INTRODUCTION
The northern area of the Humboldt Current Upwelling Ecosystem (HCUE) in front of the Peruvian coast (3°23′–10°21′S: Chavez et al., Reference Chavez, Bertrand, Guevara-Carrasco and Soler2008) holds a unique marine biodiversity due to the spatial heterogeneity of the coastline and the complex oceanographic characteristics, especially the oscillating conditions produced by the occurrence of the warm El Niño and cold La Niña events (Paredes et al., Reference Paredes, Tarazona, Canahuire, Romero, Cornejo and Cardoso1998, Reference Paredes, Cardoso and Tarazona2004; Tarazona et al., Reference Tarazona, Gutiérrez, Paredes and Indacochea2003). The diversity of marine molluscs in this region is composed of species of tropical, subtropical and Antarctic origin, resulting in a rich endemic fauna and a high number of species (Ramírez et al., Reference Ramírez, Paredes and Arenas2003; Tarazona et al., Reference Tarazona, Gutiérrez, Paredes and Indacochea2003). Although many species have been compiled and reported (see reviews in Alamo & Valdivieso, Reference Alamo and Valdivieso1997; Ramírez et al., Reference Ramírez, Paredes and Arenas2003), the information is often skewed towards reports of macro gastropods, bivalves and cephalopods with distinctive morphological characteristics (e.g. shell, valves or peaks) while some groups such as nudibranchs (Gastropoda, Nudibranchia) have received very little attention and the available information is scarce.
Even though their colourful and striking morphology may be appealing for taxonomic work, the current status of the number of species and distribution of nudibranchs on the coast of Peru is restricted to a few locations with the main research emphasis having been focused on the northern coast. Nakamura (Reference Nakamura2006, Reference Nakamura2007) registered a total of 54 species on the Peruvian coast with 17 species recorded exclusively in the northern area (~3°S). Recently a new species of the genus Corambe has been described in the northern region (Martynov et al., Reference Martynov, Brenzinger, Hooker and Schrödl2011). Clearly, much more information from the central and southern coast (approximately 2500 km of coastline) is necessary for fully understanding the diversity and composition of nudibranchs in this highly productive upwelling ecosystem.
Spurilla neapolitana Delle Chiaje, 1823 is a nudibranch of the Aeolidiidae family with circumtropical distribution, thriving from the middle intertidal down to 80 m depth (Reed & Mikkelsen, Reference Reed and Mikkelsen1987). This species can be found in rocky substratum among crevices and underneath boulders (Bertsch & Kerstitch, Reference Bertsch and Kerstitch1984), soft bottoms and kelp forest invertebrate communities (Rodriguez et al., Reference Rodríguez, Vargas and Cortés2003). It preys on sea anemones, consuming the oral disc and tentacles (García & Cervera, Reference García and Cervera1985; Schlesinger et al., Reference Schlesinger, Goldshmid, HadWeld, Kramarsky-Winter and Loya2009) and also serves as a prey item of crustaceans, star fish and a few predatory gastropods (Reed & Mikkelsen, Reference Reed and Mikkelsen1987).
In this study we report the presence of S. neapolitana for the first time in Bahía Ferrol, a location within the HCUE of the central coast of Peru. A brief description of the external morphology is presented.
MATERIALS AND METHODS
Two specimens of Spurilla neapolitana were collected in November 2009 at Hueco de la Vela (09°04′S 78°35′W) within Bahía Ferrol on the central coast of Peru (Figure 1). The samples were taken during a stock assessment of the scallop Argopecten purpuratus (Lamarck, 1819) population, conducted by IMARPE (Instituto del Mar del Peru, Peruvian Sea Research Institute). During the assessment the scallop population size is surveyed using randomly distributed sampling points (N = 15) covering the entire seabed area (~280,000 m2). At each sampling point a hooka diver placed a 1-m2 quadrate on the bottom, observing the epibenthos inside the quadrate and the surrounding marked area, and then all the biota within the quadrate was collected and stored in plastic bags. In addition, depth was recorded and water samples for measurements of bottom temperature and dissolved oxygen were taken using a Niskin bottle. Individuals of S. neopolitana were observed in the surrounding area outside a sampling quadrate and collected separately. In the laboratory, live animals were maintained in a seawater aquarium in order to take photographs and make observations. Length measurements were taken with a caliper of 0.1-mm precision and wet weight (0.01 g). Thereafter, the samples were fixed in 10% formalin solution and preserved in 70% alcohol. The sample was deposited in the marine specimens collection of the Laboratorio Costero de Chimbote (IMARPE laboratory no. 4.11.2009.MN1-LCCH).
Map of Bahia Ferrol, located at the coast of Ancash, Peru. The triangle indicates the location were S. neapolitana were collected.
RESULTS
Habitat
Spurilla neapolitana was found at 10 m depth with a water temperature of 15.7°C and 1.50 ml/l dissolved oxygen. The sediment comprised a mix of sand–gravel and shell pieces. The epibenthic community was dominated by the tube building polychaete Diopatra rizhoicola, red algae Rhodymenia sp., scallops Argopecten purpuratus and predatory crabs Platyxanthus cokeri and Cancer setosus. In addition, small white anemones were observed and likely served as food for the sea slug (Bigger, Reference Bigger1980; García & Cervera, Reference García and Cervera1985).
Diagnosis
The total length of the adult S. neapolitana was 85.5 mm and weighed 3.58 g. The body is long with an intense orange colouring and white spots along the dorsal line (Figure 2A). Distinguishing this species (García & Cervera, Reference García and Cervera1985; Domínguez et al., Reference Domínguez, Troncoso and García2008) are the perfoliate rhinophores with 18 lamella horizontally alternating, one over the other. The general yellowish and light-brown coloration gives a dark appearance to the rhinophores (Figure 2B). Oral tentacles are thin, short and rounded, translucent with white tips deployed at both sides of the mouth (Figure 2B). The oral palps are rough. The cerata are long, gross and flat closer to the tip (Figure 2B). There are between eight and 12 ceratal arcs in each side of the body. The second ceratal arc shows 60 cerata at each side. Larger cerata are located in the middle of the arc while short cerata are present in the arc extreme. The apex of the cerata is curved towards the dorsal middle line. Cerata are translucent with white spots. The brownish digestive gland can be observed through the cerata (Figure 2B). The pericardium is located in the first and second ceratal group (García & Cervera, Reference García and Cervera1985). The genital opening is on the right side of the body located below the first arc and the anus is located below the second group. The tail is short and translucent. The foot is wide, of light-orange colour. The hepatic branches look like fine trusses of dark colour. The coloration of S. neapolitana varies depending on the habitat and feeding type and food composition, however, the yellow-orange and white dotted pattern is distinctive in most of the reported individuals (Haefelfinger, Reference Haefelfinger1969; García & Cervera, Reference García and Cervera1985; Just & Edmunds, Reference Just and Edmunds1985).
Spurilla neapolitana (A) Dorsal view; (B) anterior view. Cr: cerata, Rn: rhinophore, Op: oral palps, Pr Tn: propodial tentacles, F: foot.
DISCUSSION
Taxonomic remarks
The genera Spurilla, Berghia and Aeolidiella are distinctive for having more cerata compared with other nudibranchia species (Gosliner et al., Reference Gosliner, González-Duarte and Cervera2007). Spurilla neapolitana shows external similarities to S. chromosoma (Cockerell & Eliot, 1905; Rudman, Reference Rudman1999). Both species show the dorsal part with a white dotted pattern, curved and translucent cerata with dark colouring and a white dotted pattern (García & Cervera, Reference García and Cervera1985). However, S. chromosoma shows cerata lines in the anterior region of the body and rinophores with few lamella diagonally arranged, while S. neapolitana shows ceratal arcs in a horseshoe shape and the perfoliated rinophore are completed transversal (Domínguez et al., Reference Domínguez, Troncoso and García2008).
Distributional remarks
Spurilla neapolitana (Delle Chiaje, 1841) shows a circumtropical distribution (Bertsch, Reference Bertsch, Rangel, Gamboa, Arriaga and Contreras2010) and it has been reported in several areas in the Mediterranean Sea, eastern/western Atlantic Ocean and a few places in the Pacific Ocean (Table 1). Despite its wide distribution, S. neapolitana is often reported thriving in warm waters or locations with strong seasonal changes in the oceanographic conditions. Here we report this species in the central coast of Peru, a region that even though it is at low latitude and closer to the equator, the presence of a cold, nutrient rich upwelling process resembles more a temperate region. Interestingly, the diversity of nudibranchs along the Peru–Chile coastline has been better described in ecotone areas such as the transition from the cold upwelling to the warm Equatorial province in northern Peru (Nakamura, Reference Nakamura2006, Reference Nakamura2007) or in the transition from the upwelling to the Magellanic province in southern Chile (Schrödl, Reference Schrödl2003). Whether transitional areas are more diverse in terms of nudibranch species is still a matter of further study, our knowledge about nudibranchs diversity will improve when more information coming from the core area of the upwelling system is available. The record of S. neapolitana adds support to the predictions of Gosliner (Reference Gosliner and Matthew1991) and Schrödl (Reference Schrödl2003) for findings of more nudibranch species in the region.
World distribution of Spurilla neapolitana Delle Chiaje, 1841, including sampling zone of the material study.
While this report extends the distribution range of S. neopolitana into the south-east Pacific, it is difficult to determine the source location of this species. Research effort on nudibranchs is poor in the area, so it possible that this species and others may be overlooked during surveys of benthic organisms. However, there are other processes influencing the marine benthic biota composition in the region that must be taken into account. During strong El Niño events, many mollusc species extend their distributional range towards high latitudes due to the intrusion of equatorial transporting larvae and adults from the equator down to central and southern Chile (e.g. Paredes et al., Reference Paredes, Tarazona, Canahuire, Romero, Cornejo and Cardoso1998, Reference Paredes, Cardoso and Tarazona2004). Some species may stay even longer at specific locations with suitable conditions for survival after El Niño events (e.g. Ashton et al., Reference Ashton, Riascos and Pacheco2008). During upwelling conditions, larvae transport from high latitudes towards the equator is due to the predominant northward direction of the Humboldt Current (Tarazona et al., Reference Tarazona, Gutiérrez, Paredes and Indacochea2003). Also, a great amount of invertebrates including nudibranchs can be transported through rafting (Astudillo et al., Reference Astudillo, Bravo, Dumont and Thiel2009) which may explain the local presence of several species with disjoint geographical distribution (e.g. Castilla & Guiñez, Reference Castilla and Guiñez2000; Pacheco & Laudien, Reference Pacheco and Laudien2008).
ACKNOWLEDGEMENTS
We thank Aldo Indacochea, Lucas Cervera and Jesús Troncoso for the taxonomic advice. Javier Uribe Balbín is thanked for the photographic support. Michael Schrödl provided helpful comments on an early version of this manuscript. Carrie Auld kindly revised the English of this manuscript. Jesús Tronsco is thanked for encouraging us to document this finding. Funding during scallop population assessment was provided by IMARPE. R.A.U. is supported by Programa MECE2 Educación Superior/MECESUP, Proyecto MECE ANT0711. A.S.P.'s research is supported by FONDECYT grant no. 3100085.
