New records of heterobranch sea slugs (Mollusca: Gastropoda) from Isla del Coco National Park, Costa Rica

The molluscan fauna of Isla del Coco has recently been well documented, but the heterobranch sea slugs, traditionally called “opisthobranchs”, remain poorly known. We report 13 new records, increasing the total to 40 species. Of the 13 newly discovered species, the following species had not been previously recorded along the Pacific Costa Rican mainland: Berthella californica (Dall, 1900), Peltodoris rubra (Bergh, 1905), Dendrodoris albobrunnea Allan, 1933, Doriopsilla cf. spaldingi valdés & Behrens, 1998, Glaucus cf. marginatus (Reinhardt & Bergh, 1864), and Flabellina sp. Additionally, we report Peltodoris rubra, previously known from the Indo-Pacific, for the first time in the Eastern Tropical Pacific. Rev. Biol. Trop. 64 (Suppl. 1): S205-S219. Epub 2016 Febrary 01.

Among the marine species recently reported for Isla del Coco (also known as Cocos Island), the mollusks represent the most species-rich group with 490 species (Cortés, 2012).Despite the high diversity, the heterobranch molluscan fauna, traditionally referred to as "opisthobranchs", is poorly known.
All of the previous studies bring the number of opisthobranchs of Isla del Coco to 27 species.The present study updates the knowledge on this group.We include new reports, extended distributional ranges, morphological data and illustrate some of the more relevant species for Isla del Coco.
Sampling collection: Sampling was carried out during the scientific Expeditions CIMAR-MONITOREO-COCO-I and II, between 12-20 July 2013 and 23 February 05 March 2014, respectively.The specimens were collected in subtidal areas during daylight hours at six different locations.These locations were surveyed by SCUBA diving to a depth of 15 m.
The specimens were obtained using indirect (collecting algae) and direct (collecting observed animals) methods.Specimens were brought to the laboratory on board the ship and photographed alive, then relaxed in a solution of MgCl 2 with saltwater.After relaxation, the specimens were preserved in 95 % ethanol.Some specimens were fixed in a Bouin's solution and then preserved in 70 % ethanol for morphological studies.
Additionally, we included specimens already deposited at the Museo de Zoología that were collected on different expeditions to Isla del Coco carried out by the Santa Barbara Museum of Natural History and the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), between 1997 (SBMNH), and 2007 to 2014 (CIMAR).Finally, we also include specimens from deep waters that were filmed or photographed by the submersible DeepSee (Cortés, & Blum, 2008), although just a few of these records have a voucher specimen deposited at MZUCR.

RESULTS
A total of 13 species were collected from Isla del Coco, increasing the total known opisthobranch fauna to 40 species.Of the 13 species, the following species represent new records for the Pacific Costa Rican mainland: Berthella californica (Dall, 1900), Peltodoris rubra (Bergh, 1905)

Remarks
The genus Umbraculum Schumacher, 1817 is known from both temperate and tropical seas.According to Wägele, vonnemann, & Rudman (2006), the genus Umbraculum comprises only one species with a worldwide distribution.The morphological and molecular data support U. umbraculum as the only species of the genus present in both tropical and temperate waters.

Morphological comments
The body is elongated and the parapodia completely fused, the edges of these are distinctly crenulated.The rhinophores are long and rolled.The body is olive green.The edges of the parapodia are light green with some white and pink spots that are also present on the rhinophores.

Remarks
This is an undescribed species known from the Eastern Tropical Pacific, from Baja California to Costa Rica and Islas Revillagigedo (Camacho-García et al., 2005), including Clipperton Island (Kaiser, 2007).This species has also been collected in Panama (Camacho-García, in prep.)In Costa Rica, there are a few records of this species from the Pacific mainland found on the green algae Codium isabelae W.R.

Morphological comments
Body oval, elongate.Background color light pink to dark reddish brown.Dorsum with numerous red-brown patches, and spots of the same colors.Dorsum also covered with numerous small rounded white tubercles speckled with red on the tips.Rhinophores reddish brown, with white tips.Gill light pink with whitish lines.ventral mantle and foot with numerous dark red spots.

Remarks
If we follow Dayrat (2010), the generic name for this species would be "Montereina".However, we decided not to follow this classification because this generic name represents a group of several species that cannot be characterized by any diagnostic character or geographic distribution.Due to the lack of consensus on the phylogenetic relationships of Discodoridae, which are unresolved until now, and in order to avoid any taxonomical confusion we prefer to use the generic name Peltodoris for this species.This species has been reported from the Indo-West Pacific and Central Pacific (Gosliner et al., 2008).This species is a new record for the Tropical Eastern Pacific.Considering that this is a substantial range extension, this record will need to be confirmed using morphological and molecular techniques.

Remarks
This species has been reported from the western Indian Ocean of Tanzania to Papua New Guinea and vanuatu; in the Eastern Tropical Pacific from Isla Coiba (Panamá) to Colombia, and Clipperton Island (Hermosillo, 2004;Camacho-García et al., 2005;Kaiser, 2007;Gosliner et al., 2008).Dendrodoris albobrunnea has never been found on the Pacific Costa Rican mainland.

Morphological comments
All the photographed specimens have a translucent white body, with conical tubercles on the dorsum, and a mantle margin with an iridescent blue band as in the original description (valdés, & Behrens, 1998).In this description, the 4-5 branchial leaves are bipinnate, and the rhinophores and branchial leaves are short.In contrast, in our specimens, the rhinophores are relatively long and the 4-5 branchial leaves are tripinnate and spreading.Herein, in the absence of voucher specimens, we identify this species tentatively as Doriopsilla cf.spaldingi.

Morphological comments
The general body color is bright red to orange.The oral tentacles are similarly colored and have an opaque white tip.Rhinophores are brown and white tipped.Cerata orange with brown, with some whitish pigment.

Remarks
This is an undescribed species from the Eastern Tropical Pacific.It has been reported only from Galápagos (Gosliner, 1991;Camacho-García et al., 2005), and it has not been recorded on the Pacific Costa Rican mainland.

Morphological comments
For a complete description, see Carmona et al. (2014).

Material
Provided here is a photographic record of this species taken at Isla del Coco National Park on 25.01.2008.The four living specimens were found washed up on the beach.

Remarks
Recently, morphological and molecular phylogenetic studies on the genus Glaucus revealed that Glaucus atlanticus Forster, 1777 is a cosmopolitan species, whereas the informal clade 'Marginatus' is constituted by four cryptic species with Indo-Pacific distribution.This clade includes Glaucus marginatus (Reinhardt & Bergh, 1864) from the tropical and subtropical Indo-Pacific region, Glaucus bennettae Churchill, valdés & Ó Foighil, 2014, which occurs only in the South Pacific; Glaucus thompsoni Churchill, valdés &Ó Foighil, 2014, andGlaucus mcfarlanei Churchill, valdés &Ó Foighil, 2014, from the North Pacific Ocean (Churchill et al., 2013;2014).In our case, the specimens are consistent with the external morphology of the clade 'Marginatus', possibly G. marginatus, G. thompsoni or G. mcfarlanei mainly due to their geographic distribution.There is one photographic record for this species and identification through morphological and molecular techniques is not possible.

DISCUSSION
Studies of the opisthobranch fauna from the eastern Pacific oceanic islands are scarce; the majority of research has been done in the Galápagos Islands (Gosliner, 1991).In the present study, the number of opisthobranch species reported from Isla del Coco increase by 13 species, from 27 to 40, a 32 % increase (Table 1).Excluding the eight species of pelagic thecosomes, which have different distributional patterns than the benthic opisthobranchs (Lalli, & Gilmer, 1989;Klussmann-Kolb, & Dinapoli, 2006), Isla del Coco shows an increase of 23 species and a 18 % increase of the total of species recorded for the Pacific mainland of Costa Rica (126 spp., Camacho-García, 2009).Additionally, we are including 13 new records of opisthobranchs for Isla del Coco, where seven of these species are new distributional records from the Pacific Costa Rican mainland.
In comparison to Islas Galápagos, the number of opisthobranch species found at Isla del Coco is similar.In contrast to Galápagos, three species recorded at Isla del Coco have Indo-Pacific distributions: Phestilla lugubris (Bergh, 1870), Dendrodoris albobrunnea Allan, 1933, andPeltodoris rubra (Bergh, 1905).The last species had never been reported for the Eastern Tropical Pacific (Gosliner 1991).Overall, the geographical affinities of the Isla del Coco opisthobranch fauna are clearly most related to the Panamic Province.Its position as the first point of contact with the Northern Equatorial Countercurrent (Cortés, 1997), makes the island one of the first possible settlement areas for larvae transported by this current through the Pacific Ocean, before arriving to the eastern Pacific mainland.
The most diverse "opisthobranch" groups at Isla del Coco are both the nudibranch dorids and aeolids, comprising almost a third of the species, which corresponds to the general trend observed along the Pacific Costa Rican mainland (Camacho-García, 2009).It is noteworthy to mention that several common herbivorous species such as Elysia pusilla (Bergh, 1872), Oxynoe panamensis Pilsbry &Olson, 1943, andPhyllaplysia padinae (Williams &Gosliner, 1973), found along the Pacific Costa Rican mainland, appear to be absent at Isla del Coco.Both patterns are probably the result of habitat characteristics such as the presence of reef ecosystems that provide a three-dimensional habitat for sponges, tunicates, bryozoans and hydroids, which are the preferred prey for most nudibranch dorids, and aeolids (Bruno, & Bertness, 2001;Camacho-García, 2009).On the other hand, there is a low habitat complexity provided by macroalgae, due to the dominance of calcareous red algae and filamentous green algae (Fernández, 2008) that could be affecting the composition of the opisthobranch herbivorous species at the Island.

RecentlyFamily
Carmona et al. (2014), conducted a systematic review of the genus Anteaeolidiella based on morphological and molecular data.They concluded that what had been called Aeolidiella indica from the Eastern Tropical Pacific is a new species they named Anteaeolidiella ireneae.Anteaeolidiella ireneae is reported from Clipperton Island, Isla Canal de Afuera (Panamá), Bahía de San Marte (México), Isla Socorro (México), and the Pacific coast of Costa Rica.The identity of Anteaeolidiella indica remains unclear.

TABLE 1 (
Taxa in boldface type = new records for Isla del Coco.Distribution: Car=Caribbean; CT=circumtropical, EP=Eastern Pacific; IP=Indo-Pacific; NP=North Pacific; P=Planktonic; WA=Western Atlantic.Continued) more studies are needed to enhance the knowledge of the opisthobranch fauna from Isla del Coco.Future surveys should include various sampling techniques designed to collect cryptic species, including nighttime surveys, deepwater exploration and ecological research.All of these techniques combined will help us to better understand the biodiversity of the opistobranch fauna of Isla del Coco. *