Marine Biodiversity Records, page 1 of 4. # Marine Biological Association of the United Kingdom, 2011 doi:10.1017/S1755267211000558; Vol. 4; e57; 2011 Published online Notes on the occurrence of Syngnathus rostellatus (Teleostei: Syngnathidae) in the Mediterranean pascal i. hablu¤tzel1,2 and anthony b. wilson1 1 Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland, 2Laboratory of Animal Diversity and Systematics, K.U. Leuven, Charles Deberiotstraat 32, B-3000 Leuven, Belgium Syngnathus rostellatus is a nearshore pipefish species whose distributional range extends along the European Atlantic coast between Bergen (NO) and the Bay of Biscay (ES). Several recent articles suggest that this species has experienced a major range expansion of more than 4000 km into the eastern Mediterranean, but a critical review of these studies indicates that the majority of these reports are based on specimen misidentifications. Considering a reliable report of S. rostellatus from the Mediterranean coast near Gibraltar, it appears that the current distribution of this species is restricted to the north-eastern Atlantic Ocean and the southern Mediterranean coast of the Iberian Peninsula. Keywords: range expansion, species identification, Syngnathus rostellatus, pipefish Submitted 17 November 2010; accepted 8 April 2011 INTRODUCTION There is increasing evidence that human-mediated environmental changes, including the erosion of geographical barriers, the introduction of exotic species, and habitat degradation, are influencing the distribution of species (e.g. Rahel, 2007; Hiddink & ter Hofstede, 2008). The accelerated rate of human modifications of the natural environment is paralleled by an increasing number of reports documenting extensions and contractions of the historical ranges of many species (e.g. Sax & Gaines, 2003; Azzurro, 2008; Thomas, 2010). The value of these studies is entirely dependent on the accurate identification of specimens, and the misidentification of material can lead to erroneous conclusions of major shifts in species’ ranges. Close to 40 nominal species of the globally-distributed genus Syngnathus are currently recognized in the Eschmeyer’s Catalogue of Fishes (2010). Of these, eleven are known to occur in Europe, making this the most species-rich group of syngnathid fish in the region (Dawson, 1986). While nine of these species names are in common use (e.g. Dawson, 1986), two species from the Black Sea (S. affinis, Eichwald, 1831 and S. argentatus, Pallas, 1814) were only recently reinstated by Kuiter (2009). Kuiter (2009), however, provides no justification for the reinstatement of these species names, and a more systematic analysis of Black Sea pipefish will be necessary in order to clarify their species status. The taxonomic status of at least two additional species is also unclear. The nearshore S. agassiz Michahelles, 1829 sensu Canestrini (1872) was synonymized with S. abaster by Corresponding author: P.I. Hablu¨tzel Email: pascal.habluetzel@bio.kuleuven.be Lueken (1967), but this species was reinstated by Roig (1979) on the basis of an exhaustive analysis of historical and contemporary collections from the Balearic Islands and Spanish coast, a Spanish-language report that appears to have been overlooked by subsequent researchers. Genetic and morphometric analyses of pipefish material from the Mediterranean and Black Seas suggest that S. nigrolineatus Eichwald, 1831 may also represent a distinct species (Hablu¨tzel & Wilson, unpublished data). Clearly, the taxonomy of Syngnathus pipefish is in a state of flux, and the genus is in need of a full systematic revision. Of the nine commonly-recognized species, two (S. phlegon Risso, 1827 and S. schmidti Popov, 1928) are pelagic, while the others (S. abaster Risso, 1827 sensu Canestrini (1872), S. acus Linnaeus, 1758, S. rostellatus Nilsson, 1855, S. taenionotus Canestrini, 1871, S. tenuirostris Rathke, 1837, S. typhle Linnaeus, 1758 and S. variegatus Pallas, 1811) are all nearshore inhabitants (Dawson, 1986), and are dominant members of nearshore eelgrass habitats along the European coastline. Syngnathus rostellatus (Nilsson’s pipefish) was originally described from western Sweden (Nilsson, 1855), and the northern French S. dumerilii Moreau, 1870 in Dume´ril (1870) is now considered a junior synonym of this species (Fries et al., 1895; Wheeler, 1973). Ehrenbaum (1905 –1909) described the distribution range of S. rostellatus as the Atlantic coast between Bergen and the Sea of Biscay (Figure 1). Syngnathus rostellatus is found at moderate densities in the Kattegat of western Sweden, and while there are scattered reports of individual specimens in the southern Baltic (e.g. Ehrenbaum, 1905–1909; Otterstøm, 1917), a recent exhaustive survey of this region failed to detect this species (HELCOM, 2007). These earlier descriptions have been complemented by subsequent reports of S. rostellatus from the northern Irish coast (Douglas & Egan, 1983) and sites as far south as Ma´laga, 1 2 pascal i. hablu¤ tzel and anthony b. wilson Spain (Helling (1943); Reina-Herva´s et al. (1981–1982)) (Figure 1). Syngnathus rostellatus has recently been reported from sites within the Mediterranean as far east as southern Turkey (Louisy, 2002; Go¨koglu et al., 2004; Ben Amor et al., 2008) (Figure 1), suggesting that this species may be experiencing a major range extension. Here, we provide a morphological diagnosis of S. rostellatus, and use this tool to evaluate recent reports of S. rostellatus outside its historical distributional range (Dawson, 1986). Our analyses indicate that the majority of these recent reports stem from the misidentification of specimens and that the distribution of this species remains restricted to the north-eastern Atlantic Ocean and the Mediterranean coast of the Iberian Peninsula. MATERIALS AND METHODS Pipefish individuals were identified on the basis of the meristic and morphometric data provided in the original articles and, if available, from pictures. The original description of Syngnathus rostellatus by Nilsson (1855), together with subsequent descriptions by Moreau in Dume´ril (1870) and Dawson (1986) were used as references, and these descriptions were supplemented with the analysis of ethanol-preserved specimens from northern Spain (Sada) and western Sweden (Fiskeba¨ckskil) (Table 1). Methods for the measurements and meristic counts used in this article follow Dawson (1986). RESULTS Identification Syngnathus rostellatus differs from all other European species of the genus by the following combination of characters: distal Fig. 1. The traditional distribution of Syngnathus rostellatus according to Dawson (1986) (black), extended by reports from the Irish (Douglas & Egan, 1983), Portuguese (Almeida, 1986) and Spanish (Reina-Herva´s et al., 1981 – 1982) coasts and the southern Baltic Sea (Ehrenbaum, 1905 – 1909; Otterstøm, 1917) (grey); collection localities of S. rostellatus discussed in the text are indicated (circles), as are reports of S. rostellatus based on apparent misidentifications of specimens (stars). margins of body rings without spine-like points; 13– 17 trunk rings; 35– 42 tail rings; 32 –45 dorsal fin rays; 10– 13 pectoral fin rays; lack of brown dots in the dorsal fin; and small size (,17 cm total length (TL)) (Table 1). While the meristic counts of the Black Sea population of S. abaster (S. abaster nigrolineatus sensu Berg (1949)) overlap with those of S. rostellatus, this species can be clearly distinguished from S. rostellatus both morphologically and genetically (Hablu¨tzel & Wilson, unpublished data)). Distribution Almeida (1986) reported 12 S. rostellatus specimens (including 8 pregnant males) from Vila Nova de Milfontes (PT) (Figure 1). The reproductive status of the individual specimens was not indicated in the original paper, but the data provided indicate that the smallest pregnant male in this collection had a TL of ≤ 12.1 cm. Syngnathus rostellatus, S. abaster, S. agassiz and S. typhle are the only four coastassociated species of Syngnathus in western Europe which are reported to reach sexual maturity at this size. Syngnathus abaster has fewer dorsal fin rays ( ≤ 31), S. agassiz has less tail rings ( ≤ 35) and S. typhle has more pectoral fin rays ( ≥ 14) than does S. rostellatus (Table 1). The meristic counts of the specimens collected by Almeida (1986) are thus consistent with the identification of these specimens as S. rostellatus (Table 1). Almeida (1986) also re-examined specimens from Praia de Mira (PT) (Figure 1) collected by Helling (1943) and identified these individuals as S. rostellatus. On the basis of the details provided in Almeida (1986), we conclude that all of these individuals are indeed S. rostellatus. Reports of S. rostellatus from Ma´laga (Figure 1) by Lozano & Rey (1919) and Reina-Herva´s et al. (1981 –1982) also appear to be reliable. While details on the specimens analysed by Lozano & Rey (1919) were not provided in the original publication, Reina-Herva´s et al. (1981 –1982) provided detailed information on five specimens collected from the same region. The low number of trunk rings detected in these specimens (16 –17; Table 1) clearly separates them from juvenile S. acus (trunk rings: 18 –19) which are otherwise similar in their general appearance. The S. rostellatus from Ma´laga also differ from S. abaster, S. agassiz and S. typhle in meristic counts (see above). In contrast to these reliable reports of S. rostellatus from outside its historical range, several recent descriptions of S. rostellatus from sites in Tunisia and Turkey (Figure 1) appear to be in error. Photographs of the individuals included in both of these studies are provided in the original articles (Go¨koglu et al., 2004; Ben Amor et al., 2008). Both pictures show large (18.7 cm and 21.1 cm TL), long-snouted species with high numbers of trunk rings (18 for the Tunisian and . 17 for the Anatolian individual (note that Go¨koglu et al. used a non-standard trunk counting method which differs from other publications of syngnathid pipefish (e.g. Dawson, 1986))), indicating that neither of these specimens are S. rostellatus (Table 1; Figure 2). The specimens illustrated by Go¨koglu et al. (2004) and Ben Amor et al. (2008) most closely resemble either S. tenuirostris or S. acus (Figure 2), species which are known to occur in the Mediterranean region (Kaup, 1856; Dawson, 1986). Louisy (2002) reported a single S. rostellatus female from Banyuls-sur-Mer, France (Figure 1). The author did not occurrence of syngnathus rostellatus in mediterranean Table 1. Meristic characters of Syngnathus rostellatus from the original species description (Nilsson, 1855) and from more recent studies of the species. Morphological data for specimens outside the expected range for S. rostellatus are indicated in bold. Location N Trunk rings Tail rings Dorsal fin rays Pectoral fin rays Length of largest specimen (cm TL) Conclusion Reference Sweden n.a. 16 40 32–34 10 S. rostellatus Nilsson, 1855 Coˆte du Haˆvre (FR) Europe Sada (ES) Fiskeba¨ckskil (SE) Vila Nova de Milfontes (PT) Praia de Mira (PT) Ma´laga (ES) n.a. n.a. 30 9 12 6 5 14 13–17 14–16 14–15 14–16 15 16–17 36–39 37–42 39–42 39–41 35–42 39–42 34–41 34–36 33–45 37–42 38–43 34–40 37–42 36–38 11–12 10–13 10–12 11–12 10–11 11 11–12 12.4–14.8 (5–6 tum) 10.3 17.0 13.0 13.7 14.0 16.9 n.a. S. rostellatus S. rostellatus S. rostellatus S. rostellatus S. rostellatus S. rostellatus S. rostellatus Gulf of Tunis (TN) Anatolian coast (TR) Banyuls-sur-Mer (FR) Wismar (DE) 1 1 1 2 18 > 17 n.a. n.a. 39 41 n.a. n.a. 35 33 29 or 30 n.a. 12 13 n.a. n.a. 21.1 18.7 n.a. n.a. Syngnathus sp. Syngnathus sp. S. abaster S. typhle Moreau in Dume´ril, 1870 Dawson, 1986 This study This study Almeida, 1986 Almeida, 1986 Reina-Herva´s et al., 1981–1982 Ben Amor et al., 2008 Go¨koglu et al., 2004 Louisy, 2002 Kuiter, 2009 N, number; 1 tum ¼ 2.47 cm. provide meristic data, but included two colour pictures of the living specimen. The low number of dorsal fin rays (29 or 30; Table 1) and the flattened form of the snout (versus the slightly convex snout of S. rostellatus (Figure 2)) suggest that the specimen is actually S. abaster. The report of S. taenionotus from southern France in Louisy (2002) also appears to be in error, and is based on an apparent misidentification of a S. typhle individual (data not shown). Unfortunately, the photographs and identifications used by Louisy (2002) have been incorporated into a recent global survey of syngnathid species (Kuiter, 2009), further propagating these errors. Confusion about the distributional range of S. rostellatus also exists at its north-eastern periphery in the southern Baltic Sea. Kuiter (2009) recently reported two specimens from Wismar, Germany. We argue that both pictured specimens are misidentified and in fact are S. typhle, recognizable by the elevation of the snout evident in these individuals, Fig. 2. Photographs of the head morphology of the nearshore Syngnathus species discussed in this article, along with an indication of the collection locality of the individual specimens. (A) Syngnathus abaster, Scardovari (IT); (B) S. acus, Tasende (ES); (C) S. agassiz, Naples (IT); (D) S. rostellatus, Sada (ES); (E) S. taenionotus, Scardovari (IT); (F) S. tenuirostris, Bosphorus (TR); (G) S. typhle, Venice (IT); (H) S. variegatus, Crimea (UA). Scale bar: 1 cm. Pictures (A– E, G) taken from specimens collected by the authors and collaborators (A, B, D, E, G) or from the collections of the Senckenberg Museum in Frankfurt (C, SMF 8334 and the Muse´um National d’Histoire Naturelle in Paris (F, MNHN 0000-6132; H, MNHN 0000-6134). Drawings (F, H) after Rathke (1837), see Kuiter (2009) for photographs of these species. diagnostic for this species (see Figure 2). One of the two specimens also shows a colour pattern of white spots which is known only from juvenile S. typhle and is not found in S. rostellatus. The lasting impact of historical errors on the European biogeography of Syngnathus Dawson’s (1986) key to European syngnathid species has been an important reference for researchers working on European Syngnathus species. Unfortunately, an error in the illustration included in this text has perpetuated confusion relating to species-level identification. While the meristic counts provided in Dawson (1986) are accurate, the illustration of S. rostellatus included in this report was derived from a sketch originally published in Fries et al. (1895) and subsequently reprinted by Poll (1947) in his review of Belgian marine fish. Unfortunately, while the original illustration (Fries et al., 1895) referred to S. typhle (plate XXIX, figure 1), Poll (1947) mislabelled this specimen as S. rostellatus in both the text and the figure legend of his book (p. 186, figure 126), and Dawson kept this description in his text. Poll (1947) made a second labelling error in his Fauna de Belgique, including an illustration of S. rostellatus originally published in Fries et al. (1895) in his description of S. typhle (plate XXVIII, figure 8b; note that this specimen is also inconsistently labelled as both S. rostellatus and S. acus in the original publication). Such labelling errors have undoubtedly contributed to the confusion surrounding the identification of European Syngnathus species, and we have attempted to remedy this situation here, including photographs of all of commonly recognized nearshore Syngnathus species known to occur in this region (Figure 2). CONCLUSIONS Considering the reliable reports of S. rostellatus from the Portuguese and the Spanish Mediterranean coasts, we suggest that the current range of S. rostellatus is broader than that indicated by Dawson (1986). The contemporary 3 4 pascal i. hablu¤ tzel and anthony b. wilson range of this species extends from the Norwegian coast as far south as the western Mediterranean at Ma´laga, Spain (Figure 1). This distributional pattern coincides with the present frontal system between Almeria and Oran, which separates Atlantic waters to the west from Mediterranean waters to the east (Tintore et al., 1988). Reports of S. rostellatus from Mediterranean sites east of Ma´laga appear to be erroneous, and stem from specimen misidentifications. HELCOM (2007) HELCOM Red list of threatened and declining species of lampreys and fish of the Baltic Sea. Baltic Sea Environmental Proceedings 109, 1 –40. ACKNOWLEDGEMENTS Hiddink J.G. and ter Hofstede R. (2008) Climate induced increases in species richness of marine fishes. Global Change Biology 14, 453–460. We thank Alexandra Wegmann and Jasmin Winkler for their assistance in species identification. Filip Volckaert and two anonymous referees provided helpful comments on an earlier draft of this article. We further thank the SMF and MNHN for access to their pipefish collections. The study was supported by the University of Zurich, Switzerland. the Anatolian coast (Mediterranean Sea). Journal of the Marine Biological Association of the United Kingdom 84, 1093–1094. Helling H. (1943) Novo cata´logo de peixes de Portugal em colecc¸a˜o no Museu de Zoologia da Universidade de Coimbra. Memo´rias e Estudos do Museu Zoolo´gico da Universidade de Coimbra s. 1(149), 1 –110. Kaup J.J. (1856) Catalogue of lophobranchiate fish in the collection of the British Museum. London: British Museum. Kuiter R.H. (2009) Seahorses and their relatives. Seaford: Aquatic Photographics. Louisy P. (2002) Meeresfische: Westeuropa, Mittelmeer. Stuttgart: Verlag Eugen Ulmer. REFERENCES Lozano y Rey L. (1919) Los Peces de la Fauna Ibe´rica en la Colleccio´n del Museo en 1 de enero de 1919. Trabajos del Museo Nacional de Ciencias Naturales Seria Zoolo´gica 39, 1–112. Almeida A.J. (1986) Presence des poissons Syngnathus rostellatus (Syngnathidae), Clinitrachus argentatus (Clinidae) et Sphoeroides spencleri (Tetraodontidae) sur la coˆte du Portugal. Cie¨ncia Biolo´gica: Ecology and Systematics (Portugal) 6, 1 –7. Lueken W. (1967) Su¨sswasserfische der Tu¨rkei—5. Teil Syngnathidae. Mitteilungen Hamburgisches Zoologisches Museum und Institut 64, 127–146. fishes in the questions. In Mediterranean 35 in CIESM Nilsson S. (1855) Skandinavisk fauna. Fjerde Delen: Fiskarna. Lund: Berlingska Boktryckeriet. Ben Amor M.M., Ben Salem M., Ben Soussi J. and Capape´ C. (2008) Occurrence of Nilsson’s Pipefish Syngnathus rostellatus (Osteichthyes: Syngnathidae) in the Gulf of Tunis (Central Mediterranean). Vie et Milieu—Life and Environment 58, 189–192. Poll M. (1947) Faune de Belgique: poissons marins. Brussels: Musee´ Royal d’Histoire Naturelle de Belgique. Azzurro E. (2008) The advance of thermophilic Mediterranean Sea: overview and methodological CIESM Climate warming and related changes in marine biota. Monaco: CIESM, pp. 39–45. [No. Workshop Monographs, F. Briand (ed.).] Berg L.S. (1949) Fresh-water fishes of Soviet Union and adjacent countries. III. Fresh-water Fish. USSR Guide Fauna No. 30. Washington, DC: Smithsonian Institution, by Israel Program of Scientific Translation, pp. 927–1382. [In Russian, English translation available, 1965.] Canestrini G. (1872) Fauna d’Italia—Parte terza—Pesci. Milano: Dottor Francesco Vallardi. Dawson C.E. (1986) Syngnathidae. In Whitehead P.J.P., Bauchot M.-L., Hureau J.-C., Nielson J. and Tortonese E. (eds) Fishes of the Northeastern Atlantic and the Mediterranean, volume II. Paris: UNESCO, pp. 628–639. Douglas D.J. and Egan D. (1983) The distribution of Syngnathus rostellatus Nilsson (Pisces: Syngnathidae) in Irish coastal waters. Irish Naturalists’ Journal 21, 173–175. Dume´ril A.H.A. (1870) Histoire Naturelle des Poissons ou Ichthyologie Ge´ne´rale. Tome Second. Ganoı¨des, Dipne´s, Lophobranches. Paris: Librairie Encyclope´dique de Roret. Ehrenbaum E. (1905–1909) I. Eier und Larven von Fischen. In Ehrenbaum E. (ed.) Nordisches Plankton—Zoologischer Teil—Erster Band—Eier und Larven von Fischen, andere Eier und Cystem. Kiel und Leipzig: Verlag von Lipsius & Tischer, pp. 1–414. Eschmeyer W.N. (ed.) (2010) Catalogue of fishes. Electronic version (25 October 2010). http://research.calacademy.org/ichthyology/catalog/ fishcatmain.asp Fries B., Ekstro¨m C.U. and Sundevall C.J. (1895) A history of Scandinavian fishes. Part II. 2nd edition, revised and completed by Professor F.A. Smitt. Stockholm: P.A. Norstedt & So¨ner. Go¨koglu M., Bodur T. and Kaya Y. (2004) First records of Hippocampus fuscus and Syngnathus rostellatus (Osteichthyes: Syngnathidae) from Otterstøm C.V. (1917) Danmarks Fauna—Fisk III. Fastkæbede, Buskgællede, Ganoider, Tværmunde og Rundmunde. Copenhagen: G.E.C. Gads Forlag. Rahel F.J. (2007) Biogeographic barriers, connectivity and homogenization of freshwater faunas: it’s a small world after all. Freshwater Biology 52, 696–710. Reina-Herva´s J.A., Mun˜oz R. and Blasco M. (1981–1982) Presencia de teleosteos atla´nticos en el Mediterra´neo occidental. Monografı´as y Trabajos de Zoologı´a (Universidad de Ma´laga) 3–4, 49–56. Roig A. (1979) Singnathus agassizi Kaup, Canestrini: nombre va´lido para unos singna´tidos capturados en Sa Ra´pita (Mallorca-Islas Baleares) (Pisces, Syngnathidae). Miscela´nea Zoolo´gica (Barcelona) 5, 83–92. Sax D.F. and Gaines S.D. (2003) Species diversity: from global decreases to local increases. Trends in Ecology and Evolution 18, 561–566. Thomas C.D. (2010) Climate, climate change and range boundaries. Diversity and Distribution 16, 488–495. Tintore J., Violette P.E., Blade I. and Cruzado A. (1988) A study of an intense density front in the eastern Alboran Sea: the Almeria–Oran front. Journal of Physical Oceanography 18, 1384–1397. and Wheeler A. (1973) Syngnathidae. In Hureau J.C. and Monod T. (eds) Check-list of the fishes of the north-eastern Atlantic and of the Mediterranean. Paris: UNESCO, pp. 274–279. Correspondence should be addressed to: P.I. Hablu¨tzel Laboratory of Animal Diversity and Systematics K.U. Leuven, Charles Deberiotstraat 32 B-3000 Leuven, Belgium email: pascal.habluetzel@bio.kuleuven.be