19 September 1995 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON 108(3):458-464. 1995. Within- variation in yucatanicus (Ives), with taxonomic remarks on P, pedersoni Chace (Crustacea: : : )

Mary K. Wicksten Department of Biology, Texas A&M University, College Station, Texas 77843, U.S.A.

Abstract. — The Periclimenes yucatanicus is found to vary in the number of rostral teeth, length/width ratio of the carpus of the major cheliped, color pattern and cnidarian host. Similar variation has been found in other species of Periclimenes. Morphological features and type of host have been used to distinguish between P. anthophilus Holthuis & Eibl-Eibes- feldt, and P. pedersoni Chace, but these features overlap extensively; therefore, P. anthophilus is herein considered to be a junior synonym of P. pedersoni.

Shrimp of the genus Periclimenes Costa, those of species of Periclimenes known to 1844 are among the most colorful carideans inhabit sea anemones in the area. Records of coral reefs. Species inhabiting cnidarian of shrimp species and their hosts were quan- hosts are among the best known. Four spe- tified. The results indicate that there is con- cies of Periclimenes have been reported to siderable within-species variation in at least live with cnidarians in the western Atlantic, two species of Periclimenes. Gulf of Mexico and Caribbean: P. yucatan- icus (Ives 1891), P. pedersoni Chace, 1958 P. anthophilus Holthuis & Eibl-Eibesfeldt, Methods 1964 and P. rathbunae Schmitt, 1924. (See During studies of cleaning behavior, this Chace 1972, for a key to the species of Per- writer and volunteer divers from the non- iclimenes in the area). profit organization CEDAM International, During studies of cleaning behavior of counted numbers of shrimp per species of shrimp and , species of Periclimenes were host in Key Largo, Florida, U.S.A., during observed on coral reefs near Key Largo, 11-17 July 1992, and Bonaire, Netherlands Florida, U.S.A., and Bonaire, Netherlands Antilles, during 25 July-5 August 1993 and Antilles. The shrimp were identified from 30 July-12 August 1994. Shrimp were ob- photographs and by sight. However, during served during SCUBA dives at depths of 3- night dives at Bonaire, shrimp with an un- 22 m between 0600-2200 hours. Twenty- usual color pattern, unlike that of known four photographs of all species of Pericli- species in the area, were observed. These menes were taken in Florida and 110 in shrimp were found in association with the Bonaire. Species were identified in the field giant , according to the color patterns shown in the (Weinland). popular book by Humann (1992:151); un- To identify this unknown shrimp, speci- identified ones were reported as Pericli- mens were collected and compared with menes sp. previously identified material. Photographs Five specimens (the maximum number of live were examined to compare allowed as stated on the collecting permit) color patterns of the unknown shrimp with of the unidentified shrimp were collected at VOLUME 108, NUMBER 3 459

Fig. 1. Variation in the rostrum and second pereopod of Periclimenes yucatanicus. a, left second pereopod from individual 29.8 mm in total length; b, c, left and right second pereopods from individual 16.5 mm in total length; d, rostrum from individual 29.8 mm in total length; e, rostrum from individual 13.0 mm in total length. Scales are 1 mm and refer to the drawings immediately above them.

Calabas Reef, near Kralendijk, Bonaire, previously collected material of the species, during 1994. An additional 13 were pho- there is variation in the number of rostral tographed in their natural habitat, but not teeth and the length-width ratio of the car- collected. The animals were kept alive for pus of the second (major) cheliped (Fig. 1). 5-7 days and their color patterns recorded. The rostrum can have 5-8 dorsal and 0-3 These specimens were compared with de- ventral teeth in addition to an acute apex. scriptions of known species and also with The length/width ratio of the carpus ranges 13 specimens of P. yucatanicus from the from 2.3-7.5. A more slender carpus (4x collections of the National Museum of Nat- longer than wide or more) usually occurs in ural History Smithsonian Institution, smaller shrimp (total length 16 mm or less). Washington, D.C. The color patterns also (The largest specimen measured 29.8 mm were compared with those shown in pho- in total length, orbit-telson.) In three spec- tographs of P. yucatanicus from Grand Cay- imens, the second pereopods were asy- man, British West Indies (two slides show- metrical. ing three shrimp), Isla Cozumel, Quintana The 18 shrimp of the nocturnal color Roo, Mexico (three slides showing two phase had translucent bodies with a few shrimp), the U.S. Virgin Islands (one pho- small spots of brown or white on the dorsal tograph of one shrimp) and Discovery Bay, surface, and a translucent turquoise blotch Jamaica (photograph by Colin 1978). near the gastric region. In two, there was a pale white stripe along the dorsal midline; in another two, there was a small dorsal pale Results brown spot on either the carapace or third The unidentified shrimp are a previously abdominal somite. The pereopods were unreported color variety (hereafter called the banded. Most had white antennae, but two nocturnal color phase) of P. yucatanicus. had the outer antennal flagella banded and Their bodies closely match the description the inner ones white. In two, the uropods of P. yucatanicus as given by Holthuis (1951: ended in faint white spots; in the others, 38, pi. 10, figs. a-1). In these specimens and there either were no such spots or the tail 460 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Fig. 2. Color variation in Periclimenes yucatanicus, drawn from photographs in life, a, entire , showing banded appendages, from Florida, day; b, individual from Bonaire, day; c, individual from Bonaire, night; d, individual from Bonaire, day; e, same individual as seen in drawing d, night; f, individual from Bonaire, day. fan could not be observed in the photo- the 82 photographs identifiable as P. yu- graph. catanicus taken at Bonaire, all showed Two of the individuals that were collected shrimp with the pereopods banded with at night are shown in the nocturnal color white and a contrasting darker shade of red, phase in Figs. 2c and 2e. By day, both purple or violet. Thirty-two shrimp (39%) changed their color pattern to that of large had entirely white antennae; 34 shrimp white, tan, green or purple blotches, spots (41 %) had the outer flagella banded and the and saddle marks on a translucent body. inner white, and 16 shrimp (20%) had both The same individual is shown in Figs. 2d antennal flagella banded. Eleven photo- and 2e, illustrating the marked change in graphs showed only the front of the animal, color pattern. Examination of the live spec- and thus only the color of the appendages imens and photographs revealed consider- and antennae could be seen. In the other 71 able color variation in P. yucatanicus. Some photographs, at least the carapace and first of the patterns are shown in Figure 2. Of three abdominal segments were visible. The VOLUME 108, NUMBER 3 461

color pattern typically included a large dor- of the shrimp were translucent except for sal "saddle" of pure white or pink, tan or the bands and spots. Similar color patterns green with a white border on the dorsal sur- were observed in photographs of shrimp face of the carapace, (seen in 31 shrimp, or from other areas except for one photograph 44% of the total), a saddle (sometimes in a from Grand Cayman, which showed two figure-eight pattern) of similar color on the shrimp with the same color pattern as the dorsal surface of the first and/or second ab- nocturnal color phase from Bonaire. The dominal somite (seen in 30 shrimp, or 42% photograph of P. yucatanicus by Humann of the total), and a large saddle on the third (1992) shows a shrimp with a brown back- abdominal somite (seen in 46 shrimp, or ground pigmentation. 65% of the total). The tips of the uropods Another common shrimp, Periclimenes often were marked with white and dark spots pedersoni, had very different markings which shaped like eyespots; however, the tail fan were not observed to change at night. This was visible in only 21 photographs. The species was marked with white, blue or pur- lower surface of the carapace or abdomen ple-violet lines running the length of the often had spots of white or white and dark body, similar marks on the major chelipeds, pigment and the anterior parts of the ceph- purple speckles on the maxillipeds and oth- alothorax could be speckled; however, it was er pereopods, and pure white antennae. The difficult to see these marks in many pho- white lines and antennae are readily visible tographs. Many shrimp also had "saddle" at a distance (Fig. 3). marks on the fourth abdominal somite, or Of 302 total P. yucatanicus observed in had marks that overlapped two abdominal the wild (whether photographed or not), 283 somites. Two of the largest shrimp (total were among the tentacles of Condylactis gi- body length approximately 30 mm, as es- gantea, 13 were on the sea anemone Bar- timated from photographs) had a body tholomea annulata (Lesueur) and six were background color of brownish pigment; most away from a cnidarian host. Usually, only 462 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON one shrimp was observed per host, but as 1991 :fig. 1; Colin 1978:344 as "unidentified many as five could be found per anemone. species of Periclimenes''''). It is possible that All of the unidentified shrimp at night were slight regional differences in color pattern found on C. gigantea. Periclimenes peder- may exist in these species, but such differ- soni was more abundant. Of a total of 938 ences would be difficult to see or photograph observed, 555 were on C. gigantea, 315 on in the natural habitat. B. annulata and 68 on other hosts or away Marked changes in color patterns from from a cnidarian. As many as 13 P. ped- day to night have been reported previously ersoni could be found living in a single sea in the hippolytid shrimp Hippolyte varians anemone. The two species never coexisted Heptacarpus pictus and Heptacarpus palu- on the same host. The hippolytid shrimp dicola (Green 1961, Bauer 1981). In these Thor amboinensis (De Man) often occupied species, the shrimp showed a tranluscent the same individual of C. gigantea with one blue color by night, regardless of the color of the two species; snapping shrimp (Alphe- pattern displayed by day. Divers at Key Lar- us ? armatus Rathbun) lived along the stalks go noticed a similar color change in Thor of B. annulata under the tentacles where the amboinensis, which had a pattern of white Periclimenes lived. spots against a chocolate brown background No individuals of P. rathbunae were ob- by day, and a blue background at night. served at either Key Largo or Bonaire. There are few observations of the nocturnal coloration of shrimp, especially in their nat- ural habitat, so it is difficult to determine Discussion how common diurnal/nocturnal color Holthuis (1951) noted variation in the changes are among species of Periclimenes. length/width ratio of the carpus of the sec- Spotte et al. (1991) reviewed associations ond pereopod in specimens of P. yucatan- of shrimp with cnidarians in the West Indies icus, and speculated on whether this might and Bermuda, and reported that neither P. be due to sexual difference, a growth form yucatanicus nor P. pedersoni was confined or geographic variation. This asymmetry to a single host. Periclimenes yucatanicus also could be due to loss and regeneration was listed to live with six species of sea of an appendage. The results given here sug- anemones (Order Actiniaria), the jellyfish gest that variation in the proportions of the Cassiopeia xamachana (Bigelow) and the carpus of the second pereopod exists within corallimorpharian, Rhodactis sanctaetho- P. yucatanicus. Holthuis noted similar vari- masae (Duchassaing & Michelotti). Pericli- ation in P. infraspinis (Rathbun). Chace & menes pedersoni was reported to live with Bruce (1993) noted that several Indo-Pacific six species of sea anemones, the same jel- species of Periclimenes had subequal to lyfish and a tube anemone, Cerianthus sp.. grossly unequal second pereopods. At Key Largo, diver Rick Sammon photo- The pattern of spots and lines in speci- graphed Periclimenes yucatanicus in asso- mens from Bonaire and Florida was con- ciation with another corallimorpharian, Ri- sistent with that shown in photographs of cordea florida (Duchassaing & Michelotti). P. yucatanicus from other areas. Less vari- I photographed the same association at ation was seen in the color pattern of P. Grand Cayman. pedersoni (Humann 1992:151; Sefton & Evidently, P. yucatanicus and P. peder- Webster 1986:77, figs. 117, 118; Colin 1978: soni can live on multiple hosts. However, 339-341; Voss 1980:87 and color plate). most records of either species come from has a pattern of the anemones C. gigantea and B. annulata. white and brown dots and lines, with white Goy (1990) found that more larval P. yu- dots at the tips of the uropods (Spotte et al. catanicus completed metamorphosis sue- VOLUME 108, NUMBER 3 463 cessfully if exposed to exudates of C. gi- well as with other hosts (Spotte et al. 1991). gantea than to those of other species or none Lacking additional evidence of distinctive at all; larval P. pedersoni showed better sur- coloration or species-specific behavioral or vival if exposed to exudates of B. annulata. morphological distinguishing features, P. Levine & Blanchard (1980) reported that anthophilus should be considered a junior species of Periclimenes could be stung by synonym of P. pedersoni Chace, 1958. sea anemones to which they were not ac- climated. Acknowledgments Periclimenes anthophilus Holthuis & Eibl- I am grateful to Kalli de Meyer, Bonaire Eibesfeldt (1964) was described as a distinct Marine Park, and the government of the species from Bermuda. The original au- Netherlands Antilles for permission to con- thors, and Chace (1972) remarked that it duct studies and collect specimens. Vol- was very similar to P. pedersoni, but could unteer divers from CEDAM International, be distinguished by the position of the he- especially Rick Sammon, Dave Downs and patic spine in front of the most posterior Stella Covre, and Nancy Sefton of the Cay- dorsal carapace spine; the carpus of the sec- man Islands aided immensely in photo- ond pereopod being less than half the length graphing and documenting shrimp in the of the chela and the host being Actinia ber- natural habitat. mudensis or C. gigantea. Other morpholog- ical features and the color pattern were in- distinguishable from those of P. pedersoni. Literature Cited Chace (1972) remarked on the close mor- Bauer, R. T. 1981. Color patterns of the shrimps phological similarity between the two sup- Heptacarpus pictus and H. paludicola (Caridea: posed species, and re-examined specimens. Hippolytidae). — Marine Biology 64:141-152. The only differences he found between them Chace, F. A., Jr. 1958. A new shrimp of the genus Periclimenes from the West Indies. —Proceed- were the "different habits" and the "pro- ings of the Biological Society of Washington 71: portionately shorter carpus of the major sec- 125-130. ond pereopod". However, proportions of . 1972. The shrimps of the Smithsonian-Bre- the carpus of the second pereopod vary in din Caribbean Expeditions with a summary of species of Periclimenes as well as in other the West Indian shallow-water species (Crus- tacea: Decapoda: Natantia). — Smithsonian palaemonids. In species of freshwater Contributions to Zoology 98:1-179. shrimp of the genus , for ex- , & A. J. Bruce. 1993. The caridean shrimps ample, the entire second pereopod is mark- (Crustacea: Decapoda) of the Albatross Philip- edly longer and more robust in adult males pine expedition 1907-1910, part 6: superfamily than in juveniles or females. As shown in .—Smithsonian Contributions to Zoology 543:1-152. Fig. 1, the length/width ratio of the carpus Colin, P. L. 1978. Marine invertebrates and plants can vary in specimens of Periclimenes spp., of the living reef. T.F.H. Publications, Neptune as does the length of the carpus relative to City, New Jersey, 512 pp. the chela. Costa, O. G. 1844. Su due nuovi Generi di Crostacei Although species of Periclimenes appar- Decapodi Macrouri Nota.—Annali delle Acca- demia degli Aspiranti Naturalisti, Napoli 2:285. ently have preferred hosts, they are not re- Goy, J. W. 1990. Components of reproductive effort stricted to a single species of cnidarian. The and delay of larval metamorphosis in tropical review by Spotte et al. (1991) shows this marine shrimp (Crustacea: Decapoda: Caridea lack of specificity, as does a study of shrimp and Stenopodidea). Unpublished Ph.D. disser- tation, Texas A&M University, College Station, living with sea anemones in central Japan Texas, 177 pp. (Suzuki & Hayashi 1977). Both P. pedersoni Green, J. 1961. A biology of Crustacea. H.F. & G. and P. anthophilus have been reported to Witherby, Ltd., London, 180 pp. live with C. gigantea and B. annulata, as Holthuis, L. B. 1951. A general revision of the Pa- 464 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

laemonidae (Crustacea Decapoda Natantia) of Kennis der Fauna van Curacao. Resultaten Ee- the Americas. I. The subfamilies Euryrhynchin- ner Reis van Dr. J. van der Horst in 1920.— inae and Pontoniinae.—Allan Hancock Foun- Bijdragen Tot de Dierkunde Genootschap Na- dation Occasional Papers 11:1-332. ture Artis Magistra te Amsterdam 23:61-81. , & I. Eibl-Eibesfeldt. 1964. A new species of Sefton, N., & S. Webster. 1986. A field guide to Ca- the genus Periclimenes from Bermuda (Crusta- ribbean reef invertebrates. Sea Challengers, cea, Decapoda, Palaemonidae).—Senckenber- Monterey, California, 112 pp. giana Biologica 45:185-192. Spotte, S., R. W. Heard, P. M. Bubucis, R. R. Manstan, Humann, P. 1992. Reef creature identification. & J. A. McLelland. 1991. Pattern and color- Vaughan Press, Orlando, Florida, 320 pp. ation of Periclimenes rathbunae from the Turks Ives, J. E. 1891. Crustacea from the northern coast and Caicos Islands, with comments on host as- of Yucatan, the harbor of Vera Cruz, the west sociations in other anemone shrimps of the West coast of Florida and the Bermuda Islands.—Pro- Indies and Bermuda.—Gulf Research Reports ceedings of the Academy of Natural Sciences of 8:301-311. Philadelphia (1891): 176-207. Suzuki, K. & K. Hayashi. 1977. Five caridean shrimps Levine, D. M., & O. J. Blanchard, Jr. 1980. Accli- associated with sea anemones in central Ja- mation of two species of the genus Periclimenes pan.—Publications of the Seto Marine Biolog- to sea anemones.—Bulletin of Marine Science ical Laboratory 24:193-208. 30:460-466. Voss, G. L. 1980. Seashore life of Florida and the Schmitt, W. L. 1924. The macruran, anomuran and Caribbean. Banyan Books, Inc., Miami, Florida, stomatopod Crustacea. In Bijdragen Tot de Revised edition, 199 pp.