TTrroopphhiicc EEcocolologgyy ooff FFoouurr AAppeexx PPrrededaattoorrss ooff tthhee PPelaelaggicic EEcocossyysstteemm iinn tthhee IInnddiaiann OOceaceann

LLaanncceett ffiisshh,, YeYelllloowwffiinn ttununaa,, BBiiggeeyyee ttununaa && SSwwoorrddffiisshh

Michel Potier 1, Francis Marsac 2,, Vincent Lucas 3, Richardd SSaabbaattiiéé 4,, Oliviieerr MMaauurryy 1 ,, JJeeaann--PPiieerrrree HHaalllliieerr 1 ,, Yves Chérel 5 & Frédéric Ménard 1

1 IRD,, Reunion Island 2 IRD,, Sète,, France 3 Seychelles Fishing Authority, Seychelles 4 ENSA,, Rennes,, France 5 CNRS-CEBC, Chizé, France  «« WhoWho eeaattss wwho ho ?? »» iiss aa rreelleevant aapprpproaoach to uunderstand tthhee cchaharraacctteerriissttiiccss ofof aann eeccososyysstteemm aandnd hhowow thethe ddiiffefferreentnt fufuncncttiioonanall ggrrououpsps iintnteerraacctt

No food, No future …. GGooaalsls Yellowfin (Thunnus albacares)  CComompaparree tthehe ddiieett ofof foufourr mmaajjoorr prpreeddaattoorrss  StStuuddyy tthehe ddeeggrreeee ofof ovoveerrllaap-p- pipinngg ofof fefeeeddiingng rreeggiimmeess aammonongg prpreeddaattoorrss  EEssttiimmaattee tthhee ssiizeze rraatitiosos bebettwweeeenn prpreeddaattoorrss && prpreeyy  Lancetfish (Alepisaurus ferox) IIntntrroodduuccee aa ssttaablblee iissoottopeope peperrsspepeccttiivvee

Swordfish (Xiphias gladius) Bigeye (Thunnus obesus) VVeerrttiiccaall DiDissttrriibbuuttiioonn :: wwhheerree ddoo ththeeyy lliiveve ??

What we know from ultrasonic tagging  Thee 44 pprereddators occccuuppy 0 5 10 15 2%0 0 different depth ranges :

200  Yellowfin : 0 - 200 m  Bigeye tuna : 0 – 500 m

) 400  Swordfish : 0 – 700 m m ( h t  Lancet fish : ?? p

De 600

800

1000 10 Status May 2004 5

0

-5

-10

-15

-20

-25

-30 (20) 30 35 40 45 50 55 60 65 T7ra0ine

Palangre (497) Senne (518) SSttuuddyy aarreeaa Number of stomachs collected > 1100 SSuurrvveeyy iimmpplleemmeennttaattiioonn

1199 mmonontthshs ((AAuugg.. 0011//FeFeb.b. 0033)) 2 6677 LLLL sseetsts aandnd 1100 PPSS sseetsts

0 11 ococeeaanognogrraaphphiicc ccrruuiissee RR//VV

-2  4747 CCTTDD pprrooffiilleess ((TT && DDO)O) -4  1515 mmiidwdwaatteerr ttrrawawllss

-6

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC 2001 -8 2002 Trawls No of stomachs < 5 2003 collected by 5 - 15 Total 150 111 163 PS sets longline set > 15 -10 Lancet fish Yellowfin Bigeye Swordfish Total 46 48 50 52 54 56 58 60

non-empty stomachs 128 110 17 123 378 LL %(n ebmpt) y 8 13 41 16 Size range (cm) 15 - 170 32 - 161 33 - 168 51 - 192 non-empty stomachs 34 12 46 PS %(n ebmpt) y 0 0 Size range (cm) 40-150 40-100 TThhee eennvviirroonnmmeennttaall ccoonntteexxtt :: TTempempereraattuurree && DDOO pprrooffilileses aanndd ddepeptthh rraannggee ssaampmpledled bbyy tthhee lolonnggllininee ggeaearr

Temperature Dissolved oxygen Methods … 11-- DDiieettaarryy AAnnaallyyssiiss

A Weighing the stomach content

B Sorting in large categories Fish Molluscs Crustacea

The less abundant categories (ie. molluscs and crustacea) are weighed then the main category (ie. fish) is obtained by difference

C For each category

Accumulated food s o r t i n g Fresh Food

For each item Counting the remarkable organs Species identification, counting, measuring (otoliths, beaks, mandibles,,…) the remarkable organs or entire individuals.

Reconstituted weight of the diet Methods … 22-- PPrreeyy DoDommiinnaannccee IInnddiicceess

 MoModdiififieedd CCosostteelllloo ddiiaaggrraamm (Amundsen et al. 1996)

 IIndndeexx ofof RReellaattiivvee IImmporporttaancncee ((IIRRII)) ((PPiinnkaskas eett alal.. 11971971))

IRI A  (N A %  PA %) FA % Number N, Weight P, Occurrence F IRI  (N %  P %) F % MA ethA odsA … A 33-- SiSimmiillaarriittyy IInnddeexx

 MoMorriissiittaa && HHoorrnn IInnddeexx ofof ssiimmiillaarriittyy (Magurrranan 19881988))

S S : total no of prey in regime of both predators aN : total no of prey in diet of predator A 2ani  bni i1 bN : total no of prey in diet of predator B Cmh  an : no of individuals prey i in diet predator A (da  db)(aN  bN) i bni : no of individuals prey i in diet predator B da , db : quadratic ratios Feeding regimes are compared by pairs of predators Varies from 0 (distinct feeding regimes) to 1 (identical) Above 0.6, C is reflecting a significant overlap Methods … 44-- SSiizzee MMeeaassuurreemmeennttss

Fresh Items Morphometric Remainings relationships

Crustaceans Propod (pelagic crabs) Propod (pelagic crabs) Total length Telson length

Fish Standard length Otolith length Dentary length

Lower rostral length Lower rostral length Cephalopods (LRL) (LRL) Methods … 55-- StStaabbllee iissoottooppee rraattiiooss

12 Intermediate trophic levels Tuna samples 10 3- 4‰ ? Prey2 ) 8 Prey1 ‰ Zoo ? ( N

5 Phyto ?

1 6

 1‰ ?

4 POM 2 0 -26 -24 -22 -20 -18 -16 -14 13C (‰)

 Samples of main prey,, tunaa andd bbilillflfiisshheess ((wwhhititee mmuusscclele)),, sshhararkkss  POM and Phytoppllaannkton collected but not yet analysed  Sampling of filter feeders is underway ReRessuullttss

11 –– PPrreeyy cocompmpoossititioionn aanndd ddoominminaanncece ssttuuddiedied wwitithh tthhee IRIRII aanndd CoCossttelloello ddiaiaggrraamm  YYFTFT anandd BBEETT acacrroossss ggeeaarrss  44 pprreeddaattoorrss wwiitthh lloonngglliinnee oonnllyy CComompparariisonson 22 pprreedd.. ((YFYFTT//BEBETT)) acacrroossss gegeararss :: PPSS bbllaannkk bbararss//LLLL ccoolloorreedd bbararss

%IRI 0 20 40 60 80 100 % IRI 0 20 40 60 80 100

Natosquilla investigatoris Natosquilla investigatoris crustacea crab larvae Oplophorus typus

Charybdis edwardsi other Myctophids

Hyperiids Diretmoides parini

Odontodactylus scyllarus Cubiceps pauciradiatus

Scopelarchus analis Scombrids fish unknown fish Yellowfin Paralepis atlanticus Bigeye Cubiceps pauciradiatus LL = 44 p.i. unknown squids LL = 21 p.i. Paralepis atlanticus PS = 3 p.i. Ommastrephids PS = 2 p.i. Alepisaurus ferox octopods

Ommastrephids cephalop. Onychoteuthids

100 %IRI

80 Yellowfin Bigeye

60

40

20

0 longline purse seine longline purse seine  SSuurrffacacee ddwweelllliinngg ttuunnaa ((ooppeenn cciirrcclleess))  Dominance of Natossquiillllaa  Specialisation on Scombrids (YFT) and flying squids (BET)  DDeeeepp ddwweelllliinngg ttuunnaa ((bbllacackk cciirrcclleess))  YFT :: from generalized to specialisation (swim.crabs and crab larvae)  BET :: generalilized feedining behaviiour CCoommppaarriissoonn bbeettwweeeenn 44 pprreeddaattoorrss,, lloonngglliinnee ggeeaarr

100%

80% others squids

I 60% R

I fish

% 40% crustacea

20%

0% lancet fish yellowfin tuna bigeye tuna swordfish predators sp.

TThhee pprrooppoorrttiioonn ooff eeaacchh pprreeyy ggrroouupp ((iinn wweett mmaassss)) amamoonngg tthhee pprreedatdatoorrss iiss ccoonnssiisstteenntt wwiitthh tthhee ppaatttteerrnn dedeppiicctteedd bbyy tthhee IRI IIRIRI bbyy pprreeyy iitteemm aanndd pprreeddaattoorr

0 20 40 60 0 20 40 60 80

Charybdis edwardsi Oplophorus typus Natosquilla investigatoris Natosquilla investigatoris

Platyscelus ovoides Scopelarchus analis Phrosina sp. Paralepis atlantica Alepisaurus ferox crustacea Diaphus spp. bigeye tuna Omosudis lowei Cubiceps pauciradiatus Paralepis atlantica Lancet fish Diretmoides parini Fish larvae Onykia rancureli 154 prey Carinaria sp. 1868 prey Moroteuthis lonnberggii 18 families Alciopidae 41 families Sthenoteuthis oualaniensis fish

0 20 40 60 0 20 40 60

Crab larvae Acanthephyra sp. Charybdis edwardsi Natosquilla investigatoris

Phrosina sp. Cubiceps pauciradiatus

Odontodactylus scyllarus cephalop. Diretmoides parini Yellowfin tuna Other scombrids Und. Fish swordfish Cubiceps pauciradiatus Scopelarchus analis Diaphus spp. 4916 prey Sthenoteuthis oualaniensis Alepisaurus ferox 44 families Ornithoteuthis volatilis 818 prey Sthenoteuthis oualaniensis Moroteuthis lonnbergii 28 families Ornithoteuthis volatilis Ancistrocheirus lesueuri 7 cm 3 cm NNaattoossqquiuillllaa iinvenvessttiiggaattoorriiss CChaharryybbddiiss eeddwwaarrddssii (Stomatopod) (Portunidae) 10 Only documented in the Indian Ocean Demographic bursts in 1906, 1933, 1944,1967 A new episode underway since 1999 … 100 Feb-Mar 0 larvae 70 % May 2001 80 adults 60 4 cm Jul-Jan 50 7 cm Total length 60 -10 40 40 50 60 October 2001 40 30 20 20 10 Telson size 0 0 6 7 8 9 10 11 12 13 14 mm J F M A M J J A S O N D Swarming at the surface Swarming in the mixed layer ReRessuullttss

11 –– PrPreeyy ccoommppoossiittiioonn aanndd ddoomiminnaannccee ssttududiieedd wwiitthh tthhee IIRRII aanndd CCoosstteelllloo ddiiaaggrraamm

22 -- OOvvererlalapp ooff feefeeddiningg rregegiimmeses SSiimmiillarariittyy iinnddiicceess anandd cclluustesterr aannalalyysisiss

YFT LL BET LL YFT PS BET PS YFT LL 1 BET LL 0.07 1 YFT PS 0.01 0.07 1 BET PS 0.02 0.08 0.99 1

Lancet fish Yellowfin Bigeye Swordfish Lancet fish 1 Yellowfin 0.05 1 Bigeye 0.14 0.07 1 Swordfish 0.25 0.03 0.55 1

 SSiiggnniiffiiccanantt ooveverrllapap Cluster analysis based on IRIs Lancet fish wwiitthhiinn tthhee PSPS

Swordfish  VVaalluuees close to the ssiiggnniiffiiccanantt tthhrreesshhoolldd Big eye

bbeettwweeeenn bbiiggeeyyee anandd Yellowfin sswwoorrdfdfiisshh 3200 3400 3600 3800 4000 4200 ADggistraegncatei od'nA gr Déigatstanionce FFiisshh PPrreeyy DDiissttrriibbuuttiioonn

0 10 20 30 40 50 60

Fish larvae swordfish Acanthuridae 10% Epipelagics Balistidae Carangidae big eye s Carapidae 0% c i Coryphaenidae g Dactylopteridae a lancet fish l Diodontidae e Exocoetidae 48% p i Hemiramphidae yellowfin Holocentridae 42%

Ep Monacanthidae Ostraciidae Scombridae Scorpaenidae Tétraodontidae Alepisauridae Anoplogasteridae Mesopelagics Argentinidae

s Bramidae lancet fish

c Chiasmodontidae i swordfish 19% Diretmidae g 29% a Gempylidae l

e Myctophidae

p Nomeidae

o Omosudidae s Paralepididae yellowfin e Swordfish Phosichthyidae 21% M Scopelarchidae Lancet fish Sternopthychidae Bigeye Stromateidae Yellowfin big eye Trachichthyidae 31%  TThhee ddiiffefferreenncceess // ssiimmiillaarriittiieess bebettwweeeen the verticaall ddiissttrriibubuttiionon ooff pprreeddaatortorss aarree rreeflfleecctteedd iinn tthehe prpreeyy ccoommppososiititionon ::  yyeelllloowwffiinn/l/lanancceett ffiisshh wwiitthh aa dodommiinnanantt pprrooppoorrttiioonn ooff ccrruussttacaceeaannss :: eeppiippeellaaggiicc afafffiinniittiieess  BBiiggeeyyee/s/swwoorrdfdfiisshh wwiitthh mmeessooppeelagic fish dominating the diet

Ocean Area Fish Families Authors  Atlantic Gulf of Guinea 20 Borodulina (1974) FiFissh is the most Pacific Eastern Pacific 42 Alverson (1963) Eastern Pacific 18 Moteki et al. (2001) ddiivveerrssiififieedd ggrrououpp Central Pacific 38 Reintjes and king (1953) Central Pacific 48 King and Ikehara (1956) aammongong prpreeyy :: 2244 Western Pacific 37 Watanabe (1958) Western Pacific 30 Borodulina (1982) fafammiilliieess rreeporportetedd Western Pacific 13 Kim et al . (1997) Indian Western Indian 23 Kornilova (1980) iinn tthhee YYFFTT ddiieett Sri Lanka 44 Maldenya (1996) Seychelles 24 Present study ReRessuullttss

11 –– PrPreeyy ccoommppoossiittiioonn aanndd ddoomiminnaannccee ssttududiieedd wwiitthh tthhee IIRRII

22 -- OOveverrllaapp ooff ffeeeeddiinngg rreeggiimemess

33 -- SSizeize ssppececttrruumm ooff pprreyey PPrreeyy ssiizzeess :: ttrraawwllss vvss ssttoommaacchhss

70 % 60 50 Size spectra of fish preys 40 30 20 10 0 0 10 20 30 40 50 60 70 80 90 SL (cm)

trawl lancet fish swordfish big eye tuna yellowfin tuna 70 % 60 50 Size spectra of fish preys 40 30 20 10 0 0 10 20 30 40 50 60 70 80 90 SL (cm)

trawl lancet fish swordfish big eye tuna yellowfin tuna

 SwSwoorrddfifisshh aandnd bibiggeeyyee iinnggeesstt bibiggggeerr prpreeyy tthhaann ddoo yyeellllowowfifinn aandnd lancceettfifissh.  LLaancnceettfifisshh iiss aa rraatthheerr ssllowow sswwiimmmmeerr aandnd prpreey upopon ssmmaallll oorrggaaninissmmss ((aapaparrtt frfroomm iittss cconsonspepecciifificcss).).  SwSwoorrddfifisshh hhaass aa vveerryy eeffifficcient methodod of capture iinvnvololvviingng tthehe wwhihipppipingng aaccttiioonn ofof tthehe bibillll..  TThhee rreeaall ssiizeze sspepecctrtruumm ofof prpreeyy iinn thethe wwaatteerr ccoolluummnn iiss tthhee ovoveerraallll comombibinanatitionon ofof ttrraawwll ccolollleeccttiiononss aandnd pprreeddaatortor ssttomomaacchh ccontonteentntss.. PPrreeddaattoorr--pprereyy ssiizzee rraattiiooss

 CComommmonon ssiizeze rraattiiosos ffouounndd iinn FFiisshBhBaassee :: aarrououndnd 44 ((FrFroeoessee aanndd PaPauuly 1998)  IInn tthehe pprreesseentnt sstutuddyy,, ssiizeze rraattiiooss rraangngee frfromom 1100..33 ttoo 1111..88  TThheessee hhiigghh rraattiiosos ccaann bebe iintnteerrprpreetetedd aass aann optoptiimmaall fefeeeddiingng ssttrraatteeggyy :: pprreeyyiinngg uuponpon ddeensnsee sswwaarrmmss rreedduucceess tthhee eenenerrggeetiticc ccosostt ofof cchahassiingng  TThhee ddeensnseesstt prpreeyy ccooncnceennttrraattiioonsns iinn tthehe oopepenn oocceeaann aarree mmaaddee ofof ssmmaallll--ssiizezedd iindndiivviidduuaallss ReRessuullttss

11 –– PrPreeyy ccoommppoossiittiioonn aanndd ddoomiminnaannccee ssttududiieedd wwiitthh tthhee IIRRII

22 -- OOveverrllaapp ooff ffeeeeddiinngg rreeggiimmeess

33 –– SSiizzee aannaallyyssiiss

44 –– SSttaabblele IIssoottooppee rraattiiooss 10

N = 108 5 (Status Nov 2003)

0

-5

-10

-15

-20

-25

-30 30 35 40 45 50 55 60 65 70 EEffectffect ooff liplipidid rremoemovvaall oonn 13CC mmeaeassuurremenementtss wwhhititee mumussclecle ssaammpplleses p a t u d o / A M 3 - 1 4 p a t u d o / A M 4 - 5 P A T 9 l i s t a o / K E 1 - 1 5 a l b a c o r e / A M 4 - 5 A L B 3 a l b a c o r e / A M 3 - 2 e s p a d o n / A M 3 - 1 3 e s p a d o n / A M 4 - 6 E S P 7 p a t u d o / A M 1 - 2 p a t u d o / K E 1 - 3 0 l i s t a o / K E 1 - 0 0 5 a l b a c o r e / K E 1 - 1 3 a l b a c o r e / A M 3 - 1 e s p a d o n / A M 4 - 3 E S P 3 p a t u d o / G U 1 - 9 D l i s t a o / K E 1 - 0 2 4 l i s t a o / A M 2 - 5 L I S 1 2 a l b a c o r e / A M 1 - 4 e s p a d o n / A M 2 - 7 E S P 9 e s p a d o n / A M 4 - 1 E S P 1 2 p a t u d o / K E 1 - 1 7 l i s t a o / K E 1 - 8 l i s t a o / K E 1 - 0 0 3 a l b a c o r e / A M 1 - 1 e s p a d o n / A M 2 - 3 E S P 1 1 e s p a d o n / A M 2 - 1 E S P 4 p a t u d o / K E 1 - 0 1 1 l i s t a o / K E 1 - 0 1 0 l i s t a o / K E 1 - 0 0 9 a l b a c o r e / G U 1 - 1 2 e s p a d o n / A M 2 - 1 E S P 7 e s p a d o n / A M 5 - 1 3 p a t u d o / G U 1 - 1 0 D l i s t a o / K E 1 - 6 l i s t a o / G U 1 - 3 7 a l b a c o r e / G U 1 - 1 5 e s p a d o n / A M 3 - 1 0 e s p a d o n / A M 5 - 1 p a t u d o / A M 4 - 1 B E T 6 l i s t a o / K E 1 - 0 2 5 a l b a c o r e / K E 1 - 0 3 1 a l b a c o r e / G U 1 - 1 3 D e s p a d o n / A M 3 - 1 1 e s p a d o n / A M 5 - 1 0 0 1 0 2 0 3 0 4 0 % l i s t a o p a t u d o - 1 5

- 1 6

- 1 7

- 1 8

- 1 9

- 2 0

B a l b a c o r e e s p a d o n D P .

a - 1 5 t l e d - 1 6

- 1 7

- 1 8

- 1 9

- 2 0

0 1 0 2 0 3 0 4 0 % l i p i d s 16.00 TL Top predators YFT 14.00 3.5 BET ALLaEncet fish 12.00 3 Cubiceps ) VViinncciiguerria ‰

( 2.5

N 10.00 sMqauniltiless shrimp 5 1

ð 2 ZZooooplankton 8.00 Prey + lancetfish CSAiFlky shark 1.5 Enoploteuthidae 6.00 MBAlaNck marlin Zoo 1 VSOIailfish 4.00 -21.00 -20.00 -19.00 -18.00 -17.00 -16.00 -15.00 -14.00 ð13C (‰)

DPOM = 5.4 (litterature) TLconsumer = 1 + (Dconsumer – DPOM)/TL TL = 3.52 (estimated) SSuummmmaarryy

 SuSurrfafaccee ttuunnaass eexxplplooiitt aa vveerryy lliimmiitetedd nunummbbeerr ofof prpreeyy sspepecciieess :: sstrtroongng iinnflfluueennccee ofof tthhee mmaantntiiss sshrhriimmpp eepipissododee  TTwwoo fufuncnctitioonanall ggrrououpsps uuttiilliizizingng ddiiffefferreenntt pprreeyy ccoommmmuuninittiieess :: aadduulltt yyeellllowowfifinn && llaanncceettfifissh on one side, aadduulltt bbiiggeeyyee && sswwororddffiisshh onon tthhee ototheherr ssiiddee  TThhee optoptiimmaall fefeeeddiingng ssttrraatteeggyy,, tthehe hhiigghh pprreedd--prpreeyy ssiizeze rraattiiosos ccououlldd rreevveeaall sshohorrtt aandnd ssiimmppllee ffoodood cchhaaiinsns lleeaaddiingng ttoo aapepexx prpreeddaattororss iinn tthehe IIOO eeqquuaattororiiaall eeccososyysstetemm ((PhPhyyttopkopk –– ZZoopoopkk –– CCrruussttaacceeaann –– YYeellllowowfifin)n).. NNeeeeddss ccoonfinfirrmmaattiionon ffrromom tthhee iissotopeotopess.. NNeexxtt sstteeppss ……

 IImmpplleemmeennttatatiioonn ooff aa lloonngg-tteerrmm mmoonniittoorriinngg ooff kkeeyy dedessccrriippttoorrss ooff tthhee ttrroopphhiicc ppatathhwwaayyss :: ttrracackikinngg tthhee sshhiiffttss iinn mmaxaxiimmiizziinngg tthhee bbeenneeffiitt/c/coosstt rraattiioo ;;  DDeetteerrmmiinnee tthhee bbaasseelliinnee iissoottooppee ssiiggnnatatuurree ooff tthhee ecosystem ;  IInntteeggrraattiioonn ooff oobbsseerrvatvatiioonnss iinn aa ssppatatiialalllyy eexxpplliiccit and size structured ecosystem mmoodedell.. TThhee AAPPEECOCOSSMM ttrroophphododyynanamimicc ccompoomponenennttss

 Spatially explicit pelagic ecosystem (PE)

 Spatially explicit PE weight spectrum dynamics (by funct. Groups).

 Spatially explicit PE 15N weight spectrum

og) dynamics. (l

s N s 5 1 a  om bi

E P O O

Organisms weight (log)

 Predators sample the PE: their stomach content weight spectra (by main prey functional groups) and 15N dynamics are spatially explicit.

 The model parameters will be estimated using all the stomach content and isotope data collected