scl. MAR. 5~3-4).3-17-355 SCIENTIAMARINA 19c)i
Ontogenetic changes in mouth structures, foraging beha- viour and habitat use of Scomber japoniczis and Zllex coindetii*
JOSÉ J. CASTRO and VICENTE HERNÁNDEZ-GARC~A
1NTKOL)UCTlON rlie consiiniers. Tlie body morphology md yowt1-i. hnbitat, mi animal distribution are in some way Food is one of the most important limitations to i-elated to diet (WOOTTOS.1992). Trophic evolution animal growth (WEATHERLEYand GILL,1987). The necessarily produces a double specialization. which characteristics of availabie food, q~iality.size, anci is. on the one hand inechnnical (G.ALISrt irl. 1994). üccessibility will condition the trophic behwiour of in that it has to do with how tht: animal obtains. handles 2nd in~estsfood and. on the other liand, bio- .'Rccei~edApril 13. 199-1. Accepted March 1 i. 1993. cheinical (M.AR(~..\LEF.198 1). There are two L\,;I~sof originating an efficient feeding strategy; this is eit- MATERIAL AND METHODS her obtained via time of evolution, as a result of natural selectiun, or it can be leamed during the lile This study is based on 721 indiyiduals of cycle (HART, 1986). However, in the latter case, Scomber-japonicus caught around the island of Gran there must exist a previous construction (Le. mouth Canaria (14'00'N - 15'30'W) and 414 individuals structure) which allows for adequate exploitation of of Illex coindetii caught on the continental shelf off Nnrthu~~utAfrirn (frC)m !Ao! !'N 2nd the fmc! resources. Macy speries revea! rr.orphv!n- L 7" ...S,, -0% ' ....-L. 2g0n8'N). gical adaptations which are oriented to obtain food. Mackerels were sampled from commercial carches They not only show the corresponding morphologi- using purse-seine and beach seine nets between cal adaptations, but also their behavioural pattems March 1988 and May 1989. Shortfin squids werc are totally influenced by the food type upon which obtained from the by-catch of bottom trawls for they depend (EIBL-EIBESFELDT?1979; WOOTTON, prawn and octopus, between August 1989 and April 1992). This adaptation is the consequence of the 1990. continuous interactions between the bodgl beha- Morphometric measurements were made to vioural development processes and externa1 environ- determine whether ontopenetic changes occurred in ment (HUNTINGFORD,1986; GALISet al. 1994). the structures used for feeding. The total body length Examples of these interactions are represented in (TL), lower jaw length and degrec of mouth opening many taxa (invertebrates, fish, amphibians, reptiles, were measured for each fish (Fig. 1). The dorsal birds and mammals), where normally the juveniles mantle length (DML) was also taken for each short- and adults differ in their use of resources (WERKER fin squid and the rostral lengths of the upper and and GILLIAM.1984; WOOTTON,1992: O'BRIEN, lower beaks were also measured in 200 specimens !444). (Fig. 2). A!! meusuremen.ts were t2ken fo the nearest Feeding, or to be more precise, the availability 0.01 mm with a digital caliper. The stage of maturity and accessibility of food, are just some of the rca- and levcl of pigmcntation of beaks werc recorded sons for many aspects of individual and social fi-o111a subsample of 1 16 iridividuals oF l. c.oiiidrtii behaviour (GRANT.1993) together with the spatial (55 males and 61 females). distribution of the species (WOOTTON.1992; LIRMAN,1994). Shifts in diet are often associated with, or caused by, shifts in habitat (WERNERand G~LLIAM,1984). Seasonal fluctuations of food resources force many spccics to make significant displacements during specific periods of their life cycles (MCKEOWN,1984; WOOTTON,1992). A migration between two habitats with different eco- logical conditions requires previous physiological and morphological characteristics and a new stra- tegy of exploitation (MCKEOWN,1954). The juveni- le stages are niore vulnerable to differences in envi- ronmental conditions between habitats (temperatu- re, predation risk, food quality: HJORT,1914), due to limitations imposed upon them by the leve1 of body development, and most specifically the skull structures related to the mouth, and swimming capacity. These limitations will condition the trop- hic spectrum which will not be totally defined until the animal achieves the adequate body develop- ment. The stomachs of the fish and cephalopods were In this paper, we document the existence of onto- removed and preserved in 70% ethanol. Al1 food genetic shifts in the diet and habitat of Scomber items from the stomach were placed on filter paper japonicus (Pisces. Scombridae) and Illex coindetii to remove moisture and thereafter weighed. Prey (Cephalopoda, Ommastrephidae). These ontogene- iterns were identified to the lowest taxa possible. For tic shifts are related to prcvious morphological each stomach examined, counts were made of the variations in mouth structures. number of prey items in each prey category. An
348 J.J. CASTRO and V. HERNÁNDEZ-GARC~A UPPER BEAK LOWER BEAK
HOOD
index of importance by number (IN) for each sto- mach was calculated as the mean for each prey cate- gory, where IN= ((% composition by number)-(% occurrencej)- (WINDELL,197 1, VESINCI (11. 198 1) working on a m!e of !MI where % composition hy Orrly tlie ro\ti-un1 ;~ndllie iirrterior pnrt ot ilrz Iioud are 1>i~iriciitctl.1 number = number species, x IOO/totnl number of al1 Thc piginrritntion is only prerrit in thr rosiruni :irid \lio~ilder.2 prey; and the percentage occurrence is the frequency An isolated jpot 01' pipent is preseiit ir1 the wingc. 3 Tlir irritial pigineirtati«ri «f the wings is iii propns to the Iioocl. 4 of occurrence of a prey item in the stomach. Tlis iiritial pispeiir:itioii of tlie ~~iiigsib fini~ll- joiiie~l lo tlie Iiood.5 Thc ~ing\iirr coiiipletrlq pig11ieriti.d but ~~irrountlt.
attending the morphometric, biological, ecologicai and fishery characteristics of the specimens. lñree The linear regression analysis between the mouth size-classes were identified in Scomber japonicus. smctures and the body lengths (LT and DML)sho- The juvenile chub mackerel were defined as those wed that Scomber japonicus undergo significant fish ranging in size from 1.5 to 13.5 cm TL, immatu- morphometric shift (P< 0.05) at around 13 to 15 cm re fish as those ranging between 13.6 and 22.5 cm TL TL (Fig. 3), while in Illex coindetii this significant and adults as fish longer than 22.6 cm TL (CASTRO, morphometric shift is shown at around 14 to 20 cm 1993). These size-classes are similar to hose used by DML (Fig. 4). However, when I. coindetti was sepa- WATANABE(1970) and ANGELESCU(1979) for S. rate by sex, we observed that the morphomevic japonicus from Japanese and Argentinian waters res- changes was obtained around 15 cm in males and 20 pectively. Individuais of Illex coindetii srnaller than cm in females. This means that, at these sizes, an 12.5-15.5 cm DML (12.5 cm when male and 15.5 cm important change occurs in the rhythrn of the growth when female) were defined as juvenile-immature of mouth stnictures (lower jaw in chub mackerel and since it is considered that specimens are sexually upper beak in shorfin quid) of both species which is mature after reachiig these sizes (SANCHEZ,1982) in direct re1ation to body growth. (Fig. 5). In the same way, specirnens longer than Size-classes of both species were established 12.6-15.6 cm DML were identified as adults.
Fa. 5. - Three dimensional representation of darfrening degm of lower bcaks of Illex coindetii in nlation with mantle growth and maninty (55 males and 61 females).
JSo JJ. CASlRO and V. HERN~D~OARC~A TABLE 2. - The food laxa and dominant species found in the TABLE 3. - The food laxa and dominant species found in the stomach of Scomber japonicus. stomach of Illex coindetii.
1. CHAETOGNATHA 1. AMPHIPODA 2. POLYCHAETA 2. EUPHAUSIACEA 3. CLADOCERA Thysanopoda sp. 4. OSTRACODA 3 DECAPODA 5. COPEPODA Plesionika spp. Oncaea sp. Pasiphaea sivado 6. AMPHIPODA 4. CEPHALOPODA Dexamine sp. Sepia sp 7. ISOPODA Sepia beriheloti 1 digo gp. Alloteuthis sp. 9. MYSIDACEA Abralia veranyi Gastrosaccus normani Illex coindetii Anchialina agilis Todaropsis eblanae 10. STOMATOPODA Octopus sp. 1 1. EUPHAUSIACEA 5. PISCES Euphausia spp. Maarolicus muelleri 12. DECAPODA Diaphus dumerelli 13. GASTROPODA Epigonits telescopus 14. LAMELLIBRANCHIATA Denres spp. 15. CEPHALOPODA Diploclrrs spp. Ommasrreohes barrrumi Microchirus hoscanion 16. APPEND~CULARIA Solea spp. 17. PISCES Sardina pilchardus Macroramphosus sco1opa.r bution of fish in the diet of immature chub mackerel was not significant (2.05%). Mysids, copepods and The diet of chub mackerel in the area of the fish were the most important prey in the diet of adult Canary Islands was made up of 17 taxonomic groups chub mackerel (27.496, 18.0% and 13.2% respecti- (Table 2). Copepods and mysids were the dominant vely) (Fig. 6). prey (27.0% and 24.5% respectively). Fish were less The differences between the diets of juvenile, frequent in the diet but their importance in the mass immature and adult chub mackerel are to be seen in the was moderately high. The diet of juveniles was shift from small fish and copepod prey to mysids and dominated by fish fry (24.7%) and small prey such copepods in fish lengths over 13.5 cm TL, and thereaf- as copepods and appendicularians. Copepods and ter to mysids and fish for adults over 22.5 cm TL. appendicularians were the main component of the The trophic spectrum of Illex coindetii was made diet (26.6% and 17.5% respectively) decreasing in up of 5 taxonomic groups (Table 3). The diet of importance proportionate to fish size. Immature spe- juvenile-immature of I. coindetii was mainly fish cimens presented a diet based on copepods and (45.09%) and cephalopods (20.19%), and in a lower mysids (32.9% and 20.9% respectively). The contn- proportion decapods (2 1.1 O%), euphausiids
Firh 132
Firh 2 05 Mysidr 27.4
JUVENILES IMMATURES AD ULTS
FIG.6. - Proportion of most imporiant prey items in the diet of juvenile, immature and adult Scomber japonicus.
O-NTwENETiC CHANGES iN- JAPüNic"S AND [, cüiNoEi,i 351 be competitive in the new ecological conditions. IVANOVIC,1992; ARKHIPKINand LAPTIKHOVSKY, Possibly, these morphological shifts are not totally 1994) where these crustaceans are abundant at night apparent in al1 species (GROSSMAX,1980). Perhaps (RUBIES,1976; LAPTIKIIOVSKY,1989). ln the first the species which do not need to migrate (BAS and stage and before reaching sexual maturity, shortfin MORENO,1993) do not undergo significant shifts in squids undergo suitable morphological transforma- their prey size (WERNERand GILLIAM,1984). These tion which will allow them to make significant ver- shifts are recorded in the genetic codes (with a per- tical displacements during the night-day (ARKHIPKIN manence in time which is far superior to the envi- and LAPTIKHOVSKY,1994), and even possible longi- ronmental changes which the individual suffers tudinal spawning migration as reported in Ille.~ille- during its life cycle). In the case of fluctuating envi- cchi-OSIIS(O'DOR, 1987). This morphological shift ronmental conditions in the nursery habitat (vital iinplies an adaptatioii to fast swimrning (significant space, inter and intraspecific competition and pre- increase in the mantle cavity and perfection of fin datory risk and specially available food), the species structures) (ARKHIPKINand FEDL'LOV,1986). At the search out two possible answers: a higher degree of sanle time, their ~nouthstructures (beaks) become specialization (BERGMANand GREENBERG,1994) or hürder and the animal adapts to catching faster prey migration to other more profitable areas and escaping quickly, apart from which they have (MCKEOWN,1984). Two examples of these ontoge- enough strength to break up hard fish structures. On netic behavioural changes in the niarine species are the othei- hand. adults prey on other cephalopod spe- Sconlbel- jlrponicus and Il1e.r coindetii. species cies and fish. especially fishes of the genus which migrate (daily and/or seasonally) during their Mic~wcliiixs,that are abundant in the stomach con- life history, and most especially in the adult stages tents of adult shortfin squids. This fish inhabits sand (SCHAEFER,!980: D.AW 2nd RECK. !985; or mddy-sand hnrtnms (F!SCHE~ B!, !98!!. This ARKHIPKINand FEDLLOV,1986; BRUNETTIand means that adults of l. coindetii are associated with IVANOVIC,1992). the sea bottom during the day time, as reported by Juveniles of chub mackerel live in coastal waters ROPERand SWEENEY(1981) and MANGOLD(1983). feeding on small crustaceans (especially copepods) The major presence of benthic amphipods in the diet although their voracity and mouth structures allow of adults corroborate this major dependence with the them to prey on other fish species (HUNTERand sea bottoin. Adults make significant vertical displa- KIMBRELL,1980; CASTRO,1993). This stage of cements in the water column at night where they growth is particularly rapid and is to be noted, above feed on rnyctophids (OVCHAROVet crl, 1985; all, in the head growth (LORENZO,1992). The coas- CIIESALIN,1987) and other pelngic cephalopods. tal area of the Canary Islands is an unstable environ- The possibilitq exists that I. cviidptii migate to hig- ment with a limited carrying capacity and is strongly her latitudes coinciding with spawning as uas obser- influenced by seasonal cycles (BAS and MORENO, ved in l. illei,ch~musin the Northwest Atlantic 1993). The important concentration of juveniles of (O'DOR,1987) which spawn directly on the sea bot- many fish species found during the first half of the tom. year in the coastal ecosystem produces a critica1 The ontogenetic shifts experienced by animals situation in the carrying capacity. At the end of this are important for guaranteeing the survival of the period, juveniles of chub mackerel have reached 14 species under changing environmental conditions. cm TL and are ready to migrate offshore and to show Corporal development shaped according to the gene- efficient predation on the mysids which swarm tic code of the species and expressed in phenotypic during the night (individuals of 14 cm TL were not characteristics allows the animal to face the basic foiind in catches, probably due to this migration conditions of its environnient. However. the nnato- offshore). Subsequently, when fish are sexually mical structure as described by the genes reveals maturc, thcy migratc again, once ycarly and coinci- vcry Iittlc flexibility and would not facilitatc (per se) ding wiíh spawning, between the feeding area of [he survival of individuals in a situation oS environ- adults and the spawning area (BAIRD,1977: C.~TRO, mental fluctuation. This genetic rigidity is compen- 1993). sated by the ontogenetic shift in behaviour as a com- Immature specimens of Illes coijidetii manifest a plex response to these environmental tluctuations. higher proportion of euphausiids in the diet than However, as explained by H~JNT~NGF~RD(1986) a adults, which would tend to suggest a major rela- specific behavioural pattem will only become mani- tionship with the pelagic domain (DAWEand BECK, fest uhen the anatomical structure required for its 1985; ARKH~PKINand FEDELOV, 1986; BRUNETTIand developenit is alreacly presenl.
ONTOGENETIC CHAUGES lrj 7 J.1POiLICCS AWD 1 COILDETII 353 HCNTER.J.R. and C.A. KIMBRELL.- 1980. Earlq. life history of ACKNOWLEDGEMENTS Pacific mackerel, Sconiher jal~onic~r~.~.Fisti. Birll., U.S.. 78:89- 101. HCNTISGFORD.F..4. - 1986. Development of behaviour in fishes. In: We are deeply grateful to Dr. Bas, Dr. A. Santanri T.J. Pitcher (ed.). Tlie hrhui,iour o!' teleo~rfishes. The John de! ?izo ar?Y Mrs. Margaret Hart, for their helpf~ll Hopkins University Press. Baltirnore, Ma~land.p. 47-68. HYSLOP,EJ. - 1980. Stomach content analysis - a review of met- suggestions. Thanks are also to be given to the crews hods and their application. J. Fish Biol.. 17(4):41 1-431. of the fishing vessels "Juan Carlos", "Islanza" and IVLEL,V. - 1961. E.rperinirntn1 ecolog? of rlie fec,ilin,q offislies. Yale University Press. New Haven. pp. 302. "Isla de Lanzarote". This work was supported by the KEAST,A. - 1977. Mechanisrns expanding niche uidth and rninimi- Agriculture and Fisheries Council of the zing itraspecific competition in two centrarchid fishes. In: M. Hecht er al. (ed), Ei,oli&)t~crr~Biolug~. Vol. 10. Plenum Press. Autonomous Govemment of the Canary Islands. New York, p 333-395. LAPTIKHOVSKY,V.V. - 1989. Twenty-four hours vertical rnigrations of the arrow-squid Todni-odes utigolensis Adani (Cephalopoda. Ommastrephidae) in Namibia Waters. 0kcunolo::iyi. 29W: REFERENCES 836-837. LIR.MAN,D. - 1994. Ontogenetic shifts in habita1 preferentes in the three-spot damselfish, Sre,qu.stc.s pluii~rons(Cuvier), in Roatnn ANGELESCU,V. - 1979. Trophic ecology of the mackerel of the Island, Honduras. J. E.\-p. Mar. Biol. Ecol. 180: 7 1-8 1. Argentine Continental Shelf (Scombridae, Sconiher juponicir.~ LORENZC).J.M. - 1992. Crecimiento de la caballa Sc.onihei-]cil~oiri- niurplarrnsis). Part. 1 Feeding and Growth. Rri,isto il(, c,iis (Houttuyn. 1782) en aguas de Canarias. Tesis. Univ. de La Ini~rsrigacióiiy Desurrollo Pesqicrro. I(1): 6-44. Palmas de Gran Canaria. ARKHIPKIN,A.I. and P.P. FEDLLOV.- 1986. Diel movements of MARGALEF,R. - 198 1. Ecologíu. Ed. Omega. Barcelona, 95 I pp. juvenile lllex illecehro.sirs and other cephalopods in the shelf M.\~GOI.D,K. - 1983. Food, feeding and growth in cephalopods. water-slope water frontal zone off the Scotian Slielf in spring. Men1oii.s of rhc Narioriul Mirsrirni Vic.toi.iii,44: 8 1-93. J. Nortli~,.Atl. Fish. Sci., 7: 15-24. M.-\NN,K.H. - 1982. Ecology of'cnirsral ~w/er.s.A systeni uppi.onc~11. ARKHIPKIN,A. and V. LAPTIKHOVSKY.- 1994. Seasonal and inte- University of California Press. Berkeley and Los Angeles. rannual variability in growth and maturation of winter-spaw- MANNISG,A. and M.S. DAWKI\;S.- 1992. AII ii~ri~oilircrioiiro uirimul ning Ille.~ar~~entinrrs (Cephalopoda, Ommastrephidae) in the belioi~ioirr (4th editioii). Cambridse University Press. New Southwest Atlantic. Ayirar. LiiGrig Resoiii,., 7: 22 1-233. York. BAIRD,D. - 1977. Age, growth and aspects of reproductioii of the MARTIN-ANDRES,A imd J.D. LLSA DEL CASTILLO.- 1990. mackerel, Sconlher joporricrrs, in the South African waters Bioestirtlí,stica pcii.rr c.ieiiciu.s ilc /ir snlird. Ediciones Noima. (Pizces, Scombridae). Zool. /l...12: 347-362. Madrid.
BAS, C. - 1964. Aspectos del creciiniento relativo en peces del MCKEOMI~,B.A. - 1984. Fish nii,yrirrioii.Timber Preas, Portland. Mediterraneo Occidental. liri,. Pesil., 27: 13-1 19. MI~ELII~\CI~.:.C.. C.W. OSENBEKGand M.A. LEIBOLD.- 1988. BAS. C. and T. MORENO.- 1993. Influences of the coastal environ- Trophic relatioii\ and ontogenetic niche shifts in aquatic ment on the juvenile stages of fish. Iri: Ac,/r.s dlr Colloqirr ecosystenis. In: EBERXIAN,B. and L. PERSSOY(eds.). Si:[,-.s/ixc Sciei~t~iqrreIiiternariorial OKEANOS, Montpellier (France). iirrecl /~opiilu/ioiis.Springer-Verlag. Berlin Heidelberg. 22-23 April 1993, pp. 48-55. MOOKERJI,N. and T. RAMAKRISHNARAO. - 1994. Intluence of onto- BERGMAN,E. and L.A. GREENBERG.- 1994. Competition between a genetic changes in prey selection on survival and growth of planktivore, a benthivore, and a species with ontogenetic diet rohu, Luheo i-olritir and singhi, Hctero~~iieii.sri~.sf;~,s.sili.~larvae. .l. shifts. Ecol~~qy,75(5): 1233- 1245. Fisli. Biol.. 44: 479-490. BRUNETTI,N.E. and M.L. IVANOVIC.- 1992. Distribution and abun- O'BRIEN,C.J. - 1994. Ontogeiietic changes in the diet of juvenile dance of the early life stages of squid (1llr.r argeiiriiiirsi in the brown ticer orawns Peimerrs cscirlenrir.~.Mur. E1,ol. Prov. Set... south-west Atlantic. ICES J. nini.. Sci.. 49: 175-183. 1 12: 19.5'20b.
CASTRO,J.J. - 1993. Feeding ecology of chub rnackerel (Scoinh(v. O'DOR. R.K. - 1987. llli~.i-illec~rhi.o.sir.s. Iii: P.R. BOYLE(Ed.). jupor1icus) in Canary Islands area. Sorrrli Ajkicu11 JOIII.IIUIOf Cepholopoil lfi cyc~les.Vol. 1. Acadernic Press. Loiidon. p. Maritre Science, 13: 323-328. 175-200. CHESALIN.M.V. - 1987. On the nutrition of Sflrenoteiitliis prei.opiu OVCHAKOV,O.P.. E.V. GREZEiind V.N. NIKOLSKIY.- 1985. (Steenstrup, 1855) with inyctophidae (Pisces). EXolo,qyir Moi.111. Features of the quantitative distribution of lanternfishei 25: 75-80. (Myctopliidae) near the surface. Voprosy Ikhriologii. 4: 681- DAWE,E.G. and P.C. BECK.- 1985. Distribution and size of juveni- 685.
le short-finned squid (1lle.i- i/lecehrosris) (Molluscn: ROPER,C.F.E. and M.J. SWEENEY.- 1981. Oinrnastrephiciae. In: Cephalopoda) south of Newfoundland durinz wiiiter. Vic. Fisher, W.. G. Biaiichi and W.B. Scott (eds.). FA0 spPciesrcleir- Milieii. 35(3/4): 139-147. riji(,crrioirs1recv.s forjislici~~prrrpo.\c. Easrerri Ceir/rnl Arlaiiric: EIBL-EIBESFELDT,1. - 1979. Etologíu. Inrrodiru~i611u1 csriidio conr- Fi.stiiiy 17i.cOS 34. 47 (ir! prr). Canada Funds-in-Trust. Ottawa. purado del comportanlieiito. Ed. Omega. Barcelona. 643 pp. Depnrtrnent of Fisheries aiid Oceans Canada. by arra,nement FISCHER,W.C.. G. BIANCHIand W.B. SCOTT(eds). - 198 1. FA0 with tlie Food 2nd Agriculture Orgmizntion of United Nationh. species identification sheets for fishery purposes. Easterii Vol. VI. Central Atlantic: fishing areas 34, 47 (in part). Canada Funds- Ross, S.T. - 1978. Trophic ontogeny of the leopard searobin, in-Trust. Ottawa, Department of Fisheries and Oceans Canada, Pi~ioiiorrrs.si~iri~lit.s (Pisces: Triglidae). Fish. Birll. U.S.. 76:225- by arrangemeiit with the Food nnd Agriculture Organization of 234.
the United Nations, vols. 1-7: pagvar. Rr:niEs, P. - 1976. Distribución y biomasri zooplanctónica entre C. GALIS,F.. A. TERLOUWand J.W.M. OSSE.- 1994. The relation bet- Bojador y C. Blanco (campaña "ATLOR V", Abril-Mayo ween morphology and behaviour during ontogenetic and evolu- 1974). Resultados preliminares. Res. E.i-p. Ciw. BIO Cornirlc, tionary changes. J. Fish Biol., 45(Supplement A): 13-26. 5: 209-2 16. GRANT,J.W.A. - 1993. Whether or not to defend?. The influence of S,~KCHEZ.P. - 1982. Régimen alimentario de lller coirideiii resocrce distribution. Mnr. Retmv. Ph>rinl 21: 137-153. (Verany, !837) en e! mar Catalán. /ni.. Prscl.. Vol. 46131: 443- GROSSMAN,G.D. - 1980. Ecological aspects ofontogenetic shifts in 449. prey size utilization in hay goby (Pisces: Gobiidae). Oecologitr. SCHAEFER,K.M. - 1980. Synopsis of biologiciil data on the chub 47: 233-238. mackerel, Sconiher japotiiciis Houttuyn. 1782. in the Pacific HART,P.J.B. - 1986. Foraging in teleost fishes. In: T.J. Pitcher (ed.). Ocean. Itit-Anier. Tr.op. Tiii~aComm.. Spec. Rep.. 2: 395-446. The hehaiiour of'rrlrost fishcs. The John Hopkins University UIBLEIN.F. - 199 1. Ontogenetic shifts in resource use and shoaling Press. Baltiinore, Maryland. p. 21 1-235 tendency related to body size in red sea goatfish (Parirpoieris HJORT,J. - 1914. Fluctuations in the great fisheries of northern fi~t-sskali,Mullidaej. Murirle Ecolo,qy, 12(2): 153- 161. Europe viewed in the light of biological research. Rapl~orts.c2r VESIU,J.P., W.C. LEGGETTand K.W. ABLE.- 198 1. Feeding eco- Pr0ci.s-i~erhniir Réirriioil Coseil inrer~iiorionul porir. logy of capelin (Ma1lorri.s ~Yllo,sii.s)in the estuary and western I'Esplorarioti ilr la Mer, 20, 1-28. G~ilfof SI. Lawrence and its rnultiespecies implications. Cun. .l.
354 J.J. CASTRO 2nd V. HERNÁNDEZ-GARCÍA Fish. Aqrttrr. Sci., 38(3):257-267. WERNER,E.E. nnd D.J. HALL.- 1988. Ontogeneric habitat shifts in W.AT~ABE,T. - 1970. Morphology and ecology of early stages oí' bluegill: tlie forazing rate-predation risk trade-off. Ecoloy?, life in Japanese comnion mackerel, Scomhci. jupotrrí~rrs 69(5): 1352- 1366. Houttuyn, with special reference to fluctuation of p~pulation. WL~DELL,J.T. - 197 l. Foorl analysis and ratr of diyestion. Iii: W.E. Bit//. TokpRrg Fish. Luh.. 62: 1-283. Ricker (ed.) Methodsfoi us.ressnlerit offirh /~i-oi/iri~trotiinfir.cli WEATHERLEY,A. - 1972. Gi-owtIr md c.co/o,qy of'fish popirlati~ti. wzteix. IBP Handbook No. 3, 2nd ed. Balckwell Scieiitific Academic Press, London. pp 293. Publications. Oxford and Edinburgh. p. 715-276. WEATIIERLLY,A.H. and H.S. GILL. 1987. The hiolo;.? itf fislr Woorrou. R.J. - 1992. Fish c~olo~~.Blackie and Son Ltd.. qi.oil~lr.Academic Press. London. Glasgo*. WER\EK, E.E. arid J.F. GILLIAU.- 1984. The oiitogeiietic iiiclir ;irid ZUL~TK.<,J.J. - 1972. Oii ~tieiii~portaiice of the Wadden Sea as a bprcies iriieractions in size-structurrd pupulnriurn. AI~IIKCT. niirwy ai-ea in reiation to the observatiun uf he Soutliei-ri Noi-th Eco/ S:w. 15: 393-415. Sea fisherb resources. S!.ri~p.Zool. Soc. Lotid. 29: 133-258.