Bulletin of Fish Biology Volume 10 Nos. 1/2 31.12.2008 25-38

Distribution of parasites from red mullets (Mullus surmuletus L., Mullidae) in the North Sea and the Mediterranean Sea

Verbreitung der Parasiten von Streifenbarben (Mullus surmuletus L., Mullidae) in der Nordsee und im Mittelmeer

Sven Klimpel1, Sonja Kleinertz1,2, Harry Wilhelm Palm1 1Heinrich-Heine-University Düsseldorf, Institute of Zoomorphology, Cell Biology and Parasitology, Universitätsstr. 1, D-40225 Düsseldorf, ; [email protected] 2Leibniz Center for Tropical Marine Ecology, Fahrenheitstr. 6, D-28359 Bremen, Germany

Summary: A total of 167 red mullets (Mullus surmuletus) from four geographical locations (North Sea, Ligurian Sea, Tyrrhenian Sea, Adriatic Sea) were studied for metazoan parasites and food composition. Fourteen different parasite species were found and six new records for red mullets could be established. The parasite richness among the different areas ranged from four up to ten species. The red mullets from the North Sea harboured the most species rich parasite fauna (10). This contrasts the Mediterranean locations (four to seven species) where endemic digeneans and parasites were found. The simplex s.l. and Capillaria gracilis as well as the acanthocephalan Corynosoma strumosum and the Caligus elongatus and branchialis were isolated from Mullus surmuletus from the North Sea sample, while the digeneans Opecoeloides furcatus, Timonia mediterranea and the nematode Ascarophis valentina occurred only in the Mediterranean fish. The content analysis of Mullus surmuletus revealed 19 different prey items. This wide food range can explain the observed parasite richness. Our results support a restricted distribution of endemic digeneans and a nematode within the Mediterranean Sea, while several other metazoans occurred throughout the sampled locations. Historical reasons, especially the post-Messinian history, as well as host migrations are possible reasons for the observed red mullet parasitation.

Key words: Mediterranean Sea, North Sea, metazoan fish parasites, diet composition, biotic relationships, zoogeography, biodiversity

Zusammenfassung: Insgesamt wurden 167 Streifenbarben (Mullus surmuletus) aus vier geographisch un- terschiedlichen Regionen (Nordsee, Ligurisches Meer, Tyrrhenisches Meer, Adriatisches Meer) auf ihre Parasitenfauna und die Nahrungszusammensetzung untersucht. Es konnten vierzehn verschiedene Parasi- tenarten identifiziert und sechs neue Wirtsnachweise erbracht werden. Die Parasitendiversität unterschied sich in den Untersuchungsgebieten und variierte zwischen vier und zehn Parasitenarten. Streifenbarben aus der Nordsee beherbergten mit zehn Arten die diverseste Parasitenfauna. Dieses Ergebnis steht im Gegen- satz zu den Fischen aus dem Mittelmeer mit vier bis sieben Parasitenarten, bestehend aus endemischen Digeneen und Nematoden. Die Nematoden Ansiakis simples s.l. und Capillaria gracilis sowie der Acanthoce- phale Corynosoma strumosum und die Crustaceen Caligus elongatus und wurden ausschließ- lich bei Streifenbarben aus der Nordsee gefunden. Im Gegensatz dazu wurden die Digeneen Opecoeloides furcatus, Timonia mediterranea und der Nematode Ascarophis valentina nur bei den Fischen aus dem Mittelmeer nachgewiesen. Die Mageninhaltsanalysen erbrachten 19 unterschiedliche Nahrungsorganismen. Die Para- sitierung der Streifenbarben lässt sich anhand eines unterschiedlichen Nahrungsspektrums in den Untersu- chungsgebieten erklären. Im Mittelmeer waren insbesondere endemische Digenea- und Nematodaarten zu finden, wobei andere Parasitentaxa eine kosmopolite Verbreitung aufweisen. Erdgeschichtliche Ursachen, insbesondere die sog. messinische Salinitätskrise (post-Messinian), sowie Wirtswanderungsbewegungen sind vermutliche Gründe für die nachgewiesene Parasitenfauna.

Schlüsselwörter: Mittelmeer, Nordsee, metazoische Fischparasiten, Nahrungszusammensetzung, biotische Faktoren, Zoogeographie, Biodiversität

Bull. Fish Biol. 10 (1/2) 25 1. Introduction Endemism has been estimated to characterize about 28% of the marine fauna in the Medi- One of the most interesting and dynamic terranean Sea (FREDJ et al. 1992). boundaries in the world’s oceans is the Strait Fish parasites have been successfully used as of Gibraltar, separating the biological indicators for host ecology and from the Mediterranean Sea. The closure of migration patterns (e.g. MACKENZIE & ABAUNZA the Rifian and Betic gateways between the 1998, KLIMPEL et al. 2003, 2006, 2008). Atlantic Ocean and the Mediterranean between MACKENZIE (1990) utilized fish parasites for 5.96 and 5.33 million years ago (LOURENS et al. stock separation of the Atlantic (Scom- 1996, KRIJGSMAN et al. 1999) led to the so-called ber scombrus) as well as MCCLELLAND & MELENDY Messinian salinity crisis (e.g. HSÜ et al. 1977, (2007) and MARCOGLIESE et al. (2003) identified DUGGEN et al. 2003), when the Mediterranean different stocks of the deepwater redfish (Sebas- was reduced to a series of hypersaline lakes with tes mentella) and American plaice (Hippoglossoides thick evaporite deposition. The opening of the platessoides). The distribution of parasitic Strait of Gibraltar about 5.33 mya at the end organisms directly depends on the distribution of the Miocene (LOURENS et al. 1996) was of the final and intermediate hosts, and thus followed by colonization events with most of these organisms can overcome wide distances the present-day fauna. Afterwards, the interplay if they infect migratory species. Otherwise, the between glacial and interglacial periods during occurrence in endemic or local host species can the Quaternary with associated marine regres- restrict the parasite’s distribution, resulting in sions and transgressions has provided many endemic and often high host specific parasites. opportunities for separation, diversification and Natural boundaries such as currents, tempe- speciation. ratures and straits can limit host and parasite The dramatic palaeogeographical and palaeo- distribution, and even artificial water ways not climatic events have played a crucial role in the necessarily extend the potential range (RÜCKERT evolutionary history of many marine taxa in et al. 2007). Studies on the occurrence of fish the Mediterranean region (e.g. TAVIANI 2002, parasites within and outside the Mediterranean DUGGEN et al. 2003, VALSECCHI et al. 2005). Sea are scarce. MARQUES et al. (2005) recorded Isolation and restriction of gene flow through plerocerci of the trypanorhynch cestode Progril- the Strait of Gibraltar has caused the existence lotia dasyatidis off the Portuguese coast, a species of endemism for several taxa, such as molluscs that was described from the Mediterranean off (GOFAS 1998) and ascidians (NARANJO et al. Tunisia (BEVERIDGE et al. 2004). KLIMPEL et al. 1998). Studies analysing the genetic structure (2007) genetically identified a population of the of Atlanto-Mediterranean marine species nematode Hysterothylacium aduncum, which reported from none (Nephrops norvegicus, STAMA- occurred inside the Mediterranean and also in TIS et al. 2004) to moderate or strong genetic the North Sea. MACKENZIE et al. (2008) analysed discontinuity between each side of the Gibraltar the parasite fauna of Atlantic horse mackerel Strait (e.g. QUESADA et al. 1995, BORSA et al. (Trachurus trachurus), identified three main fish 1997, PANNACCIULLI et al. 1997). For littoral and stocks and suggested evidence for fish migra- epipelagic species, this boundary is not regarded tion from the Atlantic populations into the as the main barrier between the Mediterranean extreme western part of the Mediterranean. The and the Atlantic. Surface currents transport role of different fish species ecology and parasite North Atlantic water as far as into the Alboran life cycle strategies to enable transfer inside and Sea (TINTORE et al. 1998). The resulting front outside the Mediterranean through the Gibraltar system (Almeria-Oran line) seems to mark the Strait has not yet been studied in detail. main barrier between Atlantic and Mediter- Goatfishes of the family Mullidae consist of ranean populations (MALDONALDO & URIZ 1995, approximately six genera and over 60 species QUESADA et al. 1995, PANNACCIULLI et al. 1997). (FROESE & PAULY 2008). The red mullet Mullus

26 surmuletus is one of the most abundant fish and 2.5 m), were examined for parasites and stomach widespread distributed in the sublitoral zone contents (fig. 1). All fishes were deep frozen along the Eastern Atlantic, from the North Sea immediately after catch for subsequent to the northern part of West Africa and the examination in the laboratory of the Heinrich- Mediterranean Sea. Mullus surmuletus mainly Heine-University. Prior examination, each fish occurs on broken and rough grounds but also specimen was defrosted at 0-1 °C. Morpho- over sand and soft bottoms in less than 100 m metrical data including the standard length (SL) water depth. It can be also found down to 400 m, and total weight (TW) were recorded to the where it feeds on benthic invertebrates and nearest 0.1 cm and 0.1 g. vertebrates, such as crustaceans (Decapoda, Amphipoda), polychaetes, molluscs and small 2.2. Parasitological examination fishes (FROESE & PAULY 2008). According to previous parasitological studies, Mullus surmuletus The eyes, skin, fins, gills, nostrils and mouth is highly infected with parasites in the Mediter- cavity of each fish specimen were studied for ranean Sea, hosting approximately 28 different ectoparasites. The body cavity was opened to species (e.g. HRISTOVSKI et al. 1989, BARTOLI & examine microscopically the liver, stomach, BRAY 1996, LE POMMELET et al. 1997, FERRER et pyloric caeca, intestine and gonads for endo- al. 2005, FERRER-CASTELLÓ et al. 2007). Studies parasites. Collected Acanthocephala were trans- from the North Sea region, however, are lacking ferred to freshwater allowing evagination of the (e.g. PALM et al. 1999). proboscis prior to fixation. All other isolated The purpose of the present study is an parasites were directly fixed in 4% borax- analysis of the parasite fauna of the red mullet buffered formalin and preserved in 70% Mullus surmuletus, covering its range of distribu- ethanol/5% glycerine. For identification tion in the North Sea and Mediterranean. An purposes, Nematoda and Acanthocephala were examination of the stomach content reveals dehydrated in a gradated ethanol series and information on the main prey items in the transferred to 100% glycerine (RIEMANN 1988). different regions. The comparison of the fish Digenea and Cestoda were stained with acetic stomach content between the Mediterranean carmine, dehydrated, cleared with Eugenol or and the North Sea can indicate different feeding Creosote and mounted in Canada balsam. ecology and importance of Mullus surmuletus for Crustacea were dehydrated and transferred into the parasite´s life cycle in these habitats. Possible Canada balsam. Parasite identification literature explanations for the observed patterns are given, included original descriptions. The parasito- discussing the role of the Strait of Gibraltar for logical terms follow BUSH et al. (1997): pre- the fish parasite distribution. valence (P) is the number of infected fish with one or more individuals of a particular parasite 2. Materials and methods species (or taxonomic group) divided by the number of hosts examined (expressed as a 2.1. Sample Collection percentage); intensity (of , I) is the number of individuals of a particular parasite Fish samples were collected in 2005 between species in a single infected host (expressed as a late August and November. A total of 167 numerical range); mean intensity (of infection, Mullus surmuletus (red mullet), 52 specimens mI) is the average intensity, in other words, the from the North Sea (N, 53°-55°N 003°-005°E, total number of parasites of a particular species mean catch depth 26.6 m, range 10.2 to 40.1 found in a sample divided by the number of m), 34 from the Ligurian Sea (L, 43°N 005°E, infected hosts; and mean abundance (A) is the catch depth 2.0 m), 33 from the Tyrrhenian Sea total number of individuals of a particular (T, 38°N 14°E, catch depth 3.0 m) and 48 from parasite species in a sample of a particular host the Adriatic Sea (A, 45°N 13°E, catch depth species divided by the total number of hosts

Bull. Fish Biol. 10 (1/2) 27 Fig. 1: Map of the areas of investigation: N = North Sea, L = Ligurian Sea, T = Tyrrhenian Sea, A = Adriatic Sea. Abb. 1: Karte mit den Untersuchungsgebieten: N = Nordsee, L = Ligurisches Meer, T = Tyrrhenisches Meer, A = Adriatisches Meer. of that species examined, including both and the frequency of occurrence (F %) were infected and uninfected hosts. determined (HYSLOP 1980). Using these three indices, an index of relative importance IRI 2.3. Analysis of stomach contents (PINKAS et al. 1971) was calculated. The importance of a specific prey item increases The stomach contents were sorted and food with higher values for N, W, F and IRI. items were identified to the lowest possible taxon and grouped into taxonomic categories. 3. Results In order to determine the relative importance of food items, the numerical percentage of prey The analysis of 167 Mullus surmuletus from one (N %), the weight percentage of prey (W %), representative location in the North Sea and

28 from three different geographical regions in the North Sea and the samples from the Mediter- Mediterranean Sea revealed a more species rich ranean (figs. 2, 3). More parasite species were parasite fauna in the North Sea compared to found in/on M. surmuletus from the North Sea the Mediterranean samples, where also endemic (ten) compared to the specimens from the parasites occur. A total of 14 different parasite Mediterranean (four to seven). The nematodes species were found. The prevalence, intensity, s.l. and Capillaria gracilis as well mean intensity and abundance for each parasite as the acanthocephalan Corynosoma strumosum and sample station are given in table 1. Sixteen and the crustaceans Caligus elongatus and different prey items were identified from the Lernaeocera branchialis were isolated only from stomach contents, belonging to the Bryozoa, the North Sea sample (tab. 1). In contrast the Mollusca, Annelida, Crustacea, Echinodermata digeneans Holorchis legendrei, Opecoeloides furcatus and Teleostei (tab. 2). and Timonia mediterranea solely occurred in the Mediterranean Sea (tab. 1). While the digenean 3.1. Parasite fauna and diversity Derogenes varicus was isolated from fish sampled in the North Sea and Ligurian Sea (western part The parasite fauna of Mullus surmuletus from four of the Mediterranean), both digeneans H. investigated locations consisted of ten (North legendrei and T. mediterranea were found only in Sea), seven (Ligurian Sea), four (Tyrrhenian Sea) fish samples from the Adriatic Sea (eastern part and six (Adriatic Sea) species, respectively (tab. of the Mediterranean) (tab. 1). 1). The digeneans, Derogenes varicus, Holorchis legendrei, Opecoeloides furcatus and Timonia mediterranea, 3.3. Feeding ecology occurred as adults in the digestive tract. Larval tetraphyllidean cestodes were isolated at a low The diet composition analysis of specimens infestation rate from the intestine. These from the different locations showed that M. tetraphyllideans are circumpolar distributed and surmuletus was feeding mainly on crustaceans, have been found in various fish species. However, such as different (harpacticoid, further identification is not possible without calanoid, see tab. 2), euphausiids, decapods and strobila characters or knowledge of the life cycle. amphipods. Benthic molluscs (gastropods, Four nematode species, Anisakis simplex s.l., bivalves) and polychaets, however, also Ascarophis valentina, Capillaria gracilis and represented an important part of the diet. The Hysterothylacium aduncum, were found. Ascarophis food of M. surmuletus consisted of 13 (North valentina and C. gracilis occurred as adults, A. simplex Sea), 14 (Ligurian Sea), 11 (Tyrrhenian Sea) and s.l. as third stage larvae (L3), while H. aduncum 16 (Adriatic Sea) different prey items, was isolated in the larval (L3-L4) and adult stage. respectively (tab. 2). The most diverse food The adult nematodes were isolated from the composition was found for Mullus surmuletus stomach lumen, pyloric caeca and intestine, while from the Adriatic Sea compared with the other the larvae were found exclusively in or on the locations. The most important prey categories organs of the body cavity. The cystacanth of of M. surmulteus from the North Sea were Corynosoma strumosum (Acanthocephala) was polychaets, having an Index of Relative located in the body cavity of a single M. surmuletus. Importance (IRI) of 2185.51, followed by Two adult crustaceans (Caligus elongatus, Hatschekia copepods (981.78) and euphausiids (318.04). mulli), larval stages of Gnathia sp. and juveniles of The main important prey items in the Ligurian Lernaeocera branchialis were located on the gills. Sea were amphipods (IRI 4648.79), copepods (1317.64) and gastropods (206.21). The prey 3.2. Regional parasite distribution composition of M. surmuletus from the Tyrrhenian Sea was predominated by decapods There are some obvious differences in the (6735.85), amphipods (4451.11) and parasite fauna of Mullus surmuletus from the euphausiids (3314.08), while the food

Bull. Fish Biol. 10 (1/2) 29 von vier geographisch unterschiedlichen Gebieten. P = Prävalenz, mI = mittlere Intensität, I = Intensität, A = mI = mittlere Intensität, I vier geographisch Gebieten. P = Prävalenz, unterschiedlichen von from four geographical locations. P = prevalence, mI = mean intensity, I = intensity, A = mean abundance. I = intensity, mI = mean intensity, geographicalfrom four locations. P = prevalence, Mullus surmuletus Mullus surmuletus Metazoan in/on parasites in/auf Metazoische Parasiten Tab. 1: Tab. Tab. 1: mittlere Abundanz.

30 Tab. 2: Frequency of occurrence (F), numerical percentage of prey (N), weight percentage of prey (W) and index of relative importance (IRI) of the food items identified from the stomach contents of Mullus surmuletus from four geographical locations. SL = fish standard length, TW = fish total weight. Tab. 2: Prozentuales Vorkommen (F), prozentuale Anzahl (N), prozentuales Gewicht (W) und Index der relativen Bedeutung der jeweiligen Nahrungsorganimsen isoliert aus den Mägen von Mullus surmuletus von vier geographisch unterschiedlichen Gebieten. SL = Fischstandardlänge, TW = Fischgewicht.

Bull. Fish Biol. 10 (1/2) 31 Tab. 2: continued. Tab. 2: Fortsetzung

32 Fig. 2: Parasite composition of Mullus surmuletus from four geographical locations. N = North Sea, L = Ligurian Sea, T = Tyrrhenian Sea, A = Adriatic Sea, P = prevalence. Abb. 2: Parasitenzusammensetzung von Mullus surmuletus von vier verschiedenen geographsichen Bereichen. N = Nordsee, L = Ligurisches Meer, T = Tyrrhenisches Meer, A = Adriatisches Meer, P = Prevalenz.

Fig. 3: Distribution of the recorded parasites in Mullus surmuletus of the North Sea (Atlantic Ocean) and the Mediterranean Sea (based on literature records and present study). Abb. 3: Verbreitung der nachgewiesenen Parasitenarten von Mullus surmuletus aus der Nordsee (Atlantischer Ozean) und dem Mittelmeer (basierend auf Literaturdaten und auf Daten der vorliegenden Arbeit).

Bull. Fish Biol. 10 (1/2) 33 composition in the Adriatic Sea was dominated Especially the crustaceans have been recorded by polychaets (1890.50), molluscs (1145.15, as important intermediate hosts for fish hel- including bivalves and gastropods), euphausiids minths (MARCOGLIESE 2002), being important (918.36), harpacticoid copepods (876.69) and transmitters for cestodes, nematodes and also amphipods (802.54) (tab. 2). acanthocephalans. Consequently, these taxa are commonly found in red mullets, with FERRER- 4. Discussion CASTELLÓ et al. (2007) recording 15 species from the western Mediterranean. The richest food The present study is the first large scale investi- range was observed for red mullets from the gation of red mullet (Mullus surmuletus) fish Adriatic Sea, feeding on polychaets, molluscs, parasites over its range of distribution from the amphipods, copepods and euphausiids (tab. 2). mid-Mediterranean to the North Sea. The The parasite diversity of red mullets in the parasite richness and abundance was different North Atlantic is less studied, and only three between the studied regions (North Atlantic vs. different parasite species (Lecithochirium musculus Mediterranean Sea) and localities (e.g. Ligurian (Digenea), Nybelinia riseri (Cestoda), Breizacanthus Sea), demonstrating peculiarities of habitats and chabaudi (Acanthocephala)) with a wide host parasite distribution. Having ten parasite species range and zoogeographical distribution are in the sampled North Sea location compared known (GOLVAN 1969, GIBSON & BRAY 1986, to four to seven species in the Mediterranean PALM & WALTER 2000). Hysterothylacium aduncum Sea, mullets in the North Sea (North Atlantic) is the most prevalent nematode species in the appeared to be more parasite rich than their North Atlantic (e.g. KLIMPEL & RÜCKERT 2005), Mediterranean counterparts. A total of 14 infecting a various intermediate and final parasite species were found over the whole hosts. Derogenes varicus is one of the most range, including endoparasitic helminths and common and least host specific fish digenean ectoparasitic crustaceans. Most common were in the Atlantic, and tetraphyllidean cestodes the digenean Opecoeloides furcatus and the occur from the North Sea towards the Iberian nematode Hysterothylacium aduncum, followed by Peninsula. These species were also collected both crustaceans Gnathia sp. and Hatschekia during the present study, occurring in the fish mulli. However, a rich red mullet parasite infra- from the North Sea and also the Mediterranean. community consisting of 17 different species Derogenes varicus and tetraphyllidean cestodes also from three different Mediterranean ports of infected mullets in the Mediterranean. Both has been recently recorded by FERRER- species usually utilize pelagic crustaceans such CASTELLÓ et al. (2007). These authors also as copepods as intermediate hosts (e.g. KØIE considered the above species being the most 1979, KLIMPEL et al. 2003, 2008). Capillaria common parasites of M. surmuletus in the gracilis, Corynosoma strumosum and Lernaeocera Mediterranean Sea (e.g. FERRER-CASTELLÓ et al. branchialis were collected only from red mullets 2007). Thus, a total of ten different parasite in the North Sea, having few or no records from species are known from the North Sea the Mediterranean Sea (e.g. HRISTOVSKI et al. compared with 24 (including the new records) 1989, LE POMMELET et al. 1997, FERRER-CAS- species in the Mediterranean. TELLO et al. 2007). These species are common Because of the benthic life and a wide range in the North Atlantic, and might only acci- of prey items, red mullets are suitable hosts for dentally occur in the Mediterranean through a variety of helminth fish parasites transferred their migrating hosts. through the marine food web. The stomach The crustaceans Gnathia sp. and Hatschekia content analysis of the studied M. surmuletus mulli and the nematode H. aduncum were revealed a total of 16 different prey items, recorded from the North Sea (Atlantic Ocean) belonging to the Bryozoa, Mollusca, Annelida, throughout the Adriatic Sea. KLIMPEL et al. Crustacea, Echinodermata and Teleostei. (2007) studied the genetic diversity of H.

34 aduncum from the Mediterranean to the North took place in the Mediterranean region (e.g. Sea and differentiated two genotypes. The TAVIANI 2002, DUGGEN et al. 2003), playing a Mediterranean type corresponded to specimens crucial role in the evolutionary history of from the North Sea, demonstrating gene flow several marine taxa as well as shaping the between both populations. This is not astonish- present biogeography and biodiversity of the ing, considering low host specificity of H. regional ichthyofauna (e.g. NIKULA & VÄINÖLÄ aduncum in a wide range of also migrating host 2003, VALSECCHI et al. 2005). The combination fish species. A similar result could be demon- of the opening and closing of the Strait of strated by the infection of mullets from all Gibraltar, advances and contractions of glacia- studied locations with the less host specific tion, and changes in current patters appears to larval isopod Gnathia sp. An interesting result have made the northeast Atlantic/Mediterra- is the occurrence of the parasitic copepode H. nean area a notable generator of diversity (PAN- mulli in the Mediterranean Sea and the North NACCIULLI et al. 1997). DANDO & SOUTHWARD Sea. Though it cannot be decided at present if (1981) hypothesized that the history of the the sampled specimens belong to the same or Mediterranean combined with the present different populations, this red mullet specific hydrographic pattern might have promoted and parasite might also migrate between the Medi- maintained divergence of the Mediterranean terranean and the North Sea (fig. 3). populations. Following the Messinian salinity The parasite fauna of red mullets in the crisis (HSÜ et al. 1977, MCCULLACH & DE- Mediterranean is characterized by digeneans DECKKER 1989), communication between the and nematodes, with the occurrence of species Atlantic and Mediterranean was reestablished, specific crustaceans. The predominant parasites and fully marine conditions were restored in the Mediterranean within the present study during the Pliocene (5.33 to 1.8 mya). During were the digeneans H. legendrei, Opecoeloides the Pleistocene (1.8 mya to 10.000 ya) and furcatus, Timonia mediterranea (the both latter are particularly during the Quaternary, a series of endemic species) and the crustaceans H. mulli glacial and interglacial periods with associated and Gnathia sp., while nematodes, cestodes and marine regressions and transgressions affected acanthocephalans were rare or missing. A similar the area (BLANC 1968). Atlantic and Mediter- result was presented by FERRER-CASTELLÓ et al. ranean fish populations together with their (2007), who identified these species at similar parasites presumably became physically isolated high prevalence and abundances. The stomach during these cycles. This historical separation content analyses within the present study of mullet parasites can be seen as a reason that revealed similar rich prey items for Mediter- some of the recorded digeneans O. furcatus, T. ranean mullets compared with the North Sea mediterranea and the nematode A. valentina are fish. Such wide range of invertebrates might endemic for the Mediterranean and do not explain the occurrence of two endemic dige- occur in the North Sea (fig. 3). Indeed, O. nean and one endemic nematode species (FER- furcatus, T. mediterranea and A. valentina have not RER-CASTELLÓ et al. 2007 and present study). been recorded outside the Mediterranean (e.g. Species of the Holorchis, in our case H. LE POMMELET et al. 1997, BARTOLI & BRAY 1996, legendrei, involve gastropods and bivalves as JOUSSON & BARTOLI 2000, FERRER et al. 2005). intermediate hosts in their life-cycle (JONES et al. 2005). 5. Conclusion The parasite fauna of red mullets in the Mediterranean is the consequence of recent According to the observed parasite fauna of parasite speciation and adaptation together with red mullets from the North Sea (North Atlantic) host-parasite co-evolution, possibly influenced compared with the Mediterranean, the record by palaeogeographical and palaeoclimatic of several endemic species suggests the idea events. It is well known that dramatic events of Mediterranean parasite populations that do

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