] Jfar. Bio/ . .-iJS. l".K ;_2002!. 82, 9!3 916 Printed in thc l'nited Kingdom
Changes m the cephalopod diet of southern elephant seal females at King George Island, during EI Nifio-La Nifia events
Uwe Piatkowski*, Daniel E Vergani1 and Zulma B. Stanganelli1 *Institut für Meereskunde, Universitäl Kiel, Düsternhrooker \\'eg 20, D-24105 Kid, Germany. tProyeno Cyber Atlas Centro Nacional Patag6nico, CENPA:"f-CONICE1~ Boule\·ard Alm. Browu 3500, 9120 Pm·rto Madryn, Chubut, Argentina. E-mail: atlas(dcenpat.edu.ar *Corresponding authnr, e-mail: upiatkowski(r.i"ifm.uni-kiel.de
Possiblc em~cts of "El Nüi.o' Southern Oscillation (ENSO) components 'EI Nillo' and 'La Niiia' on popu lations of southern elephant seals, A1irounga leoninn, wcrc analysed. Changcs in the ccphalopod dict composition of moulting fCmales at King Gcorge Island, Antarctic Peninsula werc considcred. The dict of f(;male elephant seals sampled in l99J .... l992 and 1992 .... 1993 (EI Niiio ycars) were compared \Vith those taken in 1995.... 1996 (La Niiia year) at the same site and employing the same methodology. The squid Ps_ychroieuthis glacialis constituted the main cephalopod prey of the seals. A reduction in the 'Index of Biomass Ingcsted' by female elephant seals (IBIF) of this prey species was observed in 'EI Nii\o' years (1992, 1993) compared witb the 'La Niii.a' year (1996). This reduction in biomass applied to all squid species in the seals' prey with the exception of Galiteuthis glacia!is, which occurred in 1ow numben, but was more abundant during EI Niiio years than in the La Niii.a year.
INTRODUCTION there is no infonnation on the feeding t:cology of post breeding elephant stals at King George Island most of Thc life cyclc of southern dephant seals comprises two thc post-moulting females vvhich had tran!led south pcriods on land, one for breeding the other for moulting. west along the coast of the Antarctic Peninsula into the Both cvents are extremely exigent in terms of energy. Hellingshausen Sca reaching the area of Alcxander Island Fernales have to store enough encrgy reserves to last the (Borncmann et aL, 2000). Possible effects of 'El ~iiio' bH·cding period fast du ring which thcy increase the birth Sout hern Oscillation ( ENSO) on hreeding population mass of thcir pups over an average of23.7 days of!actation trends (Vcrgani & Stanganelli, l990) and pup weaning (Arnbom et al., 1997). Ahead of the füllowing moulting rnass in fonale dephant seals havc al~o becn cxaminrd, period thcy have to recowr, at least in part, the biomass with weaning mass higher during 'La ]\;'iüa'. and lower lost du ring brccding to store enough reserves to cope with during 'El Niti.o', the cold and warm pha.scs of .ENSO a sccond starvation period. Although in terms of energy respectively (Vergani et al., 2001). storcs required, breeding is approximately t\vice as expen :Major effects of EI ~ifio··-· La Niiia anomalics on the siw· as the moult (Boyd et al., 1993} the feeding pcriod Antarctic e-cosystem may bc related to the seasona1 ! March·-· August) prior to breeding (\ergani, 1985; variabilit y of the pack-icc zone. This zonc is thc most Vergani & StanganeHi, 1990; Bornemann et al., 2000) productive- an~a in the Antarctic region on an annual Iasts thrce timcs Ionger than the fceding period prior to basis (Hcmpel, !985) and variation in pack ice cxtenl the moult (::"ovcmber--December). may cause pronounccd changcs in fOod availability for Female elcphant seals brccd and mou!t annually at King tCmale elephant seals. Although monthly ENSO fluctua George Island, South Shetland Islands. Breeding females tion appears to bc linkcd with month1y fluctuations in arrin· betwcen 8 and 26 September and reach breeding \Vcstern Antarctic Peninsula (\\'AP) sea ice extent (Smith scason pcak between 21 and 31 Octobt:r (\:ergani & ct aL, 1996), no direct cvidencc of changes in food aYail Sranganclli. 1990; \'ngani et al., 2001) . .Moulting fema!es ability to the fema!e elcphant scals has as yet lwen fi)Und that had brcd at King Gcorge Island as \Yell as sorne from in th<.·sc pcriods. the South Gcorgia brccding population start arriving early Deccmber and dcpart from the beadws in early :VL\TERIALS A"\D ~n;rHODS April (\Crgani, 1983; :\lcConndl et al.. !992; ~lcConndl & Fedak. 1996:. Thc group offt·males 13 of !2J which bred :\ way in which to exp!ore changcs in fOod m·ai\ability is at South Georgia f{·d to thc south-\vt'St of Adelaide bland to <:ompare biomass ingcstcd by f(·ma!c c1ephant seals :·Amarctic Peninsula). At thc time ofmoulting (Decemher during El ::'\ii'i.o and La NiJi.a ycars. The first prdiminary January) these seals wcre approximately ISOO 3000 km studi-es on dirt wcrc carried out at King Gcorge Islancl in distant from South Gcorgia (Figurc 1\ and must have 1991·· 1992 and 1992· 199:~ during thc mmdting Sf'ason completed their moult on beaches in the vicinity of the (Piatkowski & Vergani, 2000). A complementary study .-\ntarctic Peninsula: tagged individuals in South Georgia was carricd out in 1995·--1996 ( Dancri ct al., 2000). In werc found moulting at King George Island. Although thi.s study \V<' rcport on thc ccpha!opod diet of moulting
]rmmat of thr .\larin.r Biologira! A.rsociatian. qf lhe l'n.ited A"ingdam (2002) 914 U. Piatkowski ct aL Diet rhanges in elephant sealfima!eJ
At Stranger Point, King George Island (62'H'S 58°30'\\') stomach Lwages for 13 females in 1991- 1992 and 17 females in 1992 -19~ß werc done during thc moulting season fo!lowing thc tcchniquc devdnpcd by Antoncllis d al. (1987). Fbnalcs \VOT irnmobilized by ü~jection of kctamineHhydrochloridt:, stomach la\·aged and cephalopod beaks were remo\Td from the stomach contents and stored in 70~'() et hanoL Lower heaks wen· identified by refCrence collections and after Clarke (l9B6). Lower rostral length (LRL) was measured with a digital calliper to thc ncarcst ofO.l mm. Allometric equations from Clarkc {1986); Gröger ct al. (2000) and Piatkowski ct al. (200!) werc used to rdate LRL to dorsal mantlc length (~-IL, in mm) and wct mass (ing), and \vith 1995---1996 data of Dancri ct al. (2000) v..-·ho sampled 14 fcmales using thc same mcthodology. A comparativc 'Index of Biomass Ingcsted' (IBIF) (Hochbcrg, 1974) by fC.male clcphant scals \Vas calculated and relatcd to EI Niiio and La Nifla years, respectivcly, with IBIF = :E squid biomass of each sample ( B,) divided by thc total number offcmale elephant seals sampled (Nr)· '10 idcntif~.. ENSO events during the study period, the indcx ofsea surfacc temperature (SST) called 'Niflo 3.4' for the region 5"N---s~-s, 120"'E---170"\V was applied following 1fenberth (1997). On four occasions the average of SSTs in thE' El Nir1o 3.4 index exceeded the 0.4 oc lhresho!d for more than five months, indicating the occurrence of EI Niflo. On three occasions the values were helow 0.4°C Figure 1. Gt·ographical distrihution oC the squid Ps)·throleuthiJ indicating the occurrence of La l'\ifia evf'nts. glarialis according: to Xa\·ier et aL ( t 999:; and ü·t~ding arcas of !(·malt· soutlwrn dephanl scals iJfirounga !t'Onina' according to ~lrC:onnel! t'l a!., 1992), ~kConne!! & Fedak {1996·,, and Bornemann ct al. 2000,-. RESULTS
fi:-male dcphant ~wals at King Georgc- lsland in 1991 1992 Squid bcak composition analysis in female st>al stomach and 1992--1993, both EI l\'irl.o ycars, and compared it with contents takcn in 1992, 1993 and 1996 are sho,vn in Table 1. those takcn in 1995 1996 by Danni ct al. (2000) du ring a The gla6al squid Pryrhroteuthis glarialis was the most abun l.a .:'\iila ycar. dant rephalopod prcy, both numerically and in tcrms of
Table 1. Squid biomass ingested kvfema/e elt'Phant sta!s.
P~rrhmteuthn glarialis Alluroteuthis antarr tirus Galiteuthis glacialis
1992 1993 !996 1992 1993 1996 1992 1993 1996
------~------~------
:'\I 13 17 I+ 13 17 11 13 17 1+ B, 9972 7208 :18969 891 29·l 3HO 231 84 0 .\Iean:' ßj:\b !02.8 180.2 182.1 296.9 147.1 287.7 57.7 21.1 0 Sll 82.3 221.6 133.2 217.9 120.8 17L6 20.3 21.0 0 IBlFo Bs: :\f 7.5 2A !J.~j 0.2 0.1 0.9 0.3 0.2 0 ~h 97 HJ 2! -l 3 2 13 + + 0
Bmchiohuthi.> sp. kimdakoda !ongimww Dmwtu.\ an!arttimj
------~·
1992 19~n !Y96 !992 !993 1~'!96 !992 !99:) !996 ------
:\t 1"; 1 7 I! 1:; ! 7 p 13 17 I+ ß, .. j() 0 l:lO !."l 7B () 1-1:22 0 !61 16"~3 :\h·an: B, :\b 9A 7.2 789.:2 0 2!H.2 () 80.3 l6L3 SD 1.0 !l9 1(;0_2 () 212.0 () 2.9 1o:u-; lBlL Bs':\f O.:l 0.0 1.3 0.2 0 0.5 0 0.1 0.7 :\h 6 0 1B 2 0 7 0 2 10
:'\b number of dephant st·a!s sampkd; B,. total Squid Biomas"; :'\h, number ofsquid beaks; lBIF, indcx of Biomass Ingested by fCmale Elrpham Seals.
Joumaf oj tilr .\larmt Birlr,_gual .lmrtiatiOII!f/lhe Cniled kingdom (2002) Die! dwnges in elep!wnt sealfemales V. Piatko\vski et al. 915
10000
--+-- Psychroteuthis 1000 - ..._- Al!uroteuthis § 0 Galiteuthis ~"' -·* ·- 100 ~ ro ----M- Brachioteuthis E Q • • • •· • • Kondako\da "' 10 - · 8- • Gonatus
1992 1993 1996 Year
Figure 2. lndf'x ofcephalopod Biomass 1ngested by Fernale clephant seals 1 IBIFi variation.
Table 2. Variation of% biomass contribution to elephant seal However, to study squid distribution and abundance by diet at South Georgia (from Rodhause el aL., 1992). sampling their beaks from elcphant scal stomach contents ------introduce.s a serious bias. Cephalopod beaks may be 1986 !988 retaincd Ionger in the rugae of the stomach than fish remains ( Bigg & Fawcett, 1985) thus ow:rcstimating Aforoteuthis knipm•iühi +0.3 22.7 thc gcncral importance of cephalopods in tlu· dict. Ps_vchrotruthis glariali.s 3.5 26.6 Although thc mcan retention time of digesta in southcrn Kondak01•ia lon;;imana 21.0 26.9 -elephant scals is estimated to be- about 13 hours (Krockenberger & Bryden, l9~H) there arc no precise data on the retention time of cephalopod bcaks in thc biomass. In general, a reduction in IBIF orcurred during .stomachs, and thus what period of f{Jraging they rcpresent El ;\Jifio years (1992, 1993) compared with thc La ~ifia ycar (McConnell & Fcdak, 1996). At South Gcorgia the in 1996 (Figure 2). Thc reduction in IIUF was oh,·ious for rctcntion time \Vas estimated to be 2---3 days, and with an <11l major squid spccies with thc exception of Uaiiteuthis average travel spced of 61 km(day during the post moult/ g!acialis which shmved a ren·rsc pattern, although the breeding migration of f<:male elephant seals; the number and biornass of this squid '.vere comparatiYely !ow. stomach sarnpks representcd a f(·cding area locatcd ahmtt Thc increase in number and biomass of Ps]rhro!euthis 122-- un km frorn the island ( ~IcConncll & h'dak, 19961. glarialis during La Niila ycars and dccrcase during EI :'\ihn On the othcr hand, gin·n that thc kcding grounds of years could exp!ain the findings of Rodhouse ct aL (!99:2) adult femak dephant scals: from King Gcorge Island are at South Grorgia. In their study stomach samples were dosdy associatcd with the edgc of thc pack ict· zone takcn in 1986 and 1988, v.:hich werc EI ~ifio and La l'\iila Bornemann t't al. ,2{)0()':, which apparently coincides years accordiug to 'H-enherth ( 1997 ). Thc importanu of with the distrihution of the m;tior cepha!opod prcy. P glaria/is in tlw diet of dcphant scals increased by a P~whrotmthis glarialis (Xavier ct aL, !999) (Figun· 11 a l~u~tor nf sC"ven in the La 0/ifia year at South Georgia sceuario of how E~SO can eH'cct thc tt·eding pattnn of (Tabk 2). Vergani & Stangandli (1990) also suggested tiw seals can bc c·xplained as fl)l!ows: during EI ~iilo that E_:\IS() dfects on top predators vvcre scen simuha~ years w!wn thc pack icc has a minimum rowragc, lt·male neously at South Gcorgia and King Gcorge Is!and during seals han- to traw\ Ionger clistances during thc initial the l9H2 1983 EI :'\iflo events. This obsen-ation seems to transit phase from their breeding p!aces in order to H'ach be suppc>rtcd by the ÜKt that a proportion of South t(-cding areas. Hcncc, in suhsequent stomach analyst'S tlw Georgia fCmak southern dt•phant scals migrated to the prorC"ss of digcstion is more advancccl due to thc long \\'AP rcgion to fCcd ( McConndl et aL, 1992; !\lcConncll rcturn journey. resulting in lesser nurnbns of squid lx·aks. & Fcdak, 1996), a known fecding area for fCmaks from During La ~ifla years the park ice cxtension is larga, the King Gcorge Island ( Bornemannet aL, 2000\ seals do not migrate !ong distances to fecding grounds, and the stagc of digestion is not so much adYanccd. rhis would concei\'ab!y result in higher abundance of squid DISCCSSIO:-i hcaks in sromach contt•nts, This undcrlines that changes Although squid play a key rok in thc marine e(osystcm in numbers of squid bcaks in :-.tomarh comcnrs do not nf the Southern Ocean ;Ainley & Dc~Iastcr, !990 tlw ncn·s-;arily rdlut Hunuations in squid a\'ailahility in distribution of Antarctic cepha!opods is p11or!y kwJwn, the J-idd. althnugh in the Patagonian Shdf area correla~ due to, c.g. their t:tst swimming, which may mak<· them tions bctwcen sea surbce tnnpcrature :SST and squid difflcul! to s:ampk wüh col1\'('tHional rcsearch trawls abundance rdlet·ted an increasc of ~quid biomass at their (\\Ormuth & Roper, l9B3\ This is in contrast to Autarctir spawning sites, with !ower SST associated with higber top predators such as ekphant !Wals which secm to prey catche:; of //ln mgentinus ! \\·aluda ct al., 200(h Theref()re, cfil·ctively on cephalopods in order to maintain thcir high thc finding that dephant scal wcaning ma~s is higher Cllcrgy dematlds. during La ::'\ii1a years (\Crgani ct aL, 200I) could suggest
]o11111af ofthr .\larml' Biologi{(d .·h~owtf/011 1!{/he C11iiNI lo.in&dom (!002) 916 C. Piatkowski et al. Diet changf5 in t!rphant .ll'a!Jemale.\·
that P~whroteuthiJ g!arialis availabillty t.o tlw ft~rnale ck· Gröger, J.. Piatkowski, L. & Hcincmann, H., 200fl. Beak !ength phant st:als had inrreased concomitant vvith lower SST analysi!'i of the Southern Ocean squict PJ:vdtmlruthis g!acialü during La Nifia years. : Cephalopoda: Psychroteuthidae) and its usc !Or size and Bornemannet al. (2000) postulatt>d that the main prey biomass cstimation. Polar Biolog1~ 23, 70---74. HempeL G., 1985. Antarctic marine föod \Vt'bs. In Anlantir item of southern elephant seals from King George Island nutrient (:wies andfood u·eb5 {ecL \\'.R. Sicgfried ct aU, pp. 266--- would be PLeuragramma antarctirum and Brown ct al. (1999) 270. Berlin: Springer. suggested that elcphant scals of South Gcorgia probably Hochberg. Y.. 1974. Some generalisalions oftheT... method in simu1· fed on larger nototheniids and myctophid fish. However, tancous. inference. Journal of .\fultimriate Ana{ysis, 4, 224---23-1. thc rapid changcs in wcaning mass associatcd with La Krockenbuger. i\1.B. & Bryden, l\Uvl., 1994-. Rate ofpassage of ~iüa and El 1\ifio ev<'nts (Vergani ct al., 2001) scem to digesta through the alimentary tract of southern elephant seals indicate that elcphant seals depcnd on specics such as (.\liroun,f;a Iumina) t Carnimra: Phocidae). Journal rif ?,Mlogy, squid with short hf(: spans rather than on long lived 234, 229 237, spe<·ies such as thc pdagic Antarctic fish, 1~ antarrtirurn ~1cConne!l, B.J, Chambers, C. & H:dak, M.A., 1992. Foraging <"colngy of snuthern dephant seals in rdation to the bathy· vvhere thc em~ct of anomalics like ENSO probably would be secn later in thc wcakness of recruitment and not mury .and productivity of the Southern Ocean. Autarctir Scierm, 4. 393- 398. immcdiatdy. l\kConnell, B.J. & Fedak, ~..f.A., 1996. l'viovemenb of southern An integrated study of pup weaning mass, stomach elephant seals. Canadian]oumal if ?,ooiogv, 74, Irl-85·· H96. content analysis and sea ice density fluctuation during La Piatkowski, U., Pütz, K. & Heinemann, H., 2001. Cephalopod Nitla/ El Niiio events would be necessary to corroborate prey of king penguins (Aptenot[ytes patagonicus) breeding at this hypothesis, but the model represents a first attempt 10 Volunteer Beach. f·alkland Islands, during austral winter study the effect of ENSO on a top predator of t.he Ant.arctic l99G. Fishaies Research, 52, 79---90. ecosystem. Piatkmvski, U. & VCrgani, D.F., 2000. The cephalopod prey of southern elephant seals (;\Jiroun,ga !eouirw) from Stranger Point, InfOrmation presemc~d in this paperwas taken from a longHterm King Georgc Island, Antarctica. CIAC Sympo.1ium Cephalopod programme on t'lephant seals condurted by Daniel \'ergani and Biomass and Productiou. Cnh'ersity qf Aberdeeu, Scotland, 3---7 ]u{}' Zulma Stanganei!L Logistic support was received ffom Dirercibn 2000. [ Post('f presentation.J N'M·ional del Ant
Joumal if lhe ,Haritu Biolqe.iral .-bo(ialion of tht [_ 'nitrd Aingdom {2002)