INTRODUCTION
Polycera hedgpethi Er. Marcus, Reference Marcus1964 is currently considered a worldwide nudibranch species (Cervera et al., Reference Cervera, García-Gómez, Toscano and García1991 [1988]). This species was first described from California (Marcus, Reference Marcus1964) and subsequently recorded from New Zealand, the American Pacific coast, Mexico, the Costa Rican Atlantic coast, Australia, South Africa, Angola, Italy, Spain, France and Morocco (all records were recently summarized by Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012). After this sequence of reports in recent decades, suggesting dispersion via fouling on ships, this nudibranch was considered an alien species (Wilson, Reference Wilson2006).
In European waters, P. hedgpethi has been mainly reported in Mediterranean localities, the existence of stable populations being demonstrated recently (Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012). The scarce Eastern Atlantic records are limited to three geographically separate findings (see Vallés et al., Reference Vallés, Valdés and Ortega2000; Caballer & Ortega, Reference Caballer and Ortega2002; Cervera et al., Reference Cervera, Tamsouri, Moukrim and Villani2010).
During an intertidal survey at the locality of El Portil (Huelva, south-east Spain), two specimens of a previously unrecorded polycerid species in this area were collected and identified as P. The aim of this article is to update the known distribution of P. hedgpethi, adding an intermediate locality to the separate previously known Atlantic reports.
MATERIAL AND METHODS
The nudibranch specimens reported in this paper were collected in the intertidal area at the locality of El Portil (Huelva). The two specimens were found together on the lower face of a stone, with colonies of the bryozoan Bugula neritina Linnaeus, 1758 in its proximities. The material examined for this study was fixed in absolute ethanol for further molecular studies and deposited in the malacological collection of the research team Biodiversidad y Ecología de Invertebrados Marinos (BEIM), in the Faculty of Biology of the University of Seville (BEIM-mol).
The locality of El Portil is situated at the mouth of the River Piedras, and experiences fluctuating environmental conditions produced by tidal currents and variable turbidity depending on river sediment discharge. Although the sea water temperature was not measured during the collection of the specimens, general oceanographic multiannual studies (e.g. Prieto et al., Reference Prieto, Navarro, Rodríguez-Gálvez, Huertas, Naranjo and Ruiz2009: Figure 8B) show a mean sea surface temperature in the proximities of our sampling station of around 20°C. However, the temperature inside the mouth of the river could increase by a few degrees due to the retention of waters by tidal processes and solar radiation on a layer of water, thinner than in the surrounding open sea (Dr Morales, personal communication).
Despite this continuously changing environment, El Portil harbours a high diversity of nudibranchs. Indeed, the locality of El Portil, with just approximately one hectare of rocky surface, which is only visible during low tides, has been extensively reported in the malacological literature of the Iberian nudibranch as being one of the most important type localities for species new to science in southern Spain (e.g. García-Gómez et al., Reference García-Gómez, López-González and García1990; García et al., Reference García, López-González and García-Gómez1991; Cervera et al., Reference Cervera, García-Gómez and López-González1992). This locality is also known for the presence of potentially widespread common food substrata for polycerid nudibranchs, such as the bryozoans B. neritina and Zoobotryon verticillatum Delle Chiaje, 1822 (Dr C.M. López Fe de la Cuadra, personal communication; authors' personal observation).
SYSTEMATICS
Order NUDIBRANCHIA Cuvier, 1817
Suborder EUCTENIDIACEA Tardy, 1970
Family POLYCERIDAE Alder & Hancock, 1845
Genus Polycera Cuvier, 1816
Polycera hedgpethi Er. Marcus, Reference Marcus1964
MATERIAL EXAMINED
BEIM (mol-102), El Portil (Huelva, Spain), 37°12′34″N 7°3′18″W, intertidal, underside of a stone, 9 November 2014, coll. by P. Escribano, two specimens measuring 18 and 20 mm in length, respectively.
REMARKS
The external morphology and colour pattern of the specimens were in agreement with the specimens previously described in the literature (Marcus, Reference Marcus1964) (Figure 1A, B).
Polycera hedgpethi Er. Marcus, Reference Marcus1964: (A) specimen 20 mm in length; (B) both collected specimens showing reproductive behaviour.
Although it has been attributed to an Indo-Pacific origin (Cervera et al., Reference Cervera, García-Gómez, Toscano and García1991 [1988]; Cervera et al., Reference Cervera, Tamsouri, Moukrim and Villani2010), the few Atlantic localities of Polycera hedgpethi could also be the result of a scarce sampling effort or lack of experts in those key localities for this species in the Atlantic. A population molecular study is needed in order to provide more information on the connections between these localities and the possible gene fluxes. An example of a completely erroneous attribution of the Atlantic or Pacific origin of an alien invasive cnidarian species has recently been solved by these molecular techniques (Concepcion et al., Reference Concepcion, Kahng, Crepeau, Franklin, Coles and Toonen2010).
The samples of Polycera hedgpethi collected from the Gulf of Cadiz (Atlantic side of the Strait of Gibraltar) provide important data in the reconstruction of the current distribution of this species. If a stable population is finally recognized in our sampling locality, El Portil could serve as an important step for the future connection between the few known Atlantic localities and the well-documented Mediterranean areas (Figure 2A). Although just a decade ago this species was initially considered as poorly established on European coasts (Zenetos et al., Reference Zenetos, Çinar, Pancucci-Papadopoulou, Harmelin, Furnari, Andaloro, Bellou, Streftaris and Zibrowius2005), recent studies demonstrate a well-established population in some localities of Mediterranean waters (Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012), followed by recent spreading in other southern localities (Giacobbe & De Matteo, Reference Giacobbe and De Matteo2013). Information on possible Eastern Atlantic populations is scarce. Just three localities are known. The first report (in chronological order) is from the South-east Atlantic, Corimba Bay, Angola (see Vallés et al., Reference Vallés, Valdés and Ortega2000); the two other reports are from the northern hemisphere: the Bay of Santander (see Caballer & Ortega, Reference Caballer and Ortega2002), an important estuary with a high anthropogenic pressure close to a marina; and Aghroud, in Morocco, where the specimen was collected intertidally, under stones (see Cervera et al., Reference Cervera, Tamsouri, Moukrim and Villani2010).
(A) Records of Polycera hedgpethi Er. Marcus, Reference Marcus1964 from the North-eastern Atlantic and Mediterranean Sea (modified from Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012; Giacobbe & De Matteo, Reference Giacobbe and De Matteo2013), updated with the new finding at El Portil, Huelva (asterisk): 1, Aghroud, Morocco (Cervera et al., Reference Cervera, Tamsouri, Moukrim and Villani2010); 2, Bay of Santander, Spain (Caballer & Ortega, Reference Caballer and Ortega2002); 3, Étang de Thau, France (Poddubetskaia, Reference Poddubetskaia2003); 4, Sacca Sessola Island, Venice Lagoon, Italy (Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012); 5, Marina di Ravenna docks, Italy (Rudman, Reference Rudman2005; Trainito, Reference Trainito2005); 6, Rimini coast, Italy (Ioni, Reference Ioni2011); 7, Fusaro Lake, Italy (Cervera et al., Reference Cervera, García-Gómez, Toscano and García1991 [1988]); 8, Faro Lake, Italy (Giacobbe & De Matteo, Reference Giacobbe and De Matteo2013). (B) General landscape of the locality of El Portil (Huelva), where the new specimens of P. hedgpethi were found.
Environmental conditions at the mouth of the River Piedras (turbidity, tidal current regimes, salinity, temperature oscillations, etc.) (Figure 2B) and the proximity of a number of marinas and harbours in this area most likely favour the presence and/or establishment of alien or widespread species (e.g. the actiniarians Diadumene lineata (Verril, 1869) and Diadumene sp.; the nudibranchs Polycerella emertoni Verril, 1880; and the bryozoans Zoobotryon verticillatum and Bugula neritina). Polycera hedgpethi has been found associated with two species of bryozoans, B. neritina (see Miller, Reference Miller2001; Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012; Giacobbe & De Matteo, Reference Giacobbe and De Matteo2013) and Z. verticillatum (see Giacobbe & De Matteo, Reference Giacobbe and De Matteo2013: p. 360, Figure 1.2, Table 1), although a trophic relationship has only been demonstrated with B. neritina (Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012: p. 975; Giacobbe & De Matteo, Reference Giacobbe and De Matteo2013: Figure 1.3, Table 1). Both bryozoan species were also present in the study area where our specimens were collected, El Portil (Huelva). Despite the regular intertidal surveys carried out in El Portil since the 1990s, this is the first record of this Polycera species in this area. So far, Polycera hedgpethi does not seem to compete with other species (Keppel et al., Reference Keppel, Sigovini and Tagliapietra2012), although, its presence could lead to a future scenario of local food competition with its congener Polycera aurantiomarginata García-Gómez & Bobo, 1984, whose type locality is El Portil, always depending on the density of nudibranch populations and availability of food substrata.
It is well known that human activities are responsible for increasing introductions of non-indigenous species worldwide (e.g. Zenetos et al., Reference Zenetos, Çinar, Pancucci-Papadopoulou, Harmelin, Furnari, Andaloro, Bellou, Streftaris and Zibrowius2005; Molnar et al., Reference Molnar, Gamboa, Revenga and Spalding2008; Galil et al., Reference Galil, Boero, Fraschetti, Piraino, Campbell, Hewitt, Carlton, Cook, Jelmert, Macpherson, Marchini, Occhipinti-Ambrogi, Mckenzie, Minchin, Ojaveer, Olenin and Ruiz2015). Harbours or marinas are especially sensitive sites for the first attempts at establishment. However, the specimens studied in this paper were collected in natural rocky areas, and the marinas present at the mouth of the River Piedras are dedicated to small boats used for sporting and recreational fishing activities. This suggests that El Portil is probably not the first locality for Polycera hedgpethi in the Gulf of Cadiz, and that it could perhaps be found in further surveys 25 km south-eastwards, at the mouth of the rivers Tinto and Odiel. In that area, there is a complex system of canals protecting harbours dedicated to numerous industries and containing an important amount of artificial substrata and docks, which are host to intensive shipping activities.
In this paper, the possible routes of migration for Polycera hedgpethi (natural or facilitated by human activities) are not debated, however, as the sequence of findings of Polycera hedgpethi in the Eastern Atlantic is apparently random and unconnected, ship-mediated transport seems to be the most plausible mode of dispersion. Furthermore, when a sufficient number of localities are situated at the appropriate distance, gene fluxes could be established among them. The present records in the Gulf of Cadiz could be considered an opportunity to connect the isolated Eastern Atlantic records for the species with the Mediterranean ones, even taking into consideration the possible unreported presence of the species along the North African Mediterranean coast. At this moment, it is hard to hypothesize about the importance of the complex current systems in the Gulf of Cadiz (see Johnson & Stevens, Reference Johnson and Stevens2000; Criado-Aldeanueva et al., Reference Criado-Aldeanueva, García-Lafuente, Vargas, Del Río, Vázquez, Reul and Sánchez2006; García-Lafuente et al., Reference García-Lafuente, Delgado, Criado-Aldeanueva, Bruno, Del Río and Vargas2006; García-Lafuente & Ruiz, Reference García-Lafuente and Ruiz2007) regarding the future natural distribution of Polycera hedgpethi.
The collected specimens of Polycera hedgpethi showed an active reproductive (copulatory) behaviour in the laboratory (Figure 1B), making the production of egg masses in the natural environment highly probable. It seems necessary to continue with the regular monitoring of this locality at the Gulf of Cadiz to look for further findings of this and other potentially invasive species.
ACKNOWLEDGEMENTS
We thank our colleagues of the research team BEIM, University of Seville, for their helpful assistance during the sampling trip carried out in October 2014 in the framework of intertidal benthic surveys at the locality of El Portil, where the specimens reported herein were detected. Dr Carlos María López Fe de la Cuadra (Department of Zoology, University of Seville) provided useful information about cheilostomata bryozoan fauna from the locality of El Portil. The authors thank Dr Juan Antonio Morales (Department of Geology, University of Huelva) for additional information on the temperature dynamics at the mouth of the River Piedras. We also thank two anonymous referees, whose suggestions and criticisms have improved the first version of this manuscript. We thank Mr Tony Krupa for reviewing the English version of the manuscript.
