An annotated species list of regular echinoids from Sri Lanka with notes on some rarely seen temnopleurids

The first recorded regular echinoid species from Sri Lanka, “Salmacis virgulatus” (now known as S. virgulata L. Agassiz in L. Agassiz & Desor, 1846), was listed by Agassiz & Desor (1846). Knowledge of Sri Lankan regular echinoids continued to advance until the end of the 19th century. However, there is a gap in knowledge between the mid-20th and the beginning of the 21st centuries due to a lack of systematic studies, with the exception of two checklists published by the IUCN Red List in 2006 and 2012. In the present study, we compiled a species list combining published data and new data based on fieldwork between 2013 and 2015. Echinoids were sampled by snorkelling, diving, examination of fisheries bycatch, and collection of tests from beaches. The updated species list presented in this study includes 39 regular echinoids belonging to 28 genera, nine families, and five orders. Phyllacanthus imperialis (Lamarck, 1816) and Temnopleurus toreumaticus (Leske, 1778), which were not recorded during the last 90 years, were confirmed to still occur in Sri Lanka by the present study. We develop an updated species list of regular echinoids to form a basis for future systematic work. The study recommends further investigation to evaluate the status of deep-sea species and additional field work off the northern and eastern coasts of Sri Lanka.


Introduction
The Echinoidea includes more than 1,000 living species in 70 families (Kroh & Smith 2010;Appeltans et al. 2012), and can be divided into two groups, so-called "regular" and irregular, by considering their gross morphology. Only the latter group is monophyletic. In contrast to irregular echinoids, which are bilaterally symmetric and have the periproct (containing the anus) at the functionally posterior part of the body, the regular echinoids have a pentaradially symmetric body, or test (Serafy & Fell 1985). In these forms, the periproct is within the apical system at the top (aboral surface) of the animal, opposite the mouth situated on the bottom (oral surface) (Mortensen 1928;Durham & Wagner 1966;Melville & Durham 1966;Saucède et al. 2007). The regular echinoids constitute a paraphyletic assemblage (Smith & Kroh 2011) that includes slate pencil urchins (cidaroids), soft-bodied fire urchins (echinothurioids), and other sea urchins (diadematoids, camarodonts, and other carinacean forms) with large spines and a subspherical body (Mooi & Munguia 2014). Regular echinoids are considered keystone epibenthic organisms in rocky substrates and reefs (Barnes et al. 2002;Cebrian & Uriz 2006) as well as in soft bottom habitats (Hardy et al. 2011).
The present study aims to expand the knowledge about the species richness of regular echinoids in Sri Lankan waters. The results of this research, which combines data collected between 2013 and 2015 with that from existing publications, provide an updated, annotated species list of Sri Lankan regular echinoids. species were recorded during the field work are given in Appendix 1. Irregular echinoids collected during the field work were described by Arachchige et al. (2019).
In addition to the data from the present research, published literature, species deposited in the DAF, WUSL, and records of Sri Lankan samples registered in the Invertebrate Zoology collection database of the California Academy of Sciences, San Francisco (CAS) (https:// www.calacademy.org/scientists/izg-collections) were used for the compilation of the species list of "regular" echinoids of Sri Lanka. The specimens at DAF were collected by R.M.G.N. Thilakaratne and S. Jayakody during 2007Jayakody during -2008. Locality information extracted from published literature is given in Appendix 2.
Identification of specimens was based on the keys developed by Mortensen (1928Mortensen ( , 1935Mortensen ( , 1940Mortensen ( , 1943aMortensen ( , 1943b, Clark & Rowe (1971), Schultz (2005Schultz ( , 2011, and on the Echinoid Directory, which is an online key hosted by the Natural History Museum, UK (Smith & Kroh 2011). In addition, we included species that we were unable to examine but which were included in publications with references to Sri Lanka, to create the updated species list. The taxonomic list and nomenclature were organised and updated systematically according to the World Echinoidea Database (Kroh & Mooi 2018).

Results
Fifteen species were recorded and identified during the fieldwork, representing 12 genera, six families, and four orders (Table 1). In addition, two species, Astropyga radiata and Pseudoboletia maculata, were found in the DAF collection. Apart from that, 22 regular echinoid species were added to this species list based on the most recent literature compilation done by Arachchige et al. (2017). Thus, a total of 39 regular echinoid species belonging to 28 genera, nine families, and five orders are included in this species list (Table  1). Two species, Phyllacanthus imperialis and Temnopleurus toreumaticus, are recorded for the first time since they were last mentioned in a scientific publication on Sri Lankan echinoids 90 years ago. The following descriptions report only the new material collected during our fieldwork, plus the two DAF specimens. For details on species records solely based on literature records and not resampled during the present study, see Arachchige et al. (2017). Here, for the first time, we provide photographs of hitherto unillustrated test surface details of poorly known, and seldom encountered temnopleurids now known to occur in Sri Lanka. Sarasin & Sarasin (1887), Döderlein (1888), and Anderson (1894) recorded this species from Trincomalee. One denuded specimen is housed at the Department of Aquaculture and Fisheries of the Wayamba University of Sri Lanka. This specimen was collected from off Trincomalee, but its depth is unknown. white spots along the interradii instead of lines. In addition, there is a prominent red ring around the anus at the tip of the inflated anal sac. This species has been recorded consistently from the southern and eastern coasts of Sri Lanka since it was first mentioned as part of the Sri Lankan echinoid fauna (Bell 1882). According to Lessios et al. (2001), D. setosum contains two mitochondrial lineages that split 3 to 5 million years ago and are now geographically separated. No specimens from Sri Lanka were included in the study by Lessios and co-workers, but species distribution modelling by Bronstein et al. (2017) predicts that the Sri Lankan representatives belong to D. setosum clade a. Genetic analyses are needed to confirm the prediction based on modelling.

Distribution in Sri Lanka. Southern coast of Sri Lanka.
Recorded depth range in Sri Lanka. 1-2 m (present study).

Habitat. Reef flats and tide pools.
Observed occurrence in this study. Southern coast (Hiriketiya, Nilwella, and Polhena) of Sri Lanka.
Remarks. The test of E. calamaris can be distinguished from that of E. diadema by having naked adapical medial zones in the interambulacra, conspicuously inflated aboral ambulacra, no enlarged ambulacral tubercles at the ambitus and small auricles with low connecting ridges in the interambulacra. In life, E. calamaris is easily distinguished from E. diadema in having banded, usually pale or white primary spines, and concentrations of gold or light brown, poison-gland bearing spines in the ambulacra that are much shorter and more sharply pointed than the interambulacral primaries. See Coppard & Campbell (2006) for an in-depth discussion of the test features distinguishing the two species.
This species was recently added to the Sri Lankan echinoid faunal list by Jayakody (2012). Our study confirms the presence of E. calamaris in Sri Lanka. E. calamaris is widely distributed from the western Indian Ocean (Samyn 2003) to the eastern Indian Ocean (Putchakarn & Sonchaeng 2004;Sastry 2007) and beyond (see Clark & Rowe 1971 for a summary).
Observed occurrence in this study. Southern coast (Hiriketiya, Nilwella, and Hikkaduwa) of Sri Lanka.
Remarks. The test of E. diadema differs from that of E. calamaris in having no naked adapical medial zones in the interambulacra, no inflated aboral ambulacra, enlarged ambulacral tubercles at the ambitus, and large auricles with high connecting ridges in the interambulacra. In life, E. diadema tends to be black with bluish iridescence in strong sunlight, and the poison-gland bearing spines are not differentiated in color from the other primary spines.

Distribution in Sri Lanka. All coasts possess suitable habitat for this species.
Recorded depth range in Sri Lanka. 0.1-5 m (present study), 5 m (previous records).
Habitat. Subtidal rocks, common on rocky platforms, in crevices, under boulders, and in coral reefs; well adapted to areas in which wave action is high.

Remarks.
The family Stomopneustidae has only one extant species. S. variolaris can be distinguished from diadematoids (with some of which it might be confused in life) found in Sri Lanka in having imperforate, non-crenulate primary tubercles, broad multiserial pore zones from the peristomial margin to the apex, large ambulacral tubercles, and a comparatively small apical system that is firmly integrated into the corona (not loosely attached by soft tissues as is usually the case in diadematoids). S. variolaris differs from camarodonts in having an open foramen (epiphyses not joined over the teeth in the Aristotle's lantern). Characteristic features of the test include the conspicuously sunken, sinuous interradial sutures and the polygeminate ambulacra with pores that are not aborally arranged in clear arcs.
In Sri Lanka, this species is widely distributed mainly from the southern to the northwestern coasts.

Distribution in Sri Lanka. Southern and western coasts of Sri Lanka.
Recorded depth range in Sri Lanka. 0.5-1 m (present study), 0.5-5 m (previous records).
Habitat. Rocky shores, in rock crevices, among rock boulders, channels, and self-made burrows.
Observed occurrence in this study. Southern coast (Hiriketiya and Hikkaduwa) and the western coast (Beruwala) of Sri Lanka.
Remarks. E. mathaei can be distinguished from the other Sri Lankan echinometrids, except from E. oblonga, in having the test elongated through the axis between ambulacrum I and interambulacrum 3, and only four pore pairs in the pore arcs of the ambulacra.
E. mathaei and E. oblonga cannot be easily distinguished from each other. Mortensen (1943b: 394) admits that "there are no reliable characters in the test distinguishing oblonga from the typical mathaei". Hence, molecular analyses are required to distinguish these species unequivocally, although sperm morphology and spicules have been shown to be very useful in distinguishing some members of the E. mathaei species complex (Arakaki et al.

1998; Bronstein & Loya 2013).
Two colour variants, green and brown, occur in Sri Lanka. There is a high likelihood that more than one species is present on the island, pending full molecular analyses of additional specimens from across the range of echinometrids currently listed under the names E. mathaei and E. oblonga. This species was threatened by the marine curio trade and listed as a protected species in Sri Lanka under the Sri Lankan Fauna and Flora Protection Act (Amendment), No. 22 of 2009. To date, it is the only protected echinoid species in Sri Lanka.
Distribution in Sri Lanka. Southern coast of Sri Lanka.
Observed occurrence in this study. Southern coast (Hiriketiya and Dickwella), on shore. Both of these collection sites were dominated by seagrass beds at shallow depths.

Remarks.
Here, for the first time, we provide photographs of test surface details on this rarely seen temnopleurid (Fig. 2). Its test has never been figured in detail, and Mortensen (1943a) included only a photograph in lateral view, plus drawings of the apical system, ambulacral compounding, and some pedicellariae. M. ceylanicus is restricted to Sri Lanka and the Andaman Islands, and can be distinguished from other Sri Lankan regular echinoids by its light olive-green test. The test has naked interambulacral areas, each of which has a dark zigzag line along the medial sutures (Fig. 2). The spines are banded with red, brown, and white. This species is characterized by its sharply delimited naked areas in both the interambulacra and ambulacra (Mortensen 1942). Döderlein (1888) misidentified this species as M. maculatus, an error that was rectified by Mortensen (1943a). The type specimen, collected from Sri Lanka, is housed at the Zoologische Staatssammlung München (The Bavarian State Collection of Zoology, Munich). Material studied. WUSL/ER/236, 237, 238 (wet, with spines) from Godawaya; WUSL/ER/239 (dry, with spines) from Nilwella; WUSL/ER/240 (wet, with spines) and WUSL/ER/241 (dry, with spines) from Mandathiv; WUSL/ER/242 (wet, with spines) and WUSL/ER/88, 243 (dry, with spines) from Nagadeepaya; WUSL/ER/244, 245 (dry, with spines) from Point Pedro.

Distribution in Sri Lanka. Northern, southern, and western coasts of Sri Lanka.
Recorded depth range in Sri Lanka. 1-5 m (present study), 4-55 m (previous records).

Habitat. Rocky shores, among boulders and seagrass.
Observed occurrence in this study. Northern coast (Mandathiv, Nagadeepa, and Point Pedro) and the southern coast (Godawaya and Nilwella) of Sri Lanka.
Distribution in Sri Lanka. Northern, southern, and northwestern coasts of Sri Lanka. Recorded depth range in Sri Lanka. 9-12 m (present study), 59 m (previous records).

Habitat. Among seagrass beds and coral rubble.
Observed occurrence in this study. Northern coast (Mandathiv, Mulathiv, Nagadeepa, Point Pedro, and Silavathurai) of Sri Lanka.

Remarks. S. virgulata can be distinguished from others in the genus in having uniformly
purplish, unbanded primary spines with whitish bases (Fig. 4).
This was the first echinoid species recorded to occur in Sri Lanka by Agassiz & Desor (1846), who cited the locality as "Ceylan" (Sri Lanka) for "Salmacis virgulatus", an incorrect formulation of the name. The holotype (EcEh 5940) is from Sri Lanka, and is housed at the Muséum National d'Histoire Naturelle, France (Vadon et al. 1984).

Discussion
This updated checklist records 39 regular echinoid taxa found in the waters around Sri Lanka. The present research added no new records or new species to the most recent checklist compiled by Arachchige et al. (2017). However, it does provide confirmation for occurrence in Sri Lanka of Phyllacanthus imperialis and Temnopleurus toreumaticus since their last recorded sightings 90 years ago (see Arachchige et al. 2017). Out of the 39 echinoid taxa, 16 species had been recorded in the literature from waters deeper than 30 m and as such, were considered deeper water regular echinoid species (Table 1). Stylocidaris albidens and Desmechinus versicolor were also included with the deep-water regulars using the criteria of Schultz (2011), although precise depths were not recorded. Out of the 16 deep-water species recorded in the previous studies, only one species, Salmacis virgulata, was recorded during this study because of our focus on shallow-water species. Distribution data for Acanthocidaris sp., Stylocidaris albidens, Colobocentrotus (Podophora) atratus and Salmacis belli could not be found during the fieldwork and these species were historically mentioned solely with the indication "Ceylon or Sri Lanka" in the literature.
Based on the records of Clark (1925), Colobocentrotus (Podophora) atratus was included in the present species list. However, Clark does not cite an exact location, collector, or any other description, providing only a citation in a list of species found in the collection of the Museum of Natural History, UK and giving the distribution of C. (P.) atratus as "Ceylon".
As this is a littoral species restricted to the surf zone (Mortensen 1943a), it is not clear how a commonly reported littoral species has remained entirely unknown to other collectors in Sri Lanka apart from Clark's single record. This situation could pertain if the species is very rare, even though it is littoral in Sri Lankan waters. Therefore, there remains no verified presence of this species in Sri Lanka and the reported locality "Ceylon" may be attributed to an erroneous label. C. (P.) atratus is well known from Kenya in the western Indian Ocean (Samyn 2003) and the Andaman Sea in the eastern Indian Ocean (Putchakarn & Sonchaeng 2004;Sastry 2007), suggesting that it could potentially occur in Sri Lanka. However, it has not been recorded from the southeastern Arabian Sea (Parameswaran et al. 2017).
P. forcipulatus is also known in the Indian Ocean from Madras, India (Schultz 2011). On the other hand, S. indica is well known throughout the Indo-Pacific from the Arabian Sea to the Philippines and Japan (Mortensen 1928;Schultz 2011), as well as the Andaman Sea (Sastry 2007). Similarly, S. biseriatum has been recorded from the west of Sri Lanka in the Laccadive Sea by Koehler (1927). This species is also known from Kenya, the Arabian Sea, and South Africa (Clark & Courtman-Stock 1976). P. bursarium is well known from the southeastern Arabian Sea (Parameswaran et al. 2017) and the Andaman Sea (Sastry 2007). P. indiana is recorded from the Indian Ocean from eastern Africa and Madagascar (Clark & Rowe 1971). T. siamense is well known from the Indian Ocean from the Arabian Sea (Samyn 2003) to the Andaman Sea (Putchakarn & Sonchaeng 2004). Conversely, S. roseoviridis is only known from the Indian Ocean from off Sri Lanka and off the coast of Myanmar (Burma) (Mortensen 1943a;Schultz 2011). The known ranges of these species suggest that there is a high probability of occurrence of these species in Sri Lankan waters, thus making it unlikely that the single records of the species discussed in this paragraph are all based on misidentifications.
P. bispinosa, S. belli, and D. versicolor have been recorded only once from Sri Lankan waters. These are the only records available for the entire Indian Ocean. Herdman et al. (1904) recorded P. bispinosa from Sri Lankan waters. This is the only available distribution record in Clark and Rowe (1971) for this species in the Indian Ocean. However, this species is known from the Gulf of Thailand (Putchakarn & Sonchaeng 2004). S. belli has been documented from Sri Lankan waters only by Jayakody (2012). This species is distributed widely in the Pacific Ocean from the Philippines, the Malayan Archipelago, and the northern coast of Australia (Clark & Rowe 1971;Miskelly 2002;Mooi & Munguia 2014;Schultz 2005). The only available record for D. versicolor in the Indian Ocean was given by Mortensen (1943a: 345, 346). He provided coordinates for a single specimen collected from off south Sri Lanka by the R.I.M.S. "Investigator". This species is known from the Indo-Pacific, specifically from the Kei Islands, Indonesia to the China Sea (Mortensen 1943a). The ranges of all these species are consistent with the possibility that future surveys will confirm the presence of P. bispinosa, S. belli, and D. versicolor in Sri Lanka.
No management plan for the conservation and sustainable utilization of any taxon can be implemented successfully without basic biological and ecological information. Because echinoids are rapidly becoming exploited commercially as a marine delicacy (Scheibling & Mladenov 1987;Johnson et al. 2012) and are exported as decorative objects, it is time to evaluate the current status of sea urchins in Sri Lanka, and to develop new identification guides for the use of stakeholders in these growing industries. Reliable taxonomic data are also required to fill gaps in our knowledge of the ecological roles of echinoids along Sri Lankan shores. The data in the present study can be used for future work on the regular echinoid fauna of Sri Lanka, particularly in the assessment of population sizes, spatial distribution, local trophic networks, and threats to biodiversity due to natural and anthropogenic changes. Furthermore, systematic deep-water surveys are needed to increase our knowledge of echinoid species diversity in Sri Lankan waters.

Supplementary Material
Refer to Web version on PubMed Central for supplementary material.