for food with A. tenut-
rostris, and this possibility cannot be entirely excluded. However, it should be
pointed out that there are important differences between the diets of the two
species, which must tend to reduce competition between them, and which might
also result in selection favoring breeding at different times, irrespective of the
presence of the other species. One important difference is that the fish family
Gempylidae is of outstanding importance in the diet of Pr. cerulea, while in A.
tenuirostris it is only one of ten important fish families. It is thus possible—
though quite unproven—that the winter breeding season of Pr. cerulea has
evolved as a result of selection favoring breeding in the period when small
Gempylidae are especially abundant, and that this is the main reason why
breeding occurs at such different times in the two species. This is not to say, of
course, that the difference in food preferences is not itself an evolutionary conse-
quence of competition between the species.
8. DISCUSSION
The main interest in the present study lies in the fact that it includes data on
the food of nearly all the smaller members of the sea bird community of an oce-
anic island, in an equatorial region where seasonal influences are minimal. Since
all the species studied obtain their food just above, on, or just below the surface
of the ocean around Christmas Island, it is worth considering the competitive
relations between them.
First, it is necessary to assess the probability that the species are limited in
numbers by some resource other than food. Reasons for thinking that popula-
tions of many tropical oceanic birds may be limited primarily by competition
for food were presented in an earlier paper (Ashmole 1963a). However, it was
recognized that certain sea bird populations might be limited by the availability
of nest sites, and this possibility has since been further discussed by Rowan (1965)
in relation to the Great Shearwater (Puffinus gravis). She suggested that in this
and perhaps some other Procellariiformes, since there is no form of land tenure
apart from defence of the burrow itself, birds which do not own burrows can
nevertheless make unsuccessful attempts to nest on the surface in colonies which
are already overcrowded, rather than being forced to breed in other, less crowded
colonies nearby, or to found new colonies. Similarly, Robertson (1964), in his dis-
cussion of the populations of S. fuscata and A. stolidus in the Dry Tortugas, pre-
sented arguments that these populations may at present be limited by the tend-
ency for birds which cannot obtain optimal sites within the colony to attempt to
breed in suboptimal sites in the same area, rather than to establish new colonies
elsewhere. A similar tendency in A. tenutrostris on Ascension Island was discussed
previously (Ashmole 1962: 236).
Such situations raise the problem of why these colonial birds have not
evolved greater readiness to establish new colonies. Three factors may be im-
portant. First, potential colonists will generally be young birds, which have to
form pairs before they can breed; individuals which spend the courting period
in an established colony may have a higher chance of obtaining mates than those
which go elsewhere. Second, it is probable that colonial species depend rather
largely on responsiveness to the behavior of other members of the colony to en-
sure that they breed close to the optimum time (Brown and Baird 1965). One or
a few pairs establishing a new colony, especially if they were young birds, would
be likely to breed later than the main colony, and therefore to have lower breed-
ing success. Finally, if one assumes that before man became a significant factor
in their environment the populations of most sea birds were relatively stable, the
normal situation would be for there to be established colonies in all the places
suitable for breeding. Thus, for colonial species in reasonably stable environ-
ments, the best indication that a particular place was suitable for breeding would
be the presence of a colony there (cf. Crook 1965). This fact would clearly have
an important influence on the evolution of behavioral mechanisms for breed-
ing-site selection in the species. Man’s intermittent disturbance of the habitats
2
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 93
of many colonial sea birds has largely vitiated this mechanism of breeding-site se-
lection and may be largely responsible for the inadaptiveness—in certain pres-
ent-day circumstances—of the reluctance to establish new colonies. However, it
is clear that this same characteristic must hinder range expansion in response to
changing ecological conditions. Salomonsen (1965) argued that the recent spread
of the Fulmar (Fulmarus glacialis) in the boreal zone became possible only
when members of a certain population overcame—possibly through genotypic al-
terations—the strong adherence to the traditional breeding place which is nor-
mal in this species (but see also Fisher 1966).
We are now of the opinion that although most populations of tropical sea
birds probably are limited mainly by the effects of competition for food, addi-
tional density-dependent effects, differing widely in importance in different pop-
ulations, may often be exerted by competition for optimal nest sites, even when
an excess of suboptimal sites is available within the colony.
It is to be expected that since birds possess well developed behavioral mech-
anisms for selection of an appropriate nest site, a higher proportion of indi-
viduals will obtain optimal nest sites when a population is small than when it
is large. This effect will be most important in species with specialized nesting
requirements, and in areas where large numbers of equally favorable sites are
not available. For example, it seems certain that in a cliff-nesting species the
most secure sites will on average be occupied first in an expanding colony,
while in colonies of petrels nesting underground the chance of breeding failure
through burrow collapse doubtless increases slightly with the density of the
colony. Similarly, Robertson (1964) points out that in certain species nests outside
the area of the normal colony may be more exposed to weather than those in the
preferred area,
Behavioral interactions between members of a population may have the same
kind of effect. For instance, Cullen and Ashmole (1963: 440-443) frequently ob-
served A. tenuirostris chicks on Ascension Island being pecked by displaying
adults which visited their ledges, and considered that some chicks were killed in
this way. It seems probable that such intrusions would be less frequent in col-
onies in which an excess of good nesting sites were available, and observations
on Christmas Island, where A. tenuirostris build nests in trees, tend to confirm
this view. Similarly, Snow (1965), in a paper on the Red-billed Tropic-bird
(Phaethon aethereus) in the Galapagos Islands, described intense intraspecific
competition for nesting sites on one island, and a high rate of nesting failure
which was attributed to the competition, although there was a much less
crowded—and more successful—colony on a different island only 16 miles away.
Another real possibility is that predation sometimes acts density-dependently
by causing higher mortality in birds in suboptimal sites than optimal ones.
With large populations the proportion of birds in suboptimal sites will be
greater, so that the overall rate of predation might be higher than it would be
when the population was small. This effect must certainly sometimes occur, and
Robertson (1964: 43) cited a possible example in S. fuscata. A different type of
example—perhaps as yet unproven—is provided by the many species of petrels
which are subject to predation by gulls or birds of prey. In these, the chance of
survival of chicks and adults is probably inversely related to the distance be-
94 PEABODY MUSEUM BULLETIN 24
tween the burrow entrance and a place (for instance, a steep slope or cliff top)
from which they can take off.
Since effects of these kinds may be expected to exert some density-dependent
influence on breeding success, even when not all the possible nest sites are occu-
pied, one must be cautious in claiming that competition for nest sites cannot be
contributing to the regulation of a given population. However, the nesting re-
quirements of most of the Christmas Island sea birds are very unspecialized; of
the species studied, Ph. rubricauda, P. nativitatis, Pt. alba, S. fuscata, A. stoli-
dus and Pr. cerulea all breed in scrapes on the surface of the ground. Neverthe-
less, most of these species seem to prefer sites sheltered to some extent by vege-
tation, and it was suspected that in Pt. alba during the midsummer breeding
season, when vegetation was generally thin, adults at exposed sites sometimes
left the nests during the hottest part of the day, exposing their eggs to lethal
temperatures. If this phenomenon could be confirmed it would clearly provide an
example of a subtle density-dependent effect of competition for optimal sites.
However, in none of the other ground-nesting species were there any obvious in-
dications that similar effects were operating. It should also be mentioned that
in the three species of boobies, two species of frigate-birds and two species of
terns which were not included in the present study, it seemed most improbable
that competition for nest sites could exert important density-dependent effects.
The two remaining species whose food was studied, G. alba and A. tenutros-
tris, have slightly more specialized nest-site requirements. G. alba, which on
Christmas Island places its egg mainly in crevices on the branches of Messer-
schmidia argentea, probably utilized a high proportion of the best of such sites,
as well as many suboptimal ones. Furthermore, some eggs on Cook Island were
placed on coral blocks in the open, where they may have been generally less suc-
cessful; however, the biases involved in estimating breeding success made it im-
possible to be sure of this. A. tenuirostris was far more abundant than G. alba,
but since it can build nests in almost any fork of a Messerschmidia tree, there
did not seem to be a lack of potential sites.
The possibility that predation might exert a significant control on the bird
populations of Christmas Island can probably be excluded at once for all the
species except S. fuscata. Chicks of the latter species in some of the mainland
colonies are taken in large numbers by the Great Frigate-bird (Fregata minor).
However, it was rare to see a frigate-bird hunting over Cook Island. In the enor-
mous mainland colonies a much higher proportion of nests were in places
accessible to frigate-birds, and therefore suboptimal from the viewpoint of pre-
dation. An increase in numbers might raise this proportion still further, and
so perhaps increase the overall rate of predation slightly, but the density-
dependent effect would be rather small. Furthermore, since small chicks of S.
fuscata are available for such short periods (about one month, twice a year), it is
unlikely that an increase in the numbers of chicks would cause an equivalent
increase in the population of Fregata minor. Thus an increase in the numbers of
S. fuscata might even result in a decrease in the proportion of chicks predated.
It may therefore be provisionally concluded that shortage of optimal nest
sites may exert some density-dependent control on the breeding success of the
populations of Pt. alba and G. alba, but is unlikely to be of great importance in
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 95
the other species, including S. fuscata, which is by far the most numerous species
on the island.
However, another possibility which must be borne in mind when consider-
ing the results of the present study is that the populations of some of the species
may not be in equilibrium at the present time. Whereas in most bird species with
high reproductive and mortality rates any divergence from equilibrium caused
by man’s activities is likely to be quickly succeeded by a new equilibrium, this
is not necessarily true of populations of long-lived birds with low reproductive
potential.
Although Christmas Island had no indigenous human population, it has
been the scene of a wide variety of human activity (King 1955, Gallagher 1960),
culminating in the explosion of nuclear weapons at the east end of the main
island during 1958-59. The latter caused heavy mortality of Red-footed Boobies
(Sula sula), but probably had relatively small effects on the other bird species,
which are concentrated at the opposite end of the island. However, the popula-
tion of Ph. rubricauda may also not be in equilibrium at the present time,
since this species is subject to sporadic illegal slaughter by Gilbert and Ellice is-
landers, who apparently consider it a delicacy. The complex history of Christ-
mas Island makes it difficult to judge to what extent the populations of the other
birds have been affected by man, but there is no evidence that the species com-
position has altered since the early visits to the island, and S. fuscata has clearly
always been enormously abundant (King 1955).
It therefore seems reasonable to consider the sea birds of Christmas Island as
a group of species fully adapted both to their environment and to the presence of
each other, even though the situation at present probably does not represent
exactly the natural equilibrium. Furthermore, in an earlier paper (Ashmole
1963a) general arguments were presented to support the hypothesis that competi-
tion for food determines the size of many populations of tropical sea birds, and
exerts an important influence on the evolution of many aspects of their biology.
If we may conclude from the first part of the present discussion that most of
the Christmas Island sea birds are not primarily limited by shortage of nest sites
(although this may exert certain density-dependent effects), it seems most likely
that the main control is exerted—or at least was originally exerted—by compe-
tition for food. The situation on Christmas Island thus provides an opportunity
to consider the ways in which the species in a simple bird community are able to
occupy distinct feeding niches in an exceptionally uniform and_ seasonally
constant environment.
Lack (1944), although initially doubting the universal applicability to wild
bird populations of the principle of competitive exclusion, collected evidence
which suggested that sympatric species of birds always differ appreciably in their
ecology. As pointed out by Dixon (1961), subsequent work on many different
groups has generally confirmed the lack of exceptions to the principle. Mac-
Arthur (1958), in his important study of the competitive relations among five
species of warblers (Parulidae), presented a concise discussion of the problems of
coexistence of similar species. In a population controlled by density-dependent
events, the presence of many members of the species makes the environment less
suitable for other individuals of that species. Similarly, when several species are
96 PEABODY MUSEUM BULLETIN 24
sympatric, interspecific competition occurs if the presence of individuals of one
species makes the environment less suitable also for members of a different
species. Populations of sympatric species must always be limited by factors which
are sufficiently different that each species inhibits its own increase more than
it inhibits that of the others. This formulation by MacArthur implies that inter-
specific competition will be common among sympatric species, but that its in-
tensity will always be less than that of intraspecific competition. In other
words, for each of the competing species, a member of any of the other species
must be a less serious competitor than another member of the same species, if all
of them are to coexist.
If the species under consideration are limited by the availability of food, one
must expect that their feeding ecology will differ significantly. Huxley (1942) and
Lack (1944, 1945, 1946, 1947), after consideration of a variety of avian examples,
concluded that the most important kinds of ways in which ecological separation
is achieved are habitat differences, size differences (especially of the bill), and dif-
ferences in feeding methods associated with differences in the food. More recently
MacArthur (1958) has made an essentially similar statement, saying that ““I'wo
species may eat different foods for only three reasons: 1. They may feed in differ-
ent places or at different times of day; 2. They may feed in such a manner as to
find different foods; 3. They may accept different kinds of food from among those
to which they are exposed. (Of course, a combination of these reasons is also pos-
sible.) However, it must be remembered that these behavioral differences—
especially that involving choice among a number of available foods—will not by
themselves permit coexistence of two species on an evolutionary time-scale. Un-
less each species is more efficient than the other in utilizing the food which it
chooses, there will be no selective pressure favoring the maintenance of the be-
havioral differences; one or both species will become more general feeders,
and one of them will be excluded from the habitat. On the other hand, indefinite
coexistence will be possible if each species is also structurally or physiologically
adapted to its own particular feeding niche (cf. Hinde 1966: 445). The extent of
this specialization must be sufficient to ensure that when circumstances are
critical (i.e., when density-dependent limiting factors are actually operating) each
species can occupy its own feeding niche more efficiently than any of the other
sympatric species (cf. MacArthur and Levins 1964). Recher (1966) emphasized
the importance of morphological divergence in achieving ecological segregation
among shorebird species in which spatial segregation is often not possible. How-
ever, as he pointed out, morphological divergence is also characteristic of adap-
tation to “different spatial segments of the environment” (i.e., habitats).
Perhaps the most striking feature of the ecology of Christmas Island is that
seven species of terns breed on the island, and that all may be found on or near
the island at any time of year. We shall show that like the four species of terns
studied by A. N. Formosov (quoted by Gause 1934) on the island of Jorilgatch
in the Black Sea, the terns of Christmas Island all show differences in their feed-
ing ecology.
Food samples were obtained from only five of the tern species. One of the
others, Thalasseus bergii, is obviously ecologically separated from all the other
species, since it was seen feeding only close to beaches within the lagoon and
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 97
along the coast, while none of the species studied fed in these areas to a signifi-
cant extent. It is unfortunate that transportation problems made it impracti-
cable to obtain food samples from the other tern species, Sterna lunata, a close
relative of S. fuscata which is only a little smaller; this species probably feeds
mainly at sea, but also within the lagoon and at brackish water holes (Gallagher
1960).
Many ecologists, in investigating the application of the principle of compet-
itive exclusion, have concentrated their attention on congeneric species, on the
grounds that these are the most likely to compete seriously with each other.
Such a procedure would be unjustified in the present case, since although the
five species of terns are placed in four genera, some competition clearly occurs
even between those which are members of different genera.5 More important
than the taxonomic situation is the fact that all five species catch their food
exclusively within a few inches of the plane of the surface of the sea.
Among the five species of terns, the greatest similarities in diet were be-
tween the two largest species, S$. fuscata and A. stolidus. They took very similar
proportions of fish and squid, although fish were perhaps slightly more impor-
tant in A. stolidus. The mean size of the items obtained from the two species
was almost the same, and the small differences in the size-frequency distributions
probably result partly from sampling errors. The only definite difference between
the diets of the species was in the representation of certain fish families, and
even this was not dramatic. In both species Exocoetidae were the most impor-
tant family, Scombridae ranked second and Gempylidae third. However, in S.
fuscata Scombridae were almost equal in importance to Exocoetidae, while in
A. stolidus there was a much larger difference between the two families.
Both these large terns are dependent largely or entirely on the presence of
schools of large predatory fish (mainly tunas) to drive their prey to the surface
and so make it available. Since tuna schools have only a low overall density in
the tropical Pacific, the numbers of birds feeding over each school are often
high. Thus there may be severe competition for available food, even though
the total stock of potential prey is very large relative to the number of avian
predators (Ashmole 1963a: 473). If it is intraspecific competition of this kind
which limits the numbers of each of these species, it is remarkable to find that
they take prey of the same kinds and the same size, and yet coexist on so many
tropical islands.
Available information on the biology of these two species suggests that the
most important difference between them is that they feed largely in different
zones (see Section 6), A. stolidus being found mainly close to the breeding
colonies (within about 50 miles), but S. fuscata ranging much further into the
open ocean. It can be no coincidence that S. fuscata is undoubtedly the most
abundant of all tropical sea birds; it clearly owes its success to unspecialized
nest-site requirements and the ability to exploit food made available by schools
of predatory fish hundreds of miles from land, even while it is breeding. This is
5 Although Peters (1934) and Murphy (1936) maintain the genera Gygis and Procelsterna,
Moynihan (1959) merged both with Anous. While agreeing that Procelsterna should probably be
considered as congeneric with Anous stolidus and A. tenuirostris, we feel that there are ample
grounds for retaining Gygis as a monotypic genus.
98 PEABODY MUSEUM BULLETIN 24
made obvious by considering the situation which would ensue if the whole
population of S. fuscata on Christmas Island, consisting of probably more than
one million birds, tried to feed over the small number of fish schools (perhaps
about a dozen) which are present within about ten miles of the island at a
given time. Clearly there would be such intense competition for the limited
number of prey individuals which came to the surface that none of the birds
could survive. In fact, S. fuscata was not seen feeding close to shore around
Christmas Island, but A. tenuirostris did feed largely in this zone, and although
its total population is of the order of one hundredth the size of that of S. fuscata
(Table 1), the numbers of individuals present over fish schools were often so
high that it seemed certain that there was appreciable competition for available
prey (Fig. 11).
The adaptations which confer on S. fuscata the ability to feed far from the
colony even when breeding, and in which this tern is convergent with many
Procellariiformes, include the exceptional length of the incubation shifts, and
the ability of the chick to survive for several days without food, even when it is
very small, but to accept an enormous meal rapidly when a parent returns.
There may also be an ability to delay digestion of food intended for the chick,
but this has not yet been investigated. Similarly, although it is certain that S.
fuscata can remain airborne for indefinite periods (Ashmole 1963b), the aero-
dynamic, behavioral and physiological adaptations involved have not yet been
worked out. Although no proof is yet available, it seems unlikely that A. stolidus
has this ability to remain airborne for long periods, and it is probable that it
normally returns to land at night. However, unlike S. fuscata, it can rest easily
on the surface of the water (Watson 1910, Watson and Lashley 1915), and it
also makes use of floating objects as perches (Murphy 1936).
The fact that S. fuscata frequently feed at great distances from shore even
while they are breeding implies that they must often fly past feeding flocks of
noddies, including A. stolidus, to reach their oceanic foraging areas; personal
observations near Hawaii confirm that they sometimes do this, although mixed
feeding flocks certainly also occur. The results of the present study, showing that
the diets of S. fuscata and A. stolidus are very similar both in general composi-
tion and in the size of food items, indicate that food suitable for S. fuscata is
available in the areas where A. stolidus feed. The situation seems to be most
easily explained on the basis that the competition for available prey close to
shore makes it advantageous for S. fuscata to do a large part of their fishing out-
side the normal range of A. stolidus. However, since S. fuscata can forage further
from the breeding island, it is clear that A. stolidus—if its populations are food-
limited—must be at some advantage when feeding close to the island, or the
two species could not coexist.
Although the nature of this advantage is not definitely known, it seems
clear that the more extensively webbed feet and longer legs of A. stolidus (Table
8), and its swimming ability, enable this species to use a greater variety of
feeding methods than S. fuscata. Furthermore, there are indications that A.
stolidus, which does not require the capability of regularly traveling great dis-
tances, has been able to evolve greater maneuverability in flight than S.
fuscata. Although we have not analysed in detail the aerodynamic characteris-
FIGURE 11. Two views of a dense flock of Anous tenuirostris feeding over a tuna
school close to the western end of Christmas Island.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 99
tics of the two species, measurements on relaxed museum skins show that in in-
dividuals with the same ‘wing length’ the area of the distal part of the wing
(including all the primaries and secondaries) is much larger in A. stolidus than
S. fuscata (in the specimens measured the areas were 242 sq. cm and 198 sq. cm
respectively, giving a ratio of 1.2: 1). Since in the Christmas Island popula-
tions both the mean weights and the mean wing lengths are the same in the
two species (Table 8), it is clear that there is a substantial difference in wing
loading, while the area of the tail is also greater in A. stolidus. The difference
in wing area results mainly from the greater length of the secondaries and inner
primaries in A. stolidus, which makes its wing much broader. It is thus evident
that while S. fuscata has a well developed high-speed wing (see Savile 1957),
that of A. stolidus should give greater maneuverability.
Before leaving the subject of the relations between S. fuscata and A. stolt-
dus, it is of interest to consider the situation in the Dry Tortugas, which is
apparently different from that in most other colonies. Watson (1908) and
Watson and Lashley (1915) imply that around the Tortugas the two species
feed together, and they apparently do not normally go more than 17 or 18 miles
from the colony to obtain their food; Watson was of the opinion that both re-
turned to the island each night. The data already quoted, showing that S.
fuscata have much shorter incubation shifts on the Tortugas than on Ascension
and Christmas Islands, support the conclusion that the feeding ranges of this
species are remarkably different in the different areas. Considering also the evi-
dence that chicks in the Tortugas populations develop more rapidly than those
on Ascension (Watson 1908, Ashmole 1963b, Robertson 1964), it seems reason-
able to conclude, as did Robertson, that the Tortugas population of S. fuscata
is not limited by competition for food in the breeding season. If this conclu-
sion is correct, and if—as Robertson believes—the population of 4. stolidus
in the Tortugas is also limited by factors other than competition for food, the
lack of separation of the feeding zones of the two species in this area is just what
might have been expected.
The next largest tern species, G. alba, is a little larger than A. tenuirostris
but much smaller than S. fuscata and A. stolidus. Its diet is similar in general
composition to those of the latter two species, but differentiated by the larger
proportion of small food items, and also by the very different representation of
various fish families. Although G. alba may well stay at sea during the non-
breeding period, it does not spend such long periods away from the colony
while breeding as does S. fuscata. There are certain indications, already dis-
cussed, that the specialty of this species is its ability to feed in the half light of
dawn and dusk, when there is more opportunity of catching organisms which
come close to the surface at night. If this supposition is correct, it is clear that
G. alba might be less dependent than the other species of terns on the presence
of tuna schools, and so could avoid undue competition with the other species
even though it feeds in the same zones as some of them. The importance in the
diet of G. alba of three species of Blenniidae which are known to occur in open
waters rather than close to coral reefs, but which were not represented in the
diets of the other species, supports the idea that G. alba is able to exploit a
source of food which is not available to the other birds, and is consistent with
100 PEABODY MUSEUM BULLETIN 24
the idea that it does much of its feeding at times which are less utilized by the
other terns. However, it should also be remembered that the size-frequency dis-
tribution of the items obtained from G. alba, though subject to certain biases,
is intermediate between that for A. tenuirostris and those for the two larger
terns; this will also tend to reduce competition among the tern species.
A. tenuirostris, which is similar in size to G. alba but much smaller than A.
stolidus, is very like the latter species in its morphology (except size) and be-
havior, including feeding methods. Although the two species were not seen
feeding together off Christmas Island, they do so in other areas, and it seems
that the main distinctions between them are those related to size. The size-
frequency diagrams (Fig. 4) show the extent of the differences in the lengths
of the animals eaten. Although there is a considerable area of overlap, it must
be remembered that for A. stolidus the smaller prey are of relatively little volu-
metric importance, so that the great bulk of its food comprises items larger than
are taken in appreciable numbers by A. tenuzrostris.
A. tenuirostris and Pr. cerulea were the two terns most commonly seen
feeding within a few miles of the coast during the day, and they often occurred
in mixed flocks. Both eat mainly small fish and some squid, but Pr. cerulea
also takes a substantial number of small crustaceans and insects. The represen-
tation of the fish families is also different in the two species, tiny Gempylidae
being of outstanding importance in the diet of Pr. cerulea. Since these two
species feed together using very similar methods, but differ so much in body
weight and bill size (Table 8), it seems likely that the most fundamental differ-
ence in their feeding ecology lies in the size of item that they are best adapted
to catch; the difference in representation of the various fish families could
follow directly from this. However, Pr. cerulea also exploits two food sources
—marine water striders and small planktonic crustaceans—which are not uti-
lized by any of the other terns. It seems probable that the feeding action re-
quired for collecting food of this kind is impossible or uneconomic for larger
species. It is of interest in this connection that although Pr. cerulea is so much
the smallest of the terns of Christmas Island, the mean volume of the items
which it ate, and also the volume of the largest items, were much smaller rela-
tive to body weight than in the other species. This was reflected also in the fact
that although the regurgitations were small in relation to body weight, they con-
tained, on average, far more items than those of the larger terns. It thus ap-
pears that although Pr. cerulea is exploiting the smallest prey available to sea
birds in the area of Christmas Island, its body size is rather larger than might
have been expected. In fact, there are few sea birds smaller than Pr. cerulea,
and it may be that certain characteristics of their environment make extremely
small size uneconomic for sea birds.
This discussion has been restricted so far to the five species of terns whose
diets were studied, since their coexistence on a single island is of special interest.
However, it is worthwhile to consider briefly the other three species for which
we have data. Ph. rubricauda needs little comment, since its diet, and probably
also its method of feeding, are very different from those of the other species.
A high proportion of the fish and squid which it obtains are effectively outside
the size range of prey of any other species studied, while the representation of
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 101
fish families and of squid species is distinct from that in the other birds; it
seems probable that Ph. rubricauda feeds largely on dispersed fish and squid
and is relatively independent of the predatory activity of fish schools to make its
prey available. This conclusion is reasonable in the light of the observations
of Jespersen (1929), who found that scattered tropic-birds (Ph. leptwrus)
were the characteristic birds of the Sargasso Sea. This area is very poor in zoo-
plankton and presumably also in forage animals, and very few other birds were
seen there. For species feeding on scarce, dispersed prey, the ability—pos-
sessed by tropic-birds—to exploit prey of a very wide range of sizes may be a
critical adaptation; such species cannot afford to be food specialists (cf. Mac-
Arthur and Levins 1964). Ph. rubricauda probably does not compete appreci-
ably with any of the terns, or with either of the two petrels which were studied;
however, a comparison of its diet with those of the boobies of Christmas Island
would be of interest.
Some of the shearwaters (Puffinus spp.) share with tropic-birds and boobies
the ability to catch prey well below the surface of the water (Kuroda 1954).
They thus contrast with the tropical terns, which probably never obtain
prey more than a few inches below the surface. Of the two shearwaters oc-
curring on Christmas Island, samples were obtained only from P. nativitatis.
Although no observations could be made on its feeding habits, it is highly
adapted for swimming (Kuroda 1954), and doubtless obtains much of its food
below the surface. The way in which competition for food between the tropical
terns and shearwaters is minimized is immediately suggested by a personal ob-
servation on a mixed flock of noddies (Anous spp.) and P. pacificus near
Hawaii. On that occasion a school of tunas was clearly present, but the tunas
were not feeding actively at the surface, and no prey animals were seen jumping.
The noddies (mainly A. stolidus) were not fishing to any extent, and were evi-
dently waiting for prey to become more available, but the shearwaters were
diving from the air, sometimes remaining submerged for several seconds. Shear-
waters are doubtless largely dependent on tuna schools to make their prey
available, but for the diving species it is not essential that the prey be actually
at the surface. Therefore, provided that the total numbers of the prey are
limited mainly by factors other than predation by birds, there is no reason to
suppose that diving shearwaters compete significantly with terns.
Nevertheless, since shearwaters and terns often flock together over the same
tuna schools, one may expect their diets to be very similar in composition. In
the present study, there was a close similarity in the proportions of fish, squid
and other items, and in the representation of the various fish families, between
P. nativitatis and the two large terns, S. fuscata and A. stolidus. However, P.
nativitatis, in spite of its greater body weight, took a much larger proportion of
small fish than the large terns. This suggests that P. nativitatis is adapted to
catching—under water—fish smaller than S. fuscata and A. stolidus can eco-
nomically obtain at the surface. However the size-distribution of the squid eaten
was almost identical in the two large terns and in P. nativitatis and Pt. alba.
Pt. alba has a rather different diet, and evidently employs feeding methods
different from both the terns and P. nativitatis. It does not swim under water
like the latter species, and probably obtains most of its food—including many
102 PEABODY MUSEUM BULLETIN 24
very small items—by Dipping. However, as pointed out earlier, its economic
flight and its powerful cutting bill enable it also to exploit the presence in the
ocean—at very low density—of floating objects such as dead squid and fish.
It appears from this discussion of the feeding ecology of the sea birds studied,
that four main types of differences are important in reducing interspecific com-
petition between them to the level at which they can all coexist. First, there is
difference in the time of day at which most feeding occurs; although we have
few relevant data, it appears to be one of the factors important in separating
G. alba and A. tenuirostris, two species which take food rather similar in size.
Second, there is difference in feeding zone, in relation to the position of the
island on which breeding (and in some cases roosting) occurs; this is probably
critical in separating S. fuscata and A. stolidus and may be significant also be-
tween G. alba and A. tenuirostris. A difference in feeding zones is not quite
equivalent to a difference in habitat in terrestrial birds, since the sea birds may
be feeding on the same kinds of food and catching them in areas which are
very similar except in their distance from land. The ability to feed very far from
the breeding colony requires special adaptations, but the species feeding
closer to the colony must have some advantage there. We have suggested that A.
stolidus is more maneuverable than S. fuscata and more versatile in its feeding
behavior, thus probably exploiting the resources in its feeding zone more effi-
ciently than the latter species.
Differences in feeding methods, accompanied by structural specialization
and resulting in the exploitation of significantly different food sources, is the
third way in which ecological segregation is achieved. Feeding methods
and structural adaptations are generally similar in congeneric species, so one
may expect differences in feeding methods to be important in reducing inter-
specific competition mainly among less closely related species. ‘Thus, whereas all
the terns studied obtain their prey by diving from above and catching it at the
surface, P. nativitatis has the ability to catch active prey by pursuing them when
they are well below the surface. In Pt. alba different food sources are made
available by adaptations of the bill and by exceptionally efficient flight, while
Ph. rubricauda probably specializes in catching large, dispersed fish and squid
swimming below the surface.
Finally, there is separation by differences in size of body and of bill, accompa-
nied by choice of food items of different sizes. It has been recognized for about
25 years that size differences in food are often important in permitting the coex-
istence of species with otherwise similar ecology (Huxley 1942, Lack 1944, and
other references in Schoener 1965). Hutchinson (1959) in an attempt to place
quantitative limits on the extent of such differences which are necessary to per-
mit coexistence of two species, presented data on the ratios of the culmen
lengths of pairs of congeneric bird species in areas of sympatry. Since then, cul-
men length ratios of large numbers of pairs of species have been used in gen-
eral discussions of “niche size” (Klopfer and MacArthur 1961, Klopfer 1962,
Schoener 1965). Schoener has pointed out that Klopfer and MacArthur’s pre-
liminary conclusion that culmen length ratios among pairs of tropical species
are lower than those of temperate zone species is not confirmed by a more ex-
tensive compilation of data. Schoener considered that differences in ratios be-
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 103
tween different groups of species are most closely related to the kinds of food
which they eat. However, at this stage it seems worthwhile to re-emphasize the
fact that although culmen length is a convenient characteristic related to feed-
ing, it is a very unreliable index to the feeding ecology of a species. Our data
for the two species of Anous illustrate the danger: the smaller species has a
slightly longer culmen, but eats much smaller food items. Probably any natural-
ist looking at the birds in the flesh (or the photographs in Fig. 6) would pre-
dict correctly the relative sizes of their prey, but comparison of culmen lengths
alone would suggest that they ate prey of very similar size. We do not want to
deny the usefulness of culmen length ratios in comparing large numbers of pairs
of species, but merely to point out the necessity for caution in interpreting the
results, and the need for detailed studies of the overall feeding ecology of criti-
cal groups of birds.
It is of interest to note that although the five tern species fall into three
groups in terms of body weight and also of size of prey (S. fuscata and A.
stolidus; G. alba and A. tenutrostris; and Pr. cerulea), the bill lengths of the first
four species (and also of Sterna lunata, which was not studied) are very similar
to each other (Table 8). Since these four species all catch their prey when it
becomes available momentarily at or above the surface, the speed with which
the bill can be closed on the prey will be of great importance. As pointed out by
Beecher (1962), a long bill is capable of greater speed at the tip than a shorter,
more powerful one. Furthermore, the greater reach conferred by a long bill
may help in catching prey a little below the surface. However, considerable force
is required to retain a grip on a struggling prey animal, and—other things being
equal—the force which a bird can apply near the tip of its bill is inversely
related to the length of the bill. Thus the observed bill length of each species
must represent a critical compromise, which could be understood completely
only by a full functional analysis of the skull architecture and musculature
(see, for instance, Bowman 1961, Beecher 1962, Zusi 1962, Bock 1966). How-
ever, viewing the situation in its simplest terms, it appears that to evolve the
ability to exploit larger prey, without a sacrifice in bill length, a tern must in-
crease the force of the mechanical system for closing the bill. This will normally
involve an increase in the mass of the muscles and bones involved, while a
stronger (and therefore heavier) bill will also be required. Changes of this
kind will create mechanical and aerodynamic problems whose solution will
usually result in an increase in general body size. Furthermore, increase in size
with increase in size of prey may also tend to result from the fact that sea birds
such as terns which normally swallow their prey in flight (probably because of
the danger of settling on the surface where large fish are feeding), need to be
able to lift their prey from the surface in their bills.
We have included in Table 8 some dimensional relationships relevant to
consideration of the structural adaptations associated with exploitation of prey
of different sizes. It can be seen that S. fuscata and A. stolidus have evolved
very similar relationships between body size and bill size, and this is reflected
in the generally similar size of their prey. (The slightly stouter bill of A. stolv-
dus suggests that it may be able to tackle fish and squid a little bigger than S.
fuscata, and our data give some support to this possibility: Table 4 and Fig. 4.)
104 PEABODY MUSEUM BULLETIN 24
It is of interest to compare the dimensions of these two species with those of
Larosterna inca (Lesson), the Inca Tern, which is endemic to the Humboldt
Current region. It is a close relative of the noddies (Anous spp.), and has a
wing length almost the same as A. stolidus and S. fuscata (mean of 11 adults
280 mm), but it is about 20% heavier (mean of 13 adults 209 g). The bill is a
little longer (mean of 11 adults 45.2 mm), and is also substantially stouter than
those of A. stolidus and S. fuscata: its cross-section area at the proximal end of
the gonys is estimated as 31.0 sq.mm; the square root of this divided by culmen
length gives a figure of .123 (cf. .110 and .100 for A. stolidus and S. fuscata—
Table 8). It seems likely that the heavier weight and stouter bill of Larosterna
inca than of the two tropical oceanic terns are adaptations related to the fact
that by far the most abundant fish in its habitat is the Peruvian Anchovy
(Engraulis ringens), which commonly reaches lengths of 15 or 16 cm: it would
clearly be disadvantageous for Larosterna inca not to be able to exploit fish of
a size which at certain times form a high proportion of the total fish population
of the area. Fish more than 12 cm long are exceptional in the diet of S. fuscata,
and in our samples they were almost all long but thin fish; A. stolidus also
obtained very few fish between 12 and 16 cm long. Larosterna inca, on the other
hand, does take anchovies 14-16 cm long when they are available (N. P. Ash-
mole, unpublished).
A. tenuirostris, which is little more than half the weight of A. stolidus, but
has a slightly longer bill, has apparently gone far in the direction of main-
taining reach, and speed at the bill tip, at the cost of force. In such a species
the maximum size of the prey will be limited by the force which the bird can
exert near the tip of its bill; our data show that A. tenuirostris is indeed a
specialist in catching small prey. Since fish are more muscular than squid, it is
possibly significant that there is apparently a greater difference in the size of the
biggest fish taken by A. stolidus and by A. tenuirostris than there is in the size
of the biggest squid (Fig. 4 and Table 4). This line of reasoning makes it clear
why A. tenuirostris has such a slender bill (Fig. 6 and Table 8). The maximum
size of its prey is low because of the length of the bill, and additional strength
of the bill beyond the minimum necessary to avoid undue risk of breakage would
merely add unnecessary weight. G. alba is a little heavier than A. tenuirostris,
and has a slightly shorter and stouter bill; these factors, and perhaps also differ-
ences in its jaw mechanics, may account for the ability of G. alba to catch some
fish substantially larger than any taken by A. tenuirostris.
Small size, especially when associated with a relatively long bill, severely
limits the size of active prey which can be captured. However, it also confers
certain advantages. For instance, it is clear that the energy expenditure in-
volved in hunting by Dipping to the surface and returning to a height will be
so great as to make this feeding method uneconomic if the potential prey is be-
low a certain size. However, most terns cannot stay near the surface con-
tinuously while hunting, because reflections at the surface must prevent a bird
from seeing potential prey below the surface except in the area more or less
vertically below it: the higher the bird, the greater is the area in which visi-
bility will be adequate. Thus for a bird searching for fairly large and rela-
tively scarce prey, it is generally best to fly a few meters above the surface, swoop-
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 105
ing very rapidly when prey is sighted. Pr. cerulea, on the other hand, reduces
the energy expended in feeding by remaining close to the surface, using its feet
to push off from the water. There it can feed on numerous but small prey, and
it has doubtless evolved its small body size as an adaptation for minimizing
total food requirements. Furthermore, since it is almost certain that within a
group of similar species agility is inversely related to size, Pr. cerulea is prob-
ably better adapted than its larger relatives for catching small, highly mobile
prey animals. Members of the Pacific Ocean Biological Survey Program have
specifically noted that it is more maneuverable than the larger noddies (Gould,
pers. comm.), and it may be this which enables it to catch water striders, which
are not taken by any of the other terns. However, being so small, Pr. cerulea
cannot afford a very long bill because this would not provide adequate force
at the tip.
It may thus be concluded that it is primarily by reaching different morpho-
logical compromises related to differences in size, and by evolving appropriate
differences in feeding behavior, that the three species of noddies—A. stolidus,
A. tenuirostris and Pr. cerulea—are able to coexist in an area where prey ani-
mals of a wide variety of sizes are available at the surface.
SUMMARY
(The numbered sections correspond with the sections of the paper)
During nine visits to Christmas Island (Equatorial Pacific Ocean) be-
tween March 1963 and June 1964, 800 food samples (mainly regurgita-
tions) were obtained from eight species of sea birds: Phaethon rubricauda,
Puffinus nativitatis, Pterodroma alba, Sterna fuscata, Anous stolidus, Gygis
alba, Anous tenuirostris and Procelsterna cerulea. ‘These included all the
most abundant of the smaller members of the sea bird community, which
totals 17 species.
Methods used in previous studies of the food of birds (and fish) are dis-
cussed, and it is concluded that as well as analysis by number, by volume, and
by frequency of occurrence of the various food classes, the sizes of the food
items should be determined whenever possible. In the present study the
food items from each of the preserved samples were sorted into three main
classes—fish, squid, and other invertebrates—and identified as far as pos-
sible. Volumes were determined individually for all items, and the lengths
of the fish and squid were measured or estimated.
In the Species Accounts each bird species is considered under the head-
ings of Status, General description and condition of samples, Quantitative
composition of samples, Size of food items, and Identifications of food
items. The previous literature on the food of each species is briefly re-
viewed.
Fish and squid formed the bulk of the food of all the species. Fish were
especially important in A. tenuirostris and Pr. cerulea, and squid in Pt.
alba and P. nativitatis. The remaining four species took roughly equal
volumes of fish and squid, but the individual fish were on average smaller
than the squid, except in Ph. rubricauda. Only Pr. cerulea and Pt. alba
took many other invertebrates (mainly water striders and Crustacea), and
they were mostly very small.
Ph. rubricauda took some fish and squid much larger than any eaten by
the other birds. The fish and squid obtained from P. nativitatis were very
similar in size to those from Pt. alba (although Pt. alba also ate parts of
much larger squid), and both these species took fewer large fish than S.
fuscata and A. stolidus, which are smaller birds. Among the smaller terns,
which ate generally smaller items, G. alba took more large fish than A.
tenuirostris, which took many very small ones, while the diet of Pr.
cerulea contained an even higher proportion of tiny items.
Representatives of 33 fish families were found in the samples, but only
12 of these constituted more than 1% by number of all the identified fish.
106
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 107
Exocoetidae (including halfbeaks) were the most important single family,
ranking first in five of the bird species: however, in G. alba Blenniidae
barely ranked higher, in Pr. cerulea Gempylidae were far more important,
while there are no data for Pt. alba. Among the species in which Exo-
coetidae were predominant, the rest of the fish portion of the diet was
made up mainly of the same few families in P. nativitatis, S. fuscata and A.
stolidus, while in A. tenuirostris more families were important, and Ph.
rubricauda exploited—in addition to Exocoetidae—three families not much
eaten by the other birds.
The vast majority of the cephalopods taken by the birds were Ommas-
trephidae of the genus Symplectoteuthis, but a species of Abralia (Enoplo-
teuthidae) was of some importance in G. alba, and a number of addi-
tional squid families were represented in the diet of Pt. alba.
Analysis of data on the food of Yellowfin Tuna caught at the surface
close to Christmas Island and other islands in the same area, showed large
differences between the diets of these fish and the birds, although a large
proportion of the items eaten by the birds are made available at the sur-
face only by the feeding activities of tunas. Fewer squid and more other in-
vertebrates are eaten, and the representation of the various fish families is
very different. The differences probably arise mainly because certain kinds
of prey do not come to the surface even when pursued by tunas, while
other kinds (e.g., Exocoetidae) are especially subject to avian predation
while escaping from tunas,
Available information on the tropical marine environment of the birds
is discussed. Localized concentrations of plankton and nekton produced by
convergence and sinking of surface waters at ‘fronts,’ which have been sug-
gested as exerting important effects on the distribution of surface schools
of tunas in the open ocean, may also provide favorable feeding grounds
for many oceanic birds. Concentrations of tunas and birds in inshore waters
are produced by rather different factors, although eddies near islands may
share some properties with oceanic fronts. For those bird species which are
capable of feeding under conditions of low light intensity, the vertical
migration of forage animals to the surface at night may be an important
additional feature of the environment.
In assessing the feeding zones of the different species, use is made both
of direct evidence and of deductions from the length of the incubation
shifts and the proportions of reef-originating fish in the diets. Of the birds
studied, Pr. cerulea and A. tenuirostris fish largely within a few miles of the
island, while A. stolidus probably ranges somewhat further out to sea; G.
alba sometimes fishes close inshore, but is capable of feeding far from the
island. Probably all the other species regularly feed up to hundreds of miles
away, perhaps especially in the Equatorial Countercurrent: their long in-
cubation shifts and the fact that their chicks do not need frequent feeding
help to make this possible. It is not yet known whether any of these species
can delay digestion of food brought back to the young, but the secretion of
108
PEABODY MUSEUM BULLETIN 24
stomach oil by many species of petrels is viewed as an alternative adapta-
tion, which permits them to forage at great distances from the colony,
even when they are breeding.
All the birds studied catch their prey above, at, or within a short dis-
tance below the surface of the water. However, their feeding methods (de-
fined in Fig. 7) differ considerably, as do the associated morphological
adaptations. Ph. rubricauda, which feeds by Air Diving, exploits prey fur-
thest below the surface, but P. nativitatis also catches some prey below the
surface, although it doubtless also Feeds at Surface, and perhaps also by
Plunging to Surface or Dipping. Pt. alba evidently sometimes Feeds at
Surface, but Dipping may be more important. All five species of terns
feed primarily by Dipping and Plunging to Surface, the most fundamental
difference being the utilization by the noddies (Pr. cerulea, A. tenutros-
tris, and A. stolidus) of their extensively webbed feet to keep them just
above the water surface when feeding, which is a habit not shared by S.
fuscata and G. alba, whose feet are much smaller in area. The noddies
probably do not feed much at night, but the two petrels and S. fuscata al-
most certainly sometimes do so, and G. alba feeds actively at dawn, and
perhaps also at dusk.
Seasonal changes in the Central Equatorial Pacific are certainly not as
pronounced as in most marine areas, but there are still too few data to
determine the existence or extent of regular seasonal changes in the
availability of food for the sea birds of the region.
Data on the food of the birds in the different sampling periods suggests
that seasonal changes in the availability of different kinds or sizes of food
are not of great importance for most of the species. However, A. tenuiros-
tris took a far greater proportion of small fish in May 1963 and June
1964 than in the other sampling periods, suggesting an early summer peak
in the numbers of small fish in inshore waters.
At all times of year several species of sea birds may be found breeding
on Christmas Island. The species (including A. tenutrostris) with a single,
more or less definite, breeding season mostly have it in summer, but Pr.
cerulea breeds in autumn. The most numerous species (S. fuscata) has
sharp breeding seasons in both summer and winter, while some species
can be found breeding at any time, though not always in the same num-
bers.
It is argued that although there may be a shortage of optimal nest sites
on Christmas Island for certain of the bird species, populations of most of
them were probably controlled primarily by competition for available food,
before the advent of man. Thus although the populations may not all be in
equilibrium at the present time, it is of interest to consider the differences
in the feeding ecology of the various species which have permitted them to
coexist.
It is concluded that among the species which are not closely related, com-
petition is reduced mainly by differences in feeding methods, permitting
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 109
different species to exploit different types of food, or allowing members of
one species to capture prey unavailable at that moment to another species.
Also significant are the ability of at least one species to hunt under con-
ditions of low light intensity, and adaptations which enable some species
to feed at great distances from the colony, even when breeding. Among
the most closely related species, differences in body size, and in the other
morphological characteristics determining the size of prey which each
species can exploit most efficiently, are of critical importance in reducing
interspecific competition to the level at which coexistence is possible.
ACKNOWLEDGMENTS
The field work on Christmas Island was undertaken while N.P.A. was the
holder of a Yale/Bishop Museum Fellowship. We are most grateful to S.
Dillon Ripley and H. Laurence Achilles, who made this arrangement possible,
and to Roland W. Force, who gave us both niches in the Bishop Museum, and
enabled M.J.A. to do the main part of the analysis there. For help with trans-
portation and for generous hospitality, we gratefully acknowledge the Royal
Air Force and the members of the R.A.F. Officers’ Mess, Christmas Island, and
also Percy Roberts, District Commissioner. Philip Helfrich kindly arranged for
the loan of a small boat from the Hawaii Marine Laboratory.
Without the help of Gareth J. Nelson, James W. Atz and Donald W. Stras-
burg, the task of identifying the fish would have been formidable; they
gave us much of their time and it is a pleasure to thank them here. Malcolm
R. Clarke identified a large number of squid for us; we are most grateful for
his assistance, which was indispensable with this difficult group. In addition,
we received help over various problems of identification from Georgiana
B. Deevey, Willard D. Hartman, Robert T. B. Iversen, Giles W. Mead and
Robert L. Usinger.
We are deeply indebted to Garth I. Murphy and Richard S. Shomura, who
allowed us to make extensive use of their manuscript “The abundance of tunas
in the Central Equatorial Pacific in relation to the environment” in advance of
publication; John J. Magnuson gave us access to data on the food of Yellowfin
Tuna, from the records of the Bureau of Commercial Fisheries Biological
Laboratory, Honolulu. Through the kindness of Philip S. Humphrey and Patrick
J. Gould, we have been able to use data on bird numbers on Christmas Island
collected by the Pacific Ocean Biological Survey Program of the Smithsonian
Institution, and to quote a number of unpublished observations on feeding
habits. In addition, we have benefited from discussion or correspondence with
Roger S. Bailey, John R. Brooks, G. Evelyn Hutchinson, Joseph R. King,
Charles G. Sibley and George E. Watson.
Dean Amadon allowed us to measure specimens in the collection of the
American Museum of Natural History. Tony Garcia helped extensively with the
laboratory analysis, while John Howard and Carl Wester showed great skill in
the preparation of the illustrations.
We are exceedingly grateful to all these people, and it is a pleasure to thank
them here.
LITERATURE CITED
Anderson, William G., 1954. Notes on food habits of sea birds of the Pacific. Elepaio 14:
80-84.
Arata, George F., 1954. A note on the flying behavior of certain squids. Nautilus 68: 1-3.
Arimoto, K., 1962. The role of marine and fresh-water foods in the Japanese diet, p.
361-375. In Georg Borgstrom [ed.] Fish as food, 2. Academic Press, New York and
London.
Ashmole, N. P., 1961. The biology of certain terns. D. Phil.thesis, Oxford University.
, 1962. The Black Noddy Anous tenuirostris on Ascension Island. Part 1. General
biology. Ibis 103b: 235-273.
, 1963a. The regulation of numbers of tropical oceanic birds. Ibis 103b: 458-473.
, 1963b. The biology of the Wideawake or Sooty Tern Sterna fuscata on Ascension
Island. Ibis 103b: 297-364.
Ashmole, N. Philip, 1965. Adaptive variation in the breeding regime of a tropical sea
bird. Nat. Acad. Sci., Proc. 53: 311-318.
. In press. Breeding and molt in the White Tern (Gygis alba) on Christmas Island,
Pacific Ocean. Condor.
Audubon, John James, 1835. Ornithological biography, or an account of the habits of the
birds of the United States of America. Adam & Charles Black, Edinburgh. Vol. 3.
Austin, Thomas S., 1960. Oceanography of the east central equatorial Pacific as observed
during expedition Eastropic. U.S. Fish and Wildlife Serv., Fish. Bull. 60 (168):
257-282.
Bailey, R. S., 1965. Cruise of R.R.S. Discovery in the Indian Ocean. Sea Swallow 17: 52-56.
Bailey, Roger, 1966. The sea-birds of the southeast coast of Arabia. Ibis 108: 224-264.
Baker, A. de C., 1960. Observations of squid at the surface in the NE Atlantic. Deep-Sea
Research 6: 206-210.
Baker, Rollin H., 1947. Observations on the birds of the North Atlantic. Auk 64: 245-259.
, 1948. Report on collections of birds made by United States Naval Medical Re-
search Unit No. 2 in the Pacific war area. Smithsonian Misc. Coll. 107, No. 15.
74 p.
, 1951. The avifauna of Micronesia, its origin, evolution, and distribution. Univ,
Kansas Mus. Nat. Hist., Publ. 3(1). 359 p.
Barkley, Richard A., 1962. A review of the oceanography of the Central Pacific Ocean in
the vicinity of the Line Islands. Multilithed by the Biological Laboratory, Hono-
lulu, of the Bureau of Commercial Fisheries, U.S. Fish and Wildlife Service.
Bates, Donald H., 1950. Tuna trolling in the Line Islands in the late spring of 1950.
USS. Fish and Wildlife Serv., Fishery Leaflet 351. 32 p.
Beebe, William, 1926. The Arcturus adventure. G. P. Putnam’s Sons, New York. 439 p.
Beecher, William J., 1962. The bio-mechanics of the bird skull. Chicago Acad. Sci., Bull.
11 (2): 10-33.
Belopol’skii, L{[ev] Ofsipovich], 1957. Ecology of sea colony birds of the Barents Sea.
(Translation 1961, by Israel Program for Scientific Translations.) Acad. Sci. USSR,
Karelian Branch. 346 p.
110
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS Lit
Bock, Walter, 1966. An approach to the functional analysis of bill shape. Auk 83: 10-51.
Bourne, W. R. P., 1957. The Sooty Petrel of Latham, Fregetta fuliginosa (Gmelin). Brit.
Orn. Club, Bull. 77: 40-42.
, 1959. Notes on sea reports received 1958-59. Sea Swallow 12: 6-17.
, 1963. A review of oceanic studies of the biology of seabirds. Proc. XIII Intern.
Ornithol. Congr.: 831-854.
, 1965. Comment [on paper by Bruyns 1965]. Sea Swallow 17: 65-66.
Bowmaker, A. P., 1963. Cormorant predation on two central African lakes. Ostrich 34:
2-26.
Bowman, Robert I., 1961. Morphological differentiation and adaptation in the Galapagos
finches. Univ. Calif. Publ. Zo6l. 58. 326 p.
Brooks, S. C., 1934. Oceanic currents and the migration of pelagic birds. Condor 36:
185-190.
Brown, R. G. B., and D. E. Baird, 1965. Social factors as possible regulators of Puffinus
gravis numbers. Ibis 107: 249-251.
Bruyns, W. F. J. Morzer, 1965. Birds seen during west to east trans-Pacific crossing along
Equatorial Counter-current around latitude 7°N. in the autumn of 1960. Sea
Swallow 17: 57-65.
, and K. H. Voous, 1965. Night-feeding by Sooty Tern (Sterna fuscata). Ardea
Bae i.
Carrick, R., 1959. The food and feeding habits of the Straw-necked Ibis, Threskiornis
spinicollis (Jameson), and the White Ibis, T. molucca (Cuvier), in Australia.
CSIRO Wildl. Res. 4: 69-92.
Carter, Charlie Lyons, and John Malcolm, 1927. Observations on the biochemistry of
“mutton bird” oil. Biochemical J. 21: 484-493.
Clarke, M. R., 1965. Large light organs on the dorsal surfaces of the squids Ommastrephes
pteropus, ‘Symplectoteuthis oualaniensis’ and ‘Dosidicus gigas.’ Malacol. Soc. Lond.,
Proc. 36: 319-321.
Clarke, Malcolm R., 1966. A review of the systematics and ecology of oceanic squids. Adv.
Mar. Biol. 4: 91-300.
Collins, J. W., 1899. The shearwaters and Fulmar as birds and bait. Osprey 4: 35-42.
Cromwell, Townsend, 1953. Circulation in a meridional plane in the Central Equatorial
Pacific. J. Mar. Res. 12: 196-213.
, and Joseph L. Reid, 1956. A study of oceanic fronts. Tellus 8: 94-101.
Crook, John Hurrell, 1965. The adaptive significance of avian social organizations. Zool.
Soc. Lond., Symp. 14: 181-218.
Cullen, J. M., and N. P. Ashmole, 1963. The Black Noddy Anous tenutrostris on Ascen-
sion Island. Part 2. Behaviour. Ibis 103b: 423-446.
David, P. M., 1965. The Neuston net: a device for sampling the surface fauna of the
ocean. J. Mar. Biol. Ass. U.K. 45: 313-320.
Davies, P. W., and D. W. Snow, 1965. Territory and food of the Song Thrush. Brit. Birds
58: 161-175.
Davis, Peter, 1957. The breeding of the Storm Petrel. Brit. Birds 50: 85-101, 371-384.
Dixon, Keith L, 1961. Habitat distribution and niche relationships in North American
species of Parus, p. 179-216. In W. Frank Blair [ed.] Vertebrate speciation. Univer-
sity of Texas Press, Austin.
Dobben, W. H. Van, 1952. The food of the Cormorant in the Netherlands. Ardea 40:
1-63.
Dorward, D. F., 1962. Comparative biology of the White Booby and the Brown Booby
Sula spp. at Ascension. Ibis 103b: 174-220.
, 1963. The Fairy Tern Gygis alba on Ascension Island. Ibis 103b: 365-378.
112 PEABODY MUSEUM BULLETIN 24
, and N. P. Ashmole, 1963. Notes on the biology of the Brown Noddy Anous
stolidus on Ascension Island. Ibis 103b: 447-457.
Eisenmann, Eugene, 1955. The species of Middle American birds. Linn. Soc. N. Y.,
Trans. 7. 128 p.
Falla, R. A., 1934. The distribution and breeding habits of petrels in Northern New Zea-
land. Auckland Inst. Mus., Rec. 1: 245-260.
Fields, W. Gordon, 1965. The structure, development, food relations, reproduction, and
life history of the squid Loligo opalescens Berry. Calif. Dept. Fish and Game, Fish
Bull. 131. 108 p.
Fisher, James, 1952. The Fulmar. Collins, London. 496 p.
, 1966. The Fulmar population of Britain and Ireland, 1959. Bird Study 13: 5-76.
Fisher, Walter K., 1906. Birds of Laysan and the Leeward Islands, Hawaiian group. U.S.
Fish Commission, Bull. 23 (1903): 767-807.
Frith, H. J., 1959. The ecology of wild ducks in inland New South Wales. III. Food
habits. CSIRO Wildl. Res. 4: 131-155.
Gallagher, M. D., 1960. Bird notes from Christmas Island, Pacific Ocean. Ibis 102: 489-502.
Gause, G. F., 1934. The struggle for existence. Williams and Wilkins Co., Baltimore.
163 p.
Gibb, J. A., and Monica M. Betts, 1963. Food and food supply of nestling tits (Paridae)
in Breckland pine. J. Anim. Ecol. 32: 489-533.
Gibson-Hill, C. A., 1947. The normal food of tropic-birds (Phaéthon spp.). Ibis 89:
658-661.
, 1950. Notes on the birds of the Cocos-Keeling Islands. Raffles Mus., Bull. 22:
212-270.
, 1951. Notes on the nesting habits of seven representative tropical sea birds.
Bombay Nat. His. Soc., J. 48: 214-235.
Gould, Patrick J. In press. Nocturnal feeding of Sterna fuscata and Puffinus pacificus.
Condor.
Greenwood, P. Humphry, Donn E. Rosen, Stanley H. Weitzman, and George S. Myers,
1966. Phyletic studies of teleostean fishes, with a provisional classification of living
forms. Amer. Mus. Nat. Hist., Bull. 131 (4): 339-456.
Hailman, Jack P., 1964. The Galapagos Swallow-tailed Gull is nocturnal. Wilson Bull.
76: 347-354.
Hardy, A. C., 1928. The work of the Royal Research Ship “Discovery” in the Depend-
encies of the Falkland Islands. Geogr. J. 72: 209-234.
Harris, M. P., 1965. The food of some Larus gulls. Ibis 107: 43-53.
Hartley, P. H. T., 1948. The assessment of the food of birds. Ibis 90: 361-381.
Hedgpeth, Joel W., 1957. Classification of marine environments, p. 17-27. In Joel W.
Hedgpeth [ed.] Treatise on marine ecology and paleoecology. Geol. Soc. Amer.,
Mem. 67 (1). 1296 p.
Hersey, J. B., and R. H. Backus, 1962. Sound scattering by marine organisms, p. 498-539.
In M.N. Hill [ed.] The sea, 1. Interscience, New York.
Heyerdahl, Thor, 1950. The Kon-Tiki expedition. George Allen and Unwin Ltd., Lon-
don. 235 p.
Hinde, Robert A., 1966. Animal behaviour: a synthesis of ethology and comparative psy-
chology. McGraw-Hill, New York. 534 p.
Hindwood, K. A., 1940. The birds of Lord Howe Island. Emu 40: 1-86.
Hutchinson, George Evelyn, 1950. The biogeochemistry of vertebrate excretion. Amer.
Mus. Nat. Hist., Bull. 96. 554 p.
Hutchinson, G. E., 1959. Homage to Santa Rosalia or Why are there so many kinds of
animals? Amer. Nat. 93: 145-159.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 13
Huxley, Julian, 1942. Evolution. The modern synthesis. Harper and Brothers, New York
and London. 645 p.
Ikehara, Isaac I., 1953. Live-bait fishing for tuna in the central Pacific. U.S. Fish and
Wildlife Serv., Spec. Sci. Rep., Fisheries 107. 20 p.
Jespersen, P., 1929. On the frequency of birds over the High Atlantic Ocean. Verh. VI
Intern. Orn. Kongr., Kopenhagen 1926: 163-172.
Kahl, M. Philip, 1964. Food ecology of the Wood Stork (Mycteria americana) in Florida.
Ecol. Monogr. 34: 97-117.
King, Joseph E., 1955. Annotated list of birds observed on Christmas Island, October to
December 1953. Pacif. Sci. 9: 42-48.
, and Joan Demond, 1953. Zooplankton abundance in the Central Pacific. U.S.
Fish and Wildlife Serv., Fish Bull. 54 (82): 111-144.
, and Thomas S. Hida, 1957. Zooplankton abundance in the Central Pacific, Part
II. U.S. Fish and Wildlife Serv., Fish. Bull. 57 (118): 365-395.
, and Isaac I. Ikehara, 1956. Comparative study of food of Bigeye and Yellowfin
tuna in the Central Pacific. U.S. Fish and Wildlife Serv., Fish. Bull. 57 (108):
61-85.
, and Robert T. B. Iversen, 1962. Midwater trawling for forage organisms in the
Central Pacific 1951-1956. U.S. Fish and Wildlife Serv., Fish. Bull. 62 (210): 271-
321.
, and Robert L. Pyle, 1957. Observations on sea birds in the tropical Pacific.
Condor 59: 27-39.
Klopfer, Peter H., 1962. Behavioral aspects of ecology. Prentice-Hall, New Jersey. 166 p.
, and R. H. MacArthur, 1961. On the causes of tropical species diversity: niche
overlap. Amer. Nat. 45: 223-226.
Knauss, John A., 1957. An observation of an oceanic front. Tellus 9: 234-237.
Kritzler, Henry, 1948. Observations on behavior in captive fulmars. Condor 50: 5-15.
Kuroda, Nagahisa, 1954. On the classification and phylogeny of the Order Tubinares,
particularly the shearwaters (Puffinus), with special considerations on their osteol-
ogy and habit differentiation. Herald Co. Ltd., Tokyo. 179 p.
, 1955. Observations on pelagic birds of the Northwest Pacific. Condor 57: 290-300.
Lack, David, 1944. Ecological aspects of species-formation in passerine birds. Ibis 86:
260-286.
, 1945. The ecology of closely related species with special reference to Cormorant
Phalacrocorax carbo and Shag P. aristotelis. J. Anim. Ecol. 14: 12-16.
, 1946. Competition for food by birds of prey. J. Anim. Ecol 15: 123-129.
, 1947. Darwin’s finches. Cambridge University Press. 208 p.
Lane, Frank W., 1957. Kingdom of the octopus. Jarrolds, London. 287 p.
Lewis, R. W., 1966. Studies of the glyceryl ethers of the stomach oil of Leach’s Petrel
Oceanodroma leucorhoa (Viellot). Comp. Biochem. Physiol. 19: 363-377.
Loomis, Leverett Mills, 1918. A review of the albatrosses, petrels, and diving petrels.
Calif. Acad. Sci., Proc. 2 (2), No. 12: 1-187.
MacArthur, Robert H., 1958. Population ecology of some warblers of northeastern
coniferous forests. Ecology 39: 599-619.
MacArthur, Robert H., and Richard Levins, 1964. Competition, habitat selection, and
character displacement in a patchy environment. Nat. Acad. Sci., Proc. 51: 1207-
1210.
McGary, James W., 1955. Mid-Pacific oceanography, Part VI, Hawaiian offshore waters,
December 1949-November 1951. U.S. Fish and Wildlife Serv., Spec. Sci. Rep.,
Fisheries 152. 138 p.
114 PEABODY MUSEUM BULLETIN 24
Madsen, F. Jensenius, 1957. On the food habits of some fish-eating birds in Denmark.
Danish Rey. Game Biol. 3: 19-83.
Madsen, F. Jensenius, and R. Sparck, 1950. On the feeding habits of the Southern
Cormorant (Phalacrocorax carbo sinensis Shaw) in Denmark. Danish Rev. Game
Biol. 1: 45-76.
Marshall, N. B., 1960. Swimbladder structure of deep-sea fishes in relation to their system-
atics and biology. Discovery Reps. 31: 1-122.
Matthews, L. Harrison, 1949. The origin of stomach oil in the petrels, with comparative
observations on the avian proventriculus. Ibis 91: 373-392.
Mayr, Ernst, 1945. Birds of the Southwest Pacific. Macmillan, New York. 316 p.
Morris, R. O., 1963. The birds of the Gilbert Islands. Sea Swallow 16: 79-82.
Moul, E. T., 1954. Preliminary report on land animals at Onotoa Atoll, Gilbert Islands.
Atoll Res. Bull. 28. 28 p.
Moynihan, Martin, 1959. A revision of the family Laridae (Aves). Amer. Mus. Novit.
1928. 42 p.
Murphy, Garth I., and Isaac I. Ikehara, 1955. A summary of sightings of fish schools and
bird flocks and of trolling in the central Pacific. U.S. Fish and Wildlife Serv.,
Spec. Sci. Rep., Fisheries 154. 19 p.
, and Richard S. Shomura. The abundance of tunas in the Central Equatorial
Pacific in relation to the environment. Unpublished manuscript.
Murphy, Robert Cushman, 1936. Oceanic birds of South America. American Museum of
Natural History, New York. 2 vols.
, Alfred M. Bailey, and Robert J. Niedrach, 1954. Canton Island. Denver Mus.
Nat. Hist., Mus. Pict. 10. 78 p.
Nakamura, Eugene L., 1965. Food and feeding habits of Skipjack Tuna (Katsuwonus
pelamis) from the Marquesas and Tuamotu Islands. Amer. Fish. Soc., Trans. 94:
236-242.
Oliver, W. R. B., 1930. New Zealand birds. A. H. and A. W. Reed, Wellington. 661 p.
Olney, P. J. S., 1964. The food of Mallard Anas platyrhynchos collected from coastal and
estuarine areas. Zool. Soc. Lond., Proc. 142: 397-418.
Palmer, Ralph S. [ed.] 1962. Handbook of North American birds. 1. Loons through
flamingos. Yale University Press, New Haven and London. 567 p.
Pearcy, William G., 1964. Some distributional features of mesopelagic fishes off Oregon.
J. Mar. Res. 22: 83-102.
, and R. M. Laurs, 1966. Vertical migration and distribution of mesopelagic fishes
off Oregon. Deep-Sea Res. 13: 153-165.
Peters, James Lee, 1931, 1934. Check-list of birds of the world, Vol. 1 and Vol. 2. Harvard
University Press, Cambridge.
Ragotzkie, Robert A., and R. A. Bryson, 1953. Correlation of currents with the distribu-
tion of adult Daphnia in Lake Mendota. J. Mar. Res. 12: 157-172.
Recher, Harry F., 1966. Some aspects of the ecology of migrant shorebirds. Ecology 47:
393-407.
Reintjes, John W., and Joseph E. King, 1953. Food of Yellowfin Tuna in the Central
Pacific. U.S. Fish and Wildlife Serv., Fishery Bull. 54 (81): 91-110.
Rice, Dale W., and Karl W. Kenyon, 1962. Breeding cycles and behavior of Laysan and
Black-footed Albatrosses. Auk 79: 517-567.
Richardson, Frank, 1957. The breeding cycles of Hawaiian sea birds. B. P. Bishop Mus.,
Bull. 218. 41 p.
Richdale, L. E., 1945. The nestling of the Sooty Shearwater. Condor 47: 45-62.
Ridley, M. W., and Lord Richard Percy, 1958. The exploitation of sea birds in Seychelles.
Colonial Research Studies No. 25. H. M. Stationery Office, London. 78 p.
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 115
Riehl, Herbert, 1954. Tropical meteorology. McGraw-Hill Book Co., New York. 392 p.
Robertson, William B., 1964. The terns of the Dry Tortugas. Florida State Mus., Bull. 8:
1-94.
Robertson, William B., Jr., Dennis R. Paulson, and C. Russell Mason, 1961. A tern new
to the United States. Auk 78: 423-425.
Roden, Gunnar I., 1963. On sea level, temperature, and salinity variations in the central
tropical Pacific and on Pacific Ocean islands. J. Geophys. Res. 68: 455-472.
Rowan, M. K., 1965. Regulation of sea-bird numbers. Ibis 107: 54-59.
Royce, William F., and Tamio Otsu, 1955. Observation of Skipjack schools in Hawaiian
waters, 1953. U.S. Fish and Wildlife Serv., Spec. Sci. Rep., Fisheries 147. 31 p.
Ryther, J. H., 1963. Geographic variations in productivity, p. 347-380. In M. N. Hill [ed.]
The sea, 2. Interscience, New York.
Salomonsen, Finn, 1965. The geographical variation of the Fulmar (Fulmarus glacialis)
and the zones of marine environment in the North Atlantic. Auk 82: 327-355.
Savile, D. B. O., 1957. Adaptive evolution in the avian wing. Evolution 11: 212-224.
Schoener, Thomas W., 1965. The evolution of bill size differences among sympatric con-
generic species of birds. Evolution 19: 189-213.
Sette, Oscar E., 1955. Consideration of midocean fish production as related to oceanic
circulatory systems. J. Mar. Res. 14: 398-414.
Skokova, N. N., 1963. A quantitative study of the diet of fish-eating birds [in Russian].
Ornitologiya 4: 288-296.
Snow, David W., 1965. The breeding of the Red-billed Tropic Bird in the Galapagos
Islands. Condor 67: 210-214.
Stonehouse, Bernard, 1962a. Ascension Island and the British Ornithologists’ Union
Centenary Expedition 1957-59. Ibis 103b: 107-123.
, 1962b. The tropic birds (genus Phaethon) of Ascension Island. Ibis 103b: 124-161.
Storer, Robert W., 1960. Evolution in the diving birds. Proc. XII Intern. Ornithol.
Congr.: 694-707.
Tickell, W. L. N., 1964. Feeding preferences of the albatrosses Diomedea melanophris and
D. chrysostoma at South Georgia, p. 383-387. In Biologie antarctique. Premier
symposium organisé par le S.C.A.R., Paris, 2-8 Septembre 1962. Hermann, Paris.
Tinbergen, N., 1964. On adaptive radiation in gulls (Tribe Larini). Zool. Mededel. 39:
209-223.
Trautman, Carl G., 1952. Pheasant food habits in South Dakota. S. Dak. Dept. Game,
Fish., Parks, Tech. Bull. No. 1. 89 p.
Uda, M., 1938. Researches on “Siome” or Current Rip in the seas and oceans. Geophys.
Mag. 11: 307-372.
Uda, Michitaka, 1953. On the convergence and divergence in the NW Pacific in relation
to the fishing grounds and productivity. Japanese Soc. Sci. Fish., Bull. 19: 435-438.
, 1954. Studies of the relation between the whaling grounds and the hydrographical
conditions (I). Whales Res. Inst., Sci. Reps. 9: 179-187.
Vogt, William, 1964. Informe sobre las aves guaneras [in Spanish]. Bol. Corporacién
Nacional de Fertilizantes 2, 2* Epocha, (8): 9-28; (9): 6-48; (10): 5-40.
Voorhis, A. D., and J. B. Hersey, 1964. Oceanic thermal fronts in the Sargasso Sea. J.
Geophys. Res. 69: 3809-3814.
Voss, Nancy A., and Gilbert L. Voss, 1962. Two new species of squids of the genus
Calliteuthis from the Western Atlantic with a redescription of Calliteuthis reversa
Verrill. Bull. Mar. Sci. Gulf and Carribbean 12: 169-200.
Waldron, Kenneth D., 1964. Fish schools and bird flocks in the Central Pacific Ocean,
1950-1961. U.S. Fish and Wildlife Serv., Spec. Sci. Rep., Fisheries 464. 20 p.
, and Joseph E. King, 1962. Food of Skipjack in the Central Pacific. World sci-
116 PEABODY MUSEUM BULLETIN 24
entific meeting on the biology of tunas and related species. Section No. 5, Ex-
perience Paper 26. 28 p.
Warham, J., 1964. Breeding behaviour in Procellariiformes, p. 389-394. In Biologie ant-
arctique. Premier symposium organisé par le S.C.A.R., Paris, 2-8 Septembre 1962.
Hermann, Paris.
Watson, John B., 1908. The behavior of Noddy and Sooty Terns. Carnegie Inst. Wash-
ington, Tortugas Lab., Pap. 2: 187-255.
, 1910. Further data on the homing sense of Noddy and Sooty Terns. Science, N.S.,
32: 470-473.
, and K. S. Lashley, 1915. An historical and experimental study of homing. Car-
negie Inst. Washington, Dept. Mar. Biol., Pap. 7: 7-60.
Wiens, Herold J., 1962. Atoll environment and ecology. Yale Univ. Press, New Haven
and London. 532 p.
Wyrtki, Klaus, 1965. The annual and semiannual variation of sea surface temperature in
the North Pacific Ocean. Limnol. Oceanog. 10: 307-313.
Zusi, Richard L., 1962. Structural adaptations of the head and neck in the Black Skimmer
Rynchops nigra Linnaeus. Nuttall Ornithol. Club, Publ. 3. 101 p.
17
FEEDING ECOLOGY OF SEA BIRDS
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ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 125
APPENDIX 2B. SEASONAL DaTA ON SQuID MANTLE LENGTHS
Figures in parentheses refer to additional squid represented by remains only—
see Techniques section.
PHAETHON RUBRICAUDA
LENGTH (CM)
0-2 2-4 4-6 6-8 8-10 10-12 TOTALS
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May aN = 1 = 3
Jun./Jul. — — 1 6 — — 7
Aug. = == 1 2 — 3 (+3)
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Nov. —- 8 4 10 10 1 33 (+1)
1964 Jan. —- 1 7 6 1 2 17 (+4)
Feb. — > — — 1 = 1
Jun = = — — —- — 0
TOTALS 18 23 40 24 5 110 (+8) = 118
PUFFINUS NATIVITATIS
LENGTH (CM)
0-2 2-4 4-6 6-8 8-10 TOTALS
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May _— 23 Pa 8 1 53
Jun./Jul. 1 16 9 Z — 28 (+2)
Aug. —- 3 16 6 — 25
Sep. = 14 16 2 1 33 (+1)
Nov. —- 14 35 10 1 60 (+1)
1964 Jan. — 4 15 i) —— 20 (+1)
Feb. —_ 16 5 — — 21 (+1)
Jun. 1 2 27 17 _— 47
TOTALS 2 94 149 50 3 298 (+6) = 304
PTERODROMA ALBA
LENGTH (cM)
0-2 2-4 4-6 6-8 8-10 TOTALS
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May — 2 _— — 1 3 (+8)
Jun./Jul. — 1 4 2 1 8 (+3)
Aug. —_ 1 9 1 — 11 (+10)
Sep. — 6 2 3 —_— 11 (+1)
Nov. _ -— 1 2 1 4 (+2)
1964 Jan. — — _ _— _— 0 (+1)
Feb. — 11 33 10 — 56 (+16)
Jun. —_ 4 12 3 2 21 (+4)
TOTALS 3 45 as 23 a 153 (+48) = 201
126 PEABODY MUSEUM BULLETIN 24
APPENDIX 2b (continued)
STERNA FUSCATA
LENGTH (CM)
0-2 2-4 4-6 6-8 8-10 TOTALS
1963 Mar. 3 79 68 23 —_— 173
May — — —_— — — 0
Jun./Jul. — 2 7 3 —_— 12 (+3)
Aug. 1 22 81 19 2 125 (+19)
Sep. 1 23 54 17 — 95 (+9)
Nov. — 2 — — —_— 2
1964 Jan. —_ 1 6 2 — 9 (+2)
Feb. 2 32 30 6 — 70 (+1)
Jun. 1 5 6 — — 12 (+2)
TOTALS 8 166 252 70 2) 498 (+36) = 534
ANOUS STOLIDUS
LENGTH (CM)
0-2 2-4 4-6 6-8 TOTALS
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May — — — _ 0
Jun./Jul. — 1 3 2 6 (+1)
Aug. — —- — —— 0
Sep. —_— — —_— — 0
Nov. — 2 z/ — 9
1964 Jan. — 9 4 2 15 (+1)
Feb. — 1 —_— — 1 (+1)
Jun. — 3 if 6 16 (+3)
TOTALS 1 16 22 11 50 (+6) = 56
GYGIS ALBA
LENGTH (cM)
0-2 2-4 4-6 6-8 TOTALS
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May —_— — il — 1
Jun./Jul. — — — —_— 0
Aug. — — 1 —_ 1
Sep. — 5) 5 2 12
Nov. 2 15 7 Z 26
1964 Jan. — 2 2 — 4 (+1)
Feb. — 71 —_— —_ 71 (+22)
Jun. 3 7 4 — 14 (+1)
TOTALS 5 100 20 4 129 (+25) = 154
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 127
APPENDIX 2b (continued)
ANOUS TENUIROSTRIS
1963 Mar.
May
Jun./Jul.
Aug.
Sep.
Nov.
1964 Jan.
Feb.
Jun.
TOTALS
PROCELSTERNA CERULEA
1963 Mar.
0-2
0-2
2-4
LENGTH (cM)
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1 a 2
3 =r 8 (+2)
1 == 4 (+2)
2 1 6 (+1)
= = 8 (+3)
2 = SG ot)
4 — 14 (+1)
2 — 4
2 3 9 (+3)
17 4 58 (+13) = 71
LENGTH (CM)
(51)
0 (+2)
2 (+3)
117 (+6) = 123
PEABODY MUSEUM BULLETIN 24
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130 PEABODY MUSEUM BULLETIN 24
APPENDIX 4. CEPHALOPODS IN THE DIETS OF THE BIRDS*
NUMBER OF OMMASTREPHIDAE OMMASTREPHIDAE
BIRD SQUID IDENTIFIED TO IDENTIFIED TO IDENTIFIED TO
SPECIES EXAMINED» FAMILY GENUS SPECIES®
Other Symplectoteuthis
Ommastrephidae families Symplectoteuthts sp.A sp.B
Phaethon 54 53 14 34 4 3
rubricauda (47) (15) (10)
Puffinus 150 93 0 32 19 1
nativitatis (134) (43) (24) (2)
Pterodroma 71¢ 17 0 5 4 0
alba (48)
Sterna 430! 379 0 300 186 16
fuscata (419) (337) (277) (17)
Anous 10 10 0 4 3 1
stolidus (7)
Gygis 15 14 1e 13 13 0
alba
Anous 34 24 0 12 8 0
tenutrostris (32) (20)
Procelsterna 105 765 2i 0 0 0
cerulea
TOTALS 869 666 4 400 237 oA:
(786) (472) (344) (30)
NOTES:
This table is based on the squid collected in the period March through September 1963.
a.
The identifications were made by Dr. Malcolm Clarke, of the National Institute of
Oceanography, England. The figures in parentheses include those squid which were only
tentatively identified.
b. Only squid represented by mantle and/or head are included in the table; isolated lenses,
beaks, arms or pens are omitted.
c. For discussion of Symplectoteuthis species A and species B see Species Accounts: Phaethon
rubricauda.
d. Histioteuthidae?
e. In addition, some remains of other cephalopods were found in samples from Pterodroma
alba: see Species Accounts.
f. In addition, one small Argonauta sp. (Octopoda) was found.
g. Abralia sp. (Enoploteuthidae).
h. Of these 53 (from a single sample) were Rhynchoteuthis larvae, probably of one of the
Symplectoteuthis species.
. Loligo sp. (Loliginidae).
ASHMOLE & ASHMOLE: FEEDING ECOLOGY OF SEA BIRDS 131
APPENDIX 5. DETAILS OF THE STOMACH CONTENTS OF 191 YELLOWFIN TUNA
(NEOTHUNNUS MACROPTERUS), CAUGHT BY SURFACE-T ROLLING
WITHIN 10 MILEs oF CHRISTMAS, JARVIS, WASHINGTON
AND FANNING ISLANDs (LINE ISLANDs)
NUMBER VOLUME (ml) NUMBER OF SAMPLES
CONTAINING
OVERALL COMPOSITION
Fish 1161 311422 151
Squid Tf 324 586.0 91
Other invertebrates 34768 6806.5 161
FISH
*Congridae 5 Jee 3
*Synodontidae ih 2.0 1
Myctophidae 16 47.0 6
Exocoetidae 1 30.0 1
*Syngnathidae 3 1.0 1
*Priacanthidae 7 200 1
*Carangidae 17 2070.0 9
Bramidae 14 253 8
*Lutianidae 3 4.0 3
*Chaetodontidae 7 315 3
*Polynemidae 1 2.0 1
Blenniidae 37 2420 10
*Acanthuridae 524 352.2 43
Gempylidae 2 520 2
Scombridae 3 2.0 1
*Balistidae 14 110 12
*Ostraciontidae 39 47.0 20
Tetraodontidae 3 202.0 3
Molidae 1 520.0 1
TOTAL IDENTIFIED 693 3342.2
7 Four small octopods included.
* Families marked with an asterisk are considered to be primarily reef-originating (see
text); Tetraodontidae and Blenniidae are not assigned to either the reef-originating or the
pelagic category.
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