Taxonomy of family Benthopectinidae (Echinodermata: Asteroidea) in the Mexican waters of the Gulf of Mexico

Introduction: The family Benthopectinidae is composed of deep-sea sea stars distributed in eight genera and approximately 70 valid species. So far, only five species of this family have been reported for the Mexican waters of the Gulf of Mexico. Objective: To provide an updated local taxonomy of this family. Methods: A total of 566 specimens deposited in the Echinoderm National Collection, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, and the National Museum of Natural History, Smithsonian Institution, collected from 1952 to 2015, were taxonomically examined. Results: We present descriptions, photographs, and an illustrated dichotomous key for Benthopecten simplex simplex, Cheiraster (Barbadosaster) echinulatus, Cheiraster (Cheiraster) planus, Cheiraster (Christopheraster) blakei, and Cheiraster (Christopheraster) mirabilis in the region. Conclusions: The five studied species represent 6 % of the world biodiversity of the family and can now be identified with the illustrated key.

The species of this family are characterized by having five very large pointed arms, longitudinally flexible dorso-ventrally and are characterized by having a single pair of muscle bands over the arms. The disc is small, the papular areas are restricted to the proximal region of each arm, and the marginal plates are alternating and overlapping (Downey, 1973;Clark & Downey, 1992;Benavides-Serrato, Borrero-Pérez, & Diaz-Sanchez, 2011). The taxonomy of the family has only been reviewed by Ludwig (1910) when describing it as the order Notomyotida. Later, Fisher (1911a) and Verrill (1915) made some additions and modifications on the taxonomy of the Pacific species. Since then, it was only A.M. Clark (1981) and A.M. Clark & Downey (1992) who reviewed the Atlantic species. The latter works are the most important in terms of genera and species taxonomy.
The biology and distribution of the Atlantic species of Benthopectinidae has been studied by some authors (Pain et al., 1982;Vázquez-Bader et al., 2008). There are also some taxonomic studies (Mortensen, 1927;Downey, 1973;Benavides et al., 2011) and checklists of species Laguarda-Figueras et al., 2005;Alvarado & Solís-Marín, 2013). However, to date, there have been no taxonomic studies on the species found in the Mexican waters of the Gulf of Mexico. The aim of this work is to contribute to the study of deep-sea Benthopectinidae in this area and to update the external morphological characters with taxonomic value.

MATERIALS AND METHODS
Specimens from the five species of Benthopectinidae reported for the Mexican waters of the Gulf of Mexico deposited in the Echinoderm National Collection at the Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico (ICML-UNAM) and the United States National Museum of Natural History, Smithsonian Institution, United States National Museum of Natural History, Smithsonian Institution, Washington, D. C. (USNM), collected from 1952 to 2015, were taxonomically analyzed and measured using a digital caliper (TRUPER Caldi-6MP), the following measurements were taken in each specimen, if possible: major (R) and minor (r) radius in order to obtain the R/r ratio. For the taxonomic identity of the specimens, identification guides, original diagnosis and specialized literature were used (Perrier, 1881;Perrier, 1894;Sladen, 1889;Ludwig, 1910;Fisher, 1911a;Fisher, 1911b;Verrill, 1899;Verrill, 1915;Mortensen, 1927;H.L. Clark, 1941;Downey, 1973;A.M. Clark, 1981;Clark & Downey, 1992). Photographs of external taxonomical characters of each species were taken with a multifocal microscope Leica Z16 APOA at the Laboratorio de Microscopía y Fotografía de la Biodiversidad II (Instituto de Biología, Universidad Nacional Autónoma de México). A dichotomous identification key was elaborated, for which the main morphological characters used were: shape of the abactinal plates; location, shape, and number of marginal spines; shape and arrangement of papular areas; and the presence and number of spines and spinelets.
Dichotomous key to the genera, subgenera, and species of the family Benthopectinidae of the Mexican waters of the Gulf of Mexico 3. Parapaxiliform abactinal plates, not markedly convex, the most proximal crowded and highly variable in size, most of the larger plates ornamented with a central spine of more than 2 mm long surrounded by small spinules. Papular areas loosely joined and fused proximally only in large specimens, numerous pores, very small (subgenus Christopheraster). Disc spines moderately long centrally, but not more than ½ of R, spaced and frequently extending to papular areas, gradually decrease in size until reaching that of a spinelet. Marginal spines similar in size . . . . . . . . . . . . . Cheiraster (Christopheraster) blakei 3'. Few relatively very large spines, rarely more than 15, restricted to the center of the disc, without gradually decreasing in size to that of a paxillary spinelet; the spine of the fourth superomarginal plate is conspicuously enlarged, mainly widened at base and fourth inferomarginal plate reduced and sometimes without any spine. . . . . . . . . . . . . Cheiraster (Christopheraster) mirabilis 4. Irregular papular areas, restricted to the arm base and distally bilobed (except in small specimens, < 50 mm), lobes may be unequal (
Remarks: The bathymetric range of this species is extended to its shallower limit, since it was previously reported from 130 to 5 062 m (Clark & Downey, 1992;Benavides-Serrato et al., 2011), and in the present work it has been found at 29 m depth. There are two types of pectinate pedicellariae, the first ones are mounted on the surface of the actinal plates with a rounded margin, and the second ones are located between two actinal plates, half of the pedicellariae in one plate and the other half on the other, with irregular margins. These pedicellariae are not exclusive of the species, but it is important to note that both types may be observed in the same specimen, unlike the other four species that generally have only one type of pedicellariae. This was observed only in 14 % of the reviewed specimens.
Cheiraster ( Verrill, 1915;Clark & Downey, 1992): R = up to 120 mm approximately, R/r = 6.1-8.9. Disc considerably broad and arms are very long and slender, abactinal plates are uniform in size, rounded and convex with a group of spinules. On the proximal plates the average number of spinules is 10, forming a ring surrounding a central spinelet (Fig. 3A). Papular areas start with one big single median pore and develop into two double U-shaped series, being irregular only in the biggest specimens. The plates of the papular areas next to the madreporite and in the central part of the disc are larger than the rest and have numerous spines. Marginal spines are well developed, conical and broad at the base. Superomarginal spines are distinctively larger than the corresponding inferomarginals (Fig. 3C), the rest of the plate is covered with fine spinelets and there is only one accessory spine. Adambulacral plates have six to nine rounded spines and one conical subambulacral spine mounted on a convex protuberance (Fig.  3D). Pectinate pedicellariae present on the actinal plates and on the inferomarginal plates (Fig. 3B). Remarks: The bathymetric range of this species is extended to its shallower limit, since it was previously reported from 226 to 1 339 (Alvarado & Solís-Marín, 2013) and in the present work it has been found at 86.6 m depth.
Remarks: The bathymetric range of this species is extended to its shallower limit, since it was previously reported at 380 m (Alvarado & Solís-Marín, 2013), and in the present work it has been found at 342 m depth.

DISCUSSION
The family Benthopectinidae corresponds to a group of organisms that occur mainly in deep waters and whose species richness consists of eight genera, and approximately 70 valid species (Mah & Blake, 2012). This family is the only one included in the order Notomyotida described by Ludwig (1910). Mah and Foltz (2011) suggested a phylogenetic hypothesis from Valvatacea and Paxillosida orders, in which the family Benthopectinidae was supported as a sister group to Pseudarchasteridae Sladen, 1889 and was included within the order Paxillosida. This was supported by Mah and Blake (2012) since they have shown close morphological resemblance to the Goniasteridae Forbes, 1841 family, as both families occur primarily in deep-sea or high-latitude and correspond to widely distributed taxa. Also, Linchangco et al. (2017) placed the order Paxillosida as sister to Cheiraster sp., showing results similar to those presented by Mah and Foltz (2011), since they did not use morphological characters either. However, in this study, the Benthopectinidae family was considered within the order Notomyotida, following the classification proposed by A.M. Clark & Downey (1992), until a phylogenetic reconstruction method is realized including morphological characters. So far, there have been no more detailed studies that are only focused on this taxon. The only previous taxonomic work was carried out by Clark (1981) for the Atlantic species where the author redefined the genera Cheiraster and Pectinaster Perrier, 1885, reduced the genus Luidiaster Studer, 1883 to a subgenus of Cheiraster, described two more subgenera for Cheiraster, and three new species. The subdivision within the genera may be useful in some cases to identify certain morphological similarity between the species. However, the characters used for the designation of subgenera within the genera in this family cannot be applied in all cases, since the characters related to ontogeny such as the early or late development of certain spines, are highly variable, and therefore it is suggested that a complete family review that includes molecular methods and the use of morphological characters including ossicle morphology is realized to redefine the species and eliminate confusing or unnecessary subdivisions.
Five species of Benthopectinidae are reported for the Mexican waters of the Gulf of Mexico, which represents 6 % of the world diversity of this family. Since the species of this family are distributed in eight genera (Mah & Blake, 2012), the two found in these waters represent 25 % of the total genera of the family. Regarding the taxonomy of the species, Cheiraster (Christopheraster) mirabilis and Cheiraster (Christopheraster) blakei share morphological characteristics such as the shape of the papular areas of different ontogeny, this was described by Clark (1981) and showed drawings of the different arrangement that the species of the genus present, and that the development of the pores throughout the growth is very particular in these two species. The change in the pattern of pore distribution in both species is not very marked, but it can be appreciated in some of the reviewed specimens. Based on the review of the specimens from the Gulf of Mexico, we determined that, to differentiate both species, the two most important characters are: 1) the number and arrangement of spines on the disc, which are abundant and present in the entire disc, gradually decreasing in size towards the arms in C. (Christopheraster) blakei, and which are all similar in size and restricted to the center of the disc in C. (Christopheraster) mirabilis; and 2) the superomarginal spines, which are sub-equal in size in C. (Christopheraster) blakei, while in C. (Christopheraster) mirabilis the spine of the fourth superomarginal plate is much more developed than the rest. It is important to note that the last characteristic presents variation; while in the Bahamas specimens the spine of the fourth superomarginal plate is markedly larger than the rest (up to 15 mm as reported by A.M. Clark & Downey, 1992), in the Gulf of Mexico specimens, the spine is larger but not almost twice as large, as reported by Clark (1981).
In Cheiraster (Barbadosaster) echinulatus, one of the diagnostic characteristics of the species is the rectangular shape of the superomarginal plates that considerably invade the disc. The variation of shape of these plates is mainly that they tend to invade the disc, but, especially in small specimens, the plates are only slightly longer than they are wide, which means the rectangular shape is not as obvious as Perrier (1875) described. In the case of Cheiraster (Cheiraster) planus, the main characteristic is the marginal spines, since the ones in the superomarginal plates are larger in size than the corresponding inferomarginal ones. Although this species was described by Verrill (1915) from a single specimen, it is the most common species of the family in the Gulf of Mexico. Finally, Benthopecten simplex simplex, is a species whose type locality is the Gulf of Mexico, but a subspecies (Benthopecten simplex chardyi Sibuet, 1975) has been reported in the Gulf of Guinea and Gabon (Clark & Downey, 1992). This subspecies is still considered valid, since it differs from B. simplex simplex by a delayed development of the disc spines and a late appearance of the second subambulacral spine, in addition to a greater number of adambulacral plates corresponding to the first 10 inferomarginal ones. According to Clark (1981), these can be considered a combination of extremes in the characters subject to variation in B. simplex simplex. In other words, they could simply be two highly variable characteristics. However, the subspecies has not been validated or refuted since there are no records in the rest of the Atlantic of an intermediate form or specimens that may suggest that these characters are simply subject to great variation.
A more detailed study may find that the diversity of the family is much greater and that there are many cryptic or overlooked species due to lack of definition between one species and another, as is the example of the synonym of B. simplex simplex: Benthopecten armatus (Sladen, 1889), synonymized with Benthopecten spinosus Verrill, 1884 by some authors, such as Grieg (1921) which is in fact a valid species, and treated as valid by other authors like Mortensen (1927) being finally synonymized with B. simplex simplex by Clark (1981). The present study represents the first updated compilation of the species of this family present in the Gulf of Mexico, as well as the first work providing external morphological characters of taxonomic importance to distinguish them. It is the first time that a dichotomous key for these species in the Mexican waters of the Gulf of Mexico is presented.
Ethical statement: authors declare that they all agree with this publication and made significant contributions; that there is no conflict of interest of any kind; and that we followed all pertinent ethical and legal procedures and requirements. All financial sources are fully and clearly stated in the acknowledgements section. A signed document has been filed in the journal archives.

ACKNOWLEDGMENTS
We would like to thank to Ma. Esther Diupotex Chong and Alicia Durán González for their technical support at the ENC, ICML, UNAM. To Susana Guzmán Gómez for her technical support with the multifocal photography. To CONACYT for the scholarship (number 929010) and to Dave Pawson, William Moser (USNM) and the Smithsonian staff for their support. Finally, the authors would like to thank M.G. Lovegrove and A.A. Caballero-Ochoa for the valuable comments on the manuscript's English and scientific content.