doi 101098rspb20001343 151-157268 2001 Proc R Soc Lond B
MahoAndre Ancel Charles-Andreacute Bost Michel Gauthier-Clerc Yan Ropert-Coudert and Yvon Le Jean-Benoicirct Charrassin Akiko Kato Yves Handrich Katsufumi Sato Yasuhiko Naito by oesophageal temperature
ranging penguins determinedminusFeeding behaviour of free
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This journal is copy 2001 The Royal Society
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Feeding behaviour of free-ranging penguinsdetermined by oesophageal temperatureJean-Beno|ordf t Charrassin1 Akiko Kato2 Yves Handrich1 Katsufumi Sato2Yasuhiko Naito2 Andre Ancel1 Charles-Andre Bost1 Michel Gauthier-Clerc1Yan Ropert-Coudert2 and Yvon Le Maho1
1Centre drsquoEcologie et Physiologie Energetiques Centre National de la Recherche Scienticentque 23 rue Becquerel67087 Strasbourg Cedex 2 France2National Institute of Polar Research 1- 9-10 Kaga Itabashi- kuTokyo 173- 8515 Japan
Sea birds play a major role in marine food webs and it is important to determine when and how muchthey feed at sea A major advance has been made by using the drop in stomach temperature after inges-tion of ectothermic prey This method is less sensitive when birds eat small prey or when the stomach isfull Moreover in diving birds independently of food ingestion there are pounductuations in the lowerabdominal temperature during the dives Using oesophageal temperature we present here a new methodfor detecting the timing of prey ingestion in free-ranging sea birds and to our knowledge report thecentrst data obtained on king penguins (Aptenodytes patagonicus) In birds ashore which were hand-fed 2^15 gpieces of centsh all meal ingestions were detected with a sensor in the upper oesophagus Detection waspoorer with sensors at increasing distances from the beak At sea slow temperature drops in the upperoesophagus and stomach characterized a diving eiexclect per se For the upper oesophagus only abrupttemperature variations were superimposed therefore indicating prey ingestions We determined thedepths at which these occurred Combining the changes in oesophageal temperatures of marine predatorswith their diving pattern opens new perspectives for understanding their foraging strategy and aftervalidation with concurrent applications of classical techniques of prey survey for assessing the distributionof their prey
Keywords oesophageal temperature king penguin ingestion foraging diving
1 INTRODUCTION
Marine top predators are major consumers of searesources and have an important role in the marineecosystem (Furness 1982 Croxall 1992 Woehler 1995)This concerns especially the birds and marine mammalsof the Southern Ocean which may transfer to the atmo-sphere as much as 25 of the photosynthetically centxedcarbon (Huntley et al 1991) Because these top predatorsmay respond to abiotic variables there is a considerablepotential for using them to study changes in marineresources (Croxall et al 1988 Montevecchi 1993 Guinetet al 1998) Although the animals are not directly obser-vable when at sea miniaturized technology has givenaccess to certain aspects of their foraging behaviour suchas diving activity (eg Kato et al 1996 Peters et al 1998Davis et al 1999) foraging area (eg Jouventin ampWeimerskirch 1990 Bost et al 1997) and energetics (egCulik et al 1996 Wilson amp Gremillet 1996 Bevan et al1997 Handrich et al 1997 Gremillet et al 1998)However a major remaining challenge is the accuratedetermination of when and how much animals feed whileat sea This is a central question in foraging studiesbecause detecting prey ingestion may give information onprey availability and foraging success
Until now the main approach to this problem has beenbased on records of stomach temperature using remotesensing units (Wilson et al 1992 Gremillet amp Plolaquo s 1994Kato et al 1996 Wilson et al 1995 1998) Feeding can bedetected in marine endotherms since most of their preyitems are ectothermic organisms that cause a drop of thegastric temperature when ingested However the relia-bility of this method is largely dependent on the type ofpredator and type of prey (see a review by Wilson et al1995) Briepoundy the likelihood of detecting a prey ingestionwith a stomach thermistor decreases with smaller preysize and with the centlling of the stomach Also recent datahave shown that body temperatures of diving sea birdscan pounductuate independently of their feeding activity(Culik et al 1996 Wilson amp Gremillet 1996 Bevan et al1997 Handrich et al 1997) Indeed there is a drop in thelower abdominal temperature during diving which contri-butes to the long duration of the dives due to the loweroxygen consumption of cooled tissues (Handrich et al1997)
These considerations led Ancel et al (1997) to testdetection of prey ingestion in captive sea birds bymeasuring their oesophageal temperature The lumen ofthe oesophagus is much smaller than the stomach volumeand prey do not accumulate in the oesophagus We havenow deployed this promising technique in free-rangingpredators Here we report results of the centrst measure-ments of oesophageal temperature in the free-rangingking penguin (Aptenodytes patagonicus) This pelagic deep-diving bird depends on small (2^9 g) schooling centsh themyctophids (Cherel amp Ridoux 1992) which form one of
Proc R Soc Lond B (2001) 268 151^157 151 copy 2001 The Royal SocietyReceived 6 July 2000 Accepted 2 October 2000
doi 101098rspb20001343
Author and address for correspondence Laboratoire drsquoOceanographiePhysique Museum National drsquoHistoire Naturelle 75231Paris Cedex 05France ( jbcmnhnfr )
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
the most important food resources of the Southern Ocean(Sabourenkov 1991 Pakhomov et al 1996) The aims ofthe present work were (i) to validate this method incaptive penguins and (ii) to assess the feeding activity atsea of free-ranging birds by measuring their oesophagealtemperature
2 MATERIAL AND METHODS
The study was carried out at Possession Island Crozet Archi-pelago Southern Indian Ocean (46825rsquo S 51845rsquo E) at the`Grande Manchotiecopy rersquo colony of king penguins (40 000 breedingpairs Weimerskirch et al 1992) during the 1996 and 1997breeding seasons
(a) Temperature sensors and time^depth recordersData loggers used to monitor stomach temperature (in
captive birds) oesophageal temperature and dive depth in the0^200m range were manufactured by the Little Leonardo Co(Tokyo Japan) and had 1^2 Mb of poundash memory In captivebirds oesophageal temperatures were measured by a four-channel temperature logger linked to an oesophageal probe withfour thermistors the logging unit was housed in an aluminiumcylinder (8 bits 90 mmpound14 mm diameter resolution 01 8C)stomach temperatures were recorded by a cylindrical two-channel logger (12 bits 90 mmpound19 mm diameter resolution002 8C accuracy 01 8C)
In free-ranging birds oesophageal temperature and divedepth in the 0^200m range were measured by a cylindricalthree-channel logger (12 bits 90 mmpound 20 mm diameter and ca50 g temperature and depth resolution 002 8C and 01mrespectively) Cylindrical oesophageal thermistors (5 mmpound 3 mm) were plastic coated and had an accuracy of 03 8CEach thermistor was linked to the central unit by a 05^1m elec-tric cable (diameter 12 mm) Stomach temperatures wererecorded by a cylindrical logger (Driesen and Kern GmbH BadBramstedt Germany 8 bits 105 mm pound16 mm diameter and ca80 g resolution 01 8C 025 Mb memory) The thermal time-constant of oesophageal sensors (32 s) was nine and 14 timesshorter than for the stomach sensors used in captive and free-ranging birds respectively Dive depth in the 200^500m range
was measured by an MK5 time^depth recorder (WildlifeComputers (Redmond WA USA) 65 mmpound 38 mmpound15 mmand ca 50 g 2 m resolution 05 Mb memory)
(b) Feeding captive birdsWe centrst examined the temperature changes in the oesophagus
and the stomach in response to ingestion of meals of known sizeand temperature in centve non-breeding adults Each bird wasinduced to swallow a stomach sensor (1s sampling interval)attached to a thin plastic line (used to remove the unit after theexperiment) The four-channel temperature logger (2 s samplinginterval) was then taped onto the back feathers and the bird wasinduced to swallow the oesophageal probe Care was taken toreduce handling stress The oesophageal probe consisted of a30 cm poundexible plastic tube diameter 07 cm with four regularlyspaced thermistors In the oesophagus the sensors were at 9 1625 and 34 cm from the beak junction (sensors a b c and drespectively) The birds were kept in a fenced enclosure for30 min to allow the thermistors to reach body temperature Atotal of 220 centsh pieces (mass and temperature ranges 16^147 gand 05^9 8C respectively) simulating the temperature and thesize of the prey usually caught by king penguins (Cherel ampRidoux 1992) were hand-fed to them at 2^6 min intervalsduring sessions lasting on average 100 min
152 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
oesophageal temperature sensor
tunnelledcable
timendashtemperaturendashdepthrecorder
stomach temperature recorder
Figure 1 View of a king penguin showing the location ofequipment deployed on free-ranging individuals Cableswere tunnelled under the skin from the oesophagus to alogger unit taped onto the feathers recording dive depth andoesophageal temperature A second logger recorded thestomach temperature
33
36
39
30
33
36
39
30
30
33
36
27
33
36
39
30
40
3638
time (min)
oeso
phag
eal t
empe
ratu
re (
deg C)
0 10 20 30 40 50 60
(e)stomach
34 cm
25 cm
16 cm
9 cmexperimental feedings
(d)
(c)
(b)
(a)
Figure 2 Changes in temperature as a result of the ingestionof 20 centsh pieces recorded by four thermistors located in theoesophagus of a captive king penguin The thermistors werelocated at 9 16 25 and 34 cm from the beak (sensor a b cand d respectively) and in the stomach (e) Fish temperaturewas 8 8C and the mass of each piece was about 9 g
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
(c) Equipping free-ranging birdsSeven birds at the brood stage were surgically implanted
under halothane anaesthesia with an intraluminal oesophagealtemperature sensor and a tracheal temperature sensor at 6^10 cm from the beak junction The cables of the sensors werecentxed with absorbable suture threads onto the external walls ofthe oesophagus and trachea at 15 mm and 5 mm from thesensors respectively The body of the unit (2 s sampling interval)was attached externally onto the lower back with the cablestunnelled up to the upper oesophagus and the trachea (seecentgure 1) The tunnellization was performed using a specialsterile stainless steel tube Cutaneous wounds were closed usingabsorbable suture threads The transcutaneous transition wasprotected and anchored by a non-absorbable suture thread Sixout of the seven penguins were induced to swallow a stomachtemperature sensor (16 s sampling interval) Four out of theseven individuals were implanted with an MK5 recorder in theabdominal cavity as described by Handrich et al (1997) Divedepths were sampled every 4 s The work was performed in ashelter within the colony site and the birds were thereafterreturned to their breeding spot There using a portable enclo-sure they were protected from neighbours and predators untilfull recovery from the anaesthesia All equipment was removedunder anaesthesia after the birds returned and the individualswere released in apparently good condition None of the birdsimplanted with thermistors showed infection Moreover allcontinued to breed (chick brooding) after the removal of theequipment The procedure complied with current laws of theFrench authorities Authorization of the Ministecopy re de lrsquoAgricul-ture et de la Foreordf t (no 04196) followed by approbation of thesurgical protocol by the Ethics Committee of the FrenchInstitute for Polar Research In this study we will report onoesophageal and stomachal temperatures and diving behaviour
(d) Data analysisData were downloaded and analysed using Jensen System
Software programs (Laboe Germany) and custom-made Fox-base programs In the stomach and the oesophagus theexpected temperature signal following ingestion of a cold preyitem by endotherms is a precipitous droprsquo of the sensor tempera-ture followed by an exponential risersquo to the body value (PDER)The PDER repoundects the cooling and rewarming of the sensorafter contact with the cold item (Wilson et al 1992 1995)However because temperature changes in divers may repoundecteither prey ingestion (PDER) or non-feeding events (ietemperature changes due to diving per se) (Handrich et al 1997)we examined in detail at-sea temperature drops to identifyfeeding and non-feeding events For this we compared the
oesophageal temperature drops for the two main categories ofdives previously observed in king penguins (Kooyman et al1992 Charrassin et al 1998 PIumltz et al 1998) shallow (430 m)and deep (4 30 m) dives Means are given thorn se
3 RESULTS
(a) Experimental feedingsAll 220 items fed to the penguins were detected
(temperature drop 503 8C) by sensor a except for centvemeals that were not swallowed The proportion of eventsshowing a PDER at the upper sensor (a) was 20 (range0^61 n ˆ 9 feeding sessions) Non-PDER events (ieeither a non-precipitous drop (slower drop) or a slow rise)repoundected a chaotic passage of the prey over the sensorIndeed based on the behaviour of the birds they oftendid not swallow the food at once sometimes alternatelytrying to regurgitate and swallow the food We assumethis does not occur in a free-ranging feeding bird Theresponse to ingestion was best in the upper thermistorand with increasing distance from the beak detection ofthe prey was less certain (centgure 2) Ingestions were notdetected by the stomach sensor although the temperaturedropped from 382 to 377 8C during that period(centgure 2) The progression velocity of prey items betweenthe sensors a and b b and c and c and d averaged
Prey ingestion inpenguins J-B Charrassin and others 153
Proc R Soc Lond B (2001)
Table 1 Foraging characteristics of three king penguins equipped with data loggers monitoring their oesophageal temperatureand diving behaviour in early February 1997 at Crozet Archip elago
(The birds were at the brood stage A dive was considered as successful when at least one ingestion was detected Meansare sect se)
duration stomach oeso- total no mean meanmean no per cent
of oeso- content phageal prey no no ingestions successful
foragingdates
phagealrecord
at thebirdrsquos
tempera-ture range
ingestions(RTD5
preyingestions
dives430 m
per dive dives
(1997) (days) return (kg) (8C) 0068 Csiexcl1) dayiexcl1 dayiexcl1 430 m 430 m 4 30 m430 m
(b) Prey ingestion and diving behaviour in free-ranging penguins
Out of the seven birds equipped four remained at seafor 119 sect 09 days on average (range 101^145 days) Thestomach content upon return was sampled using thewater oiexcl-loading technique (Wilson 1984) It rangedfrom 05 to 1kg One bird spent 15 days at sea Two indi-viduals stayed in the colony Out of the four birds whichwent to sea with a stomach recorder two lost the recorderby regurgitation of the unit at sea and two had retainedit when they came back Continuous oesophagealtemperature records lasting six to seven days wereobtained from three birds and a total of 4900 dives from1^291m depth were recorded simultaneously (table 1)
As shown in centgure 3 both stomach and oesophagealtemperatures showed slow and regular variations whichcoincided with the dives However for oesophagealtemperature large and rapid drops which were not seenfor stomach temperature were superimposed on thesevariations Only when numerous rapid drops in oesopha-geal temperature occurred did stomach temperaturedecrease further During the intensive diving that kingpenguins make during their foraging trips at sea (seecentgure 4) their drops in oesophageal temperature didreach as much as 133 8C Still dives with only minorchanges in oesophageal temperature (centgure 5a)contrasted with dives with large variations in oesophagealtemperature (centgure 5b)
For the 650 sect 60 temperature drops 5002 8C recordedon average per day for each of the three birds (n ˆ 19days) two groups of temperature drops were character-ized according to their amplitude and duration (centgure 6)The centrst group corresponded to slow drops showing asmall amplitude (1^2 8C or below) and lasting for up to3 min Based on their rate of temperature decrease (RTDdecentned as the amplitude of the temperature drop divided
by the drop duration) slow drops accounted for most ofthose occurring during shallow dives (95 of drops hadan RTD 5 006 8C s71) but were also observed duringdeep dives (centgure 6) They corresponded to the cyclicvariations already described in centgure 3 which occurringin relation to the dives repoundect the tissue cooling due todiving per se (Handrich et al 1997)
The other group included large (up to 133 8C) andshort (530 s) drops which occurred mainly during deepdives (centgure 6) During deep dives 50 of these dropshad an RTD greater than 006 8C s71 Because such rapiddrops were much shorter than the duration of the divesduring which they occurred they indicate cooling by coldprey Fast temperature drops (RTD5006 8C s71) weretherefore assumed to repoundect prey ingestion Feeding eventsinferred from oesophageal temperature are shown incentgure 5b
(c) Feeding frequency and feeding depthThe number of ingestions per day varied from 95 to
300 among the birds and the number of ingestions pershallow dive (430 m) was much smaller than for deepdives (table 1) Bird 3 apparently experienced a muchlower foraging success than the others Feeding depthswere obtained from the dive procentles recorded simulta-neously with oesophageal temperature In bird 2 preyingestions occurred mainly between 80 and 170 m where70 of ingestions were detected (centgure 7) Duringdiving 5 sect 3 41 sect 2 and 54 sect 5 of prey ingestions tookplace during the descent bottom and ascent parts of thedives respectively (n ˆ 3 birds and 4200 dives4 70 m)
4 DISCUSSION
This study is based on the assessment of oesophagealtemperature of free-ranging diving birds as a new
154 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
36
32
28
20
24
0
100
200
300
time (d)
oeso
phag
eal t
empe
ratu
re
(degC
)de
pth
(m)
1 Feb 2 3 4 5 6 7 8
Figure 4 Changes in upper oesophageal temperature inrelation to dive depth in a king penguin foraging at CrozetArchipelago during seven days after departure from thecolony The total trip duration was 11 days
32
28
2024
0
100
200
local solar houroe
soph
agea
lte
mpe
ratu
re
(degC
)
3634
oeso
phag
eal
tem
pera
ture
(deg
C)
dept
h (m
)
0
100
200
dept
h (m
)
0455 0505 0515
1525 1535 1545
(a)
(b)
36
Figure 5 Changes in upper oesophageal temperature inrelation to dive depth indicating non-feeding dives (a) andfeeding dives (b) in a foraging king penguin Arrows indicateprey ingestion Grey boxes show periods spent at the surface
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
method for detection of food ingestion Our techniqueallows detection of ingestion of prey items as small asmyctophid centsh in relation to depth
(a) Implantation of oesophageal probesin free-ranging penguins
Four birds went to sea and showed normal foragingbehaviour as judged by dive depth and food brought tothe chick (Kooyman et al 1992 Charrassin et al 1998PIumltz et al 1998) Why two birds stayed at the colony isunclear However recent work (Y Le Maho unpublisheddata) suggests that the passage of the cables in the neckmay particularly disturb some individuals Accordinglyfuture work with data transmission to the logger unitrather than a cable connection may solve the issueHowever implantation of the sensor in the oesophaguseliminates the possibility of losing the logger by regurgita-tion as can occur for stomach sensors (this study Wilsonet al 1998)
(b) Relevance of oesophageal probe for detectingsmall prey ingestions
Since all experimental feedings gave a detectableresponse we conclude that our system is sensitive enoughfor small-sized prey items The low thermal inertia of thesmall sensor accounts for its good sensitivity (Ancel et al1997) Such a small size reduces the probability of contactwith prey but is counterbalanced by the small cross-sectional area of the oesophagus Prey items were lessoften detected with increasing distances from the beakand detection was almost impossible in the stomach ofcaptive penguins However prey detection in the stomachcould be less reliable in our captive individuals than infree-ranging birds since movements during diving maycontinually change the sensor position in the stomach(Wilson et al 1995) thereby favouring contact with preyProgression of food items is faster in the upper part of theoesophagus This lessens the time between prey ingestion
and prey^sensor contact and favours detection byreduced warming of the prey Prey ingestion is then easierto distinguish from physiological changes due to diving(Handrich et al 1997) if the probe is located in the upperoesophagus rather than deeper in the body (eg in thestomach) Based on the 06 cm siexcl1 displacement of preyitems in the upper oesophagus found in captive birds thedelay for reaching a sensor located 9 cm from the beak is15 s Such a short interval allows a quasi real-time detec-tion of food ingestion
(c) Detecting prey ingestion in free-ranging penguinsKing penguins feed on patchily distributed mesopelagic
centsh (Adams amp Klages 1987 Cherel amp Ridoux 1992Olsson amp North 1997) Oesophageal temperaturesrecorded in free-ranging birds showed large variations( 413 8C) that indicated feeding events and feedingdepths when combined with dive procentles The typicalfast short and precipitous temperature drops clearly indi-cate prey ingestions as opposed to the slow temperaturevariations corresponding to the tissue cooling due tophysiological responses to diving (Handrich et al 1997)Furthermore these prey ingestions were concentrmed as therapid temperature drops mainly occurred during deepdives (exclusively performed during daylight by kingpenguins see centgure 4 Kooyman et al 1992 Charrassinet al 1998 PIumltz et al 1998) which correspond to thedepths where myctophids concentrate during the day(Zaselrsquosliy et al 1985 Duhamel 1998)
Based on a penguinrsquos average vertical velocity duringdiving of 13 m s71 (PIumltz et al 1998) and with an ingestion^detection delay of 15 s the accuracy of depth where inges-tion occurs is ca 20 m ie 10 of the dive depth if thebird reaches 200 m Being validated with concurrentapplication of a classical technique such as hydroacousticprey survey or net trawl this method may provide aunique means to assess the prey distribution over depthFor instance one of the three birds fed mainly at 80^170 m where it probably encountered dense prey patchesUsing average prey mass of king penguins (74 and 17 g
Prey ingestion inpenguins J-B Charrassin and others 155
Proc R Soc Lond B (2001)
9
6
3
0
12
temperature drop duration (s)
tem
pera
ture
dro
p (deg
C)
0 50 100 150
non-feedingevents
feedingevents
dives gt 30 mdives pound 30 m
200
Figure 6 Relationships between amplitude and duration oftemperature drops in the upper oesophagus recorded in aking penguin during shallow dives (430 m n ˆ 1951 drops)and deep dives ( 4 30 m n ˆ 2450 drops) The dashed lineindicates the rate of temperature decrease above whichtemperature drops were considered as repoundecting prey ingestion(006 8C s71 see frac12 3) The period covered six foraging days
1020
08
04
06
02
00
30
depth of temperature drop (m)
rate
of
tem
pera
ture
dec
reas
e (deg
C s
- 1)
0 50 100 150 200 250 300
Figure 7 Depths at which temperature drops of the upperoesophagus occurred in a king penguin foraging for 75 days(n ˆ 6209 drops 5002 8C) Considering that a rate oftemperature decrease 5006 8C s71 (dashed line) indicatesfeeding most prey ingestion occurred at depths from about80 to 170 m
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
for the two main prey species in proportions of 75 and15 of the diet respectively Cherel amp Ridoux 1992) thedaily mass of centsh ingested by birds 1 and 2 was ca 16 kgand was 06 kg for bird 3 These values are comparablewith those ranges found in studies based on energetics(Kooyman et al 1992) and argue for the reliability of ourmethod
In conclusion measurement of oesophageal tempera-ture appears to be a promising tool for detecting preyingestion by marine predators Beside new information onthe feeding ecology of these predators an interestingperspective is their use to infer the prey distribution atdepth in particular for small schooling centsh dicurrencult todetect by conventional methods but which are keymarine resources in the Southern Ocean
The National Institute for Polar Research (Japan) the InstitutFrancdeg ais pour la Recherche et la Technologie Polaires and theTerres Australes et Antarctiques Francdeg aises provided centnancialand logistical support for this work The Centre National de laRecherche Scienticentque (GDRE no 1069 and PICS no 347) alsohelped in the funding We are indebted to the Penguin Fund(Tokyo Japan) for providing J-BC with a grant We thankC Marchand for help with surgeryY Clerquin and G Froget forcenteldwork assistance and members of the 33rd and 34th Missionsat Crozet Islands for a generous welcome The Little LeonardoCo (Tokyo Japan) is thanked for their ecurrencient cooperation andJ Lage (Jensen Software System) is acknowledged for writingcustomized software for data analysisWe are also very grateful toKnut Schmidt-Nielsen and to anonymous reviewers whosenumerous suggestions greatly improved our paper
REFERENCES
Adams N J amp Klages N T 1987 Seasonal variation in the dietof the king penguin (Aptenodytes patagonicus) at sub-AntarcticMarion Island J Zool 212 303^324
Ancel A Horning M amp Kooyman G L 1997 Prey ingestionrevealed by oesophagus and stomach temperature recordingsin cormorants J Exp Biol 200 149^154
Bevan R M Boyd I L Butler P J Reid K Woakes A Jamp Croxall J P 1997 Heart rates and abdominal temperaturesof free-ranging South Georgian shags Phalacrocorax georgianusJ Exp Biol 200 661^675
Bost C-A Georges J-Y Guinet C Cherel Y PIumltz KCharrassin J-B Handrich Y Zorn T Lage J amp LeMaho Y 1997 Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozetarchipelago Mar Ecol Prog Ser 150 21^33
Charrassin J-B Bost C-A PIumltz K Lage J Dahier TZornT amp Le MahoY 1998 Foraging strategies of incubatingand brooding king penguins Aptenodytes patagonicus Oecologia114 194^201
Cherel Y amp Ridoux V 1992 Prey species and nutritive value offood fed during summer to king penguin Aptenodytes patagonicachicks at Possession Island Crozet Archipelago Ibis 134 118^127
Croxall J P 1992 Southern Ocean environmental changeseiexclect on sea bird seal and whale populations Phil Trans RSoc Lond B 338 319^328
Croxall J P McCann T S Prince P A amp Rothery P 1988Reproductive performance of sea birds and seals at SouthGeorgia and Signy Island South Orkney Islands 1976^1987implications for Southern Ocean monitoring studies InAntarctic Ocean and resources variability (ed D Sahrhage)pp 261^285 Berlin and Heidelberg Germany Springer
Culik B M PIumltz K Wilson R P Bost C-A Le Maho Yamp Verselin J L 1996 Core temperature variability in divingking penguins (Aptenodytes patagonica) a preliminary analysisPolar Biol 16 371^378
Davis R W Fuiman L A Williams T M Collier S OHagey W P Kanatous S B Kohin S amp Horning M 1999Hunting behavior of a marine mammal beneath the Antarcticfast ice Science 283 993^996
Duhamel G 1998 The pelagic centsh community of the PolarFrontal Zone oiexcl the Kerguelen Islands In Fishes of AntarcticaA biological overview (ed G di Prisco E Pisano amp E Clarke)pp 63^74 Milan Italy Springer
Furness R W 1982 Competition between centsheries and seabirdsrsquo communities Adv Mar Biol 20 225^307
Gremillet D J H amp Plolaquo s A L 1994 The use of stomachtemperature records for the calculation of daily food intake incormorants J Exp Biol 189 105^115
Gremillet D J H Tuschy I amp Kierspel M 1998 Bodytemperature and insulation in diving great cormorants andEuropean shags Funct Ecol 12 386^394
Guinet C Chastel O Koudil M Durbec J-P amp JouventinP 1998 Eiexclect of warm sea-surface temperature anomalies onthe blue petrel at the Kerguelen Islands Proc R Soc LondB 265 1001^1006
Handrich Y Bevan R M Charrassin J-B Butler P JPIumltz K Woakes A J Lage J amp Le Maho Y 1997Hypothermia in foraging king penguins Nature 388 64^67
Huntley M E Lopez M D G amp Karl D M 1991 Top preda-tors in the Southern Ocean a major leak in the biologicalcarbon pump Science 253 64^66
Jouventin P amp Weimerskirch H 1990 Satellite tracking ofwandering albatrosses Nature 343 746^748
Kato A Naito Y Watanuki Y amp Shaughnessy P D 1996Diving pattern and stomach temperatures of foraging kingcormorants at subantarctic Macquarie Island Condor 98844^848
Kooyman G L Cherel Y Le Maho Y Croxall J PThorson P H Ridoux V amp Kooyman C A 1992 Divingbehavior and energetics during foraging cycles in kingpenguins Ecol Monogr 62 143^163
MontevecchiW A 1993 Birds as indicators of change in marineprey stocks In Birds as monitors of environmental change (edR W Furness amp J J D Greenwood) pp 217^266 LondonChapman amp Hall
Olsson O amp North A W 1997 Diet of the king penguinAptenodytes patagonicus during three summers at SouthGeorgia Ibis 139 504^512
Pakhomov E A Perissinotto R amp McQuaid C D 1996 Preycomposition and daily rations of myctophid centshes in theSouthern Ocean Mar Ecol Prog Ser 134 1^14
Peters G Wilson R P Scolaro J A Laurenti S Upton Jamp Galleli H 1998 The diving behavior of Magellanicpenguins at Punta Norte Peninsula Valdes Argentina ColonWaterbird 21 1^10
PIumltz K Wilson R P Charrassin J-B Raclot T Lage JLe MahoY Kierspel M A M Culik B M amp Adelung D1998 Foraging strategyof kingpenguins (Aptenodytes patagonicus)during summer at the Crozet Islands Ecology 79 1905^1921
Sabourenkov E N 1991 Myctophids in the diet of Antarcticpredators In Selected scienticentc papers 1990 (ScienticentcCommittee-CCAMLR-XBG6) (ed Commission for theConservation of Antarctic Marine Living Resources(CCAMLR)) pp 335^360 Hobart Australia CCAMLR
Weimerskirch H Stahl J-C amp Jouventin P 1992 Thebreeding biology and population dynamics of king penguinsAptenodytespatagonica on the Crozet Islands Ibis 134 107^117
Wilson R P 1984 An improved stomach pump for penguinsand other sea birds J Field Ornithol 55 9^12
156 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
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Feeding behaviour of free-ranging penguinsdetermined by oesophageal temperatureJean-Beno|ordf t Charrassin1 Akiko Kato2 Yves Handrich1 Katsufumi Sato2Yasuhiko Naito2 Andre Ancel1 Charles-Andre Bost1 Michel Gauthier-Clerc1Yan Ropert-Coudert2 and Yvon Le Maho1
1Centre drsquoEcologie et Physiologie Energetiques Centre National de la Recherche Scienticentque 23 rue Becquerel67087 Strasbourg Cedex 2 France2National Institute of Polar Research 1- 9-10 Kaga Itabashi- kuTokyo 173- 8515 Japan
Sea birds play a major role in marine food webs and it is important to determine when and how muchthey feed at sea A major advance has been made by using the drop in stomach temperature after inges-tion of ectothermic prey This method is less sensitive when birds eat small prey or when the stomach isfull Moreover in diving birds independently of food ingestion there are pounductuations in the lowerabdominal temperature during the dives Using oesophageal temperature we present here a new methodfor detecting the timing of prey ingestion in free-ranging sea birds and to our knowledge report thecentrst data obtained on king penguins (Aptenodytes patagonicus) In birds ashore which were hand-fed 2^15 gpieces of centsh all meal ingestions were detected with a sensor in the upper oesophagus Detection waspoorer with sensors at increasing distances from the beak At sea slow temperature drops in the upperoesophagus and stomach characterized a diving eiexclect per se For the upper oesophagus only abrupttemperature variations were superimposed therefore indicating prey ingestions We determined thedepths at which these occurred Combining the changes in oesophageal temperatures of marine predatorswith their diving pattern opens new perspectives for understanding their foraging strategy and aftervalidation with concurrent applications of classical techniques of prey survey for assessing the distributionof their prey
Keywords oesophageal temperature king penguin ingestion foraging diving
1 INTRODUCTION
Marine top predators are major consumers of searesources and have an important role in the marineecosystem (Furness 1982 Croxall 1992 Woehler 1995)This concerns especially the birds and marine mammalsof the Southern Ocean which may transfer to the atmo-sphere as much as 25 of the photosynthetically centxedcarbon (Huntley et al 1991) Because these top predatorsmay respond to abiotic variables there is a considerablepotential for using them to study changes in marineresources (Croxall et al 1988 Montevecchi 1993 Guinetet al 1998) Although the animals are not directly obser-vable when at sea miniaturized technology has givenaccess to certain aspects of their foraging behaviour suchas diving activity (eg Kato et al 1996 Peters et al 1998Davis et al 1999) foraging area (eg Jouventin ampWeimerskirch 1990 Bost et al 1997) and energetics (egCulik et al 1996 Wilson amp Gremillet 1996 Bevan et al1997 Handrich et al 1997 Gremillet et al 1998)However a major remaining challenge is the accuratedetermination of when and how much animals feed whileat sea This is a central question in foraging studiesbecause detecting prey ingestion may give information onprey availability and foraging success
Until now the main approach to this problem has beenbased on records of stomach temperature using remotesensing units (Wilson et al 1992 Gremillet amp Plolaquo s 1994Kato et al 1996 Wilson et al 1995 1998) Feeding can bedetected in marine endotherms since most of their preyitems are ectothermic organisms that cause a drop of thegastric temperature when ingested However the relia-bility of this method is largely dependent on the type ofpredator and type of prey (see a review by Wilson et al1995) Briepoundy the likelihood of detecting a prey ingestionwith a stomach thermistor decreases with smaller preysize and with the centlling of the stomach Also recent datahave shown that body temperatures of diving sea birdscan pounductuate independently of their feeding activity(Culik et al 1996 Wilson amp Gremillet 1996 Bevan et al1997 Handrich et al 1997) Indeed there is a drop in thelower abdominal temperature during diving which contri-butes to the long duration of the dives due to the loweroxygen consumption of cooled tissues (Handrich et al1997)
These considerations led Ancel et al (1997) to testdetection of prey ingestion in captive sea birds bymeasuring their oesophageal temperature The lumen ofthe oesophagus is much smaller than the stomach volumeand prey do not accumulate in the oesophagus We havenow deployed this promising technique in free-rangingpredators Here we report results of the centrst measure-ments of oesophageal temperature in the free-rangingking penguin (Aptenodytes patagonicus) This pelagic deep-diving bird depends on small (2^9 g) schooling centsh themyctophids (Cherel amp Ridoux 1992) which form one of
Proc R Soc Lond B (2001) 268 151^157 151 copy 2001 The Royal SocietyReceived 6 July 2000 Accepted 2 October 2000
doi 101098rspb20001343
Author and address for correspondence Laboratoire drsquoOceanographiePhysique Museum National drsquoHistoire Naturelle 75231Paris Cedex 05France ( jbcmnhnfr )
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
the most important food resources of the Southern Ocean(Sabourenkov 1991 Pakhomov et al 1996) The aims ofthe present work were (i) to validate this method incaptive penguins and (ii) to assess the feeding activity atsea of free-ranging birds by measuring their oesophagealtemperature
2 MATERIAL AND METHODS
The study was carried out at Possession Island Crozet Archi-pelago Southern Indian Ocean (46825rsquo S 51845rsquo E) at the`Grande Manchotiecopy rersquo colony of king penguins (40 000 breedingpairs Weimerskirch et al 1992) during the 1996 and 1997breeding seasons
(a) Temperature sensors and time^depth recordersData loggers used to monitor stomach temperature (in
captive birds) oesophageal temperature and dive depth in the0^200m range were manufactured by the Little Leonardo Co(Tokyo Japan) and had 1^2 Mb of poundash memory In captivebirds oesophageal temperatures were measured by a four-channel temperature logger linked to an oesophageal probe withfour thermistors the logging unit was housed in an aluminiumcylinder (8 bits 90 mmpound14 mm diameter resolution 01 8C)stomach temperatures were recorded by a cylindrical two-channel logger (12 bits 90 mmpound19 mm diameter resolution002 8C accuracy 01 8C)
In free-ranging birds oesophageal temperature and divedepth in the 0^200m range were measured by a cylindricalthree-channel logger (12 bits 90 mmpound 20 mm diameter and ca50 g temperature and depth resolution 002 8C and 01mrespectively) Cylindrical oesophageal thermistors (5 mmpound 3 mm) were plastic coated and had an accuracy of 03 8CEach thermistor was linked to the central unit by a 05^1m elec-tric cable (diameter 12 mm) Stomach temperatures wererecorded by a cylindrical logger (Driesen and Kern GmbH BadBramstedt Germany 8 bits 105 mm pound16 mm diameter and ca80 g resolution 01 8C 025 Mb memory) The thermal time-constant of oesophageal sensors (32 s) was nine and 14 timesshorter than for the stomach sensors used in captive and free-ranging birds respectively Dive depth in the 200^500m range
was measured by an MK5 time^depth recorder (WildlifeComputers (Redmond WA USA) 65 mmpound 38 mmpound15 mmand ca 50 g 2 m resolution 05 Mb memory)
(b) Feeding captive birdsWe centrst examined the temperature changes in the oesophagus
and the stomach in response to ingestion of meals of known sizeand temperature in centve non-breeding adults Each bird wasinduced to swallow a stomach sensor (1s sampling interval)attached to a thin plastic line (used to remove the unit after theexperiment) The four-channel temperature logger (2 s samplinginterval) was then taped onto the back feathers and the bird wasinduced to swallow the oesophageal probe Care was taken toreduce handling stress The oesophageal probe consisted of a30 cm poundexible plastic tube diameter 07 cm with four regularlyspaced thermistors In the oesophagus the sensors were at 9 1625 and 34 cm from the beak junction (sensors a b c and drespectively) The birds were kept in a fenced enclosure for30 min to allow the thermistors to reach body temperature Atotal of 220 centsh pieces (mass and temperature ranges 16^147 gand 05^9 8C respectively) simulating the temperature and thesize of the prey usually caught by king penguins (Cherel ampRidoux 1992) were hand-fed to them at 2^6 min intervalsduring sessions lasting on average 100 min
152 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
oesophageal temperature sensor
tunnelledcable
timendashtemperaturendashdepthrecorder
stomach temperature recorder
Figure 1 View of a king penguin showing the location ofequipment deployed on free-ranging individuals Cableswere tunnelled under the skin from the oesophagus to alogger unit taped onto the feathers recording dive depth andoesophageal temperature A second logger recorded thestomach temperature
33
36
39
30
33
36
39
30
30
33
36
27
33
36
39
30
40
3638
time (min)
oeso
phag
eal t
empe
ratu
re (
deg C)
0 10 20 30 40 50 60
(e)stomach
34 cm
25 cm
16 cm
9 cmexperimental feedings
(d)
(c)
(b)
(a)
Figure 2 Changes in temperature as a result of the ingestionof 20 centsh pieces recorded by four thermistors located in theoesophagus of a captive king penguin The thermistors werelocated at 9 16 25 and 34 cm from the beak (sensor a b cand d respectively) and in the stomach (e) Fish temperaturewas 8 8C and the mass of each piece was about 9 g
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
(c) Equipping free-ranging birdsSeven birds at the brood stage were surgically implanted
under halothane anaesthesia with an intraluminal oesophagealtemperature sensor and a tracheal temperature sensor at 6^10 cm from the beak junction The cables of the sensors werecentxed with absorbable suture threads onto the external walls ofthe oesophagus and trachea at 15 mm and 5 mm from thesensors respectively The body of the unit (2 s sampling interval)was attached externally onto the lower back with the cablestunnelled up to the upper oesophagus and the trachea (seecentgure 1) The tunnellization was performed using a specialsterile stainless steel tube Cutaneous wounds were closed usingabsorbable suture threads The transcutaneous transition wasprotected and anchored by a non-absorbable suture thread Sixout of the seven penguins were induced to swallow a stomachtemperature sensor (16 s sampling interval) Four out of theseven individuals were implanted with an MK5 recorder in theabdominal cavity as described by Handrich et al (1997) Divedepths were sampled every 4 s The work was performed in ashelter within the colony site and the birds were thereafterreturned to their breeding spot There using a portable enclo-sure they were protected from neighbours and predators untilfull recovery from the anaesthesia All equipment was removedunder anaesthesia after the birds returned and the individualswere released in apparently good condition None of the birdsimplanted with thermistors showed infection Moreover allcontinued to breed (chick brooding) after the removal of theequipment The procedure complied with current laws of theFrench authorities Authorization of the Ministecopy re de lrsquoAgricul-ture et de la Foreordf t (no 04196) followed by approbation of thesurgical protocol by the Ethics Committee of the FrenchInstitute for Polar Research In this study we will report onoesophageal and stomachal temperatures and diving behaviour
(d) Data analysisData were downloaded and analysed using Jensen System
Software programs (Laboe Germany) and custom-made Fox-base programs In the stomach and the oesophagus theexpected temperature signal following ingestion of a cold preyitem by endotherms is a precipitous droprsquo of the sensor tempera-ture followed by an exponential risersquo to the body value (PDER)The PDER repoundects the cooling and rewarming of the sensorafter contact with the cold item (Wilson et al 1992 1995)However because temperature changes in divers may repoundecteither prey ingestion (PDER) or non-feeding events (ietemperature changes due to diving per se) (Handrich et al 1997)we examined in detail at-sea temperature drops to identifyfeeding and non-feeding events For this we compared the
oesophageal temperature drops for the two main categories ofdives previously observed in king penguins (Kooyman et al1992 Charrassin et al 1998 PIumltz et al 1998) shallow (430 m)and deep (4 30 m) dives Means are given thorn se
3 RESULTS
(a) Experimental feedingsAll 220 items fed to the penguins were detected
(temperature drop 503 8C) by sensor a except for centvemeals that were not swallowed The proportion of eventsshowing a PDER at the upper sensor (a) was 20 (range0^61 n ˆ 9 feeding sessions) Non-PDER events (ieeither a non-precipitous drop (slower drop) or a slow rise)repoundected a chaotic passage of the prey over the sensorIndeed based on the behaviour of the birds they oftendid not swallow the food at once sometimes alternatelytrying to regurgitate and swallow the food We assumethis does not occur in a free-ranging feeding bird Theresponse to ingestion was best in the upper thermistorand with increasing distance from the beak detection ofthe prey was less certain (centgure 2) Ingestions were notdetected by the stomach sensor although the temperaturedropped from 382 to 377 8C during that period(centgure 2) The progression velocity of prey items betweenthe sensors a and b b and c and c and d averaged
Prey ingestion inpenguins J-B Charrassin and others 153
Proc R Soc Lond B (2001)
Table 1 Foraging characteristics of three king penguins equipped with data loggers monitoring their oesophageal temperatureand diving behaviour in early February 1997 at Crozet Archip elago
(The birds were at the brood stage A dive was considered as successful when at least one ingestion was detected Meansare sect se)
duration stomach oeso- total no mean meanmean no per cent
of oeso- content phageal prey no no ingestions successful
foragingdates
phagealrecord
at thebirdrsquos
tempera-ture range
ingestions(RTD5
preyingestions
dives430 m
per dive dives
(1997) (days) return (kg) (8C) 0068 Csiexcl1) dayiexcl1 dayiexcl1 430 m 430 m 4 30 m430 m
(b) Prey ingestion and diving behaviour in free-ranging penguins
Out of the seven birds equipped four remained at seafor 119 sect 09 days on average (range 101^145 days) Thestomach content upon return was sampled using thewater oiexcl-loading technique (Wilson 1984) It rangedfrom 05 to 1kg One bird spent 15 days at sea Two indi-viduals stayed in the colony Out of the four birds whichwent to sea with a stomach recorder two lost the recorderby regurgitation of the unit at sea and two had retainedit when they came back Continuous oesophagealtemperature records lasting six to seven days wereobtained from three birds and a total of 4900 dives from1^291m depth were recorded simultaneously (table 1)
As shown in centgure 3 both stomach and oesophagealtemperatures showed slow and regular variations whichcoincided with the dives However for oesophagealtemperature large and rapid drops which were not seenfor stomach temperature were superimposed on thesevariations Only when numerous rapid drops in oesopha-geal temperature occurred did stomach temperaturedecrease further During the intensive diving that kingpenguins make during their foraging trips at sea (seecentgure 4) their drops in oesophageal temperature didreach as much as 133 8C Still dives with only minorchanges in oesophageal temperature (centgure 5a)contrasted with dives with large variations in oesophagealtemperature (centgure 5b)
For the 650 sect 60 temperature drops 5002 8C recordedon average per day for each of the three birds (n ˆ 19days) two groups of temperature drops were character-ized according to their amplitude and duration (centgure 6)The centrst group corresponded to slow drops showing asmall amplitude (1^2 8C or below) and lasting for up to3 min Based on their rate of temperature decrease (RTDdecentned as the amplitude of the temperature drop divided
by the drop duration) slow drops accounted for most ofthose occurring during shallow dives (95 of drops hadan RTD 5 006 8C s71) but were also observed duringdeep dives (centgure 6) They corresponded to the cyclicvariations already described in centgure 3 which occurringin relation to the dives repoundect the tissue cooling due todiving per se (Handrich et al 1997)
The other group included large (up to 133 8C) andshort (530 s) drops which occurred mainly during deepdives (centgure 6) During deep dives 50 of these dropshad an RTD greater than 006 8C s71 Because such rapiddrops were much shorter than the duration of the divesduring which they occurred they indicate cooling by coldprey Fast temperature drops (RTD5006 8C s71) weretherefore assumed to repoundect prey ingestion Feeding eventsinferred from oesophageal temperature are shown incentgure 5b
(c) Feeding frequency and feeding depthThe number of ingestions per day varied from 95 to
300 among the birds and the number of ingestions pershallow dive (430 m) was much smaller than for deepdives (table 1) Bird 3 apparently experienced a muchlower foraging success than the others Feeding depthswere obtained from the dive procentles recorded simulta-neously with oesophageal temperature In bird 2 preyingestions occurred mainly between 80 and 170 m where70 of ingestions were detected (centgure 7) Duringdiving 5 sect 3 41 sect 2 and 54 sect 5 of prey ingestions tookplace during the descent bottom and ascent parts of thedives respectively (n ˆ 3 birds and 4200 dives4 70 m)
4 DISCUSSION
This study is based on the assessment of oesophagealtemperature of free-ranging diving birds as a new
154 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
36
32
28
20
24
0
100
200
300
time (d)
oeso
phag
eal t
empe
ratu
re
(degC
)de
pth
(m)
1 Feb 2 3 4 5 6 7 8
Figure 4 Changes in upper oesophageal temperature inrelation to dive depth in a king penguin foraging at CrozetArchipelago during seven days after departure from thecolony The total trip duration was 11 days
32
28
2024
0
100
200
local solar houroe
soph
agea
lte
mpe
ratu
re
(degC
)
3634
oeso
phag
eal
tem
pera
ture
(deg
C)
dept
h (m
)
0
100
200
dept
h (m
)
0455 0505 0515
1525 1535 1545
(a)
(b)
36
Figure 5 Changes in upper oesophageal temperature inrelation to dive depth indicating non-feeding dives (a) andfeeding dives (b) in a foraging king penguin Arrows indicateprey ingestion Grey boxes show periods spent at the surface
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
method for detection of food ingestion Our techniqueallows detection of ingestion of prey items as small asmyctophid centsh in relation to depth
(a) Implantation of oesophageal probesin free-ranging penguins
Four birds went to sea and showed normal foragingbehaviour as judged by dive depth and food brought tothe chick (Kooyman et al 1992 Charrassin et al 1998PIumltz et al 1998) Why two birds stayed at the colony isunclear However recent work (Y Le Maho unpublisheddata) suggests that the passage of the cables in the neckmay particularly disturb some individuals Accordinglyfuture work with data transmission to the logger unitrather than a cable connection may solve the issueHowever implantation of the sensor in the oesophaguseliminates the possibility of losing the logger by regurgita-tion as can occur for stomach sensors (this study Wilsonet al 1998)
(b) Relevance of oesophageal probe for detectingsmall prey ingestions
Since all experimental feedings gave a detectableresponse we conclude that our system is sensitive enoughfor small-sized prey items The low thermal inertia of thesmall sensor accounts for its good sensitivity (Ancel et al1997) Such a small size reduces the probability of contactwith prey but is counterbalanced by the small cross-sectional area of the oesophagus Prey items were lessoften detected with increasing distances from the beakand detection was almost impossible in the stomach ofcaptive penguins However prey detection in the stomachcould be less reliable in our captive individuals than infree-ranging birds since movements during diving maycontinually change the sensor position in the stomach(Wilson et al 1995) thereby favouring contact with preyProgression of food items is faster in the upper part of theoesophagus This lessens the time between prey ingestion
and prey^sensor contact and favours detection byreduced warming of the prey Prey ingestion is then easierto distinguish from physiological changes due to diving(Handrich et al 1997) if the probe is located in the upperoesophagus rather than deeper in the body (eg in thestomach) Based on the 06 cm siexcl1 displacement of preyitems in the upper oesophagus found in captive birds thedelay for reaching a sensor located 9 cm from the beak is15 s Such a short interval allows a quasi real-time detec-tion of food ingestion
(c) Detecting prey ingestion in free-ranging penguinsKing penguins feed on patchily distributed mesopelagic
centsh (Adams amp Klages 1987 Cherel amp Ridoux 1992Olsson amp North 1997) Oesophageal temperaturesrecorded in free-ranging birds showed large variations( 413 8C) that indicated feeding events and feedingdepths when combined with dive procentles The typicalfast short and precipitous temperature drops clearly indi-cate prey ingestions as opposed to the slow temperaturevariations corresponding to the tissue cooling due tophysiological responses to diving (Handrich et al 1997)Furthermore these prey ingestions were concentrmed as therapid temperature drops mainly occurred during deepdives (exclusively performed during daylight by kingpenguins see centgure 4 Kooyman et al 1992 Charrassinet al 1998 PIumltz et al 1998) which correspond to thedepths where myctophids concentrate during the day(Zaselrsquosliy et al 1985 Duhamel 1998)
Based on a penguinrsquos average vertical velocity duringdiving of 13 m s71 (PIumltz et al 1998) and with an ingestion^detection delay of 15 s the accuracy of depth where inges-tion occurs is ca 20 m ie 10 of the dive depth if thebird reaches 200 m Being validated with concurrentapplication of a classical technique such as hydroacousticprey survey or net trawl this method may provide aunique means to assess the prey distribution over depthFor instance one of the three birds fed mainly at 80^170 m where it probably encountered dense prey patchesUsing average prey mass of king penguins (74 and 17 g
Prey ingestion inpenguins J-B Charrassin and others 155
Proc R Soc Lond B (2001)
9
6
3
0
12
temperature drop duration (s)
tem
pera
ture
dro
p (deg
C)
0 50 100 150
non-feedingevents
feedingevents
dives gt 30 mdives pound 30 m
200
Figure 6 Relationships between amplitude and duration oftemperature drops in the upper oesophagus recorded in aking penguin during shallow dives (430 m n ˆ 1951 drops)and deep dives ( 4 30 m n ˆ 2450 drops) The dashed lineindicates the rate of temperature decrease above whichtemperature drops were considered as repoundecting prey ingestion(006 8C s71 see frac12 3) The period covered six foraging days
1020
08
04
06
02
00
30
depth of temperature drop (m)
rate
of
tem
pera
ture
dec
reas
e (deg
C s
- 1)
0 50 100 150 200 250 300
Figure 7 Depths at which temperature drops of the upperoesophagus occurred in a king penguin foraging for 75 days(n ˆ 6209 drops 5002 8C) Considering that a rate oftemperature decrease 5006 8C s71 (dashed line) indicatesfeeding most prey ingestion occurred at depths from about80 to 170 m
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
for the two main prey species in proportions of 75 and15 of the diet respectively Cherel amp Ridoux 1992) thedaily mass of centsh ingested by birds 1 and 2 was ca 16 kgand was 06 kg for bird 3 These values are comparablewith those ranges found in studies based on energetics(Kooyman et al 1992) and argue for the reliability of ourmethod
In conclusion measurement of oesophageal tempera-ture appears to be a promising tool for detecting preyingestion by marine predators Beside new information onthe feeding ecology of these predators an interestingperspective is their use to infer the prey distribution atdepth in particular for small schooling centsh dicurrencult todetect by conventional methods but which are keymarine resources in the Southern Ocean
The National Institute for Polar Research (Japan) the InstitutFrancdeg ais pour la Recherche et la Technologie Polaires and theTerres Australes et Antarctiques Francdeg aises provided centnancialand logistical support for this work The Centre National de laRecherche Scienticentque (GDRE no 1069 and PICS no 347) alsohelped in the funding We are indebted to the Penguin Fund(Tokyo Japan) for providing J-BC with a grant We thankC Marchand for help with surgeryY Clerquin and G Froget forcenteldwork assistance and members of the 33rd and 34th Missionsat Crozet Islands for a generous welcome The Little LeonardoCo (Tokyo Japan) is thanked for their ecurrencient cooperation andJ Lage (Jensen Software System) is acknowledged for writingcustomized software for data analysisWe are also very grateful toKnut Schmidt-Nielsen and to anonymous reviewers whosenumerous suggestions greatly improved our paper
REFERENCES
Adams N J amp Klages N T 1987 Seasonal variation in the dietof the king penguin (Aptenodytes patagonicus) at sub-AntarcticMarion Island J Zool 212 303^324
Ancel A Horning M amp Kooyman G L 1997 Prey ingestionrevealed by oesophagus and stomach temperature recordingsin cormorants J Exp Biol 200 149^154
Bevan R M Boyd I L Butler P J Reid K Woakes A Jamp Croxall J P 1997 Heart rates and abdominal temperaturesof free-ranging South Georgian shags Phalacrocorax georgianusJ Exp Biol 200 661^675
Bost C-A Georges J-Y Guinet C Cherel Y PIumltz KCharrassin J-B Handrich Y Zorn T Lage J amp LeMaho Y 1997 Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozetarchipelago Mar Ecol Prog Ser 150 21^33
Charrassin J-B Bost C-A PIumltz K Lage J Dahier TZornT amp Le MahoY 1998 Foraging strategies of incubatingand brooding king penguins Aptenodytes patagonicus Oecologia114 194^201
Cherel Y amp Ridoux V 1992 Prey species and nutritive value offood fed during summer to king penguin Aptenodytes patagonicachicks at Possession Island Crozet Archipelago Ibis 134 118^127
Croxall J P 1992 Southern Ocean environmental changeseiexclect on sea bird seal and whale populations Phil Trans RSoc Lond B 338 319^328
Croxall J P McCann T S Prince P A amp Rothery P 1988Reproductive performance of sea birds and seals at SouthGeorgia and Signy Island South Orkney Islands 1976^1987implications for Southern Ocean monitoring studies InAntarctic Ocean and resources variability (ed D Sahrhage)pp 261^285 Berlin and Heidelberg Germany Springer
Culik B M PIumltz K Wilson R P Bost C-A Le Maho Yamp Verselin J L 1996 Core temperature variability in divingking penguins (Aptenodytes patagonica) a preliminary analysisPolar Biol 16 371^378
Davis R W Fuiman L A Williams T M Collier S OHagey W P Kanatous S B Kohin S amp Horning M 1999Hunting behavior of a marine mammal beneath the Antarcticfast ice Science 283 993^996
Duhamel G 1998 The pelagic centsh community of the PolarFrontal Zone oiexcl the Kerguelen Islands In Fishes of AntarcticaA biological overview (ed G di Prisco E Pisano amp E Clarke)pp 63^74 Milan Italy Springer
Furness R W 1982 Competition between centsheries and seabirdsrsquo communities Adv Mar Biol 20 225^307
Gremillet D J H amp Plolaquo s A L 1994 The use of stomachtemperature records for the calculation of daily food intake incormorants J Exp Biol 189 105^115
Gremillet D J H Tuschy I amp Kierspel M 1998 Bodytemperature and insulation in diving great cormorants andEuropean shags Funct Ecol 12 386^394
Guinet C Chastel O Koudil M Durbec J-P amp JouventinP 1998 Eiexclect of warm sea-surface temperature anomalies onthe blue petrel at the Kerguelen Islands Proc R Soc LondB 265 1001^1006
Handrich Y Bevan R M Charrassin J-B Butler P JPIumltz K Woakes A J Lage J amp Le Maho Y 1997Hypothermia in foraging king penguins Nature 388 64^67
Huntley M E Lopez M D G amp Karl D M 1991 Top preda-tors in the Southern Ocean a major leak in the biologicalcarbon pump Science 253 64^66
Jouventin P amp Weimerskirch H 1990 Satellite tracking ofwandering albatrosses Nature 343 746^748
Kato A Naito Y Watanuki Y amp Shaughnessy P D 1996Diving pattern and stomach temperatures of foraging kingcormorants at subantarctic Macquarie Island Condor 98844^848
Kooyman G L Cherel Y Le Maho Y Croxall J PThorson P H Ridoux V amp Kooyman C A 1992 Divingbehavior and energetics during foraging cycles in kingpenguins Ecol Monogr 62 143^163
MontevecchiW A 1993 Birds as indicators of change in marineprey stocks In Birds as monitors of environmental change (edR W Furness amp J J D Greenwood) pp 217^266 LondonChapman amp Hall
Olsson O amp North A W 1997 Diet of the king penguinAptenodytes patagonicus during three summers at SouthGeorgia Ibis 139 504^512
Pakhomov E A Perissinotto R amp McQuaid C D 1996 Preycomposition and daily rations of myctophid centshes in theSouthern Ocean Mar Ecol Prog Ser 134 1^14
Peters G Wilson R P Scolaro J A Laurenti S Upton Jamp Galleli H 1998 The diving behavior of Magellanicpenguins at Punta Norte Peninsula Valdes Argentina ColonWaterbird 21 1^10
PIumltz K Wilson R P Charrassin J-B Raclot T Lage JLe MahoY Kierspel M A M Culik B M amp Adelung D1998 Foraging strategyof kingpenguins (Aptenodytes patagonicus)during summer at the Crozet Islands Ecology 79 1905^1921
Sabourenkov E N 1991 Myctophids in the diet of Antarcticpredators In Selected scienticentc papers 1990 (ScienticentcCommittee-CCAMLR-XBG6) (ed Commission for theConservation of Antarctic Marine Living Resources(CCAMLR)) pp 335^360 Hobart Australia CCAMLR
Weimerskirch H Stahl J-C amp Jouventin P 1992 Thebreeding biology and population dynamics of king penguinsAptenodytespatagonica on the Crozet Islands Ibis 134 107^117
Wilson R P 1984 An improved stomach pump for penguinsand other sea birds J Field Ornithol 55 9^12
156 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
the most important food resources of the Southern Ocean(Sabourenkov 1991 Pakhomov et al 1996) The aims ofthe present work were (i) to validate this method incaptive penguins and (ii) to assess the feeding activity atsea of free-ranging birds by measuring their oesophagealtemperature
2 MATERIAL AND METHODS
The study was carried out at Possession Island Crozet Archi-pelago Southern Indian Ocean (46825rsquo S 51845rsquo E) at the`Grande Manchotiecopy rersquo colony of king penguins (40 000 breedingpairs Weimerskirch et al 1992) during the 1996 and 1997breeding seasons
(a) Temperature sensors and time^depth recordersData loggers used to monitor stomach temperature (in
captive birds) oesophageal temperature and dive depth in the0^200m range were manufactured by the Little Leonardo Co(Tokyo Japan) and had 1^2 Mb of poundash memory In captivebirds oesophageal temperatures were measured by a four-channel temperature logger linked to an oesophageal probe withfour thermistors the logging unit was housed in an aluminiumcylinder (8 bits 90 mmpound14 mm diameter resolution 01 8C)stomach temperatures were recorded by a cylindrical two-channel logger (12 bits 90 mmpound19 mm diameter resolution002 8C accuracy 01 8C)
In free-ranging birds oesophageal temperature and divedepth in the 0^200m range were measured by a cylindricalthree-channel logger (12 bits 90 mmpound 20 mm diameter and ca50 g temperature and depth resolution 002 8C and 01mrespectively) Cylindrical oesophageal thermistors (5 mmpound 3 mm) were plastic coated and had an accuracy of 03 8CEach thermistor was linked to the central unit by a 05^1m elec-tric cable (diameter 12 mm) Stomach temperatures wererecorded by a cylindrical logger (Driesen and Kern GmbH BadBramstedt Germany 8 bits 105 mm pound16 mm diameter and ca80 g resolution 01 8C 025 Mb memory) The thermal time-constant of oesophageal sensors (32 s) was nine and 14 timesshorter than for the stomach sensors used in captive and free-ranging birds respectively Dive depth in the 200^500m range
was measured by an MK5 time^depth recorder (WildlifeComputers (Redmond WA USA) 65 mmpound 38 mmpound15 mmand ca 50 g 2 m resolution 05 Mb memory)
(b) Feeding captive birdsWe centrst examined the temperature changes in the oesophagus
and the stomach in response to ingestion of meals of known sizeand temperature in centve non-breeding adults Each bird wasinduced to swallow a stomach sensor (1s sampling interval)attached to a thin plastic line (used to remove the unit after theexperiment) The four-channel temperature logger (2 s samplinginterval) was then taped onto the back feathers and the bird wasinduced to swallow the oesophageal probe Care was taken toreduce handling stress The oesophageal probe consisted of a30 cm poundexible plastic tube diameter 07 cm with four regularlyspaced thermistors In the oesophagus the sensors were at 9 1625 and 34 cm from the beak junction (sensors a b c and drespectively) The birds were kept in a fenced enclosure for30 min to allow the thermistors to reach body temperature Atotal of 220 centsh pieces (mass and temperature ranges 16^147 gand 05^9 8C respectively) simulating the temperature and thesize of the prey usually caught by king penguins (Cherel ampRidoux 1992) were hand-fed to them at 2^6 min intervalsduring sessions lasting on average 100 min
152 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
oesophageal temperature sensor
tunnelledcable
timendashtemperaturendashdepthrecorder
stomach temperature recorder
Figure 1 View of a king penguin showing the location ofequipment deployed on free-ranging individuals Cableswere tunnelled under the skin from the oesophagus to alogger unit taped onto the feathers recording dive depth andoesophageal temperature A second logger recorded thestomach temperature
33
36
39
30
33
36
39
30
30
33
36
27
33
36
39
30
40
3638
time (min)
oeso
phag
eal t
empe
ratu
re (
deg C)
0 10 20 30 40 50 60
(e)stomach
34 cm
25 cm
16 cm
9 cmexperimental feedings
(d)
(c)
(b)
(a)
Figure 2 Changes in temperature as a result of the ingestionof 20 centsh pieces recorded by four thermistors located in theoesophagus of a captive king penguin The thermistors werelocated at 9 16 25 and 34 cm from the beak (sensor a b cand d respectively) and in the stomach (e) Fish temperaturewas 8 8C and the mass of each piece was about 9 g
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
(c) Equipping free-ranging birdsSeven birds at the brood stage were surgically implanted
under halothane anaesthesia with an intraluminal oesophagealtemperature sensor and a tracheal temperature sensor at 6^10 cm from the beak junction The cables of the sensors werecentxed with absorbable suture threads onto the external walls ofthe oesophagus and trachea at 15 mm and 5 mm from thesensors respectively The body of the unit (2 s sampling interval)was attached externally onto the lower back with the cablestunnelled up to the upper oesophagus and the trachea (seecentgure 1) The tunnellization was performed using a specialsterile stainless steel tube Cutaneous wounds were closed usingabsorbable suture threads The transcutaneous transition wasprotected and anchored by a non-absorbable suture thread Sixout of the seven penguins were induced to swallow a stomachtemperature sensor (16 s sampling interval) Four out of theseven individuals were implanted with an MK5 recorder in theabdominal cavity as described by Handrich et al (1997) Divedepths were sampled every 4 s The work was performed in ashelter within the colony site and the birds were thereafterreturned to their breeding spot There using a portable enclo-sure they were protected from neighbours and predators untilfull recovery from the anaesthesia All equipment was removedunder anaesthesia after the birds returned and the individualswere released in apparently good condition None of the birdsimplanted with thermistors showed infection Moreover allcontinued to breed (chick brooding) after the removal of theequipment The procedure complied with current laws of theFrench authorities Authorization of the Ministecopy re de lrsquoAgricul-ture et de la Foreordf t (no 04196) followed by approbation of thesurgical protocol by the Ethics Committee of the FrenchInstitute for Polar Research In this study we will report onoesophageal and stomachal temperatures and diving behaviour
(d) Data analysisData were downloaded and analysed using Jensen System
Software programs (Laboe Germany) and custom-made Fox-base programs In the stomach and the oesophagus theexpected temperature signal following ingestion of a cold preyitem by endotherms is a precipitous droprsquo of the sensor tempera-ture followed by an exponential risersquo to the body value (PDER)The PDER repoundects the cooling and rewarming of the sensorafter contact with the cold item (Wilson et al 1992 1995)However because temperature changes in divers may repoundecteither prey ingestion (PDER) or non-feeding events (ietemperature changes due to diving per se) (Handrich et al 1997)we examined in detail at-sea temperature drops to identifyfeeding and non-feeding events For this we compared the
oesophageal temperature drops for the two main categories ofdives previously observed in king penguins (Kooyman et al1992 Charrassin et al 1998 PIumltz et al 1998) shallow (430 m)and deep (4 30 m) dives Means are given thorn se
3 RESULTS
(a) Experimental feedingsAll 220 items fed to the penguins were detected
(temperature drop 503 8C) by sensor a except for centvemeals that were not swallowed The proportion of eventsshowing a PDER at the upper sensor (a) was 20 (range0^61 n ˆ 9 feeding sessions) Non-PDER events (ieeither a non-precipitous drop (slower drop) or a slow rise)repoundected a chaotic passage of the prey over the sensorIndeed based on the behaviour of the birds they oftendid not swallow the food at once sometimes alternatelytrying to regurgitate and swallow the food We assumethis does not occur in a free-ranging feeding bird Theresponse to ingestion was best in the upper thermistorand with increasing distance from the beak detection ofthe prey was less certain (centgure 2) Ingestions were notdetected by the stomach sensor although the temperaturedropped from 382 to 377 8C during that period(centgure 2) The progression velocity of prey items betweenthe sensors a and b b and c and c and d averaged
Prey ingestion inpenguins J-B Charrassin and others 153
Proc R Soc Lond B (2001)
Table 1 Foraging characteristics of three king penguins equipped with data loggers monitoring their oesophageal temperatureand diving behaviour in early February 1997 at Crozet Archip elago
(The birds were at the brood stage A dive was considered as successful when at least one ingestion was detected Meansare sect se)
duration stomach oeso- total no mean meanmean no per cent
of oeso- content phageal prey no no ingestions successful
foragingdates
phagealrecord
at thebirdrsquos
tempera-ture range
ingestions(RTD5
preyingestions
dives430 m
per dive dives
(1997) (days) return (kg) (8C) 0068 Csiexcl1) dayiexcl1 dayiexcl1 430 m 430 m 4 30 m430 m
(b) Prey ingestion and diving behaviour in free-ranging penguins
Out of the seven birds equipped four remained at seafor 119 sect 09 days on average (range 101^145 days) Thestomach content upon return was sampled using thewater oiexcl-loading technique (Wilson 1984) It rangedfrom 05 to 1kg One bird spent 15 days at sea Two indi-viduals stayed in the colony Out of the four birds whichwent to sea with a stomach recorder two lost the recorderby regurgitation of the unit at sea and two had retainedit when they came back Continuous oesophagealtemperature records lasting six to seven days wereobtained from three birds and a total of 4900 dives from1^291m depth were recorded simultaneously (table 1)
As shown in centgure 3 both stomach and oesophagealtemperatures showed slow and regular variations whichcoincided with the dives However for oesophagealtemperature large and rapid drops which were not seenfor stomach temperature were superimposed on thesevariations Only when numerous rapid drops in oesopha-geal temperature occurred did stomach temperaturedecrease further During the intensive diving that kingpenguins make during their foraging trips at sea (seecentgure 4) their drops in oesophageal temperature didreach as much as 133 8C Still dives with only minorchanges in oesophageal temperature (centgure 5a)contrasted with dives with large variations in oesophagealtemperature (centgure 5b)
For the 650 sect 60 temperature drops 5002 8C recordedon average per day for each of the three birds (n ˆ 19days) two groups of temperature drops were character-ized according to their amplitude and duration (centgure 6)The centrst group corresponded to slow drops showing asmall amplitude (1^2 8C or below) and lasting for up to3 min Based on their rate of temperature decrease (RTDdecentned as the amplitude of the temperature drop divided
by the drop duration) slow drops accounted for most ofthose occurring during shallow dives (95 of drops hadan RTD 5 006 8C s71) but were also observed duringdeep dives (centgure 6) They corresponded to the cyclicvariations already described in centgure 3 which occurringin relation to the dives repoundect the tissue cooling due todiving per se (Handrich et al 1997)
The other group included large (up to 133 8C) andshort (530 s) drops which occurred mainly during deepdives (centgure 6) During deep dives 50 of these dropshad an RTD greater than 006 8C s71 Because such rapiddrops were much shorter than the duration of the divesduring which they occurred they indicate cooling by coldprey Fast temperature drops (RTD5006 8C s71) weretherefore assumed to repoundect prey ingestion Feeding eventsinferred from oesophageal temperature are shown incentgure 5b
(c) Feeding frequency and feeding depthThe number of ingestions per day varied from 95 to
300 among the birds and the number of ingestions pershallow dive (430 m) was much smaller than for deepdives (table 1) Bird 3 apparently experienced a muchlower foraging success than the others Feeding depthswere obtained from the dive procentles recorded simulta-neously with oesophageal temperature In bird 2 preyingestions occurred mainly between 80 and 170 m where70 of ingestions were detected (centgure 7) Duringdiving 5 sect 3 41 sect 2 and 54 sect 5 of prey ingestions tookplace during the descent bottom and ascent parts of thedives respectively (n ˆ 3 birds and 4200 dives4 70 m)
4 DISCUSSION
This study is based on the assessment of oesophagealtemperature of free-ranging diving birds as a new
154 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
36
32
28
20
24
0
100
200
300
time (d)
oeso
phag
eal t
empe
ratu
re
(degC
)de
pth
(m)
1 Feb 2 3 4 5 6 7 8
Figure 4 Changes in upper oesophageal temperature inrelation to dive depth in a king penguin foraging at CrozetArchipelago during seven days after departure from thecolony The total trip duration was 11 days
32
28
2024
0
100
200
local solar houroe
soph
agea
lte
mpe
ratu
re
(degC
)
3634
oeso
phag
eal
tem
pera
ture
(deg
C)
dept
h (m
)
0
100
200
dept
h (m
)
0455 0505 0515
1525 1535 1545
(a)
(b)
36
Figure 5 Changes in upper oesophageal temperature inrelation to dive depth indicating non-feeding dives (a) andfeeding dives (b) in a foraging king penguin Arrows indicateprey ingestion Grey boxes show periods spent at the surface
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
method for detection of food ingestion Our techniqueallows detection of ingestion of prey items as small asmyctophid centsh in relation to depth
(a) Implantation of oesophageal probesin free-ranging penguins
Four birds went to sea and showed normal foragingbehaviour as judged by dive depth and food brought tothe chick (Kooyman et al 1992 Charrassin et al 1998PIumltz et al 1998) Why two birds stayed at the colony isunclear However recent work (Y Le Maho unpublisheddata) suggests that the passage of the cables in the neckmay particularly disturb some individuals Accordinglyfuture work with data transmission to the logger unitrather than a cable connection may solve the issueHowever implantation of the sensor in the oesophaguseliminates the possibility of losing the logger by regurgita-tion as can occur for stomach sensors (this study Wilsonet al 1998)
(b) Relevance of oesophageal probe for detectingsmall prey ingestions
Since all experimental feedings gave a detectableresponse we conclude that our system is sensitive enoughfor small-sized prey items The low thermal inertia of thesmall sensor accounts for its good sensitivity (Ancel et al1997) Such a small size reduces the probability of contactwith prey but is counterbalanced by the small cross-sectional area of the oesophagus Prey items were lessoften detected with increasing distances from the beakand detection was almost impossible in the stomach ofcaptive penguins However prey detection in the stomachcould be less reliable in our captive individuals than infree-ranging birds since movements during diving maycontinually change the sensor position in the stomach(Wilson et al 1995) thereby favouring contact with preyProgression of food items is faster in the upper part of theoesophagus This lessens the time between prey ingestion
and prey^sensor contact and favours detection byreduced warming of the prey Prey ingestion is then easierto distinguish from physiological changes due to diving(Handrich et al 1997) if the probe is located in the upperoesophagus rather than deeper in the body (eg in thestomach) Based on the 06 cm siexcl1 displacement of preyitems in the upper oesophagus found in captive birds thedelay for reaching a sensor located 9 cm from the beak is15 s Such a short interval allows a quasi real-time detec-tion of food ingestion
(c) Detecting prey ingestion in free-ranging penguinsKing penguins feed on patchily distributed mesopelagic
centsh (Adams amp Klages 1987 Cherel amp Ridoux 1992Olsson amp North 1997) Oesophageal temperaturesrecorded in free-ranging birds showed large variations( 413 8C) that indicated feeding events and feedingdepths when combined with dive procentles The typicalfast short and precipitous temperature drops clearly indi-cate prey ingestions as opposed to the slow temperaturevariations corresponding to the tissue cooling due tophysiological responses to diving (Handrich et al 1997)Furthermore these prey ingestions were concentrmed as therapid temperature drops mainly occurred during deepdives (exclusively performed during daylight by kingpenguins see centgure 4 Kooyman et al 1992 Charrassinet al 1998 PIumltz et al 1998) which correspond to thedepths where myctophids concentrate during the day(Zaselrsquosliy et al 1985 Duhamel 1998)
Based on a penguinrsquos average vertical velocity duringdiving of 13 m s71 (PIumltz et al 1998) and with an ingestion^detection delay of 15 s the accuracy of depth where inges-tion occurs is ca 20 m ie 10 of the dive depth if thebird reaches 200 m Being validated with concurrentapplication of a classical technique such as hydroacousticprey survey or net trawl this method may provide aunique means to assess the prey distribution over depthFor instance one of the three birds fed mainly at 80^170 m where it probably encountered dense prey patchesUsing average prey mass of king penguins (74 and 17 g
Prey ingestion inpenguins J-B Charrassin and others 155
Proc R Soc Lond B (2001)
9
6
3
0
12
temperature drop duration (s)
tem
pera
ture
dro
p (deg
C)
0 50 100 150
non-feedingevents
feedingevents
dives gt 30 mdives pound 30 m
200
Figure 6 Relationships between amplitude and duration oftemperature drops in the upper oesophagus recorded in aking penguin during shallow dives (430 m n ˆ 1951 drops)and deep dives ( 4 30 m n ˆ 2450 drops) The dashed lineindicates the rate of temperature decrease above whichtemperature drops were considered as repoundecting prey ingestion(006 8C s71 see frac12 3) The period covered six foraging days
1020
08
04
06
02
00
30
depth of temperature drop (m)
rate
of
tem
pera
ture
dec
reas
e (deg
C s
- 1)
0 50 100 150 200 250 300
Figure 7 Depths at which temperature drops of the upperoesophagus occurred in a king penguin foraging for 75 days(n ˆ 6209 drops 5002 8C) Considering that a rate oftemperature decrease 5006 8C s71 (dashed line) indicatesfeeding most prey ingestion occurred at depths from about80 to 170 m
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
for the two main prey species in proportions of 75 and15 of the diet respectively Cherel amp Ridoux 1992) thedaily mass of centsh ingested by birds 1 and 2 was ca 16 kgand was 06 kg for bird 3 These values are comparablewith those ranges found in studies based on energetics(Kooyman et al 1992) and argue for the reliability of ourmethod
In conclusion measurement of oesophageal tempera-ture appears to be a promising tool for detecting preyingestion by marine predators Beside new information onthe feeding ecology of these predators an interestingperspective is their use to infer the prey distribution atdepth in particular for small schooling centsh dicurrencult todetect by conventional methods but which are keymarine resources in the Southern Ocean
The National Institute for Polar Research (Japan) the InstitutFrancdeg ais pour la Recherche et la Technologie Polaires and theTerres Australes et Antarctiques Francdeg aises provided centnancialand logistical support for this work The Centre National de laRecherche Scienticentque (GDRE no 1069 and PICS no 347) alsohelped in the funding We are indebted to the Penguin Fund(Tokyo Japan) for providing J-BC with a grant We thankC Marchand for help with surgeryY Clerquin and G Froget forcenteldwork assistance and members of the 33rd and 34th Missionsat Crozet Islands for a generous welcome The Little LeonardoCo (Tokyo Japan) is thanked for their ecurrencient cooperation andJ Lage (Jensen Software System) is acknowledged for writingcustomized software for data analysisWe are also very grateful toKnut Schmidt-Nielsen and to anonymous reviewers whosenumerous suggestions greatly improved our paper
REFERENCES
Adams N J amp Klages N T 1987 Seasonal variation in the dietof the king penguin (Aptenodytes patagonicus) at sub-AntarcticMarion Island J Zool 212 303^324
Ancel A Horning M amp Kooyman G L 1997 Prey ingestionrevealed by oesophagus and stomach temperature recordingsin cormorants J Exp Biol 200 149^154
Bevan R M Boyd I L Butler P J Reid K Woakes A Jamp Croxall J P 1997 Heart rates and abdominal temperaturesof free-ranging South Georgian shags Phalacrocorax georgianusJ Exp Biol 200 661^675
Bost C-A Georges J-Y Guinet C Cherel Y PIumltz KCharrassin J-B Handrich Y Zorn T Lage J amp LeMaho Y 1997 Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozetarchipelago Mar Ecol Prog Ser 150 21^33
Charrassin J-B Bost C-A PIumltz K Lage J Dahier TZornT amp Le MahoY 1998 Foraging strategies of incubatingand brooding king penguins Aptenodytes patagonicus Oecologia114 194^201
Cherel Y amp Ridoux V 1992 Prey species and nutritive value offood fed during summer to king penguin Aptenodytes patagonicachicks at Possession Island Crozet Archipelago Ibis 134 118^127
Croxall J P 1992 Southern Ocean environmental changeseiexclect on sea bird seal and whale populations Phil Trans RSoc Lond B 338 319^328
Croxall J P McCann T S Prince P A amp Rothery P 1988Reproductive performance of sea birds and seals at SouthGeorgia and Signy Island South Orkney Islands 1976^1987implications for Southern Ocean monitoring studies InAntarctic Ocean and resources variability (ed D Sahrhage)pp 261^285 Berlin and Heidelberg Germany Springer
Culik B M PIumltz K Wilson R P Bost C-A Le Maho Yamp Verselin J L 1996 Core temperature variability in divingking penguins (Aptenodytes patagonica) a preliminary analysisPolar Biol 16 371^378
Davis R W Fuiman L A Williams T M Collier S OHagey W P Kanatous S B Kohin S amp Horning M 1999Hunting behavior of a marine mammal beneath the Antarcticfast ice Science 283 993^996
Duhamel G 1998 The pelagic centsh community of the PolarFrontal Zone oiexcl the Kerguelen Islands In Fishes of AntarcticaA biological overview (ed G di Prisco E Pisano amp E Clarke)pp 63^74 Milan Italy Springer
Furness R W 1982 Competition between centsheries and seabirdsrsquo communities Adv Mar Biol 20 225^307
Gremillet D J H amp Plolaquo s A L 1994 The use of stomachtemperature records for the calculation of daily food intake incormorants J Exp Biol 189 105^115
Gremillet D J H Tuschy I amp Kierspel M 1998 Bodytemperature and insulation in diving great cormorants andEuropean shags Funct Ecol 12 386^394
Guinet C Chastel O Koudil M Durbec J-P amp JouventinP 1998 Eiexclect of warm sea-surface temperature anomalies onthe blue petrel at the Kerguelen Islands Proc R Soc LondB 265 1001^1006
Handrich Y Bevan R M Charrassin J-B Butler P JPIumltz K Woakes A J Lage J amp Le Maho Y 1997Hypothermia in foraging king penguins Nature 388 64^67
Huntley M E Lopez M D G amp Karl D M 1991 Top preda-tors in the Southern Ocean a major leak in the biologicalcarbon pump Science 253 64^66
Jouventin P amp Weimerskirch H 1990 Satellite tracking ofwandering albatrosses Nature 343 746^748
Kato A Naito Y Watanuki Y amp Shaughnessy P D 1996Diving pattern and stomach temperatures of foraging kingcormorants at subantarctic Macquarie Island Condor 98844^848
Kooyman G L Cherel Y Le Maho Y Croxall J PThorson P H Ridoux V amp Kooyman C A 1992 Divingbehavior and energetics during foraging cycles in kingpenguins Ecol Monogr 62 143^163
MontevecchiW A 1993 Birds as indicators of change in marineprey stocks In Birds as monitors of environmental change (edR W Furness amp J J D Greenwood) pp 217^266 LondonChapman amp Hall
Olsson O amp North A W 1997 Diet of the king penguinAptenodytes patagonicus during three summers at SouthGeorgia Ibis 139 504^512
Pakhomov E A Perissinotto R amp McQuaid C D 1996 Preycomposition and daily rations of myctophid centshes in theSouthern Ocean Mar Ecol Prog Ser 134 1^14
Peters G Wilson R P Scolaro J A Laurenti S Upton Jamp Galleli H 1998 The diving behavior of Magellanicpenguins at Punta Norte Peninsula Valdes Argentina ColonWaterbird 21 1^10
PIumltz K Wilson R P Charrassin J-B Raclot T Lage JLe MahoY Kierspel M A M Culik B M amp Adelung D1998 Foraging strategyof kingpenguins (Aptenodytes patagonicus)during summer at the Crozet Islands Ecology 79 1905^1921
Sabourenkov E N 1991 Myctophids in the diet of Antarcticpredators In Selected scienticentc papers 1990 (ScienticentcCommittee-CCAMLR-XBG6) (ed Commission for theConservation of Antarctic Marine Living Resources(CCAMLR)) pp 335^360 Hobart Australia CCAMLR
Weimerskirch H Stahl J-C amp Jouventin P 1992 Thebreeding biology and population dynamics of king penguinsAptenodytespatagonica on the Crozet Islands Ibis 134 107^117
Wilson R P 1984 An improved stomach pump for penguinsand other sea birds J Field Ornithol 55 9^12
156 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
(c) Equipping free-ranging birdsSeven birds at the brood stage were surgically implanted
under halothane anaesthesia with an intraluminal oesophagealtemperature sensor and a tracheal temperature sensor at 6^10 cm from the beak junction The cables of the sensors werecentxed with absorbable suture threads onto the external walls ofthe oesophagus and trachea at 15 mm and 5 mm from thesensors respectively The body of the unit (2 s sampling interval)was attached externally onto the lower back with the cablestunnelled up to the upper oesophagus and the trachea (seecentgure 1) The tunnellization was performed using a specialsterile stainless steel tube Cutaneous wounds were closed usingabsorbable suture threads The transcutaneous transition wasprotected and anchored by a non-absorbable suture thread Sixout of the seven penguins were induced to swallow a stomachtemperature sensor (16 s sampling interval) Four out of theseven individuals were implanted with an MK5 recorder in theabdominal cavity as described by Handrich et al (1997) Divedepths were sampled every 4 s The work was performed in ashelter within the colony site and the birds were thereafterreturned to their breeding spot There using a portable enclo-sure they were protected from neighbours and predators untilfull recovery from the anaesthesia All equipment was removedunder anaesthesia after the birds returned and the individualswere released in apparently good condition None of the birdsimplanted with thermistors showed infection Moreover allcontinued to breed (chick brooding) after the removal of theequipment The procedure complied with current laws of theFrench authorities Authorization of the Ministecopy re de lrsquoAgricul-ture et de la Foreordf t (no 04196) followed by approbation of thesurgical protocol by the Ethics Committee of the FrenchInstitute for Polar Research In this study we will report onoesophageal and stomachal temperatures and diving behaviour
(d) Data analysisData were downloaded and analysed using Jensen System
Software programs (Laboe Germany) and custom-made Fox-base programs In the stomach and the oesophagus theexpected temperature signal following ingestion of a cold preyitem by endotherms is a precipitous droprsquo of the sensor tempera-ture followed by an exponential risersquo to the body value (PDER)The PDER repoundects the cooling and rewarming of the sensorafter contact with the cold item (Wilson et al 1992 1995)However because temperature changes in divers may repoundecteither prey ingestion (PDER) or non-feeding events (ietemperature changes due to diving per se) (Handrich et al 1997)we examined in detail at-sea temperature drops to identifyfeeding and non-feeding events For this we compared the
oesophageal temperature drops for the two main categories ofdives previously observed in king penguins (Kooyman et al1992 Charrassin et al 1998 PIumltz et al 1998) shallow (430 m)and deep (4 30 m) dives Means are given thorn se
3 RESULTS
(a) Experimental feedingsAll 220 items fed to the penguins were detected
(temperature drop 503 8C) by sensor a except for centvemeals that were not swallowed The proportion of eventsshowing a PDER at the upper sensor (a) was 20 (range0^61 n ˆ 9 feeding sessions) Non-PDER events (ieeither a non-precipitous drop (slower drop) or a slow rise)repoundected a chaotic passage of the prey over the sensorIndeed based on the behaviour of the birds they oftendid not swallow the food at once sometimes alternatelytrying to regurgitate and swallow the food We assumethis does not occur in a free-ranging feeding bird Theresponse to ingestion was best in the upper thermistorand with increasing distance from the beak detection ofthe prey was less certain (centgure 2) Ingestions were notdetected by the stomach sensor although the temperaturedropped from 382 to 377 8C during that period(centgure 2) The progression velocity of prey items betweenthe sensors a and b b and c and c and d averaged
Prey ingestion inpenguins J-B Charrassin and others 153
Proc R Soc Lond B (2001)
Table 1 Foraging characteristics of three king penguins equipped with data loggers monitoring their oesophageal temperatureand diving behaviour in early February 1997 at Crozet Archip elago
(The birds were at the brood stage A dive was considered as successful when at least one ingestion was detected Meansare sect se)
duration stomach oeso- total no mean meanmean no per cent
of oeso- content phageal prey no no ingestions successful
foragingdates
phagealrecord
at thebirdrsquos
tempera-ture range
ingestions(RTD5
preyingestions
dives430 m
per dive dives
(1997) (days) return (kg) (8C) 0068 Csiexcl1) dayiexcl1 dayiexcl1 430 m 430 m 4 30 m430 m
(b) Prey ingestion and diving behaviour in free-ranging penguins
Out of the seven birds equipped four remained at seafor 119 sect 09 days on average (range 101^145 days) Thestomach content upon return was sampled using thewater oiexcl-loading technique (Wilson 1984) It rangedfrom 05 to 1kg One bird spent 15 days at sea Two indi-viduals stayed in the colony Out of the four birds whichwent to sea with a stomach recorder two lost the recorderby regurgitation of the unit at sea and two had retainedit when they came back Continuous oesophagealtemperature records lasting six to seven days wereobtained from three birds and a total of 4900 dives from1^291m depth were recorded simultaneously (table 1)
As shown in centgure 3 both stomach and oesophagealtemperatures showed slow and regular variations whichcoincided with the dives However for oesophagealtemperature large and rapid drops which were not seenfor stomach temperature were superimposed on thesevariations Only when numerous rapid drops in oesopha-geal temperature occurred did stomach temperaturedecrease further During the intensive diving that kingpenguins make during their foraging trips at sea (seecentgure 4) their drops in oesophageal temperature didreach as much as 133 8C Still dives with only minorchanges in oesophageal temperature (centgure 5a)contrasted with dives with large variations in oesophagealtemperature (centgure 5b)
For the 650 sect 60 temperature drops 5002 8C recordedon average per day for each of the three birds (n ˆ 19days) two groups of temperature drops were character-ized according to their amplitude and duration (centgure 6)The centrst group corresponded to slow drops showing asmall amplitude (1^2 8C or below) and lasting for up to3 min Based on their rate of temperature decrease (RTDdecentned as the amplitude of the temperature drop divided
by the drop duration) slow drops accounted for most ofthose occurring during shallow dives (95 of drops hadan RTD 5 006 8C s71) but were also observed duringdeep dives (centgure 6) They corresponded to the cyclicvariations already described in centgure 3 which occurringin relation to the dives repoundect the tissue cooling due todiving per se (Handrich et al 1997)
The other group included large (up to 133 8C) andshort (530 s) drops which occurred mainly during deepdives (centgure 6) During deep dives 50 of these dropshad an RTD greater than 006 8C s71 Because such rapiddrops were much shorter than the duration of the divesduring which they occurred they indicate cooling by coldprey Fast temperature drops (RTD5006 8C s71) weretherefore assumed to repoundect prey ingestion Feeding eventsinferred from oesophageal temperature are shown incentgure 5b
(c) Feeding frequency and feeding depthThe number of ingestions per day varied from 95 to
300 among the birds and the number of ingestions pershallow dive (430 m) was much smaller than for deepdives (table 1) Bird 3 apparently experienced a muchlower foraging success than the others Feeding depthswere obtained from the dive procentles recorded simulta-neously with oesophageal temperature In bird 2 preyingestions occurred mainly between 80 and 170 m where70 of ingestions were detected (centgure 7) Duringdiving 5 sect 3 41 sect 2 and 54 sect 5 of prey ingestions tookplace during the descent bottom and ascent parts of thedives respectively (n ˆ 3 birds and 4200 dives4 70 m)
4 DISCUSSION
This study is based on the assessment of oesophagealtemperature of free-ranging diving birds as a new
154 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
36
32
28
20
24
0
100
200
300
time (d)
oeso
phag
eal t
empe
ratu
re
(degC
)de
pth
(m)
1 Feb 2 3 4 5 6 7 8
Figure 4 Changes in upper oesophageal temperature inrelation to dive depth in a king penguin foraging at CrozetArchipelago during seven days after departure from thecolony The total trip duration was 11 days
32
28
2024
0
100
200
local solar houroe
soph
agea
lte
mpe
ratu
re
(degC
)
3634
oeso
phag
eal
tem
pera
ture
(deg
C)
dept
h (m
)
0
100
200
dept
h (m
)
0455 0505 0515
1525 1535 1545
(a)
(b)
36
Figure 5 Changes in upper oesophageal temperature inrelation to dive depth indicating non-feeding dives (a) andfeeding dives (b) in a foraging king penguin Arrows indicateprey ingestion Grey boxes show periods spent at the surface
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
method for detection of food ingestion Our techniqueallows detection of ingestion of prey items as small asmyctophid centsh in relation to depth
(a) Implantation of oesophageal probesin free-ranging penguins
Four birds went to sea and showed normal foragingbehaviour as judged by dive depth and food brought tothe chick (Kooyman et al 1992 Charrassin et al 1998PIumltz et al 1998) Why two birds stayed at the colony isunclear However recent work (Y Le Maho unpublisheddata) suggests that the passage of the cables in the neckmay particularly disturb some individuals Accordinglyfuture work with data transmission to the logger unitrather than a cable connection may solve the issueHowever implantation of the sensor in the oesophaguseliminates the possibility of losing the logger by regurgita-tion as can occur for stomach sensors (this study Wilsonet al 1998)
(b) Relevance of oesophageal probe for detectingsmall prey ingestions
Since all experimental feedings gave a detectableresponse we conclude that our system is sensitive enoughfor small-sized prey items The low thermal inertia of thesmall sensor accounts for its good sensitivity (Ancel et al1997) Such a small size reduces the probability of contactwith prey but is counterbalanced by the small cross-sectional area of the oesophagus Prey items were lessoften detected with increasing distances from the beakand detection was almost impossible in the stomach ofcaptive penguins However prey detection in the stomachcould be less reliable in our captive individuals than infree-ranging birds since movements during diving maycontinually change the sensor position in the stomach(Wilson et al 1995) thereby favouring contact with preyProgression of food items is faster in the upper part of theoesophagus This lessens the time between prey ingestion
and prey^sensor contact and favours detection byreduced warming of the prey Prey ingestion is then easierto distinguish from physiological changes due to diving(Handrich et al 1997) if the probe is located in the upperoesophagus rather than deeper in the body (eg in thestomach) Based on the 06 cm siexcl1 displacement of preyitems in the upper oesophagus found in captive birds thedelay for reaching a sensor located 9 cm from the beak is15 s Such a short interval allows a quasi real-time detec-tion of food ingestion
(c) Detecting prey ingestion in free-ranging penguinsKing penguins feed on patchily distributed mesopelagic
centsh (Adams amp Klages 1987 Cherel amp Ridoux 1992Olsson amp North 1997) Oesophageal temperaturesrecorded in free-ranging birds showed large variations( 413 8C) that indicated feeding events and feedingdepths when combined with dive procentles The typicalfast short and precipitous temperature drops clearly indi-cate prey ingestions as opposed to the slow temperaturevariations corresponding to the tissue cooling due tophysiological responses to diving (Handrich et al 1997)Furthermore these prey ingestions were concentrmed as therapid temperature drops mainly occurred during deepdives (exclusively performed during daylight by kingpenguins see centgure 4 Kooyman et al 1992 Charrassinet al 1998 PIumltz et al 1998) which correspond to thedepths where myctophids concentrate during the day(Zaselrsquosliy et al 1985 Duhamel 1998)
Based on a penguinrsquos average vertical velocity duringdiving of 13 m s71 (PIumltz et al 1998) and with an ingestion^detection delay of 15 s the accuracy of depth where inges-tion occurs is ca 20 m ie 10 of the dive depth if thebird reaches 200 m Being validated with concurrentapplication of a classical technique such as hydroacousticprey survey or net trawl this method may provide aunique means to assess the prey distribution over depthFor instance one of the three birds fed mainly at 80^170 m where it probably encountered dense prey patchesUsing average prey mass of king penguins (74 and 17 g
Prey ingestion inpenguins J-B Charrassin and others 155
Proc R Soc Lond B (2001)
9
6
3
0
12
temperature drop duration (s)
tem
pera
ture
dro
p (deg
C)
0 50 100 150
non-feedingevents
feedingevents
dives gt 30 mdives pound 30 m
200
Figure 6 Relationships between amplitude and duration oftemperature drops in the upper oesophagus recorded in aking penguin during shallow dives (430 m n ˆ 1951 drops)and deep dives ( 4 30 m n ˆ 2450 drops) The dashed lineindicates the rate of temperature decrease above whichtemperature drops were considered as repoundecting prey ingestion(006 8C s71 see frac12 3) The period covered six foraging days
1020
08
04
06
02
00
30
depth of temperature drop (m)
rate
of
tem
pera
ture
dec
reas
e (deg
C s
- 1)
0 50 100 150 200 250 300
Figure 7 Depths at which temperature drops of the upperoesophagus occurred in a king penguin foraging for 75 days(n ˆ 6209 drops 5002 8C) Considering that a rate oftemperature decrease 5006 8C s71 (dashed line) indicatesfeeding most prey ingestion occurred at depths from about80 to 170 m
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
for the two main prey species in proportions of 75 and15 of the diet respectively Cherel amp Ridoux 1992) thedaily mass of centsh ingested by birds 1 and 2 was ca 16 kgand was 06 kg for bird 3 These values are comparablewith those ranges found in studies based on energetics(Kooyman et al 1992) and argue for the reliability of ourmethod
In conclusion measurement of oesophageal tempera-ture appears to be a promising tool for detecting preyingestion by marine predators Beside new information onthe feeding ecology of these predators an interestingperspective is their use to infer the prey distribution atdepth in particular for small schooling centsh dicurrencult todetect by conventional methods but which are keymarine resources in the Southern Ocean
The National Institute for Polar Research (Japan) the InstitutFrancdeg ais pour la Recherche et la Technologie Polaires and theTerres Australes et Antarctiques Francdeg aises provided centnancialand logistical support for this work The Centre National de laRecherche Scienticentque (GDRE no 1069 and PICS no 347) alsohelped in the funding We are indebted to the Penguin Fund(Tokyo Japan) for providing J-BC with a grant We thankC Marchand for help with surgeryY Clerquin and G Froget forcenteldwork assistance and members of the 33rd and 34th Missionsat Crozet Islands for a generous welcome The Little LeonardoCo (Tokyo Japan) is thanked for their ecurrencient cooperation andJ Lage (Jensen Software System) is acknowledged for writingcustomized software for data analysisWe are also very grateful toKnut Schmidt-Nielsen and to anonymous reviewers whosenumerous suggestions greatly improved our paper
REFERENCES
Adams N J amp Klages N T 1987 Seasonal variation in the dietof the king penguin (Aptenodytes patagonicus) at sub-AntarcticMarion Island J Zool 212 303^324
Ancel A Horning M amp Kooyman G L 1997 Prey ingestionrevealed by oesophagus and stomach temperature recordingsin cormorants J Exp Biol 200 149^154
Bevan R M Boyd I L Butler P J Reid K Woakes A Jamp Croxall J P 1997 Heart rates and abdominal temperaturesof free-ranging South Georgian shags Phalacrocorax georgianusJ Exp Biol 200 661^675
Bost C-A Georges J-Y Guinet C Cherel Y PIumltz KCharrassin J-B Handrich Y Zorn T Lage J amp LeMaho Y 1997 Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozetarchipelago Mar Ecol Prog Ser 150 21^33
Charrassin J-B Bost C-A PIumltz K Lage J Dahier TZornT amp Le MahoY 1998 Foraging strategies of incubatingand brooding king penguins Aptenodytes patagonicus Oecologia114 194^201
Cherel Y amp Ridoux V 1992 Prey species and nutritive value offood fed during summer to king penguin Aptenodytes patagonicachicks at Possession Island Crozet Archipelago Ibis 134 118^127
Croxall J P 1992 Southern Ocean environmental changeseiexclect on sea bird seal and whale populations Phil Trans RSoc Lond B 338 319^328
Croxall J P McCann T S Prince P A amp Rothery P 1988Reproductive performance of sea birds and seals at SouthGeorgia and Signy Island South Orkney Islands 1976^1987implications for Southern Ocean monitoring studies InAntarctic Ocean and resources variability (ed D Sahrhage)pp 261^285 Berlin and Heidelberg Germany Springer
Culik B M PIumltz K Wilson R P Bost C-A Le Maho Yamp Verselin J L 1996 Core temperature variability in divingking penguins (Aptenodytes patagonica) a preliminary analysisPolar Biol 16 371^378
Davis R W Fuiman L A Williams T M Collier S OHagey W P Kanatous S B Kohin S amp Horning M 1999Hunting behavior of a marine mammal beneath the Antarcticfast ice Science 283 993^996
Duhamel G 1998 The pelagic centsh community of the PolarFrontal Zone oiexcl the Kerguelen Islands In Fishes of AntarcticaA biological overview (ed G di Prisco E Pisano amp E Clarke)pp 63^74 Milan Italy Springer
Furness R W 1982 Competition between centsheries and seabirdsrsquo communities Adv Mar Biol 20 225^307
Gremillet D J H amp Plolaquo s A L 1994 The use of stomachtemperature records for the calculation of daily food intake incormorants J Exp Biol 189 105^115
Gremillet D J H Tuschy I amp Kierspel M 1998 Bodytemperature and insulation in diving great cormorants andEuropean shags Funct Ecol 12 386^394
Guinet C Chastel O Koudil M Durbec J-P amp JouventinP 1998 Eiexclect of warm sea-surface temperature anomalies onthe blue petrel at the Kerguelen Islands Proc R Soc LondB 265 1001^1006
Handrich Y Bevan R M Charrassin J-B Butler P JPIumltz K Woakes A J Lage J amp Le Maho Y 1997Hypothermia in foraging king penguins Nature 388 64^67
Huntley M E Lopez M D G amp Karl D M 1991 Top preda-tors in the Southern Ocean a major leak in the biologicalcarbon pump Science 253 64^66
Jouventin P amp Weimerskirch H 1990 Satellite tracking ofwandering albatrosses Nature 343 746^748
Kato A Naito Y Watanuki Y amp Shaughnessy P D 1996Diving pattern and stomach temperatures of foraging kingcormorants at subantarctic Macquarie Island Condor 98844^848
Kooyman G L Cherel Y Le Maho Y Croxall J PThorson P H Ridoux V amp Kooyman C A 1992 Divingbehavior and energetics during foraging cycles in kingpenguins Ecol Monogr 62 143^163
MontevecchiW A 1993 Birds as indicators of change in marineprey stocks In Birds as monitors of environmental change (edR W Furness amp J J D Greenwood) pp 217^266 LondonChapman amp Hall
Olsson O amp North A W 1997 Diet of the king penguinAptenodytes patagonicus during three summers at SouthGeorgia Ibis 139 504^512
Pakhomov E A Perissinotto R amp McQuaid C D 1996 Preycomposition and daily rations of myctophid centshes in theSouthern Ocean Mar Ecol Prog Ser 134 1^14
Peters G Wilson R P Scolaro J A Laurenti S Upton Jamp Galleli H 1998 The diving behavior of Magellanicpenguins at Punta Norte Peninsula Valdes Argentina ColonWaterbird 21 1^10
PIumltz K Wilson R P Charrassin J-B Raclot T Lage JLe MahoY Kierspel M A M Culik B M amp Adelung D1998 Foraging strategyof kingpenguins (Aptenodytes patagonicus)during summer at the Crozet Islands Ecology 79 1905^1921
Sabourenkov E N 1991 Myctophids in the diet of Antarcticpredators In Selected scienticentc papers 1990 (ScienticentcCommittee-CCAMLR-XBG6) (ed Commission for theConservation of Antarctic Marine Living Resources(CCAMLR)) pp 335^360 Hobart Australia CCAMLR
Weimerskirch H Stahl J-C amp Jouventin P 1992 Thebreeding biology and population dynamics of king penguinsAptenodytespatagonica on the Crozet Islands Ibis 134 107^117
Wilson R P 1984 An improved stomach pump for penguinsand other sea birds J Field Ornithol 55 9^12
156 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
(b) Prey ingestion and diving behaviour in free-ranging penguins
Out of the seven birds equipped four remained at seafor 119 sect 09 days on average (range 101^145 days) Thestomach content upon return was sampled using thewater oiexcl-loading technique (Wilson 1984) It rangedfrom 05 to 1kg One bird spent 15 days at sea Two indi-viduals stayed in the colony Out of the four birds whichwent to sea with a stomach recorder two lost the recorderby regurgitation of the unit at sea and two had retainedit when they came back Continuous oesophagealtemperature records lasting six to seven days wereobtained from three birds and a total of 4900 dives from1^291m depth were recorded simultaneously (table 1)
As shown in centgure 3 both stomach and oesophagealtemperatures showed slow and regular variations whichcoincided with the dives However for oesophagealtemperature large and rapid drops which were not seenfor stomach temperature were superimposed on thesevariations Only when numerous rapid drops in oesopha-geal temperature occurred did stomach temperaturedecrease further During the intensive diving that kingpenguins make during their foraging trips at sea (seecentgure 4) their drops in oesophageal temperature didreach as much as 133 8C Still dives with only minorchanges in oesophageal temperature (centgure 5a)contrasted with dives with large variations in oesophagealtemperature (centgure 5b)
For the 650 sect 60 temperature drops 5002 8C recordedon average per day for each of the three birds (n ˆ 19days) two groups of temperature drops were character-ized according to their amplitude and duration (centgure 6)The centrst group corresponded to slow drops showing asmall amplitude (1^2 8C or below) and lasting for up to3 min Based on their rate of temperature decrease (RTDdecentned as the amplitude of the temperature drop divided
by the drop duration) slow drops accounted for most ofthose occurring during shallow dives (95 of drops hadan RTD 5 006 8C s71) but were also observed duringdeep dives (centgure 6) They corresponded to the cyclicvariations already described in centgure 3 which occurringin relation to the dives repoundect the tissue cooling due todiving per se (Handrich et al 1997)
The other group included large (up to 133 8C) andshort (530 s) drops which occurred mainly during deepdives (centgure 6) During deep dives 50 of these dropshad an RTD greater than 006 8C s71 Because such rapiddrops were much shorter than the duration of the divesduring which they occurred they indicate cooling by coldprey Fast temperature drops (RTD5006 8C s71) weretherefore assumed to repoundect prey ingestion Feeding eventsinferred from oesophageal temperature are shown incentgure 5b
(c) Feeding frequency and feeding depthThe number of ingestions per day varied from 95 to
300 among the birds and the number of ingestions pershallow dive (430 m) was much smaller than for deepdives (table 1) Bird 3 apparently experienced a muchlower foraging success than the others Feeding depthswere obtained from the dive procentles recorded simulta-neously with oesophageal temperature In bird 2 preyingestions occurred mainly between 80 and 170 m where70 of ingestions were detected (centgure 7) Duringdiving 5 sect 3 41 sect 2 and 54 sect 5 of prey ingestions tookplace during the descent bottom and ascent parts of thedives respectively (n ˆ 3 birds and 4200 dives4 70 m)
4 DISCUSSION
This study is based on the assessment of oesophagealtemperature of free-ranging diving birds as a new
154 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
36
32
28
20
24
0
100
200
300
time (d)
oeso
phag
eal t
empe
ratu
re
(degC
)de
pth
(m)
1 Feb 2 3 4 5 6 7 8
Figure 4 Changes in upper oesophageal temperature inrelation to dive depth in a king penguin foraging at CrozetArchipelago during seven days after departure from thecolony The total trip duration was 11 days
32
28
2024
0
100
200
local solar houroe
soph
agea
lte
mpe
ratu
re
(degC
)
3634
oeso
phag
eal
tem
pera
ture
(deg
C)
dept
h (m
)
0
100
200
dept
h (m
)
0455 0505 0515
1525 1535 1545
(a)
(b)
36
Figure 5 Changes in upper oesophageal temperature inrelation to dive depth indicating non-feeding dives (a) andfeeding dives (b) in a foraging king penguin Arrows indicateprey ingestion Grey boxes show periods spent at the surface
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
method for detection of food ingestion Our techniqueallows detection of ingestion of prey items as small asmyctophid centsh in relation to depth
(a) Implantation of oesophageal probesin free-ranging penguins
Four birds went to sea and showed normal foragingbehaviour as judged by dive depth and food brought tothe chick (Kooyman et al 1992 Charrassin et al 1998PIumltz et al 1998) Why two birds stayed at the colony isunclear However recent work (Y Le Maho unpublisheddata) suggests that the passage of the cables in the neckmay particularly disturb some individuals Accordinglyfuture work with data transmission to the logger unitrather than a cable connection may solve the issueHowever implantation of the sensor in the oesophaguseliminates the possibility of losing the logger by regurgita-tion as can occur for stomach sensors (this study Wilsonet al 1998)
(b) Relevance of oesophageal probe for detectingsmall prey ingestions
Since all experimental feedings gave a detectableresponse we conclude that our system is sensitive enoughfor small-sized prey items The low thermal inertia of thesmall sensor accounts for its good sensitivity (Ancel et al1997) Such a small size reduces the probability of contactwith prey but is counterbalanced by the small cross-sectional area of the oesophagus Prey items were lessoften detected with increasing distances from the beakand detection was almost impossible in the stomach ofcaptive penguins However prey detection in the stomachcould be less reliable in our captive individuals than infree-ranging birds since movements during diving maycontinually change the sensor position in the stomach(Wilson et al 1995) thereby favouring contact with preyProgression of food items is faster in the upper part of theoesophagus This lessens the time between prey ingestion
and prey^sensor contact and favours detection byreduced warming of the prey Prey ingestion is then easierto distinguish from physiological changes due to diving(Handrich et al 1997) if the probe is located in the upperoesophagus rather than deeper in the body (eg in thestomach) Based on the 06 cm siexcl1 displacement of preyitems in the upper oesophagus found in captive birds thedelay for reaching a sensor located 9 cm from the beak is15 s Such a short interval allows a quasi real-time detec-tion of food ingestion
(c) Detecting prey ingestion in free-ranging penguinsKing penguins feed on patchily distributed mesopelagic
centsh (Adams amp Klages 1987 Cherel amp Ridoux 1992Olsson amp North 1997) Oesophageal temperaturesrecorded in free-ranging birds showed large variations( 413 8C) that indicated feeding events and feedingdepths when combined with dive procentles The typicalfast short and precipitous temperature drops clearly indi-cate prey ingestions as opposed to the slow temperaturevariations corresponding to the tissue cooling due tophysiological responses to diving (Handrich et al 1997)Furthermore these prey ingestions were concentrmed as therapid temperature drops mainly occurred during deepdives (exclusively performed during daylight by kingpenguins see centgure 4 Kooyman et al 1992 Charrassinet al 1998 PIumltz et al 1998) which correspond to thedepths where myctophids concentrate during the day(Zaselrsquosliy et al 1985 Duhamel 1998)
Based on a penguinrsquos average vertical velocity duringdiving of 13 m s71 (PIumltz et al 1998) and with an ingestion^detection delay of 15 s the accuracy of depth where inges-tion occurs is ca 20 m ie 10 of the dive depth if thebird reaches 200 m Being validated with concurrentapplication of a classical technique such as hydroacousticprey survey or net trawl this method may provide aunique means to assess the prey distribution over depthFor instance one of the three birds fed mainly at 80^170 m where it probably encountered dense prey patchesUsing average prey mass of king penguins (74 and 17 g
Prey ingestion inpenguins J-B Charrassin and others 155
Proc R Soc Lond B (2001)
9
6
3
0
12
temperature drop duration (s)
tem
pera
ture
dro
p (deg
C)
0 50 100 150
non-feedingevents
feedingevents
dives gt 30 mdives pound 30 m
200
Figure 6 Relationships between amplitude and duration oftemperature drops in the upper oesophagus recorded in aking penguin during shallow dives (430 m n ˆ 1951 drops)and deep dives ( 4 30 m n ˆ 2450 drops) The dashed lineindicates the rate of temperature decrease above whichtemperature drops were considered as repoundecting prey ingestion(006 8C s71 see frac12 3) The period covered six foraging days
1020
08
04
06
02
00
30
depth of temperature drop (m)
rate
of
tem
pera
ture
dec
reas
e (deg
C s
- 1)
0 50 100 150 200 250 300
Figure 7 Depths at which temperature drops of the upperoesophagus occurred in a king penguin foraging for 75 days(n ˆ 6209 drops 5002 8C) Considering that a rate oftemperature decrease 5006 8C s71 (dashed line) indicatesfeeding most prey ingestion occurred at depths from about80 to 170 m
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
for the two main prey species in proportions of 75 and15 of the diet respectively Cherel amp Ridoux 1992) thedaily mass of centsh ingested by birds 1 and 2 was ca 16 kgand was 06 kg for bird 3 These values are comparablewith those ranges found in studies based on energetics(Kooyman et al 1992) and argue for the reliability of ourmethod
In conclusion measurement of oesophageal tempera-ture appears to be a promising tool for detecting preyingestion by marine predators Beside new information onthe feeding ecology of these predators an interestingperspective is their use to infer the prey distribution atdepth in particular for small schooling centsh dicurrencult todetect by conventional methods but which are keymarine resources in the Southern Ocean
The National Institute for Polar Research (Japan) the InstitutFrancdeg ais pour la Recherche et la Technologie Polaires and theTerres Australes et Antarctiques Francdeg aises provided centnancialand logistical support for this work The Centre National de laRecherche Scienticentque (GDRE no 1069 and PICS no 347) alsohelped in the funding We are indebted to the Penguin Fund(Tokyo Japan) for providing J-BC with a grant We thankC Marchand for help with surgeryY Clerquin and G Froget forcenteldwork assistance and members of the 33rd and 34th Missionsat Crozet Islands for a generous welcome The Little LeonardoCo (Tokyo Japan) is thanked for their ecurrencient cooperation andJ Lage (Jensen Software System) is acknowledged for writingcustomized software for data analysisWe are also very grateful toKnut Schmidt-Nielsen and to anonymous reviewers whosenumerous suggestions greatly improved our paper
REFERENCES
Adams N J amp Klages N T 1987 Seasonal variation in the dietof the king penguin (Aptenodytes patagonicus) at sub-AntarcticMarion Island J Zool 212 303^324
Ancel A Horning M amp Kooyman G L 1997 Prey ingestionrevealed by oesophagus and stomach temperature recordingsin cormorants J Exp Biol 200 149^154
Bevan R M Boyd I L Butler P J Reid K Woakes A Jamp Croxall J P 1997 Heart rates and abdominal temperaturesof free-ranging South Georgian shags Phalacrocorax georgianusJ Exp Biol 200 661^675
Bost C-A Georges J-Y Guinet C Cherel Y PIumltz KCharrassin J-B Handrich Y Zorn T Lage J amp LeMaho Y 1997 Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozetarchipelago Mar Ecol Prog Ser 150 21^33
Charrassin J-B Bost C-A PIumltz K Lage J Dahier TZornT amp Le MahoY 1998 Foraging strategies of incubatingand brooding king penguins Aptenodytes patagonicus Oecologia114 194^201
Cherel Y amp Ridoux V 1992 Prey species and nutritive value offood fed during summer to king penguin Aptenodytes patagonicachicks at Possession Island Crozet Archipelago Ibis 134 118^127
Croxall J P 1992 Southern Ocean environmental changeseiexclect on sea bird seal and whale populations Phil Trans RSoc Lond B 338 319^328
Croxall J P McCann T S Prince P A amp Rothery P 1988Reproductive performance of sea birds and seals at SouthGeorgia and Signy Island South Orkney Islands 1976^1987implications for Southern Ocean monitoring studies InAntarctic Ocean and resources variability (ed D Sahrhage)pp 261^285 Berlin and Heidelberg Germany Springer
Culik B M PIumltz K Wilson R P Bost C-A Le Maho Yamp Verselin J L 1996 Core temperature variability in divingking penguins (Aptenodytes patagonica) a preliminary analysisPolar Biol 16 371^378
Davis R W Fuiman L A Williams T M Collier S OHagey W P Kanatous S B Kohin S amp Horning M 1999Hunting behavior of a marine mammal beneath the Antarcticfast ice Science 283 993^996
Duhamel G 1998 The pelagic centsh community of the PolarFrontal Zone oiexcl the Kerguelen Islands In Fishes of AntarcticaA biological overview (ed G di Prisco E Pisano amp E Clarke)pp 63^74 Milan Italy Springer
Furness R W 1982 Competition between centsheries and seabirdsrsquo communities Adv Mar Biol 20 225^307
Gremillet D J H amp Plolaquo s A L 1994 The use of stomachtemperature records for the calculation of daily food intake incormorants J Exp Biol 189 105^115
Gremillet D J H Tuschy I amp Kierspel M 1998 Bodytemperature and insulation in diving great cormorants andEuropean shags Funct Ecol 12 386^394
Guinet C Chastel O Koudil M Durbec J-P amp JouventinP 1998 Eiexclect of warm sea-surface temperature anomalies onthe blue petrel at the Kerguelen Islands Proc R Soc LondB 265 1001^1006
Handrich Y Bevan R M Charrassin J-B Butler P JPIumltz K Woakes A J Lage J amp Le Maho Y 1997Hypothermia in foraging king penguins Nature 388 64^67
Huntley M E Lopez M D G amp Karl D M 1991 Top preda-tors in the Southern Ocean a major leak in the biologicalcarbon pump Science 253 64^66
Jouventin P amp Weimerskirch H 1990 Satellite tracking ofwandering albatrosses Nature 343 746^748
Kato A Naito Y Watanuki Y amp Shaughnessy P D 1996Diving pattern and stomach temperatures of foraging kingcormorants at subantarctic Macquarie Island Condor 98844^848
Kooyman G L Cherel Y Le Maho Y Croxall J PThorson P H Ridoux V amp Kooyman C A 1992 Divingbehavior and energetics during foraging cycles in kingpenguins Ecol Monogr 62 143^163
MontevecchiW A 1993 Birds as indicators of change in marineprey stocks In Birds as monitors of environmental change (edR W Furness amp J J D Greenwood) pp 217^266 LondonChapman amp Hall
Olsson O amp North A W 1997 Diet of the king penguinAptenodytes patagonicus during three summers at SouthGeorgia Ibis 139 504^512
Pakhomov E A Perissinotto R amp McQuaid C D 1996 Preycomposition and daily rations of myctophid centshes in theSouthern Ocean Mar Ecol Prog Ser 134 1^14
Peters G Wilson R P Scolaro J A Laurenti S Upton Jamp Galleli H 1998 The diving behavior of Magellanicpenguins at Punta Norte Peninsula Valdes Argentina ColonWaterbird 21 1^10
PIumltz K Wilson R P Charrassin J-B Raclot T Lage JLe MahoY Kierspel M A M Culik B M amp Adelung D1998 Foraging strategyof kingpenguins (Aptenodytes patagonicus)during summer at the Crozet Islands Ecology 79 1905^1921
Sabourenkov E N 1991 Myctophids in the diet of Antarcticpredators In Selected scienticentc papers 1990 (ScienticentcCommittee-CCAMLR-XBG6) (ed Commission for theConservation of Antarctic Marine Living Resources(CCAMLR)) pp 335^360 Hobart Australia CCAMLR
Weimerskirch H Stahl J-C amp Jouventin P 1992 Thebreeding biology and population dynamics of king penguinsAptenodytespatagonica on the Crozet Islands Ibis 134 107^117
Wilson R P 1984 An improved stomach pump for penguinsand other sea birds J Field Ornithol 55 9^12
156 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
method for detection of food ingestion Our techniqueallows detection of ingestion of prey items as small asmyctophid centsh in relation to depth
(a) Implantation of oesophageal probesin free-ranging penguins
Four birds went to sea and showed normal foragingbehaviour as judged by dive depth and food brought tothe chick (Kooyman et al 1992 Charrassin et al 1998PIumltz et al 1998) Why two birds stayed at the colony isunclear However recent work (Y Le Maho unpublisheddata) suggests that the passage of the cables in the neckmay particularly disturb some individuals Accordinglyfuture work with data transmission to the logger unitrather than a cable connection may solve the issueHowever implantation of the sensor in the oesophaguseliminates the possibility of losing the logger by regurgita-tion as can occur for stomach sensors (this study Wilsonet al 1998)
(b) Relevance of oesophageal probe for detectingsmall prey ingestions
Since all experimental feedings gave a detectableresponse we conclude that our system is sensitive enoughfor small-sized prey items The low thermal inertia of thesmall sensor accounts for its good sensitivity (Ancel et al1997) Such a small size reduces the probability of contactwith prey but is counterbalanced by the small cross-sectional area of the oesophagus Prey items were lessoften detected with increasing distances from the beakand detection was almost impossible in the stomach ofcaptive penguins However prey detection in the stomachcould be less reliable in our captive individuals than infree-ranging birds since movements during diving maycontinually change the sensor position in the stomach(Wilson et al 1995) thereby favouring contact with preyProgression of food items is faster in the upper part of theoesophagus This lessens the time between prey ingestion
and prey^sensor contact and favours detection byreduced warming of the prey Prey ingestion is then easierto distinguish from physiological changes due to diving(Handrich et al 1997) if the probe is located in the upperoesophagus rather than deeper in the body (eg in thestomach) Based on the 06 cm siexcl1 displacement of preyitems in the upper oesophagus found in captive birds thedelay for reaching a sensor located 9 cm from the beak is15 s Such a short interval allows a quasi real-time detec-tion of food ingestion
(c) Detecting prey ingestion in free-ranging penguinsKing penguins feed on patchily distributed mesopelagic
centsh (Adams amp Klages 1987 Cherel amp Ridoux 1992Olsson amp North 1997) Oesophageal temperaturesrecorded in free-ranging birds showed large variations( 413 8C) that indicated feeding events and feedingdepths when combined with dive procentles The typicalfast short and precipitous temperature drops clearly indi-cate prey ingestions as opposed to the slow temperaturevariations corresponding to the tissue cooling due tophysiological responses to diving (Handrich et al 1997)Furthermore these prey ingestions were concentrmed as therapid temperature drops mainly occurred during deepdives (exclusively performed during daylight by kingpenguins see centgure 4 Kooyman et al 1992 Charrassinet al 1998 PIumltz et al 1998) which correspond to thedepths where myctophids concentrate during the day(Zaselrsquosliy et al 1985 Duhamel 1998)
Based on a penguinrsquos average vertical velocity duringdiving of 13 m s71 (PIumltz et al 1998) and with an ingestion^detection delay of 15 s the accuracy of depth where inges-tion occurs is ca 20 m ie 10 of the dive depth if thebird reaches 200 m Being validated with concurrentapplication of a classical technique such as hydroacousticprey survey or net trawl this method may provide aunique means to assess the prey distribution over depthFor instance one of the three birds fed mainly at 80^170 m where it probably encountered dense prey patchesUsing average prey mass of king penguins (74 and 17 g
Prey ingestion inpenguins J-B Charrassin and others 155
Proc R Soc Lond B (2001)
9
6
3
0
12
temperature drop duration (s)
tem
pera
ture
dro
p (deg
C)
0 50 100 150
non-feedingevents
feedingevents
dives gt 30 mdives pound 30 m
200
Figure 6 Relationships between amplitude and duration oftemperature drops in the upper oesophagus recorded in aking penguin during shallow dives (430 m n ˆ 1951 drops)and deep dives ( 4 30 m n ˆ 2450 drops) The dashed lineindicates the rate of temperature decrease above whichtemperature drops were considered as repoundecting prey ingestion(006 8C s71 see frac12 3) The period covered six foraging days
1020
08
04
06
02
00
30
depth of temperature drop (m)
rate
of
tem
pera
ture
dec
reas
e (deg
C s
- 1)
0 50 100 150 200 250 300
Figure 7 Depths at which temperature drops of the upperoesophagus occurred in a king penguin foraging for 75 days(n ˆ 6209 drops 5002 8C) Considering that a rate oftemperature decrease 5006 8C s71 (dashed line) indicatesfeeding most prey ingestion occurred at depths from about80 to 170 m
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
for the two main prey species in proportions of 75 and15 of the diet respectively Cherel amp Ridoux 1992) thedaily mass of centsh ingested by birds 1 and 2 was ca 16 kgand was 06 kg for bird 3 These values are comparablewith those ranges found in studies based on energetics(Kooyman et al 1992) and argue for the reliability of ourmethod
In conclusion measurement of oesophageal tempera-ture appears to be a promising tool for detecting preyingestion by marine predators Beside new information onthe feeding ecology of these predators an interestingperspective is their use to infer the prey distribution atdepth in particular for small schooling centsh dicurrencult todetect by conventional methods but which are keymarine resources in the Southern Ocean
The National Institute for Polar Research (Japan) the InstitutFrancdeg ais pour la Recherche et la Technologie Polaires and theTerres Australes et Antarctiques Francdeg aises provided centnancialand logistical support for this work The Centre National de laRecherche Scienticentque (GDRE no 1069 and PICS no 347) alsohelped in the funding We are indebted to the Penguin Fund(Tokyo Japan) for providing J-BC with a grant We thankC Marchand for help with surgeryY Clerquin and G Froget forcenteldwork assistance and members of the 33rd and 34th Missionsat Crozet Islands for a generous welcome The Little LeonardoCo (Tokyo Japan) is thanked for their ecurrencient cooperation andJ Lage (Jensen Software System) is acknowledged for writingcustomized software for data analysisWe are also very grateful toKnut Schmidt-Nielsen and to anonymous reviewers whosenumerous suggestions greatly improved our paper
REFERENCES
Adams N J amp Klages N T 1987 Seasonal variation in the dietof the king penguin (Aptenodytes patagonicus) at sub-AntarcticMarion Island J Zool 212 303^324
Ancel A Horning M amp Kooyman G L 1997 Prey ingestionrevealed by oesophagus and stomach temperature recordingsin cormorants J Exp Biol 200 149^154
Bevan R M Boyd I L Butler P J Reid K Woakes A Jamp Croxall J P 1997 Heart rates and abdominal temperaturesof free-ranging South Georgian shags Phalacrocorax georgianusJ Exp Biol 200 661^675
Bost C-A Georges J-Y Guinet C Cherel Y PIumltz KCharrassin J-B Handrich Y Zorn T Lage J amp LeMaho Y 1997 Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozetarchipelago Mar Ecol Prog Ser 150 21^33
Charrassin J-B Bost C-A PIumltz K Lage J Dahier TZornT amp Le MahoY 1998 Foraging strategies of incubatingand brooding king penguins Aptenodytes patagonicus Oecologia114 194^201
Cherel Y amp Ridoux V 1992 Prey species and nutritive value offood fed during summer to king penguin Aptenodytes patagonicachicks at Possession Island Crozet Archipelago Ibis 134 118^127
Croxall J P 1992 Southern Ocean environmental changeseiexclect on sea bird seal and whale populations Phil Trans RSoc Lond B 338 319^328
Croxall J P McCann T S Prince P A amp Rothery P 1988Reproductive performance of sea birds and seals at SouthGeorgia and Signy Island South Orkney Islands 1976^1987implications for Southern Ocean monitoring studies InAntarctic Ocean and resources variability (ed D Sahrhage)pp 261^285 Berlin and Heidelberg Germany Springer
Culik B M PIumltz K Wilson R P Bost C-A Le Maho Yamp Verselin J L 1996 Core temperature variability in divingking penguins (Aptenodytes patagonica) a preliminary analysisPolar Biol 16 371^378
Davis R W Fuiman L A Williams T M Collier S OHagey W P Kanatous S B Kohin S amp Horning M 1999Hunting behavior of a marine mammal beneath the Antarcticfast ice Science 283 993^996
Duhamel G 1998 The pelagic centsh community of the PolarFrontal Zone oiexcl the Kerguelen Islands In Fishes of AntarcticaA biological overview (ed G di Prisco E Pisano amp E Clarke)pp 63^74 Milan Italy Springer
Furness R W 1982 Competition between centsheries and seabirdsrsquo communities Adv Mar Biol 20 225^307
Gremillet D J H amp Plolaquo s A L 1994 The use of stomachtemperature records for the calculation of daily food intake incormorants J Exp Biol 189 105^115
Gremillet D J H Tuschy I amp Kierspel M 1998 Bodytemperature and insulation in diving great cormorants andEuropean shags Funct Ecol 12 386^394
Guinet C Chastel O Koudil M Durbec J-P amp JouventinP 1998 Eiexclect of warm sea-surface temperature anomalies onthe blue petrel at the Kerguelen Islands Proc R Soc LondB 265 1001^1006
Handrich Y Bevan R M Charrassin J-B Butler P JPIumltz K Woakes A J Lage J amp Le Maho Y 1997Hypothermia in foraging king penguins Nature 388 64^67
Huntley M E Lopez M D G amp Karl D M 1991 Top preda-tors in the Southern Ocean a major leak in the biologicalcarbon pump Science 253 64^66
Jouventin P amp Weimerskirch H 1990 Satellite tracking ofwandering albatrosses Nature 343 746^748
Kato A Naito Y Watanuki Y amp Shaughnessy P D 1996Diving pattern and stomach temperatures of foraging kingcormorants at subantarctic Macquarie Island Condor 98844^848
Kooyman G L Cherel Y Le Maho Y Croxall J PThorson P H Ridoux V amp Kooyman C A 1992 Divingbehavior and energetics during foraging cycles in kingpenguins Ecol Monogr 62 143^163
MontevecchiW A 1993 Birds as indicators of change in marineprey stocks In Birds as monitors of environmental change (edR W Furness amp J J D Greenwood) pp 217^266 LondonChapman amp Hall
Olsson O amp North A W 1997 Diet of the king penguinAptenodytes patagonicus during three summers at SouthGeorgia Ibis 139 504^512
Pakhomov E A Perissinotto R amp McQuaid C D 1996 Preycomposition and daily rations of myctophid centshes in theSouthern Ocean Mar Ecol Prog Ser 134 1^14
Peters G Wilson R P Scolaro J A Laurenti S Upton Jamp Galleli H 1998 The diving behavior of Magellanicpenguins at Punta Norte Peninsula Valdes Argentina ColonWaterbird 21 1^10
PIumltz K Wilson R P Charrassin J-B Raclot T Lage JLe MahoY Kierspel M A M Culik B M amp Adelung D1998 Foraging strategyof kingpenguins (Aptenodytes patagonicus)during summer at the Crozet Islands Ecology 79 1905^1921
Sabourenkov E N 1991 Myctophids in the diet of Antarcticpredators In Selected scienticentc papers 1990 (ScienticentcCommittee-CCAMLR-XBG6) (ed Commission for theConservation of Antarctic Marine Living Resources(CCAMLR)) pp 335^360 Hobart Australia CCAMLR
Weimerskirch H Stahl J-C amp Jouventin P 1992 Thebreeding biology and population dynamics of king penguinsAptenodytespatagonica on the Crozet Islands Ibis 134 107^117
Wilson R P 1984 An improved stomach pump for penguinsand other sea birds J Field Ornithol 55 9^12
156 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
for the two main prey species in proportions of 75 and15 of the diet respectively Cherel amp Ridoux 1992) thedaily mass of centsh ingested by birds 1 and 2 was ca 16 kgand was 06 kg for bird 3 These values are comparablewith those ranges found in studies based on energetics(Kooyman et al 1992) and argue for the reliability of ourmethod
In conclusion measurement of oesophageal tempera-ture appears to be a promising tool for detecting preyingestion by marine predators Beside new information onthe feeding ecology of these predators an interestingperspective is their use to infer the prey distribution atdepth in particular for small schooling centsh dicurrencult todetect by conventional methods but which are keymarine resources in the Southern Ocean
The National Institute for Polar Research (Japan) the InstitutFrancdeg ais pour la Recherche et la Technologie Polaires and theTerres Australes et Antarctiques Francdeg aises provided centnancialand logistical support for this work The Centre National de laRecherche Scienticentque (GDRE no 1069 and PICS no 347) alsohelped in the funding We are indebted to the Penguin Fund(Tokyo Japan) for providing J-BC with a grant We thankC Marchand for help with surgeryY Clerquin and G Froget forcenteldwork assistance and members of the 33rd and 34th Missionsat Crozet Islands for a generous welcome The Little LeonardoCo (Tokyo Japan) is thanked for their ecurrencient cooperation andJ Lage (Jensen Software System) is acknowledged for writingcustomized software for data analysisWe are also very grateful toKnut Schmidt-Nielsen and to anonymous reviewers whosenumerous suggestions greatly improved our paper
REFERENCES
Adams N J amp Klages N T 1987 Seasonal variation in the dietof the king penguin (Aptenodytes patagonicus) at sub-AntarcticMarion Island J Zool 212 303^324
Ancel A Horning M amp Kooyman G L 1997 Prey ingestionrevealed by oesophagus and stomach temperature recordingsin cormorants J Exp Biol 200 149^154
Bevan R M Boyd I L Butler P J Reid K Woakes A Jamp Croxall J P 1997 Heart rates and abdominal temperaturesof free-ranging South Georgian shags Phalacrocorax georgianusJ Exp Biol 200 661^675
Bost C-A Georges J-Y Guinet C Cherel Y PIumltz KCharrassin J-B Handrich Y Zorn T Lage J amp LeMaho Y 1997 Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozetarchipelago Mar Ecol Prog Ser 150 21^33
Charrassin J-B Bost C-A PIumltz K Lage J Dahier TZornT amp Le MahoY 1998 Foraging strategies of incubatingand brooding king penguins Aptenodytes patagonicus Oecologia114 194^201
Cherel Y amp Ridoux V 1992 Prey species and nutritive value offood fed during summer to king penguin Aptenodytes patagonicachicks at Possession Island Crozet Archipelago Ibis 134 118^127
Croxall J P 1992 Southern Ocean environmental changeseiexclect on sea bird seal and whale populations Phil Trans RSoc Lond B 338 319^328
Croxall J P McCann T S Prince P A amp Rothery P 1988Reproductive performance of sea birds and seals at SouthGeorgia and Signy Island South Orkney Islands 1976^1987implications for Southern Ocean monitoring studies InAntarctic Ocean and resources variability (ed D Sahrhage)pp 261^285 Berlin and Heidelberg Germany Springer
Culik B M PIumltz K Wilson R P Bost C-A Le Maho Yamp Verselin J L 1996 Core temperature variability in divingking penguins (Aptenodytes patagonica) a preliminary analysisPolar Biol 16 371^378
Davis R W Fuiman L A Williams T M Collier S OHagey W P Kanatous S B Kohin S amp Horning M 1999Hunting behavior of a marine mammal beneath the Antarcticfast ice Science 283 993^996
Duhamel G 1998 The pelagic centsh community of the PolarFrontal Zone oiexcl the Kerguelen Islands In Fishes of AntarcticaA biological overview (ed G di Prisco E Pisano amp E Clarke)pp 63^74 Milan Italy Springer
Furness R W 1982 Competition between centsheries and seabirdsrsquo communities Adv Mar Biol 20 225^307
Gremillet D J H amp Plolaquo s A L 1994 The use of stomachtemperature records for the calculation of daily food intake incormorants J Exp Biol 189 105^115
Gremillet D J H Tuschy I amp Kierspel M 1998 Bodytemperature and insulation in diving great cormorants andEuropean shags Funct Ecol 12 386^394
Guinet C Chastel O Koudil M Durbec J-P amp JouventinP 1998 Eiexclect of warm sea-surface temperature anomalies onthe blue petrel at the Kerguelen Islands Proc R Soc LondB 265 1001^1006
Handrich Y Bevan R M Charrassin J-B Butler P JPIumltz K Woakes A J Lage J amp Le Maho Y 1997Hypothermia in foraging king penguins Nature 388 64^67
Huntley M E Lopez M D G amp Karl D M 1991 Top preda-tors in the Southern Ocean a major leak in the biologicalcarbon pump Science 253 64^66
Jouventin P amp Weimerskirch H 1990 Satellite tracking ofwandering albatrosses Nature 343 746^748
Kato A Naito Y Watanuki Y amp Shaughnessy P D 1996Diving pattern and stomach temperatures of foraging kingcormorants at subantarctic Macquarie Island Condor 98844^848
Kooyman G L Cherel Y Le Maho Y Croxall J PThorson P H Ridoux V amp Kooyman C A 1992 Divingbehavior and energetics during foraging cycles in kingpenguins Ecol Monogr 62 143^163
MontevecchiW A 1993 Birds as indicators of change in marineprey stocks In Birds as monitors of environmental change (edR W Furness amp J J D Greenwood) pp 217^266 LondonChapman amp Hall
Olsson O amp North A W 1997 Diet of the king penguinAptenodytes patagonicus during three summers at SouthGeorgia Ibis 139 504^512
Pakhomov E A Perissinotto R amp McQuaid C D 1996 Preycomposition and daily rations of myctophid centshes in theSouthern Ocean Mar Ecol Prog Ser 134 1^14
Peters G Wilson R P Scolaro J A Laurenti S Upton Jamp Galleli H 1998 The diving behavior of Magellanicpenguins at Punta Norte Peninsula Valdes Argentina ColonWaterbird 21 1^10
PIumltz K Wilson R P Charrassin J-B Raclot T Lage JLe MahoY Kierspel M A M Culik B M amp Adelung D1998 Foraging strategyof kingpenguins (Aptenodytes patagonicus)during summer at the Crozet Islands Ecology 79 1905^1921
Sabourenkov E N 1991 Myctophids in the diet of Antarcticpredators In Selected scienticentc papers 1990 (ScienticentcCommittee-CCAMLR-XBG6) (ed Commission for theConservation of Antarctic Marine Living Resources(CCAMLR)) pp 335^360 Hobart Australia CCAMLR
Weimerskirch H Stahl J-C amp Jouventin P 1992 Thebreeding biology and population dynamics of king penguinsAptenodytespatagonica on the Crozet Islands Ibis 134 107^117
Wilson R P 1984 An improved stomach pump for penguinsand other sea birds J Field Ornithol 55 9^12
156 J-B Charrassin and others Prey ingestion inpenguins
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
Wilson R P amp Gremillet D 1996 Body temperatures of free-living African penguins (Spheniscus demersus) and bankcormorants(Phalacrocoraxneglectus) J Exp Biol 199 2215^2223
Wilson R P Cooper J amp Plolaquo tz J 1992 Can we determinewhen marine endotherms feed A case study with sea birdsJ Exp Biol 167 267^275
Wilson R P PIumltz K Gremillet D Culik B M Kierspel MRegel J Bost C-A Lage J amp Cooper J 1995 Reliabilityof stomach temperature changes in determining feeding char-acteristics of sea birds J Exp Biol 198 1115^1135
Wilson R P Peters G Regel J Gremillet D PIumltz KKierspel M Weimerskirch H amp Cooper J 1998 Shortretention times of stomach temperature loggers in free-living
sea birds is there hope in the spring Mar Biol 130 559^566
Woehler E J 1995 Consumption of Southern Ocean marineresources by penguins In The penguins ecology and management(ed P Dann I Norman amp P Reilly) pp 267^291 ChippingNorton Australia Surrey Beatty and Sons
ZaselrsquosliyV S Kudrin B D PoletayevV A amp Chechenin S C1985 Some features of the biology of Electona carlsbergi(Taning) (Myctophidae) in the Atlantic sector of theAntarctic J Ichthyol 25 163^166
As this paper exceeds the maximum length normally permittedthe authors have agreed to contribute to production costs
Prey ingestion inpenguins J-B Charrassin and others 157
Proc R Soc Lond B (2001)
on October 14 2011rspbroyalsocietypublishingorgDownloaded from
