Crepidula Badisparsa Sp. Nov. (Gastropoda: Calyptraeidae) from Bocas Del Toro Province, Panama

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Crepidula badisparsa sp. nov. (Gastropoda: Calyptraeidae) from Bocas Del Toro Province, Panama

RACHEL COLLIN

Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Ancon, Republic of Panama. [email protected]

ABSTRACT.—The taxonomy of calyptraeid gastropods is made difficult by their morphologically simple, plastic shells and the numerous instances of morphological convergence within the family. The small speckled species of Crepidula from the West Atlantic have all previously been referred to as C. convexa Say, 1822. Recent developmental and genetic work has shown that there are two species along the coast of North America, C. convexa and C. ustulatulina, and that there are at least two other species in the southern Caribbean. Here I describe, Crepidula badisparsa sp. nov., the small speckled species from the Caribbean coast of Panama and augment the original description of C. navicula from Venezeula and the Lesser Antillies. These species are easily distinguished from the more northern C. convexa and C. ustulatulina by the absence of the right muscle scar, and from each other by genetic, conchological, and anatomical characters.

KEYWORDS.—Calyptraeidae, Crepidula riisei, Crepidula convexa, Crepidula navicula

INTRODUCTION and that a morphologically similar species, C. depressa Say, 1822 occurs along the coast Slipper snails in the genus Crepidula are of the Gulf of Mexico (Collin 2000, 2001). well known for the taxonomic difficulties Other species that were previously thought posed by their plastic shells and conserva- to be wide-ranging (e.g., Bostrycapulus acu- tive anatomy (Hoagland 1977, 1984, 1986; leatus) are also comprised of several more Collin 2000a, 2002, 2003b, 2005). Although narrowly distributed cryptic species (Col- the Crepidula fauna of the east coast of lin, 2005). North America is well known after consid- Animals with small, speckled shells from erable scientific study, the southern extent eastern North America are generally re- of the species ranges are still not well- ferred to as Crepidula convexa Say, 1822. documented. Likewise, the identities and This name has also been applied to animals geographic ranges of calyptraeid species from Mexico (Carnes 1975; Bolivar de Car- from the Caribbean and the tropical Ameri- ranza and Hidalgo-Escalante 1990), the cas are poorly known. Animals from these West Indies (Abbott 1974), Columbia (Ban- regions with shells similar to species found del 1976) and Venezuela (Simone 2002). De- in North America are generally referred to tailed research on the development and ge- by the northern names and, therefore, netics of C. convexa s. l. (Hoagland 1984, single species are often cited as ranging 1986; Collin 2000) in North America along an entire coast of the Americas. For showed that it was comprised of two spe- example, Hoagland (1977) lists C. plana Say, cies, C. convexa Say, 1822 and C. ustulatulina 1822 as ranging from Canada to Argentina. Collin, 2002. Crepidula convexa extends from Subsequent examination of developmental New England to Georgia and C. ustulatu- and genetic data showed that C. plana lina ranges from southeastern Florida ranges only as far south as Georgia, USA through the Gulf Coast of the United States and the Yucatan Peninsula (Collin 2001). The southern range endpoint of this species ms. received August 23, 2004; accepted March 31, has not yet been determined. 2005 Animals with similar habits and external 269 270 RACHEL COLLIN shell morphology to C. ustulatulina also oc- cies from Panama is most closely related to cur along the Caribbean coast of Panama C. cf. incurva from Peru, while the small and in Venezuela (Fig. 1 and 2). Samples of spotty Crepidula from Venezuela is geneti- both were included in previous compara- cally very similar to a larger brown species tive studies of calyptraeid development referred to as C. aplysioides form Venezuela (Hoagland 1986; Collin 2003a; Miloslavich (Fig. 3; Collin 2003c). These two speckled et al. 2003), morphology (Collin 2003b) and species can also be distinguished from each DNA sequence data (Collin 2003c). Mor- other by subtle morphological differences. phologically, these animals are easily dis- There are two possibly available names tinguished from C. convexa and C. ustulatu- for these Caribbean species. The syntypes lina, because shells of the latter have a large of Crepidula navicula (Mörch 1877) collected muscle scar on the animal’s right side by Riise from St. Thomas (ZMUC GAS- which is absent in the Caribbean species. 237), and other possible syntypes of this Although the development of animals from species collected by Hornbeck from Vie- both Venezuela and Panama is similar and ques (ZMUC collection) (Fig. 4) are similar both hatch as pediveligers (Miloslavich et to the shells from both Panama and Ven- al. 2003; Collin 2003a), mitochondrial cyto- ezuela. The other possible name is C. riisei chrome oxidase c subunit I and 16S ribo- Dunker 1852 from Puerto Rico. This species somal DNA sequence data show they are is described as pale with brown speckles, two distinct species (Collin 2003c). Phylo- the apex is terminal, and the edge of the genetic analysis of DNA sequence data for shelf is sinuous medially and deeply emar- 95 calyptraeid species shows that the spe- ginate on the left. The synonym of C. riisei

FIG. 1. Photographs of the shells of C. badisparsa. The type of C. badisparsa is indicated with an arrow. Scale bar = 5.0 mm. CREPIDULA TAXONOMY 271

FIG. 2. Photographs of the shells of C. navicula from Morrocoy National Park, Venezuela. Scale bar = 5.0 mm. with C. plana in Yong and Coomans (1988) is dubious, but C. riisei has also been syn- onymized with Crepidula fornicata (Tryon 1886; Hoagland 1977). It is not clear to FIG. 3. Bayesian estimate of the phylogeny of Cre- which side of the shell the “left” refers as pidula s.s. showing the relationships of C. convexa, C. several works of this age illustrate the ani- ustulatulina, C. badisparsa and C. navicula. Topology mal inverted with respect to the shell. Al- from Collin (2003c). though there is a subtle notch on the right cies. The types of C. navicula come from side of the shelf of shells from Venezuela, localities close to the origin of the Venezu- neither of the species discussed here has a elan animals and therefore it is appropriate deep notch on either side of the shell. The to apply that name to the Venezuelan spe- shell length of “7 lin” cited by Dunker cies and to describe the Panamanian spe- (1852) is somewhat large for this species cies as new. I formalize this taxonomic (15.3 mm based on a Prussian inch of 26.15 scheme below. mm employed by Dunker) but is small for Crepidula fornicata. I have been unable to TAXONOMIC DESCRIPTION locate the types of this species, which Hoag- land (1977) lists as lost. There are no re- GENUS: Crepidula Lamarck, 1822 cords of these types in Berlin (M. Glau- Crepidula navicula (Mörch 1877) brecht pers. com. 2004), and they cannot be (Fig. 2 and 4; Table 1) located in Copenhagen (A. Joergensen pers. Synonymy: com. 2004), Stockholm (A. Warén pers. com. 2005) or London (pers. obs. 2001 and Crypta navicula Mörch, 1877: 105. K. Way pers. com. 2005). Since there is no Crepidula cerithicola Guppy, 1894 from figure in the original description, it will be Trinidad and Tobago (non C. cerithicola difficult to resolve the identity of this spe- Adams, 1852). 272 RACHEL COLLIN

FIG. 4. Photographs of the syntype of Crepidula navicula (Mörch, 1877) collected by Riise from St. Thomas (ZMUC GAS-237) (left), and other 3 possible syntypes of this species collected by Hornbeck from Vieques (ZMUC collection). Scale bar = 5.0 mm.

TABLE 1. Summary of species differences.

Character C. badisparsa sp. nov. C. navicula (Mo¨rch 1877) Maximum length 13 mm 10 mm Shell color White with brown spots or streaks, with White with brown spots or streaks, more than 50% brown predominantly pale Shelf margin Slightly bowed or slightly sinuous Slightly sinuous, notch on the right Apex Excavated Not excavated Stage at hatching Pediveliger Pediveliger Egg size 286 ␮m 350 ␮m (Miloslavich et al. 2003) Hatching size 515 ␮m 550-1170 ␮m (Miloslavich et al. 2003) Osphradium 6-11 filaments 3-6 filaments Salivery glands Near the buccal mass Extend along neck Right shell muscle Small and in lateral position Absent

Crepidula convexa Say: Hoagland, 1977: 369 Original description: “T. convexa, an- (partly). gusta, maculis oblongis fuscis. Long. 10 Crepidula navicula (Mörch): Collin, mm, lat 5 mm.” 2003a,b,c. Miloslavich et al., 2003. Types: Hoagland (1977) lists the types of CREPIDULA TAXONOMY 273

C. navicula as lost. However a syntype col- mas but the shelves are broken, obscuring lected by Riise from St. Thomas, (Copenha- this feature on the other possible syntypes. gen, ZMUC GAS-237; length = 9.3 mm), Maximum length is 10 mm. and other possible syntypes collected by Morphology: External body color is dark Hornbeck from Vieques (ZMUC collection; gray and black along the dorsal side of the lengths = 1.0, 7.4, 6.0 mm) were located in head and neck. Because the available mate- Copenhagen Museum of Zoology (Figure rial was all preserved, the presence of yel- 4). The status of the Vieques material as low or cream pigment could not be as- types is questionable as only Isla Margarita sessed. The general anatomy is similar to was mentioned in the original description. Crepidula fornicata described in detail by The location of the syntypes collected by Werner and Grell (1950), and to general Krebs in St. Martin is unknown. None of Crepidula s.s. anatomy as described by Si- the types were figured by Mörch. mone (2002) and Collin (2003b). The black Type locality: Mörch lists the habitat as gill extends about two thirds to three quar- “Terra firma” (Hornbeck) St. Martin ters of the way to the end of the viscera. (Krebs), St. Thomas (Riise), and I. Mar- There is no shell muscle but the small dor- garita (Hornbeck). sal attachment muscle is present in the Distribution and habitat: The extent of mantle anterior to the heart. The mono- the distribution of C. navicula is not well pectinate osphradium consists of 3-6 documented. However this species is closely spaced simple leaflets. These occur known from the coast of Venezuela (type in a tight cluster that does not overlap with description and the material examined the food pouch and covers less than half of here) and the Lesser Antillies (the syn- the mantle opening. The tubular salivary types). It commonly occurs on other snails glands extend along the neck halfway to in shallow water. In Morrocoy National the nerve ring. The visceral mass does not Park, Falcón, Venezuela they occur com- bulge into mantle cavity on the left side. monly on Modulus modulus in Thalassia beds Female genital papilla (fgp) extends well (Miloslavich et al. 2003). into the mantle cavity with a wide, shallow Description: The anatomical description groove and blunt, rounded distal tip. The presented here is drawn from lot capsule gland and albumen gland together FMNH293349 and ANSP 412185 from Mor- form a round bulge in the mantle cavity at rocoy, Venezuela. the base of the fgp. The penis is slightly Shell. Fig. 2 and 4. The shell is small flattened, and tapers gradually to the long, somewhat convex and curved laterally. thin distal papilla which is not as distinct Shell shape is strongly dependent on the from the rest of the penis as in many spe- shape of the substrate. Animals living on cies. small snails often have a compressed left Development: Development of this species side or are compressed on both sides. The was described by Miloslavich et al. (2003). shell is usually white with dark brown All of the uncleaved 350 ␮m eggs develop spots and streaks, with white predominat- initially but a slight decrease in the number ing. The periostracum is not visible. The of eggs per capsule during development shell apex is at the level of the aperture and was noted (Miloslavich et al. 2003). This is not noticeably excavated. The protoconch was attributed to intrabrood canabalism, is usually eroded from the edge of the ap- but different broods were examined at dif- erture. There is no sculpture other than ferent stages and female size was not taken growth lines. There are no muscle scars. into account. Therefore it may also be an The shelf is flat and white, and extends artifact of differences in maternal size. The slightly less than half the length of the shell. small differences are most likely due to the The anterior margin of the shelf is often occasional consumption of disintegrating slightly sinuous, with a medial inflection. embryos rather than development special- There is a small notch where the shelf con- ized for the consumption of nurse eggs as nects to the shell on the left side. This notch observed in Crepidula coquimbensis or Crepi- is just intact on the syntype from St. Tho- patella dilatata. Pediveligers hatch at about 274 RACHEL COLLIN

800 ␮m (Miloslavich et al. 2003) but are re- Diagnosis: Crepidula badisparsa is distin- ported to be retained below the female un- guished from other similar species of Cre- til they crawl away, so it is unclear if they pidula by the following suite of characters. were ever observed to swim. Small, speckled shell with a slightly arched Available DNA sequences: DNA sequences shelf margin and no muscle scar, a small are available from GenBank from a single right shell muscle located vernto-laterally individual from Morrocoy, Venezeula for in the visceral mass, and development with mitochondrial cytochrome oxidase I and a pediveliger. 16S rDNA, and nuclear 28S rDNA Distribution and habitat: I have col- #AF546040, AF545980, AF545903, respec- lected C. badisparsa from Bocas del Toro, tively. Panama and Hoagland (1986) collect ani- Notes: I have chosen to attribute these mals that may be the same species (see be- animals to C. navicula on the basis of simi- low) from Coco Solo, Limon Bay, Panama larities between their shells and the types, (ANSP A12043 and ANSP A12044). In both and on geographic proximity. The shells of cases the animals were collected living at- the types are slightly larger and more ro- tached to other snails and were found in bust than the material from Morrocoy. shallow (1-2 m) water. They are certainly more similar to this material than to the flatter, more gracile Description: samples from Isla Margarita attributed to C. aplysioides (Miloslavich et al. 2003; Collin Shell. Fig. 1. The shell is small and convex 2003a,b,c). Crepidula riisei appears to be or arched dorsal-ventrally, but not curved similar but the animals described here do laterally. Shell shape is strongly dependent not have a deep notch on either side of the on the shape of the substrate. Animals liv- shelf. Examination of the anatomy, devel- ing on small snails often have a compressed opment, and DNA of material from left side or are compressed on both sides. throughout the Caribbean and especially The shell is usually white with dark brown Puerto Rico is necessary before we can de- spots and streaks, with the brown predomi- termine how many species are present and nating over the white. The periostracum is can therefore assess the validity of this not visible. The shell apex is well-excavated older name. ventral to the shelf, directed posteriorly, and curves ventrally to the level of the ap- Crepidula badisparsa sp. nov. erture. The protoconch is smooth and often (Fig. 1 and 3, Table 1) eroded. There is no sculpture other than growth lines. There are no muscle scars. Synonymy: The white shelf is flat and extends slightly less than half the length of the shell. The Crepidula convexa Say: Hoagland, 1977: 369 anterior margin of the shelf is often slightly (partly). bowed with the half on the animal’s left C. cf. convexa: Hoagland, 1986. side running laterally and the right side ex- “C. convexa Bocas”: Collin, 2003a,b tending slightly further forward. In others C. cf. navicula: Collin, 2003c the shelf margin runs laterally across the Holotype: ANSP 412182. Figure 1. Fe- entire shell, but it is still bowed near the male. Length = 9.0 mm; width = 5.5 mm; midline. There is no notch where the shelf height 3.7 mm; 3 figured paratypes from connects to the shell on the left side. type locality ANSP 412183. Anatomy: External body color is dark Other material from the type locality: gray and black along the dorsal side of the FMNH 282355, ANSP 412184. head and neck, with splotches of cream and Type locality: C. badisparsa were col- yellow along the neck lappets, tentacles lected from Cerithium living on the Thalassia and lips. The general anatomy is similar to meadow behind the Smithsonian’s Bocas Crepidula fornicata described in detail by del Toro Research Station (9°21’4.3ЉN, Werner and Grell (1950), and to general 82°15’25.6ЉW) at 1-2 meters depth. Crepidula s.s. anatomy as described by Si- CREPIDULA TAXONOMY 275 mone (2002) and Collin (2003b). The black are available from GenBank from a single gill extends about three quarters of the way individual of C. badisparsa from Bocas del to the end of the visceral mass. A shell Toro, Panama for mitochondrial cyto- muscle extends dorsally from the anterior chrome oxidase I and 16S rDNA, and right portion of the foot to attach the animal nuclear 28S rDNA AF546036, AF545975, to the shell. This muscle attaches to the an- AF545898, respectively. terior margin of the shelf from the under- Etymology: The species name badisparsa is side of the viscera and wraps around to the a Latin adjective, referring to the brown right side of the viscera (ventral and lateral spots on the shell of this species. to the capsule and albumin glands) attach- Notes: Hoagland (1986) describes the de- ing to the shell at the intersection of the velopment of what appears to be the same shell and the shelf. In other Crepidula spe- species (her C. cf. convexa) from Limon Bay, cies with a right shell muscles the muscle Panama, but she obtained slightly different extends from the dorsal side of the viscera results. She reports a larger egg size (300 and attaches to the shell roof. The osphra- ␮m; 260-400 ␮m) and a larger hatching size dium consists of 5-11 tightly packed mono- (800 ␮m) than C. badisparsa from Bocas del pectinate leaflets. The most medial leaflets Toro. The presence of a single nurse egg are covered by the left side of the food per capsule (Hoagland 1986, Table 3) is not pouch. The osphradium covers most of the in accordance with her observation of “ex- mantle cavity opening. The tubular salivary tensive brood cannibalism” (Hoagland glands are clustered around the buccal 1986, pg. 182) and so the exact nature of the mass and the neck is full of connective tis- nurse eggs and the details of embryonic de- sue making it difficult to find them. The velopment remain unclear. Hoagland’s for- visceral bulges extensively into mantle cav- malin-preserved vouchers, however, do ity on the left side. Female genital papilla demonstrate the diagnostic morphology of (fgp) extends well into the mantle cavity the left shell muscle and the pointed fgp with a wide shallow groove and somewhat that distinguish C. badisparsa from C. na- angled or pointed tip. The capsule gland vicula. Unfortunately, no living material and albumin gland together form a round from Limon Bay is currently available to bulge into the mantle cavity at the base of repeat Hoagland’s observations of develop- the fgp. The penis is evenly tapered and the ment. seminal groove extends to the distal tip. Development: In Bocas del Toro, Panama, Acknowledgments.— C. badisparsa lay eggs in thin transparent I thank the Smithso- capsules typical of most calyptraeids. Un- nian’s Marine Science Network and the cleaved eggs are 286 ␮m (n = 11; s.d. = 5.8 Smithsonian’s Women’s Committee for ␮m). Embyros develop into encapsulated their support of invertebrate taxonomic pediveligers which have a clear mid-sized work in Bocas del Toro. I am grateful to R. head vesicle, and a single embryonic kid- Cooke for translating the species descrip- C. riisei ney on each side. Embryos hatch as pedi- tion of , T. Schiøtte for finding the C. navicula veligers with a shell length of 515 ␮m(n= types of , A. Valdés and A. 10; s.d. = 30 ␮m). The hatchlings have an Warén for commenting on the manuscript, operculum, unpigmented velum, a clear in- and the curators and collection managers of testine, and a smooth, transparent shell. Al- USNM, BMNH, CAS, ANSP, MCZ, ZMUC though this is a small hatching size with and LACM for loans of type material and respect to the egg size and the larvae for accepting vouchers. I also thank the Au- clearly had yolk reserves at hatching, they toridad Marítima de Panamá for issuing me settled within several hours of hatching. collecting and export permits. Because these larvae were release by undis- turbed females that were maintained in the ITERATURE CITED laboratory, it is unlikely that they hatched L prematurely. Abbott, R. T. 1974. American seashells. 2d ed.: New Available DNA sequences: DNA sequences York, Van Nostrand Reinhold Company. 276 RACHEL COLLIN

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