Parasitism of dolphinfishes , Coryphaena hippurus and Coryphaena equiselis , in the western Mediterranean ( Balearie Islands ) and central-eastern Atlantic ( Canary Islands j *

A total of 648 doiphinfishes were exarnined for interna1 and exiernal parasties in western Mediterrane;in (Balearic Islands) and central-eastern Atlantic (Canary Islands) waters in order to iiiake a comparative study beiween thc two areas. The specirnens studied from the Mediterranean Sea was Coqphnrt~cr Iiip1n1vrr.i. wiih 62 large individuals coptured from May to Sepiember and 497 juveniles captured from August to December. The specimens studied from the cenrral-easiern Arlaniic were 39 adulr C. liippurrts and 49 adult Coryphaena equise1i.r. Parasites were found in 70%of ihe fish exaniined. and represented a ioial of riine endoparasitic taxa: six digeneans (Class Tremaioda. Subclass Digenea: Diiirrrrr.c ro171o/irs. Dinrrrus hr<virlrrcm. Dintrrtts lotigisitius. Lecrrlio<.lcrdiurn excrsum. Burli,vc.o!\'lr hrui1chia1r.s and Hirrrdinelln sp. ). iwo nemaiodes (Class Nematoda. Order Spirurida: P l i i l o ~ r ~ i e sp. and Me;d>rot~citr<r tnu~t~c i ) and one acanthocephaliin (Phylluni Acanthocephala; Rlic~dinorli~~ricl~ir.~ pr srrs). Seven crustacean copepod ectoparasires were ideniified: Colipts qu~drmrr.~. Coli.~ir.s prodtrctits. Cct1i~ir.s hotiirr~. C(rlrgu.5 c-oryhien<re (Family Caligidae) and Errryl~orrts ~rynphoc (Faniily Euriphoridae) were found in gil1 niucus masses or on the inner surface of the opercuiurn, the lernaeopodid N~ol>rcr<h~~ll (r c?~.~?;?!!o:,!!::r (F;!!??i!y Lernue~po&&e) -2% a!:;&& :o gil! fi!amci;;; ai;d ;he p i ;e ! l id ,D<.jjiie,'/ü,5/ii~¿j ( h m i i y i>eñnziliijac) Was anchored to íins and n y s or. deeply. to muscu\ür iissue and abdominal caviiy. The relationships beiween feedin: habiis. parasiie recruitmeni and parasiie transrnission were analysed. some ecological aspects of al1 [he parasitic specics are di<cussed. ;ind sonie comments are made on parasire-hoit relaiionships.


INTRODUCTION
water ternperarures exceed 20°C (Gibbs 2nd Collette, 1959).In the Atlantic, they are natural inhab-The dolphinfishes (Pisces: Coryphaenidae), itants and their spawning is probably year round.cornrnon dolphinfish (Coryphaena hlpp~rl-u.rL.) although it is rnost intense during the inonths with and pompano dolphin (Corvphaena equiseliz L.); hieher water surface ternperaturec (Shcherhachw.are epipelagic species distributed world-wide in 1973).In the Mediterranean Sea, C. hippur-rr.7 tropical and subtropical waters where surface appear seasonally and undergo a reproductive cycle during the surnrner rnonths, t'ollowing [he 'Receivcd June 15. 1998Accepted May 8. 1999 appearance 0f adult specimens every yeilr ¡n M a y -June, when the water surface temperature reaches >18"C (Massuli and ,Morales-IYin, 199511.Juveniles are captured from Iate August to early December and then, when water iemperatures fall [o lI°C, they possibly rriigra~e to thc: warnxr waters of the Atlantic Ocean.Dolphinfishes are top-leve1 prdators, but rhey arz not very selective and fced on a wide rangc of pelagic organisms.In adaition, they are ve-' agile and capable of rakin; fasi-moving prey (Palko e! al., 1982j.C. hippurus grows rapidly throughout its life and has a maximum life span of about 4 yrars, reaching lengths and weights in excess of onc m m e and 10 kg respectively (Beardsle!, 1967;  Rosz and  Hassler, 1968).C. equiseiis is a relative11 Iirrle known species which does not reach such a large size as C. hippurus, and its maximum known length is 74 cm (Herald, 1961).C. equiseiis is more pelagic and oceanic, and consequmtiy is rarely caught in coastal waters.Its distribution ranpe is more tropical and according LO Mather and Dtij (1954) it is not generaliy found in waters with surface water temperatures Iower than 24°C.C. eyuiselis does nor extend as f u beyond the rropics as C. hippurus.There are few reports of C. equiselis in the Mediterranean Sea. and hence its presence in these waters is no[ well known.
Although severa1 authors have reponed parasites oi doiphinfishrs in every ocean.and án exhaus~ive iis; icin be found in Palko er al. (1982), only r few focus on rhe study of the parasire community of Therefore the objective of this study was to carry out.for the first time.a complete analysis of the parasiric community of dolphinfishes in the eastem A4tlantic and the Mediterranean, and to study thz reiaiionshipj between diet and parasite recruitment in order to identify possible pathways of parasitic infection and life cycle.Special referente is rnade to the paasites which C. hippurus probably bnngs from h e Atlantic to the Mediterranean Sea and those which this species acquires in the Meditsmnean anu c h e s to Atlantic waters.Our aim is to provide basic informaiion that will allow parasites to be used as porer:-tia1 biolopical tags for C. hippurus in rhe study of its migrato?routes between these two areas.

MATERIALS AND METHODS
The fishes were collected fiorn two areas, Cne Balearic Islands jwestern Mediteii-anean) and the Canary Islands (central-eastem Atlanticj.In the laboratory, the fish were measured ro thr nearest c mtirrierre fork length (FL), weighed and sexed.Intc~ument, fins, natural openings and gilIs of every ficn were exarnined.The gills were dissected in order to survey al1 [he gil1 arches for parasites.In aII cases, the parasites were collected and, in addition to their number, size, shape and location, any pathological a:iZiaiiOliS .&sererecoided.A-,.-u i r ~c a i i j ---e.-:,--puiU ~~L G J were found.they were fixtd in buffered glureraldehyde ( 10%) for larer identification, directly or aftzr being cleared with lactophenol.
From the Mediterranean area, a total of 62 adult C. hippurus, ranging from 60 to 124 cm FL, were sampled during May-September in 1990, 199 1 and ir%. in iiie sañie years, 497 juveniies íi4-58 cm FL) were obtained from August to early December.
From the Atlantic area, 25 adult (69-102 cm FL) and 24 juvenile (38-53 cm FL) specimens of C. hippurus were sampled during June and October in 1994 and 1995 respectively.In this area, 49 C. equiselis between 36 and 52 cm FL were also sampled during June in 1995.
To establish differences in parasitism as a function of size, the fish exarnined were differentiated into six size intervals in order to obtain a sufficient number of sFciiíieiis pi gicrUp.Sizr.iniervais, n"m'mr "f fjsh analysed per size group, year and month of capture and the surface water ternperature range are sumrnarised in Table 1.For each parasite, the infection leve1 by size group was analysed according to standard methods (Margolis et al., 1982).

Endoparasites
Endoparasites were found in 390 of the specimens exarnined (70%).A total of eleven parasitic taxa could be identified (seven digeneans, one ces-tode, two nernatodes and one acanthocephalan), of which nine were to species level.The change in prevalence, intensity and abundance of the main species in reiation to the size of the hosis is presenied in Table 2 and 3 For the prevalence and other ecological parameters there were marked differences depending on the annual cycles, but in general adult fish were the most infected in both areas.
Lecithocladium excisum (Rudolphi, 18 19) Looss. 1907 This other gastric hemiurid was only found in the Mediterranean, from juvenile fish 4 0 cm FL in the Pleroczrci were f m n d in spe,-inizns of C. +i,?,v:¿rus larser than 3V c n FL captured in both x e a s .A ~orai of 9i q s r s conrining 2 singie picrsczrioic were collected from the ci~domina!cavity a n l tl-i?surfare srrosa of th? vissera.C ~s i size \+as cririablz and ranged frorn 20 to 50 rnm.The shape oí thi c p ~s aiso showed a greut cririeiy of i'orrns, but they always had a rerrninrtl globuix reg'ion, where [he : x v a occurred, anci a tail-like srruciure.The-smallesr cysts 1:4-7 rnm in Iength) showed a n enlarged nr hoad-like scoIex with t\vo rounded exirnsions.Tne rnedium sized larvae measured 10-12 rnm and ha3 :entades and tivi?leaflike bothridia.T h e larges: pieroceícoiifs (15-25 in ieligti:; showcd iyqo deeply CLASS N ELI .\TODAOrder Spirurida Farnilq Cystidicolidae Metubronema (Qistidicoloides) magna (Taylor, 1925) Some cysts were collected from thr walls of the pyloric caeca and in the pancreatic rissue of C. h ppurus specimens captured in the Mediterranean.They contained several adult nematodes belongin; to Chis species.The cysts measured 30-50 mm in length and 20-30 mrn in width.and they were poor-1y defined, solid, opaque and included in the iissues.Most of the cysts were calcified.The infection appeared in small fish, and the prevaience increased rapidlt, rernaining high at aII fish sizes, ahhough ir was on1: possible to follow the chariges o? [he iniection diiring the 1995 cycle.In rhz youn;esr fish, the cysts constituted a soiid mass of conjunctive tissur which coniainrd a rnale aiid various females encrusted irrzgulariy in the rnass.in the larser !ish, the calcification ufas constan1 and complete, with most of the nematodes being broken and fragmented.

Ectoparasites
Seven species were found, al1 of which were crustacean copepods.Their infection parameters are given in Table 4 and 5. Class COPEPODA Order Shiponostomatoida.
Collected in the gills of C. hippurus captured in !he Medi?errme~r!2nd t h r e ~g h e ~! a!! !he sizr intervals considered.Caligus quadratus Shiino, 1957 was the dominant species.Other species of this genus, such as C. coryphaenae Steenstrup and Lütken, i 86 i , C. bonito Wiison, i 905 ana C. producrus Müller, 1785 were also found.They were located in large masses of mucus surrounding the gills (60%) and on the inner surface of the operculum (40%).C. hippurus and C. equiselis from the Atlantic area were not infected by these copepods.The prevalence in juvenile fish was higher than in adults.I t was also higher during the months with higher water surface temperature.Parasite females WPK EKXX ahmdan!thar! ma!es, u/i!h !he sex-rctb being 7: 1 .

S n / r
Curypizorus nymphae Sreenstrup ana Lüiken, I ao i Collected from both species in specimens bigger than 40 cm FL captured in Atlantic waters.The proportion between parasite females and males was 2: 1.This species, as well a s Caligus spp., produced an abundan1 mucus hypersecretion in the gills, and the parasites were found in this mucus mass.They were also present on [he inner surface of the operculum.Though the examined fish were dead, the parrtsites uere still highly active and they could be found in íiie ora; cavicy, skin on rne head and oiher skin iocations.30% of the materia!iourid corresponded to premetamorphii forms that lacked cephaiii homs and showed simple branrhial filaments, wirhcw!ramifications or ar most with prirnary branchcs rhai always arose frorn the main branch.Thev uere premetamorphic females with a fragiie, whitish body of smali size (45~-14 rnm in lengtti; ranpe 22-í3 mmj.The rest were composed of pregravid aná gravid females with three wrli-developed horns, an inienseiy keriiiinizeá boáy anli a dark brown coiour.The sizt: h a s 4 1 -1 3 mm (59115 nim).The gilis consisted ~7f rhe main fiiarnenr i r x n wnicr!prima-, secondary and even tenia?hranches arose, hut thzy were always withoui anastamosis.

DISCUSSION
The results obtained allowed the little existing infomation concernin; the parasite fauna of dolphinfishes in the Mediterranean and Centrai-Eastem .4rlantic to be extended.None of the species found in the hlediterranean had been reported in this area until now.The Mediterranean records were limited to Dollfus (1927), who reported a metacercaria of the hemiurid trematode Dinurus notarus.Lozano-Cabo ( 196 1 ) who found the isopod Anilocro ph~sodes, and Delamare-Deboutteviiie and Nunes-Riiivo (195s) who reported the two parasitic gil1 copepods Brachielia LO-phaenae and Caligus befone.By contrast, al1 the species found in the Canary Islands had been reported ir1 Atiantic ivaters, although most of these records correspond to the western toas[ (e.g Cable and Linderoth, 1963;Ho, !363).The on!i avui!ah!e i n f ~r m x i ~r !from the cmtral-western Atlantic were studiec on trematodes frorri fishes off Ghana and Senegal (Fischthal, 1972; Fischthal and Thomas, 1 W2b).

Endoparasi tism
The presence o! gastric herniurid digenean parasirrs in juvconik and adult specimens of C. hippurru suggesis tnat infection takes place ;n Mediterranean 2s i i ~l !ss in Ailanri: iv3cers.The iife ¿yci,~ of ihrae a: : deveiop, whereas meiasercariae occur in [he haemocoe!o i copepo2s and rhaeto_gnarns.This author also sho?ifed ihat sume ciecaood ianlae may be infected by eating the cercariae and that thz de5nitive hosts wcre clupzids, scomhrids and oiher plankton-feeding M e s ..As al\ these 0rpa.i.isrns are present in the Me~iterranean 2nd .4ílzr,ticwaiers, ir ap?ears thai C. izi,-.;.urits couid dcqiiire rne parasites either through the ingestion of copepods and other crustaceans with metacercariae or through eating small infected fish, which act as second intermediate hosts (Gibson and Bray, 1986).These authors seem to conclude that non clupeid fish could acquire the hemiurids by feeding upon clupeids or other plankton-feeders.The infection of metacercariae herniurid digeneans from clupeid fish and crustaceans has been recorded in C. hippurus by severa1 authors (Dollfuss, 1927; Yamaguti, 197 1 ; Manooch et al.,  1984).
Sirnilarly to other areas of the Pacific and Atlantic, fish.crustaceans and cephalopods have been reponed as main components of the diet of C. lzippurus in the Mediterranean (Massutí et al., 1998).Nevertheless, an important change takes place during the ontogenic development of the species.Whereas amphipod and crustacean larvae make up more than 50% of the diet of juvenile specimens smaller than 30 cm, cephalopods and mainly fish are the most important preys for bigger fish.Taking into account that the Dinurus species appeared in juveniles (>40 cm FL) and adult specimens (>60 cm FL), [he transrnission mechanism from invertebrates does not seem probable and their infection is likely to be produced frorn ingestion of clupeid or other plankton-feeder fishes such as carangids, which are an irnportant component of the C. hippurus diet.
The only data thai we possess on the biological cycle of the species of Dinurus are due to Dollfus (! 927) 2nd Szidx ( ! 950).The f;,rs! autho: mggests that cenain metacercariae found in the body cavity of the crustacean decapod Cerataspis monstrosa belong to Dinurus notarus, a stornach parasite of C. liippurus, for which two fornis of transmission are quoted as being possible: through invertebrates (copepods, decapods and chaetognaths) or through vertical migratory fish (clupeids: carangids and scombrids).Szidat (1950).on the other hand, considers that the clupeids are intermediate hosts for Dinurus breviductus.whose rnetacercariae encyst or ertcapsüiaie i ñ the skiñ O¡' Snrdinü piichordu~ and Sardinel10 ciurita, where the parasite produces a type of "black spot disease".
On the other hand, ihe other gastric hemiurid Lecirhoclirdiurn excisutn was only found in juveniles.This species is reported for the first time in C. hippurus.Its cycle is known through the experirnental gi'&-r ~f Knie (199! ).As in Binilr!,~, i t q first intermediare hosts are gasrropod molluscs and the cercariae are found i n the haemocoel of calanoid copepod crustaceans.Metacercariae have also been described in jellyfish, in the ctenophores P ~E L I ~Obrachia, in diverse species of Sagitta and in the coelorn of the polychaete Totnopteris.These noncrustacean invertebrates are certainly infected when eating copepods with metacercariae, and should therefore be considered as paratenic hosts.In our case( the infection by this trematode is early, which suggests that i t took place when C. hippurus juveniles preyed on pelagic crustaceans, although the possible infection route by paratenic hosts such as Sagitta and other invertebrate components of the pelagic system cannot be ruled out. The other two digeneans Barhycoryle branchialis and Hirudinella sp.only appeared in a few cases in Mediterranean waters, and can be considered rare as secondary parasitic species.B. branchialis had been previously reported in the gills of large C. hippurus specimens frorn the Straits of Florida (Burnett-Herkes, 1974), although it is not proved whether this parasite infects the gills or is vomited from the stomach, as we have found in Dinurus spp.Two species of Bathycotyle have been described, B. branchialis in scornbrids and B. conphaenae in C. hippurus.The only data to differentiate them is the presence of an external opening of the Laurer's canal in the first species (Gibson and Bray. 1979).Although it is not clear whether the Laurer's canal has an external opening or not, we have seen a dorsal opening in our specimens and in consequence we have considered thern as B. branchiaiis.The life history of this . .spec:es :S m! kmvín.The gp,i,u ,~irudf?t,~!!c is 8 typical stornach parasite of rnarine teleosts (mainly scombrids and tunas), although coryphaenids are habitual hosts (Yamaguti.197 1 ).Due to their great morphological variability, many studies have described up to fourteen different species of this genus, although Yarnaguti ( 197 1 ) stated that a wideranging revision is required.The life cycle of this endoparasite is also unknown.observations of Nakajima and Egusa (1972g), who dernonstrared that copepod and teleost fish are necessary for procercoid maturation and otner tsleosts ior plerocercoid developrnent.hfetabronema nzagnn is a nematode common in the stomachs of sairnonids (.4nderson, 1992).ln marine fish, ir had only been dzscribed in CUI-anx sp. and S,uarus sp.(Skrjabin, 1991).This spirurid requires the participation of an intermediate host such as rhe crustacean arnphipods, deiapods and wnich thz third larval stage can develop.Atthough rhey have been found in iish of al1 sizes and a,aes, i r rnust be supposed that early infectioh takes place when C izippurus feed on amphipods and decapods.The fact that the cysts generated by thess nematodes are made of conjunctive tissue in fish u,ith sizes rmailer [han 50-60 c m FL and are inmpieteiy cal,^fird in larger s i z d fish seerns to jüggesi that [he infection has been early.Givm the rspid growrn of C. 1zi.pu.ru (Beardsiry, 1967;Roce 2nd Hassier, 1968) however, ir is no! tinespeirec tnat conjunrtiv: c y s s have been ohszrved Ir) fich frorn ¿O m 60 cm FL..The other spirurid nematode Philornetroiác..i sp. is also repoitzd b r tiw iirsl time in C. h i p p ~t r u ~.However, in contrast, i t only appeared in ~1 few swecimens frorn hlediterranean haters.The only p r c l e s of this genus known to dare is Pizilonre:tnia'r.s.sorir!- ;no, iuhi_-h \ U' S &r+-r~d jn mayjn-!-~h e s fr93-; Japanse waters (Skrjabifi, 1491).Our specimens k,ave rhe i;ipical cuiiculer l a t e c of thi', spxie?. bu: we are no! cure if tney belong ro it.
-~ i ne scaxhocephaian Kizudin~rhvnc~:lr';.i pristis ap?eared in fish r'rom both areas, bu: wiih icw przvaiente.This species was reporred for tne rirst time i n dolphinfishes from Cari bbean waters (Cable and Lindrroth. 19631, although ir is widzly distributed in a great number of epipelagic fishes (Yamaguti, 1963; Yetrochenko, 107 1 ).The irict tnat this endoparasire has bzen found in C. eydiseks spzcirnens betaern 30 and 30 cm FL, and that in C. hippm-u: ir only appearzd in adulr fish, sugsests that [he infection of this species could occur in .4tlanticwarers, before the seasonal migration of thesr specimens to the hlediterranean.lt is known that [he pararenic hosts have great importante in (he biological cycles of the acanthocephalans.Thus, infection could occur when both species eat pararenic teleosts.ii.re¿: other ,",cm (Kabara, 1979).A i w , \ve rnusí iake Inio vccounr rne reiarionship betwsen corypnaenicis and floating objects, which have beeri postuiaied as cleaning srarions ivhere pelagi: fishes go &o have rheir parasites removed by other-fish (Goodin; and i\/lagnusonn.196?j Eurjphorw njrr:,pi2«r is aiso 3 woriíi-wide swecics that has been recorded as s n ectoparasile a i cnryphatn!d';.Th!.: cope@ P~r2Si!j72S ik? ' ; ~n j ~ habirat as Cu!ig~is spp.and i i seenis :har iilthougr: it ii ~r e \ .~ú ! e ~: C .P S L ~Z ~ surface temperatures, since they ranged between 1 6 and 27°C in the Mediterranean Sea, whereas in the Atlantic the temperatures were less variable, ranging frorn 20 io 2 3 T .We cannoi eiiher expiain the fact that the other ectoparasite copepod Neobrachiella corypl~aenae was only found during 1995 in the Mediterranean and was absent in 1990 and 199 1 and in Atlantic waters.The life history of this species is direct and the postembryonic stages belong to the planktonic community, which rises every night to surface waters (Kabata,198 1 ).

Cniigus quadratus and the other
Per~rtella fifosa is a mesoparasitic copepod which has been reported in Xipltias gladius, Mofa mofa, in some tuna species and in marine mammals (Kabata, 1992).Recently, P filosa has been found embedded in the flesh of LRpidocybiurn f7avobrunneum captured in the northwestern Atlantic (Benz and Hogans, 1993).Only Pennello pustulosa and Pen-~zella varians had been reported in C. hippurus from Australian and Atlantic waters respectively (Yamaguti. 1963).Nevertheless, it is probable that both species could be synonymous with P. Jfilosa, due to the great morphological variability of this pennellid copepod (Kabata, 1979;Hogans, 1987;Raibaut, 199 1 ).This anatomic plasticity has also been observed by us, and although it is related to parasite age, it is mainly related to its location.In effect, there are important morphological differences if the parasite is attached to hard surfaces (fin rays) or if it is deeply anchored in muscular tissue or in the ebdorninal cavity.
P filoso has an incompletely known life cycle, due to the lack of data on its chalimus larval phases and the rnetamorphosis of the infective preadults.However, it is probably similar to other pennellid species.which are the only copepod parasites that shew a !tiíe-hest !ife cyc!e.Seme telees: fish (semetimes the same final host) and cephalopods have been reported as intermediate hosts of pennellids (Kabata.198 1 ).Rose and Hanion (1953) have also repoi-ted chaiinius stages and i'ree maies of P jiosn in the gills of the cephalopods Sepin and Loligo.This parasite is characteristic of large specirnens, which have a diet coniposed of almost 20% cephalopods and 60% teleost fish (Massutí e/ al., 1998).Thus, its infection as the fish became older could be related to a higher catch and predation activity on squids (Illex-coirtcleiii and Todarodes .sagiitrrtu.s) and other cephalopods (Histioteuthis spp.).The predatory contacts rnight allow the invasion of infective forrns from the gills and rnantle of squids to the skin oí' C. 11ippr~i.s.P filosa has not been found parasitising C. hippurus in any sea or ocean of the world.The only references to this parasite refer to the previously mentionea fish where the presence of I ?jiosa has always been occasional, with the collection of only a few parasites which very often appear to be incornplete due to the lack of the head.In our case, we obtained a total of 160 parasites, al1 them exclusively parasitising the large breeding fish that every year visit the Mediterranean Sea.The presence of 30% prernetarnorphic parasites, as well as young females, makes us suspect that infection takes place in the Mediterranean Sea after the breeding fish cross the Strait of Gibraltar and subsequently disperse through the whole sea.On the other hand, Pascual (pers.corn.),studying cephalopods captured in the Alborán Sea and other areas of the southwestern Mediterranean, has proved that al1 the cuttlefishes and squids captured in these areas were parasitised (100%) in the mantle and gills by larval chalimus phases, possibly belonging to copepod pennellids.
Consequently, i! " p .y p-&&!p.[ha! h @ p r ~d r ir infected when predating on these cephalopods during its passage through the southwestern Mediterranean.

CONCLUSIONS
The study of the relationships between diet and parasite recruitment allows sorne cornments to be made on the life cycles of sorne of the parasites found.Regarding the endoparasites (Fig. 1 ), a cycle of three hosts can be proposed for Dinurus spp., in which the benthic gastropod inolluscs and planktophage fish, mainly clupeids.would take part as C. equiselis being the detinitive or final hosts.A similar cycle could be applied to the other gastric herniurid Lecithocladiuni c.~ci.s~int but in this case the secondary hosts wouid be iarvae of copepods and pelagic decapods.The neniatode Metabrortemn ri~nsna and the acanthocephalan Rhadinorhyitchu.~prisris would have a cycle of two hosts, the first being pelagic amphipods and the second being larvae of diverse crustaceans in whose haemocoel the stage 111 infective larvae and the cystacanths would develop respectively.Finally, a cycle of four hosts is suggested for the cestode Floriceps saccatus, with crustacean larvae as priniary hosts, planktophage fish as secondary hosts, C. 1iippuru.ras the tertiary hosi and various sharks as linal hosts.recruitment of parasites is qualitatively similar to that of the large fish whose diet is based almost exclusively on teleost fish.Therefore, the feeding habits, surface water temperature, and length and body weight of fishes are related to parasite recruitments (Fig. 3).
This study shows that there are severa1 parasites of Cj. hhippurus that are potentially useful as biological tags for studying its migratory movements and stock differentiation within the Mediterranean, and between this area and adjacent Atlantic waters.Within the endoparasites, the trypanorhynch species F: saccatus, widely recognised as a long-lived parasite, and the acanthocephalan R. pristis, despite its low prevalence, probably have the greatest potential as biological tags.These species have a sufficient life span and remain in an identifiable form in C. hippurus long enough to cover the time scale of the investigation.For the same reason, the usually short life spans (<1 year) of adult digeneans in the alimentary tract of fish, tends to limit the use of these species as bioiogicai tags.Of t'ne ectoparasite copepods found, /? jlosa has a particular advantage as a tag because it is a large, very easily seen ectoparasite that leaves a prominent scar after its death, thereby extending its usefulness as a tag beyond its actual life span.
-Herkes (1 974.1 analysed [he ectoparüsites on the gills and in the buccal iiavity cf C. hlppilrus, whereas Manooch e! al. (1984) studied its gastrointesrinal parasites.Both studies werr carried out along [he South-Eastem and Gulf coasts of the United States in rhe Western Atlantic.
and most numerous endoparasites were four species of the genus Dinurus Looss, '1907.These were D. tornatus (Rud.18 19) Looss, i9 i7, D. barbaius (Cuiin, i902j Looss, i907, D. breviductus Looss, 1907 and D. longisinus Looss, 1907.D. tornatus was the dominant species.These parasites were found in the stomach of specimens of C. hippurus and C. equiselis captured in both areas. Family Lemaeopodidar .Veobrachiella coryphaenidae Pearse, 1 952 Collected from C. hippurus juvenile and adult specimens captured in the Mediienanean.The infection took place in juvenile fish during [he months with high water temperarures, and in every case parasices were attached to the gil1 filaments by rheir appendages.0 ~1 ~. a few parasites carried d w a d males.Mucus hypersecretion or any other iinaromical alterat~on were not observed.Family Pennellidae Pennellu filosa Linnaeus, 1 758 Collected only from large specimens o i C. hippurus captured in Mediterranean waters during May-Seprember in 1990, 1991 and 1995.Young fish caughr in this sea, and the ones from the C a n a q Islands, were not infected by this parasite.Although the ecological paramerers were different during the three years studied, in e v e p case they showed an i ~~~t a ~i F L o t e n r i ~m ~\ ~ fiSh h ~~a ~~~e O j d c ~-The Q L"'U"'-: parasites ufere mainly attached to the dorsal and anal fins (50%j.to dorsolareral muscular tissue ( 2 5 % ) and to the abdominal cavity (2W¿).Mised parasite locations were frequent in fish larger [han 100 cm FL (40%).The depth at which the cephalothorax or radicular apparatus \vas anchored varird according to parasite location.Thus, it was deeper in the abdorninai cavity and rnuscularure [han in fin rays C!isubcutaneous tissur.Some parasites ivere hyperparasitized by tne cirriped Conckxierm~: au,ritut,;.Skin , , .:r. . . .e , , ,l...,.,.rrlirli,, . .m -t L . 3 nllu i i i u ~~u i u i i i ~~i u > i > W G I L a i w u y a p i c s c i i ., L : : ~L i i i ~ head and horns o i he parasice were immtrsed ir) ii bioody and infiammatory esudate mass.The cephalothorax was surrounded b) a fibrous conjunctive tissue capsuie and the adjacenr tissues showed different ratec of inflan~marory alterations wirlh iis- tulizations.

rfi
Jspa;as;:ej 1s re:;iijt.ij.v ci,ííipii:<, i:v,pi:al of many i-:elmintn parasites.with set,eral iniermediate hoats.Ir may foiiow the typical modd drscribed by Koie ( 1 579, i940b, 1590c), who reponed benthic gasrropods as first intermediate hosrs where [he ~* r c a r ~--O Fforiceps saccatus plerocerci have been recorded in teleosts, whereas adult cestodes are gut parasites Pacific Oceans(Campbell and Beveridge, 1994).The only reference for these plerocercoids i n coryphaenids was reported byDollfus (1946) from specirnens caught in French Atlantic waters.Its presence in C. hippurus coming from the Atlantic Ocean as well as in the juvenile fish born i n the Mediterranean Sea indicated that the recruitrnent of this parasite is possible in both areas.The absence of parasitism in C. c.qui.~eli.c.n-iay be due to the small size of these specimens in [he sample, which included individuals in the 110-52 cm fork length range.ln the samz way, the diet composition may possrbly play a role in the rexuitment of the parasiles.Thz high prevalence observed in adulr fish(Carbonell et  ai., 1998)  could suggest that &he develcpment iif the cysts in C. hippurus is slow or thai :he) get the infection late.Lnfonunately, the time nsedea by the ingested procercoid iarvae ro develop inro plerocercoid larvae, and the time needed for the defence mechanisms o i C. hippiuus to produce the iarge cysts of conjunctive tissue are both unknown.In any case, thc above mentioned authors have postuiated a four host cycle for this species, with crustaceans and plankton-feeder fishes as intermediate hosrs for procercoid larvae, C. izippicrus as a pararenic host for plerocercoid larvae and sharks as final hosts where [he s t p p mzt~rps.This ~grep_s ~i t h e?;n~rim~ntal Y-' " "-" '"' Ccll!:rts species O have been recorded in al1 oceans as ectoparas~tes of O O, coryphaenids.They have been found in the skin as e E well as in the oral cavit!;, operculum, gil1 cavity and gil1 filaments (Palko er al., 1983).They are monose-5 nous copepods whose copepodite infecti1.eforms have ilat bodies with a circular dorsal carapace, and e rhey swim frcely in thc water within thr pelagic O ecosyctem.As the enrire life cycle of C. htppurus g rakes place in the same habitar, ii is not unusual rhat as adult stages.The infectiori stans in [he early growth period, reaches its maximum in inrermediate aged fish and decreases in adulrs.This could sug;est an irnmunogenic condition in large specimens, which acquire resistance as [he)-.becorns oider due to the repeated contacts betiveen parasites and has!.N-verfh~!rc-, i ! is diffic-!! re& any dsfinirive eonclusions about rhe infection dala sincz tkc caligids hsve :he abiiity ro 1rai:e rheir hoai and .- t r , , , ; , h P,~,-....I.-,#.~"L;...-.#.-.#" .-."AI I I L L I I I I L U I U L L I I U J L 3 , W I L L I L < I I \ / I I I L < C f l U I L L / I p U l U J 4 1 1 U j ; -Three-host model lor Leclthocladlurn excisum j . . . . . . . ... . . . . . . . 3 Three-host model tor Dinurusspp.!, , -Ywo-host model for Rhodlnorhynchus pristfi L 1 ; + C , M O B W C ~~~ Regarding the ectopxasites (Fig. 2).PPUP?PI!C -fiiosa is a copepod that needs two hosts, a fish o: a cetacrirn as a definitive hcist and cephalopod moiiuscc as intermediate tiosts.These last ones, are infec~ed by copepodite larvae thar develop four c hai-: -.,. a.n"..-: # * t ., .-.A l ¡ .%..A * L ., .l,.c, -4-~\,L:*L. ., -A A:; I I I I U ~ a i a s c 3 i i i L I I L i i i u i i u .~, i i i ~ iaJL vi n i i i c i .ulr. u i iferentiatec sexiidly arid are fenilised.Tne males rhen disa~pear and the knilised females : n f m C. ,i:+purus where they unaergo extensive metamorphosis.This explains ths great imporrarice of ihe physicai contacts betweeri definitive ara in~ermeai-ate hasts.The rrmainin; copepod parasites nave copepodite and pelagic chalimus phaszs which iorm part o i the planktonic community, here re !he ii?urrn chalirnus stagc difierzntiates into ~r e a d u t ~ miles anO females thar ar? rhe infxtive iormc ior [he silis ei & .c ..-.A,-.,nb.fl,-..;A.-L i i L c U i J p i L d L I l i U 3 .The presrnr siudy shows that [he Iife q c l e arid brna\iour-of C. Aippurus 2nd C. eauiseíi.;Are of ;real imponanx in Irte rzxaitrnen:, 3evzis?mr,t, and transrnlssiar.3i parasites in the Aririnti< Ocean and in [he Mediterranean Sea.Ir1 borh species, the PLnhrruc C I U L W S ( Chl ro C M ) P(uihmc NAUPUUS Fic. 2. -Proposed life cycles for the ectoparasites.Left: Cycle for Pennellajiloso.Right: Caligid cycle for Caligus spp and Euryphorus nyrnphae.Lemeopodid cycle for Neobrachiella coryphaenae.

prevalence; n E second row: mean intensity t SD; third row: mean abundance f SD; fourth row: range).
a , , n i YY i cycie.its prevaience, intensity anci abunuance were low.

TABLE 4 .
lnfection parameters of the copepod species (Cdigus spp.. Pennellufilosa and Neohracliiella coryplioenidae) of Cotyliaena Iiippirrus captured in Mediterranean waters (FL: fork length in cm: first row: prevalence: second row: mean intensity I SD; third row: mean abundance k SD; fourth row: range).

Table 5
.lnfestation paraeters of the copepod speciesuryphorus nynpltof Coryphaena hippurus and Con.phaenu equiselis captured in Atlantic waters (FL: fork length in cm; first row: prevalence; second row: mean intensity I SD; third row: mean abundance f SD; founh row: range).