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Ascidia ceratodes (Huntsman, 1912) (Tunicata: Ascidiidae) off the northern Chilean coast: new record.

The ascidian fauna of the Chilean coast comprises around 72 species. Over the last decade, our knowledge about this taxon and its distribution in the Chilean coast has improved (Clarke & Castilla, 2000; Sanamyan & Schories, 2003; Lagger et al., 2009; Sanamyan et al., 2010; Tatian & Lagger, 2010; Madariaga et al., 2014; Schories et al., 2015; Turon et al., 2016a,b); however, in order to accurately assess ascidians biodiversity, including the presence and distribution of nonindigenous species, new areas along the Chilean coast need to be studied (Turon et al., 2016a,b). For example, Rocha et al. (2012) reported 26 species of the family Ascidiidae from the Atlantic coast of South America, while only nine species were reported on the Pacific coast (Van Name, 1945; Lambert & Lambert, 1998; Nova-Bustos et al., 2010; Carman et al., 2011; Monniot, 2013). This trend of greater diversity on the southwest Atlantic compared to Pacific coast has also been highlighted by Miloslavich et al. (2011) and by Clarke & Castilla (2000), Sanamyan & Schories (2003), Lagger et al. (2009), Sanamyan et al. (2010), Shenkar & Swalla (2011), Tatian & Lagger (2010), Madariaga et al. (2014), Schories et al. (2015) and Turon et al. (2016a,b).

Recent surveys of ascidians biodiversity on the northern Chilean coast (Clarke & Castilla, 2000; Schories et al., 2015; Turon et al., 2016a, 2016b) did not make any reference to members of the genus Ascidia. Only one previous study reported the species A. meridionalis Herdman, 1880 and A. tenera Herdman, 1880 from Magellan Strait, southern Chile (Schories et al., 2015).

Van Name (1945) described the geographical distribution of A. ceratodes as ranging along the northern American Pacific coast from Bristish Columbia south to California; however, he also referred to several questionable specimens collected from Ecuador to the northern Chilean coast (Tocopilla; 22[degrees]05'S, 70[degrees]11'W). Van Name (1954) only cited the presence of A. ceratodes in the northern Chilean coast to spite to collect intertidal ascidians between Iquique and Antofagasta (Stations 129, 131, 133 and 159 sampled during Lund University Chile Expedition 1948-1949). More recently, Carman et al. (2011) and Bonnet et al. (2013) reported the presence of A. ceratodes in the Pacific waters off Panama and replay the comment of Van Name (1945) on the possible presence of this species in the northern Chilean coast.

The study of the marine benthic communities of the northern Chilean coast is of great importance because the intense maritime traffic makes this region more susceptible to the introduction and establishment of tropical and subtropical, exotic species of ascidians (Turon et al., 2016a, 2016b). Additionally, this area is under the influence of El Nino-Southern Oscillation (ENSO) events, putting it at risk of colonization of the northern Chilean coast by ascidians or other organisms from tropical latitudes (Lord et al., 2015).

The most recent assessment of the northern Chilean ascidians only reached as far south as 25[degrees]S (Schories et al., 2015). We aim to establish a new, extended record based mainly on a recent collection of intertidal ascidians sampled between Arica (18[degrees]S) and Iquique (20[degrees]S), including a report of A. ceratodes. Here, we confirm their presence in the northern Chilean intertidal rocky shore.

Sampling was performed in August, 2016. Localities around Arica and Iquique (Table 1) were surveyed by hooka diving, by pulling up ropes and raft cages as well as searching under intertidal boulders in rocky shore pools. Additionally, at each site, we sampled artificial substrates (docks, pilings, break-waves), shellfish markets (including the analysis of bivalves shells such as Choromytilus chorus and Aulacomya ater) and some intertidal natural communities. However, specimens of A. ceratodes were only collected under intertidal boulders settled on sandy beaches and in tide pools. Sampling was exhaustive, i.e., it was continued until no further species were detected; typically, surveys lasted around 3 h and ranged from 0 to 1 m of depth. There is an important link between the temperature and the proportion of nonindigenous ascidians (Madariaga et al., 2014; Lord et al., 2015); temperature of the seawater found in tidal pools was therefore recorded using a digital thermometer ([+ or -] 0.1[degrees]C).

Ascidians were photographed in vivo, carefully collected in Ziploc bags, and taken to the laboratory within 2 h of collection. There, they were placed in trays and relaxed using a combination of menthol and cold treatment, keeping the trays in a freezer until ice formed on the surface (Turon et al., 2016a,b). Samples were then split for preservation: most of the material was fixed in 4% formaldehyde for morphological observation, while some parts (usually muscular tissue) were preserved in absolute ethanol for molecular analyses. The observation of morphological features was routinely enhanced by staining with Bengal Rose or Methyl Blue stain. Specimens were identified to species level using the relevant literature (Rocha et al., 2012) and in particular the available studies of the genus Ascidia in Central America (Van Name, 1945; Tokioka, 1972; Carman et al., 2011; Bonnet et al., 2013). Taxonomy followed the guidelines of the World Register of Marine Species (Rocha et al., 2013) and our comparative analysis was based mainly in the description of Bonnet et al. (2013). Additionally, five specimens of A. ceratodes were sent to Nadia Bonnet (Laboratorio de Sistematica e Ecologia de Invertebrados Marinhos, Departamento de Zoologia, Universidade Federal do Parana, Curitiba, Parana, Brazil) to corroborate the identification. Specimens preserved in formaldehyde were deposited in the Systematic Room, Ascidian Collection, Department of Zoology, Universidade Federal do Parana, Brazil (N. Bonnet and R.A. Rocha, pers. comm.) (5 specimens; DZUPASC 239) and in the Invertebrate Taxonomic Room, Universidad Catolica del Norte, Coquimbo, Chile (J. Sellanes,pers. comm.) (3 specimens).

Ascidia ceratodes (Huntsman, 1912) (Figs. 1-2)

Sinonymy

Phallusia ceratodes Hunstman, 1912, p. 114, p. 121; 1912a, p. 117, pl. 10, Fig. 9, pl. 15, Figs. 3, 4, 7. Ascidia californica Ritter & Forysth, 1917, p. 454, pl. 38, Fig. 6, pl. 41, Figs. 24-27; Johnson & Snook, 1927, p. 593, fig. 692; Pratt, 1935, p. 745; MacGinitie, 1939, pp. 443, 446. Ascidia eiseni Michaelsen, 1923, p. 38, fig. 8. A. ceratodes Van Name, 1945, pp. 196-197, Fig. 109; Van Name, 1954, p. 16 (only cited); Bonett et al. 2013, pp. 354-355, Fig. 2 (references to the presence of this species in the northern Chilean coast based on comments of Van Name, 1945).

Material examined

St 1: Arica, Laucho Beach (18[degrees]29'12.26"S, 70[degrees]19' 36.00"W; intertidal pool, August, 2016; two specimens; sea water temperature 19.6[degrees]C). St. 2: Arica, Lisera Beach (18[degrees]29'34.52"S, 70[degrees]19'37.46"W; intertidal pool, 2 August 2016; five specimens; sea water temperature 18.6[degrees]C). St. 3: Iquique, Huaiquique (20[degrees]16'16.58"S, 70[degrees]07'52.90'W; intertidal pool; 4 August 2016; two specimens; sea water temperature 17.3[degrees]C). St. 4: Iquique, off Regional Government Building (20[degrees]13'03.63"S, 70[degrees]09'21.45'W; intertidal pool, 5 August 2016; four specimens; sea water temperature 18.2[degrees]C). All sites have <1 m depth, with the bottoms dominated by small boulders (30 to 40 cm of diameter), where the specimens were collected.

Description

Specimens are small (up to 2.5 cm total length) and are fixed to the substrate by the left side of the body, as is typical for other members of the family Ascidiidae (Monniot et al., 1991). The living animal is yellowish with dark orange siphons, although these colors disappear after fixation. The tunic is translucent, depressed, with cartilaginous consistency (Fig. 1a). The body is oval, 1.0-2.0 cm long (including the oral siphon) and 0.5-2.0 cm wide, without the tunic. The color of the right side is different from that of the left side (Figs. 1b-1c). Usually, both siphons are small, but the oral siphon is the longer of the two. It has eight to nine lobes and six to eight red eye spots, while the atrial siphon has six lobes and six red eye spots (Figs. 2a-2b); both siphons present orange dots between the lobes, and neither has any projections on the margin. The atrial siphon is directed towards the posterior region of the body, at a right angle (Figs. 1b-1c). The V-shaped neural ganglion is closer to the oral siphon. On the right side, the musculature is formed by a net of thick fibers (Fig. 1c). On the left side, the longitudinal muscles extending from the oral siphon are short. A band of short parallel transverse fibers is found in the dorsal region (Fig. 1c). The longitudinal muscle fibers in the siphons are not organized in bands (Figs. 2a-2b). An unknown typical brown net associated with the stomach and external wall of the posterior intestine was observed (Fig. 2c). According to Monniot et al. (1991; p. 22), this net could be tubules of the "pyloric gland" with possible excretory and digestive function.

Renal vesicles were not observed between the stomach and the ascendant loop of the intestine as suggested by Bonett et al. (2013). In the basis of the oral siphon, it was possible to detect an area between 80 and 127 oral tentacles, of three sizes are present; the largest is 1.5-2.0 mm long and 90 [micro]m wide (Fig. 2d). The line of tentacles and the parapharyngeal groove is closed, with or without papillae. The peri-tubercular area is short, and the dorsal tubercle aperture is Ushaped, with or without enrolled ends. Anteriorly, the dorsal lamina is double and passes by the left of the esophageal aperture to the end of the pharynx, close to the stomach; no papillae are present on the right side of the dorsal lamina at the level of the esophagus. There is a narrow lamina on the right of the esophageal aperture. The pharynx has 24-38 longitudinal vessels on the right side, 23-35 longitudinal vessels on the left, and 47-81 transverse vessels; it is pleated, with five to seven stigmata per mesh (Fig. 2f). Distance between transversal vessels is 1.0 mm, that between longitudinal vessels, 0.6 mm spaces (Fig. 2g). The primary papillae in the pharynx are simple, bi or trilobed, this last form being the most common (Fig. 2g). There are secondary papillae in some parts of the pharynx. The alimentary canal occupies half or more of the left side of the body (Fig. 1b). The stomach is oval and large, with 9-11 internal longitudinal folds. The intestine forms a primary and a secondary loop (Fig. 1b). The anus is located very near the oral tentacles; it has a smooth or bilobed rim (Fig. 2e). The ovary is compact and localized inside the primary intestinal loop, where it is visible both from the outside and from the atrial cavity (Fig. 1b). The testicular follicles are elongated and overlie part of the stomach and intestine (Figs. 2h, 2i). Gonoducts open posterior to the anus aperture (Fig. 2e).

Taxonomic remarks

Van Name (1945) described A. ceratodes as similar to juveniles of A. interrupta Heller, 1978. Bonnet et al. (2013) agree that the absence of projections in the surface of the tunic, the larger number of oral tentacles, low number of longitudinal vessels in the pharynx, isodiametric intestine and conspicuous renal vesicles are characteristics, which distinguish A. ceratodes from A. interrupta. Northern Chilean specimens show a smaller number of oral tentacles and both siphons are shorter than Panamian specimens (Bonnet et al., 2013).

Geographic distribution

According to Van Name (1945), the geographical distribution of A. ceratodes ranges from British Columbia to California. His report makes reference to several specimens from Ecuador and northern Chile, which were catalogued as questionable due to the fact that the mantle musculature is coarser and heavier than in specimens from California. Later, Tokioka (1972) reported the species in Costa Rica, and Carman et al. (2011) extended its range to Panama. It is uncertain whether these tropical populations are in their native region and whether the species is hence expected to be found all along the Central America Pacific coast, or whether the northern Chilean populations were introduced through anthropogenic activities, such as maritime transport or dispersed by currents associated with previous or recent ENSO events. Sanamyan & Schories (2004) report four ascidians species from two locations in southern Peru, without reference to A. ceratodes. A possible reason for this may be that his sampling including only diving in subtidal rocky communities.

Ecological comments

The northern Chilean coast has been under persistent and sporadic influence of El Nino event of different magnitude in the last seven decades (1945-2015). However, A. ceratodes population persist living in the intertidal zone. This finding could be an example of littoral marine taxa that can resist the negative impacts of climate warming and a native species along the temperate coast from Bristish Columbia, Canada to Tocopilla, Chile (Carman et al., 2011), including the northern Chilean coast. This wide geographical distribution is surprising since it covers approximately 71[degrees] latitude along the eastern Pacific coast.

A. ceratodes is a native species of the west coast of USA and have a thermal niche ranged between 16.2 and 26.7[degrees]C (Lord et al., 2015; see Table 4). Thus, in physiological terms A. ceratodes could be classified as native, eurythermal species and could be a good bioindicator species for monitoring climate warming of mid-latitudes of the Chilean exposed coast.

DOI: 10.3856/vol47-issue1-fulltext-21

ACKNOWLEDGEMENTS

The authors thank the Direccion de Investigacion y Postgrado, University of Magallanes, for the financial support of this project (Code: 026504). Special thanks go to the Bocas del Toro Station, Smithsonian Tropical Research Institute (STRI), which provided the opportunity to learn about the ecology and taxonomy of tropical ascidians during their 2011 PASI course. Special thanks to Dr. Xavier Turon (CSIC-CEABGirona, Spain), Rosana M. Rocha & Nadia Bonnet (Universidade Federal do Parana, Brazil) to stimulate me to finish this manuscript on Chilean ascidians.

REFERENCES

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Corresponding editor: Claudia Bremec

Received: 22 December 2017; Accepted: 21 June 2018

Juan I. Canete (1), Jose L. Lopez (2) & Erika Mutschke (3)

(1) Departamento de Ciencias y Recursos Naturales, Facultad de Ciencias Universidad de Magallanes, Punta Arenas, Chile

(2) Departamento de Biologia, Escuela de Medicina, Facultad de Ciencias de la Salud Universidad de Tarapaca, Arica, Chile

(3) Laboratorio Hidrobiologia, Instituto de la Patagonia, Universidad de Magallanes, Punta Arenas, Chile

Corresponding author: Juan I. Canete (ivan.canete@umag.cl)

Caption: Figure 1. a) Living specimen of Ascidia ceratodes collected under intertidal boulder in the Lisera Beach, Arica, Chile (August, 2016). Bar scale = 20 mm length, b) same specimen without tunic; left view; c) same specimen, right view; white, fine lines are a reticulated of muscle fibers; oral siphon not showed.

Caption: Figure 2. Internal anatomy of Ascidia ceratodes: a) oral siphon in contraction, viewed from the left side, b) atrial siphon, lateral view, c) unknown net associated to stomach and external wall of the posterior intestine; according to Monniot et al. (1991; page 22), could be tubules of the "pyloric gland", d) oral tentacles, e) reproductive ducts and rectum in connection to atrial cavity, f) section of the pharynx, showing the branchial sac and arrangement of transverse and longitudinal vessels, g) primary papillae located at the posterior end of each longitudinal vessel, h) detail of the male gonad, viewed from the left side, i) portion of the male gonad and the first intestinal loop.
Table 1. Locations of specimens of Ascidia ceratodes collected in
northern Chile. All sites were intertidal pools (<1 m depth) with
a bottom dominated by small boulders (30 to 40 cm of size).
Specimens were collected under these boulders. Numbers of
specimens/boulder are shown in brackets.

Location                               Date           Latitude

Arica, Laucho Beach, (2 specimens)   2-8-2016   18[degrees]29'12.26"S
Arica, Lisera Beach, (5 specimens)   2-8-2016   18[degrees]29'34.52"S
Iquique, Huaiquique, (2 specimens)   4-8-2016   20[degrees]16'16.58"S
Iquique, off Regional, Government    5-8-2016   20[degrees]13'03.63"S
Building, (4 specimens)

Location                                   Longitude

Arica, Laucho Beach, (2 specimens)   70[degrees]19'36.00"W
Arica, Lisera Beach, (5 specimens)   70[degrees]19'37.46"W
Iquique, Huaiquique, (2 specimens)   70[degrees]07'52.90"W
Iquique, off Regional, Government    70[degrees]09'21.45"W
Building, (4 specimens)

Location                             T ([degrees]C)

Arica, Laucho Beach, (2 specimens)        19.6
Arica, Lisera Beach, (5 specimens)        18.6
Iquique, Huaiquique, (2 specimens)        17.3
Iquique, off Regional, Government         18.2
Building, (4 specimens)
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Title Annotation:Short Communication
Author:Canete, Juan I.; Lopez, Jose L.; Mutschke, Erika
Publication:Latin American Journal of Aquatic Research
Date:Mar 1, 2019
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