A new secretive, yet brightly colored hermit crab species of the family Paguridae, Pylopaguropsis mollymullerae sp. n., is fully described based on specimens from the reefs of Bonaire, Lesser Antilles, southern Caribbean Sea. Populations of this new species were discovered and photographed in the Bonaire National Marine Park under a large coral ledge, at a depth of 13.7 m, living in crevices known by scuba divers to serve as den to a pair of “flaming reef lobsters” Enoplometopus antillensis, or a “broad banded moray” Channomuraena vittata. This new species is only the second species of Pylopaguropsis Alcock, 1905 known from the western Atlantic, the 20^th named worldwide, and belongs in the teevana group of species of the genus. It is remarkably similar, and herein considered geminate, to the tropical eastern Pacific congener, P. teevana (Boone, 1932), the two being characterized and uniquely different from all other species of the genus, by the striking and deeply excavated, scoop-like ventral surface of the chela of the right cheliped. Minor differences separate this new species from P. teevana in the relative length of the antennal acicles (exceeding the corneas versus not exceeding the corneas in P. teevana); dorsal armature of the right chela (smooth or with scattered minute tubercles versus with numerous small tubercles in P. teevana); surface shape of the lateral face of the dactyl of right pereopod 3 (evenly convex versus flattened in P. teevana); and coloration (red bright red stripes versus brown stripes in P. teevana). The highly visible color pattern of bright red stripes on white background typical of decapods known to have cleaning symbioses with fish, dense setation on the flagella of the antennae, and preference for a crevicular habitat, combined with brief in situ nocturnal observations, suggests the possibility that P. mollymullerae sp. n. engages in “cleaner” activities or functions as a “den commensal” with moray eels. The morphology and possible meaning of the observed behavior is discussed. A tabular summary of the distribution, habitat, and published information on all species of Pylopaguropsis is presented. Supplemental photographs and a video of live P. mollymullerae sp. n. are included.

Bonaire, Caribbean, “cleaner”, “den commensal”, hermit crab, new species, Paguridae , Pylopaguropsis

The genus Pylopaguropsis Alcock, 1905, currently includes a group of 19 morphologically striking species that typically live in hard bottoms on or near coral reefs, and at depths ranging from the subtidal to the upper continental slope (0–610 m). One additional species remains undescribed (Arima 2014, Komai pers. comm.). Most species are distributed in the Indo-West Pacific region to Central and South Pacific as far east as Easter Island, with only two species known so far from elsewhere: P. teevana (Boone, 1932), from the eastern tropical Pacific, and P. atlantica Wass, 1963, from the tropical western Atlantic. In addition to their distinctive coloration patterns that typically consist of dark stripes or brightly colored appendages (Asakura 2000, Asakura and Paulay 2003, Komai and Osawa 2004, Osawa and Okuno 2007, McLaughlin et al. 2010, Asakura 2010, Rahayu and Komai 2013, Arima 2014), species of this genus stand out by having a characteristically massive right cheliped, with a large operculate or semioperculate chela, and a dactyl that articulates obliquely with the palm. Other defining diagnostic characters include 13 pairs of biserial phyllobranchiate gills; crista dentata of third maxilliped with accessory tooth; male with unpaired left pleopods 3–5; and females with paired pleopods 1 modified as gonopods, and unpaired left pleopods 2–5 (for full diagnosis see Asakura 2000: 72, and McLaughlin 2003: 126).

The taxonomic history of Pylopaguropsis was discussed by McLaughlin and Haig (1989) in a review of this genus which they divided into the magnimanus group (species with dactyls of left and right pereopods 3 dissimilar), and the teevana group (species with dactyls of left and right pereopods 3 similar). Briefly, this genus was originally described by Alcock (1905) as monotypic, to accommodate P. magnimanus Henderson, 1896, a species that Alcock found to be related to, but that differed significantly from species of Pylopagurus A. Milne Edwards & Bouvier, 1891. A second species was added to this genus by Forest (1955), who concluded that Eupagurus (= Pagurus) zebra Henderson, 1896 belonged in Pylopaguropsis. Subsequently, a third species and first from the Atlantic, was added, P. atlantica Wass, 1963. McLaughlin and Haig (1989) found that the monotypic Galapagurus Boone, 1932 agreed with the more senior Pylopaguropsis, proceeded to synonymize the two genera, and thus changed the genus of its single eastern Pacific species, G. teevanus Boone, 1932, as well as the spelling of Boone’s species name to teevana in order to agree with the feminine Pylopaguropsis. McLaughlin and Haig also added seven new species, all from the Indo-West to the Central or South Pacific islands, bringing to 11 the total number of species of Pylopaguropsis known at the time. In a review of Japanese species of Pylopaguropsis, Asakura (2000) described two more new species from Japan, and later Asakura and Paulay (2003) added yet another new species from French Polynesia. Komai and Osawa (2004), and Osawa and Okuno (2007) each added one more new species from Japanese waters. Finally, three more new species were described from the Philippines, one by Asakura (2010), two by Rahayu and Komai (2013), and as previously mentioned, yet another one remains undescribed (Arima 2014). Although all known species of Pylopaguropsis are now well documented from a taxonomic and morphological point of view, their biology and ecology is at best poorly known.

Recent underwater photographs and video obtained using scuba by Ms Ellen Muller at several dive sites in the National Marine Park of the southern Caribbean island of Bonaire, Lesser Antilles, revealed the presence of a small (a few millimeters in size), intriguing and brightly colored red-striped pagurid hermit crab that appeared to belong to Pylopaguropsis. The specimens in the photographs, however, could not be matched using images alone, to any of the known species of the genus from the western tropical Atlantic, and seemed to represent and undescribed species. A specimen of this hermit crab was first photographed inadvertently alongside an individual of the “flaming reef lobster”, Enoplometopus antillensis (Lütken, 1865), sighted while observing reef invertebrates that aggregate in crevices under a large coral ledge, and subsequently additional specimens of this hermit crab were again photographed in a nearby crevice inhabited by a “broad banded moray” Channomuraena vittata (Richardson, 1845). In order to study in detail and determine the identity of this unusual hermit crab, permits were obtained from the Government of the Island Territory of Bonaire to collect a few specimens and ship them for study to the National Museum of Natural History, Smithsonian Institution, Washington DC, USA (USNM). Close examination of the specimens collected confirmed not only that indeed they are of a new species of Pylopaguropsis, but also that this new species is remarkably similar and undoubtedly more closely related, to the single eastern tropical Pacific member of this genus, P. teevana. Furthermore, the morphological characteristics, color pattern, and observed reclusive behavior in proximity to the moray eel, suggest the possibility that this new species might function in some capacity as a “cleaner”, or perhaps is ecologically associated as a commensal with the moray eel. This new species is herein fully described and illustrated, including color photographs, and video of live specimens in the habitat where it was found. A list of all known species of Pylopaguropsis from the world is included, with a summary of their geographic distributions, depth ranges, and recorded habitats (Table 1).

The holotype and paratypes of the new species described herein are deposited in the collections of the National Museum of Natural History, Smithsonian Institution, Washington DC (USNM). The specimens were collected by hand, using scuba, and during late afternoon or night dives, by E Muller. General terminology follows that used by McLaughlin and Haig (1989), Lemaitre (1995), and McLaughlin (2003). Pereopods and pleopods are indicated with a number, except for the chelipeds, which correspond to pereopods 1. Measurement indicated for the specimens are of shield length, measured in millimeters (mm), taken from the midpoint of rostral lobe to midpoint of posterior margin of shield.

Several aspects of Pylopaguropsis mollymullerae sp. n. merit commentary. As previously noted, the morphological similarity of this new species with the eastern Pacific congener, P. teevana, is so remarkable that there is little doubt the two are closely related and geminate species that have barely diverged since the complete ocean separation by the central American isthmus. Among the Paguridae that occur in the tropical western Atlantic–tropical eastern Pacific region, very few genera (e.g., Phimochirus McLaughlin, 1981, Spathapagurus Lemaitre & Felder, 2011) have species that have been declared to contain geminates, although the two regions share a considerable number of genera and have a close geologic history. In addition to the similarity of the deeply excavated, scoop-like ventral surface of the right chela, both species also have the antennal flagella with long setae which in life are set at about 90° angle to the axis of the flagellum (Fig. 6A, B). The function, if any, of the unusual shape of the right chela, and the antennal flagella, is intriguing. A video of an individual of P. mollymullerae sp. n. taken in situ (see Suppl. materials 1–3) shows the hermit crab walking while maintaining the right cheliped partially retracted or bent against the body, so that the chela is positioned in a shield-like manner. When the hermit crab is in motion, the dorsal surface of the chela is facing the substrate, and is clearly used to push itself along the bottom. Despite the scoop-like shape of the ventral surface of the chela which suggests it might be used for gathering materials or maybe digging, no such uses were observed. The long antennal flagella are held straight out on the sides in wing-like fashion, and parallel to the substrate. While these observations of live crabs do not show conclusively any particular function, it seems clear that the odd morphology must represent a specialized adaptation that deserves further study.

Given that Pylopaguropsis mollymullerae sp. n. lives in relatively shallow (scuba depth) habitats in reefs with crystal clear waters, has a conspicuous, bright color pattern, and individuals are of sufficiently large size to be visible to the naked eye, it is surprising that this new species had not been previously discovered. If what we know of the distribution of other pagurids in the western Atlantic is any indication (species are generally broadly distributed), it is unlikely that the occurrence P. mollymullerae sp. n. is geographically restricted to Bonaire. It seems more probable that its presence had not been detected before, in part, because of its secretive, crevicular, nocturnal behavior, apparent association with menacing moray eels that detract collectors, and preference to live in environments such as large coral ledges that are difficult to reach unless using scuba. Based on the few observations that have been made (E Muller, pers. comm.), this new species ventures out of the coral crevices only for short distances during night time. Regrettably, knowledge of the biology or ecology of other species of Pylopaguropsis is fragmentary at best, and thus it is not possible to make significant extrapolations or comparisons except that most species of this genus have, as previously mentioned, bright and often spectacular colorations (Asakura 2000, 2010, Asakura and Paulay 2003, Komai and Osawa 2004, Osawa and Okuno 2007, McLaughlin et al. 2010, Rahayu and Komai 2013, Arima 2014). Based on the information available (Table 1), most congeners except for P. magnimanus and P. pygmaeus, have been documented to prefer hard bottoms in coral environments. Komai and Osawa (2004: 99) did note that some species usually “inhabit crevices of coral and rocky reefs or among large dead coral plates or blocks”; Osawa and Okuno (2007: 40) found that P. bellula lives in “submarine caves or crevices on fore reef slopes”; and Arima (2014) documented that nine Japanese species (including one undescribed) preferred subtidal reefs and typically dark crevices on coral or rock bottoms and rocky walls.

The behavior of Pylopaguropsis mollymullerae sp. n. is also intriguing. Is there an ecological association of this new species with the “broad banded moray” or other moray species? Could this new hermit crab species function as a “cleaner” or a “den commensal”? At least in one instance, an individual was observed crawling on the body of a moray eel (Fig. 6E) with which this new hermit crab species seems to share a den. It is tempting to speculate that this individual of P. mollymullerae sp. n. was feeding on mucus or other materials present on the body surface of the moray eel, and thus, this could be interpreted as a “cleaning” activity or existence of some kind of symbiotic relationship between hermit crab and moray. The brightly colored pattern with red stripes and setose antennae typical of most crustacean “cleaners”, tends to support this interpretation. However, as pointed out by Bauer (2004), cleaning symbiosis is a controversial topic, in part because the term “cleaner” has been applied based largely on anecdotal evidence to most of the 43 species of decapods that have been categorized as “cleaners”, all of which are caridean or stenopodidean shrimp except for two species of brachyurans (Spotte 1998, Côté 2000, Becker and Grutter 2004, Wicksten 2009). The term “cleaner” in the literature has been used for a wide range of presumed symbiotic associations that are not always clear, although studies have focused much more on “cleaner” fishes (e.g., Losey 1987 and references therein). It would be improbable for a hermit crab that carries a heavy shell as housing, to easily hop on hosts such as fishes that are most often suspended on the water column while “cleaner” activity is to take place. However, moray eels are typically in contact with the bottom inside their dens, and thus it would be possible for a hermit crab to access or climb on the body of the moray eel more easily, as observed for P. mollymullerae sp. n. (Fig. 6E). Alternatively, the apparent preference of P. mollymullerae sp. n. to inhabit caves alongside a moray eel, might indicate a case of “den commensalism” (as defined by Wicksten 2009) where the hermit crab can scavenge remains of food eaten by the moray eel. It would be of interest to conduct further, detailed studies on the behavior and ecology of P. mollymullerae sp. n. to ascertain if any of the above interpretations are valid.

I thank Dr A Anker, who first saw the hermit crab photographs sent to him by Ms E Muller, and suspecting they were of interest, suggested my name as specialist to determine their identity; thus, providing me with the opportunity to describe this beautiful new species. I am most grateful to Ms E. Muller for her environmental awareness, sharp eye and patient efforts to dive, photograph, video, and eventually collect and ship the specimens to my lab for study at the USNM, and allow permission to use her color photographs and videos in this paper. “VIP Diving” in Bonaire is gratefully acknowledged for making possible the diving activities of Ms. E. Muller. I am particularly thankful in Bonaire to the following individuals: Mr F van Slobbe and Mr A Nahr, who as official functionaries of the Bonaire Island Government, kindly and expeditiously processed and approved the permits to collect and export the hermit crab specimens from the Marine Park of Bonaire to the USNM; and Dr RBJ Peachy, Director of the Council of International Education and Exchange Research Station in Bonaire, for her invaluable assistance and guidance to both Ms E Muller and myself, and for arranging the shipping of specimens to USA. Dr DL Felder kindly collaborated by taking the photographs used in Fig. 4B–E, and Drs RT Bauer, C Baldwin, N Chadwick, and MK Wicksten, provided useful comments and references related to “cleaner” organisms. Drs K Baba and T Komai provided valuable information on Japanese publications, and kindly sent very useful translations from the Japanese. Drs T Komai and DL Rahayu provided invaluable comments to the manuscript. Last but not least, Ms R Gulledge is once again profusely acknowledged for her assistance in the preparation of electronic versions of figures.