The shallow-water chitons (Mollusca, Polyplacophora) of Caldera, Region of Atacama, northern Chile

The Molluscan species of the northern littoral of Chile have been sparsely studied. This work reviews for the first time the diversity of polyplacophoran molluscs around the port of Caldera, in the Region of Atacama (26°45’49”S; 70°45’17”W to 27°20’23”S; 70°56’46”W), northern Chile. Eleven species were found in this study: Acanthopleura echinata (Barnes, 1824); Callistochiton pulchellus (Gray, 1828); Calloplax vivipara (Plate, 1899), Chaetopleura peruviana (Lamarck, 1819); Chiton cumingsii Frembly, 1827; Chiton granosus Frembly, 1827; Chiton magnificus Deshayes, 1827; Enoplochiton niger (Barnes, 1824), Radsia barnesii (Gray, 1828), Tonicia atrata (G. B. Sowerby II, 1840) and Tonicia chilensis (Frembly, 1827). All of the species occurring in the area have distributions in the southeastern Pacific Ocean, from Ecuador to central Chile, and three of them are species endemic to the Chilean coasts (Calloplax vivipara, Radsia barnesii, and Tonicia atrata). This diversity of species is comparable to that of better surveyed faunas of central and southern Chile or Patagonia. Of the eleven species recorded, the geographic distribution records for Callistochiton pulchellus, Radsia barnesii and Tonicia atrata are extended, and Calloplax vivipara is found alive again after 40 years, filling a gap in its known distribution. Illustrations of living specimens in their habitat, distribution records and a taxonomic key for all the studied taxa are also provided.


Introduction
Research on marine molluscs of northern Chile began with the descriptions of some species by Sowerby (1832), d'Orbigny (1847), Hupé (1854) and Philippi (1860) in the late 19 th century. Further works include the studies done by Dall (1909), mostly in deep water areas along the Chilean and Peruvian coasts; Gigoux (1934), which listed the species found in the Region of Atacama, Marincovich (1973), describing the intertidal molluscs of Iquique; Acuña (1977), Bretos (1980), Bretos et al. (1983) and McLean (1984) dealing with fissurellid limpets and, more recently, the works of Guzmán et al. (1998) which studied material from between Iquique (20°S) in northern Chile to Punta Arenas (53°S) in the extreme south of the country. Most of the subsequent works dealing with chitons have been focused on species from central and southern Chile (Castellanos 1948, 1951, Stuardo 1959, Osorio and Reid 2004, Schwabe and Sellanes 2004, 2010, Sirenko 2006, with a few works including shallow water species (Schwabe et al. 2006, Sirenko 2007. Further recent works including species from the Region of Atacama or northern Chile in particular only include the Kaas and Van Belle monograph series (Kaas and Van Belle 1985a, 1985b, 1987, 1990, 1994 which studied the worldwide chitons and, among them, Chilean species. This molluscan class is often overlooked in Chile, as their species are mostly small and hard to collect and to preserve, however, three of the large species of Chilean chitons (Acanthopleura echinata (Barnes, 1824), Chiton (Chiton) magnificus Deshayes, 1827 and Chiton (Chiton) granosus (Frembly, 1827)) are collected with gastronomic purposes (Osorio 2002), and some species are used in traditional medicine in northern Chile. Chitons play a role in controlling the green algal cover in mid-intertidal exposed rocky-shores of central Chile (Aguilera and Navarrete 2007) eating encrusting corallines (Camus et al. 2012), newly settled barnacles (Aguilera 2005) and other sessile and mobile invertebrates , and thus they have a direct impact on the intertidal ecosystem.
The coast of the Region of Atacama consists of rocky formations of volcanic origin with a few sandy beaches. The intertidal area of most of the coast, with the exception of a few scattered bays, is narrow (up to 20 m) and presents a diverse geography including cliffs, rocky plat- forms, intertidal pools, and boulder fields. The exposed side of rocks and boulders are exposed to strong surf, with just a few sheltered areas, particularly in the area of the Bay of Caldera, Obispito and Calderilla (Table 1). This work presents an overview, with distributions and illustrations, of all the species of Polyplacophora found in the Region of Atacama, northern Chile. The distribution range and a taxonomic key to all the studied species is also provided. The aim of this preliminary paper is thus to contribute on the knowledge of the molluscan fauna, in particular of northern Chile.
Description. Animal of small size, up to 11.5 mm in examined specimens, elongate oval, moderately elevated, color of tegmentum creamy white or bright white. Head valve semicircular, sculpture with 10-15 low rounded, equally spaced, nodulose, annulate, radial ribs, becoming obsolete towards the apex, the posterior ribs being strongest and more nodulose. Intermediate valves rectangular, lateral areas well defined, sculptured with two strong radial ribs. Central area with two series of equally spaced, diagonal lirae, forming rounded depressions in the interspaces. Tail valve semi-oval, slightly less wide than head valve, sculptured like head valve, with 8-11 weaker radial ribs. Girdle rather wide, yellowish white, dorsally covered with small, oval, imbricating scales (After Kaas and Van Belle 1994).

Material examined.
Specimens found under sunken rocks in tidal pools in Playa El Pulpito (SBMNH 452240, 1 speci men), Sur de Playa Ramada and Playa El Pulpo (Table 1).
Remarks. This is a small (under 12 mm) chiton, easily overlooked but for its bright whitish color. It is a fairly rare species; they were not abundant and were found only in two of the studied locations (Table 1), under rocks sunken in tidal pools, associated to small communities of Acar pusilla Sowerby, 1832, Liotia cancellata Gray, 1842, Rissoina inca Sowerby, 1832, encrusting algae and sponges. It has been reported that this species feeds on sponges, bryozoa and diatoms (Aguilera 2005). This species can be mistaken for Calloplax vivipara (Plate, 1902), differing from this species in having a less elongate body shape, with a much finer and subtle sculpture (especially noticeable on the terminal valves), it differs from C. vivipara in having rounded depressions in the central-lateral areas of the valves, especially in the middle valves.
Remarks. This is a rare species, found in only two of the locations under study; in both places this species was found under rocks sunken in tidal pools, associated to encrusting sponges and to communities of the small mussel Brachidontes granulata (Hanley, 1843). According to Plate (1899) this species is ovoviviparous; that cited author found about 15 embryos, some with seven shell valves, in the ovary of a single specimen. In fact, this is the only chiton species ever reported to be ovoviviparous (Pearse 1979). This species is somewhat similar to Callistochiton pulchellus (Gray, 1828), differing in the coarse sculpture (especially in the anterior valve, with fewer and stronger ribs), the presence of longitudinal riblets in the central areas, and the more yellowish body color.  fig. 2A.

Description.
Animal of medium to large size, up to 45 mm long in examined specimens. Oval to elongate oval, slightly depressed, color of tegmentum greenish-brown to dark brown. Head valve semicircular, front slope straight, posterior margin V-shaped. Intermediate valves broadly rectangular. Tail valve less than semicircular, almost as wide as head valve. Girdle profusely beset with very long (up to 10 mm) thick, coarse, corneous hairs, not only interspersed throughout girdle but in girdle bridges, protruding at sutures and extending over valves. Tegmentum pustulose sculptured with minute and neatly separated pustules, on the end valves the pustules are arranged in radiating rows. Body width/length, mean 0.66; height/ length, mean 0.22 (After Ferreira 1983).
Material examined. Specimens found in almost all locations, with the exception of Bahia Cisne, Puerto Viejo and Playa Rodillo up to Obispito (Table 1). Calderilla (MPC-CL 3072014C, 1 specimen).
Remarks. This species is easily distinguished from all other chitons in the region by the presence of hairs covering the valves and sutures. A similar species, Chaetopleura (Chaetopleura) benaventei Plate, 1899 is slightly smaller in size and differs in the overall coloration and in the absence of the corneous bristles. Chaetopleura hennahi (Gray, 1828) found between El Callao, Peru and Arica, Chile (Kaas and Van Belle 1987) has a wine-red to reddish brown tegmentum and lacks the blackish corneous hairs which protrude at the sutures in Chaetopleura peruviana.

Acanthopleura echinata (Barnes, 1824)
Plate 1, Fig. 1; Table 2 Chiton echinatus Barnes, 1824: 71, pl Description. Animal of very large size, up to 158 mm in examined specimens. Tegmentum smooth to shiny (but often eroded), dark reddish-brown, with occasional small blue spots. Lateral areas hardly raised, smooth except for two radial rows, one of 5-9 round granules indenting sutural edge. Anterior valve with some 10 radial rows of round granules; space between rows smooth. Central areas with raised, well-defined, smooth jugal band bordered by shallow, longitudinal grooves with short, wavy, longitudinally oriented riblets on pleural areas. Girdle upper surface with erect, strong, spike-like spines, round in cross section, up to 8 mm long in large specimens (longer if not broken), often encrusted. Girdle bridges empty (After Ferreira 1986). According to Osorio (2002) this is a dioecious species, which can reach a maximum length of 200 mm.
Material examined. Specimens found in two locations; Norte Bahía de Caldera (MPCCL 3072014A, 1 specimen) and in Playa Mansa, in subtidal areas in exposed rocks and in rocks associated with the giant kelp Lessonia nigrescens Bory de Saint-Vincent, 1826.
Remarks. This is one of the largest polyplacophoran in Chile, differing from the also large Enoplochiton niger in having conspicuous spines in the girdle, not sparse scales as in E. niger. This species prefers the subtidal zone and wave-exposed shores, and it is often covered with algae and epibionts (Scurria species, Mytilus species, etc) which allow this species to blend in with its surroundings. The spines are often covered with encrusting algae in older specimens. This is a commercially important species (Osorio 2002).
1/3 of girdle), up to 1.5-2 mm long in specimens 50 mm long (larger in larger specimens), vaguely striate, usually eroded at upper edge, clearly separated from each other by area as wide as scale; on outer 1/5 of girdle, scales much smaller, shorter, dark brown, erect, spine-like; girdle surface completely covered otherwise with minute, dark brown, lanceolate spicules, up to 100 μm long, 25 μm thick. Girdle bridges, empty in middle third, but crowded with small, dark brown spiculoid elements (akin to those on girdle proper) in outer thirds (After Ferreira 1986).
Material examined. Specimens found exposed on large boulders in the surf-zone, in Playa Rodillo, Playa El Pulpito (MPCCL 3072014E, 1 specimen) and in Norte Bahía de Caldera.

Remarks.
With sizes up to 200 mm (Sanhueza et al. 2008), this is one of the largest polyplacophoran species in the country. It lives almost exclusively in exposed rocks or in the surf zone. Although this species is mostly herbivore, it has been described also as a generalist polyphagous consumer, and a potential omnivorous, (Sanhueza et al. 2008). A brown-colored variety of the limpet species, Scurria variabilis (Sowerby, 1839), lives on the valves of this species, having been found in all the specimens examined in this study. An unidentified barnacle was also observed on the valves of a few specimens. In some places (Rodillo beach, Obispito bay; Table 1) juvenile specimens can be found among crevices of large boulders. It was observed that this species is predated by the common gull, Larus dominicanus (Lichtenstein, 1823), an omnivore species that also predates on the intertidal large keyhole limpets of the genus Fissurella (Bahamondes & Castilla, 1986).

Chiton (Chiton) cumingsii Frembly, 1827
Plate 1, Fig. 5; Table 2 Chiton cumingsii Frembly, 1827: 198, suppl. pl. 16, fig. 3;Dall 1909: 247.  Remarks. This colorful species is the most common and abundant chiton distributed in the zone; found in almost all the locations. It is commonly found in accumulations of several individuals on the underside of rocks at low tide, crawling quickly to the dark if exposed to sunlight. Among the examined specimens, some of them had a pink/orange coloration when juveniles with some adult specimens retaining a uniform pink coloration. This species has been cited as an introduced species in Las Palmas Port, Canary Islands (28°06'N, 15°25'W), being one of the few alien polyplacophoran found in European waters (Arias and Anadón 2013).
Remarks. This species is somewhat uncommon in shallower waters; it is found mostly in crevices and in rocky outcrops, mostly in clustered distributions. Juvenile specimens are somewhat similar to the juvenile specimens of Chiton cumingsii differing in the paler coloration (of various shades of green), the granulation on the valves and in the overall wider body. It has been reported that this species feeds on barnacle cyprids (Moreno and Jaramillo 1983, Aguilera 2005) and is preyed on by the common gull Larus dominicanus (Lichtenstein, 1823). It was observed also that some specimens had barnacles on the valves. This species is a physiological omnivore, having the digestive flexibility and enzymatic capacity to digest and assimilate animal preys (Camus et al. 2009) and it is also a commercially important species (Osorio 2002).  Bullock (1988: 163).

Chiton (Chiton) magnificus Deshayes, 1827
Description. Animal of large size, reaching 115 mm in examined specimens. Body dark bluish-grey, broad-oval, slightly carinated, rather flat. Valves flattened to moderately carinated. Anterior valve sligthtly convex, semicircular, with wide V-shaped to straight posterior margin unnotched in middle, with numerous radially arranged, shallow ribs; intermediate valves rectangular with slight-ly concave posterior margin at both sides of faintly protruding apex, lateral areas slightly elevated, sculptured with up to 5 radial ribs between a wider diagonal ridge and a very wide posterior rib; tail valve semicircular with an anterior mucro; post-mucronal area with same sculpture as head valve and lateral areas (After Schwabe et al. 2006). According to Osorio (2002), this species can reach a maximum length of 174 mm.
Material examined. Specimens found in Aguas Verdes, Sur de Playa Ramada and in Playa Chorrillos, in subtidal areas attached to large boulders.
Distribution. Bullock (1988) gives a distribution for this species from Isla San Lorenzo, Peru south to Bahía Tictoc (43°36'40"S; 72°57'15"W), Chiloé Province, southern Chile. This species can be found in rock pools and boulder fields with strong water exchange, from the intertidal down to a maximum of 30.5 m depth at the Comau Fjord (42°23'S; 72°27'W), Region of Aysén (Schwabe et al. 2006). Smith and Ferreira (1977) considered the records of this species from Galapagos Islands as erroneous.

Remarks.
A shiny, large and conspicuous chiton, this species has been overlooked in recent molluscan literature, being cited by Valdovinos (1999) as Chiton latus and by Osorio (2002) as Chiton magnificus boweni. It seems to be an uncommon species, restricted to specific localities along the coast of Chile. Juvenile specimens may be misidentified as Chiton cumingsii, differing from this species in having a wider and flatter body, with smoother sculpture and with bright blue spots on the valves, which are cream white to greenish yellow in color. Apparently, in northern Chile this species is found only in subtidal areas. This is a commercially important species (Osorio 2002).
Material examined. Specimens found in three locations; Peninsula Calderilla, Sur de Playa Ramada and in Playa El Pulpo Beach (Table 1). Collected under rocks and rock slabs, Peninsula Calderilla (MZUC 39614, 1 specimen).
Remarks. This species was uncommon in the zone under study; only a few specimens were found in the undersides of rocks at low tide. This species is clearly identified from the other species found in this work by having a wide, flat shell, with narrower valves and a pattern of clear and darker alternating bands in the girdle. It can be misidentified as Chiton granosus; differing from this species in the smaller size, the much smaller girdle scales, a much weak valve sculpture and in the alternating bands of the perinotum, absent in Chiton granosus.
Description. Animal of medium to large size, reaching 51 mm in examined specimens. Shell elongate-oval, moderately elevated, subcarinated dorsum. Color reddish brown to blackish purple. Head valve semicircular, with straight posterior valve margin unnotched in middle; intermediate valves broadly rectangular, with distinct protruding apex and concave posterior valve margins. Lateral area hardly elevated, but clearly indicated by faint depression in front of diagonal ridge. Jugal area weakly developed, but showing partly a more or less distinct keel, especially in the more posterior intermediate valves. Tail valve with centrally situated, forward-directed, and slightly elevated mucro, straight antemucronal area and rather steep, straight postmucronal slope. Jugal area of tail valve extending towards anterior. Tegmentum without sculpture, except for growth marks and faint radial striations on terminal valves and lateral areas. Perinotum wide and fleshy (After Schwabe et al. 2006).
Distribution. According to Reid and Osorio (2000), this species distributes in Chile between 40°S and 54°S, at Tierra del Fuego and around the Falkland Islands. The species ranges in depth from the low eulittoral to a depth of 36 m (Schwabe et al. 2006). The record presented here (at 27°S) is now the northernmost record for this species.
Remarks. Two specimens of this species were found in a single location; among a community of Tonicia chilensis, from which it distinguishes in attaining larger sizes and in having a darker body and almost smooth valves with minute granulation at the sides. It is interesting to note also that the valves of the examined specimens were widely separated, almost as in Tonicia disjuncta (Frembly, 1827). The presence of this species extends considerably the northernmost record of this species in about 1040 km (from 40°S to 27°S).
Description. Animal of medium to large size, reaching 43 mm in examined specimens. Shell elongate-oval, not much elevated, the dorsal ridge rounded, side-slopes straightened. Color umber-brown at the sides, becoming chestnut in the middle, delicately and peculiarly speckled and blotched and streaked with buff or buff-white. Lateral areas hardly raised, but separated from the central areas by an obtuse diagonal ridge bearing a series of low tubercles, sometimes subobsolete; sculptured with subradiating rows of small granules, and showing a band of irregularly placed black eyes on the forward part. Central area of second valve having in the middle, a keel or a group of lirae; central areas of the other valves having a narrow smooth dorsal band with several longitudinal furrows on each side of it; and at the sides there are longitudinal diverging delicate rows of granules. End valves radially sub-granulate, and crowded with eye-spots subradially arranged (After Pilsbry 1893).
Material examined. Specimens found on rocks at low tide in Aguas Verdes, Sur de Playa Ramada, Playa Mansa (MPCCL 3072014F, 1 specimen), Sur Bahía de Caldera and in Calderilla.
Distribution. According to Reid and Osorio (2000) this species distributes in Chile and Peru between latitudes 12° and 54°S. It has a bathymetric range from 0-28 m (Schwabe et al. 2006).
Remarks. This species has large and colorful mantles and plates of variable shades, which are similar to the encrusting calcareous algae commonly found in the rocky coasts. Due to the high diversity of forms, several synonyms have been described (see Kaas and Van Belle 1998), and this species needs a complete revision according to Schwabe et al. (2006). This species was found only in the lower intertidal to the subtidal areas, especially in protected locations. Schwabe and Sellanes (2010) reported 41 species of chitons from Chilean waters. Our results from the Region of Atacama, with eleven species found, accounts for 27 % of those reported species. All of the species occurring in the area have distributions in the southeastern Pacific Ocean, from Peru to southern Chile, with Calloplax vivipara, Radsia barnesii and Tonicia atrata as the only species endemic to the Chilean coast. The polyplacophoran diversity of the Region of Atacama is thus comparable to that described for southern areas of Chile, including central Chile (Aldea and Valdovinos 2005), the Comau fjord (Schwabe et al. 2006) and the Estero Elefantes and Laguna San Rafael areas (Osorio and Reid 2004), from where a similar diversity of this molluscan class has been recorded (with eleven, nine and nine species, respectively). With the exception of Callistochiton pulchellus, all of the species found in the Region of Atacama also occur in central and southern Chile.

Discussion
All of the studied species can be classified in two main groups according to their habitat; species with a higher relative frequency on exposed areas include the very large species Acanthopleura echinata and Enoplochiton niger. The other group includes species associated with protected intertidal areas: Callistochiton pulchellus, Calloplax vivipara, Chiton cumingsii, Chiton granosus (mostly found in rock fissures and crevices) and Radsia barnesii. Chiton magnificus was found in the Region of Atacama only in subtidal areas, always near large boulders in holdfast communities of the giant kelp Lessonia nigrescens. Chiton magnificus, however, is much more common in central and southern Chile, being found mostly in intertidal areas (Osorio 2002). The small-bodied species, Callistochiton pulchellus and Calloplax vivipara, were always restricted to submerged rocks in the bottom of tidal pools. This last habitat may explain the feeding behaviour of these small species, living over encrusting sponges and calcareous algae. Regarding feeding preferences; most of the large species of chitons from the Region of Atacama should have generalist diets, however it is possible that the smaller species have more specific diets, for example feeding in sponges, algal species, diatoms or barnacles.
The new distribution records of Callistochiton pulchellus, Radsia barnesii and Tonicia atrata and the new record of Calloplax vivipara may reflect the lack of sampling in the Atacama region or in northern Chile in general, where the scientific studies on invertebrates are still lacking. In particular, Callistochiton pulchellus and Calloplax vivipara may be more widespread in the country; however their particular habitat (and small adult size) may prevent their sampling by traditional methods. Some of these species may have also been overlooked or misidentified as juvenile specimens of other chiton spe-cies (for example Radsia barnesii as Chiton granosus). The considerable new range extension of Tonicia atrata found in this study may reflect the current complicated, unresolved status of the genus Tonicia in Chile; the revision of some particular species or species-groups is thus imperative, considering the great diversity in the valve and mantle morphology, which has derived in a large synonymy for some species, for instance for Tonicia chilensis (Schwabe et al. 2006).
The absence of other species, for example those cited by Valdovinos (1999) in the last complete revision of the Chilean mollusks (which have been traditionally considered as having distribution records in northern Chile), including Acanthochitona hirudiniformis (Sowerby, 1832), Acanthopleura granulata (Gmelin, 1791), Chaetopleura benaventei Plate, 1902, Chaetopleura hennahi (Gray, 1828), Ischnochiton imitator (Smith, 1881), Ischnochiton (Ischnochiton) punctulatissimus (Sowerby in Broderip & Sowerby, 1832) or Ischnochiton pusio (Sowerby, 1832) may be explained because the sampling activities in the Region of Atacama were restricted to, at most, sublittoral areas (2 m depth). Deep water areas must definitely harbor more unrecorded or undescribed species, as is the case with other invertebrate groups like sponges (Reiswig and Araya 2014) or stony corals (Araya et al. in prep.). It is, then, very probable that the number of chitons known from the Region of Atacama, or northern Chile in general, will increase with larger collecting efforts, including additional sampling methods such as dredges and samples from greater depths, even subtidal waters (incorporating also the bycatch of the commercial deep water fisheries). Like other zones of Chile, the deep water areas off Caldera (or off northern Chile in general) have not been investigated in detail and could yield interesting results.

Identification key
This key is primarily macroscopic (intended for identification of adult specimens) including external characters as shell features and general girdle features.