Tumidotheres, a New for margarita Smith, 1869, and Pinnotheres maculatus Say, 1818 (Brachyura: ) Author(s): Ernesto Campos Source: Journal of Biology, Vol. 9, No. 4 (Nov., 1989), pp. 672-679 Published by: The Crustacean Society Stable URL: http://www.jstor.org/stable/1548597 Accessed: 31/10/2008 12:55

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http://www.jstor.org JOURNAL OF CRUSTACEAN BIOLOGY, 9(4): 672-679, 1989

TUMIDOTHERES, A NEW GENUS FOR PINNOTHERES MARGARITA SMITH, 1869, AND PINNOTHERES MACULATUS SAY, 1818 (BRACHYURA: PINNOTHERIDAE)

Ernesto Campos

ABSTRACT The genus Tumidotheresis erectedto receive its type species Pinnotheresmargarita Smith, 1869, from the East Pacific, and P. maculatusSay, 1818, from the West Atlantic. It differs from other pinnotheridgenera principally in 3 features:(1) the gastricand cardiacregions are separatedfrom the branchiohepaticarea by depressions,all these regions tumid; (2) the palp of the third maxilliped is composed of 3 articles, with the carpus shorterthan the spatulate propodus,the dactylusnarrowly spatulate, inserted medially on the propodalinner marginand not overreachingthe tip of this latter article;and (3) male and female abdomen composed of 7 free abdominal somites. An analysis of morphologyof several postplanktonicstages of T. (formerlyPinnotheres) margarita suggested that this species should be consideredas a senior synonym of P. pubescens(Holmes, 1894), which apparentlywas describedfrom a hard-stage female.In addition,the life history,phylogenetic relationships, and larvalmorphology of Tum- idotheresare discussed.

RESUMEN Un nuevo genero de cangrejopinoterido, Tumidotheres,genus novum, es nombrado para recibira su especietipo, Pinnotheresmargarita Smith, 1869, del Pacificooriental, y P. maculatus Say, 1818, del Atlantico occidental.Morfologicamente este g6nerodifiere de otros asignadosa Pinnotheridaeen tres caracteristicasprincipales: (1) la regi6n cardiacay la gastricaestin se- paradasdel area branquio-hepaticapor depresiones,siendo todas estas regionesdel caparaz6n tumidas;(2) el palpo del tercermaxilipedio estf formadopor tres artejos,el carpusmas corto que el espatuladopropodus y el dactilus,el cual es angostamenteespatulado, esta inserto en la regi6n media del propodusy su extremo distal no sobrepasala punta de este iltimo artejo;y (3) el abdomen del macho y de la hembra estan compuesto por siete somitos libremente articulados.Adicionalmente se reconoceque Pinnotherespubescens(Holmes, 1894) fue descrito en base a una hembraen fase dura de T. (ex Pinnotheres)margarita (Smith, 1869) la cual por haber sido descritaprimero debe considerarseun sin6nimo antiguo y el nombre vilido para esta singularespecie. Comentariosadicionales sobre el ciclo de vida, relacionesfilogeneticas y morfologialarval se discuten para Tumidotheresy g6nerosemparentados.

The pinnotheridsare a groupof symbiotic forms that are termed the post-hard stages that undergo a complex metamor- I-V. Differencesamong them have been re- phosis during their postplanktonic devel- corded in carapaceshape, abdominalwidth opment. According to previous studies and length, and development of pleopods (Christensenand McDermott, 1958; Pearce, (Christensenand McDermott, 1958; Pearce, 1966; Jones, 1977) the male passes through 1966; Jones, 1977). Changes in the sym- two forms after the invasive stage: (1) the metry of the walking legs and swimming prehard-stage,which has a soft, bare cara- setae can also be observed. The morpho- pace, with no swimming setae on the walk- logical changes that take place during the ing legs, and (2) the hard-stage,with a hairy, life history have been confused by taxono- hardcarapace and natatorysetae on the sec- mists. This has resulted in the naming of ond and third walkinglegs. In contrast,sev- two or more species that representeddif- en stages are recorded in the female. The ferent stages of development in the same first two, the prehard-and hard-stages,are species (e.g., Pinnotheresmuliniarum [=P. nearly identical morphologically with the reticulatus= P. jamesi], Campos, in prep- same stagesobserved in the male, and differ aration). mainly in the number of abdominal ap- During October 1984 I collected a swim- pendages.The last five stages are feminine ming pinnotheridfemale in the upper Gulf 672 CAMPOS: SYSTEMATICS OF PINNOTHERES MARGARITA AND P. MACULATUS 673 of Californiathat was attempting to infest above-mentioned type species, the western the vagile mollusc Lima pacifica Orbigny, Atlantic Pinnotheresmaculatus must be as- 1846. Close examination of this and signed to this genus. Other species that per- its comparison with the description of the haps could be included in this genus are: eastern Pacific pinnotherid crabs by Rath- Pinnotheresguerini H. Milne Edwards,1853 bun (1918) indicated that I had captureda (Cuba and Puerto Rico), P. hirtimanus H. female of the enigmatic crab Pinnotheres Milne Edwards, 1853 (Cuba), P. leleouffi pubescens (Holmes, 1894). One year later, Crosnier,1969 (Cote d'Ivoire, West Africa), additional collection of two solitary males, and P. tellinaeManning and Holthius, 1981 housed in Lima pacifica, and two sexual (Pointe Noire, Congo). The latter four couples, found in the mantle cavity of Bar- species do not agreewith Pinnotheressensu batia reeveana(Orbigny, 1846), allowed me stricto and should be excluded from that to conclude that P. pubescenswas described genus. A morphological study is necessary from a subadult female of P. margarita to resolve the taxonomic position and sys- Smith, 1869. The solitary males and the tematics of these particularspecies, which males found together with the young fe- possess a third maxilliped similar to that of males were almost identical to the male of Tumidotheres. P. margaritafigured by Campos-Gonzalez Generic Relationships. -Excluding those and Campoy-Favela(1988). that the third with of the mor- genera possess maxilliped Furthermore, comparison palp articles placed end to end, and those phology and life history indicates that P. which are similar to Pin- is allied to the western morphologically margarita closely nixa White, 1846, the genus Tumidotheres AtlanticP. maculatus,and that both species can be separatedfrom the remaininggenera possess several morphologicalfeatures that in the Pinnotheridae the structure theirexclusion from Pinnotheressen- by unique justify of the third maxilliped (Fig. 2a, b). It is su stricto and their inclusion in a new genus differentfrom Pinnotheressensu stricto of Pinnotheridae. by the form of the palp. Tumidotherespos- sesses a spatulate dactylus inserted in the DESCRIPTIVEACCOUNT middle of the propodus, and Pinnotheres Tumidotheres,new genus sensu stricto possesses a styliform dactylus inserted on the ventral broad- proximally margin Diagnosis.-Carapace suborbicular, of the propodus. The dactylus of Tumi- er than long, thick and firm but not hard; dotheresdiffers from that of Fabia. In Fabia surface covered with short, dense, and de- the is and there ciduous tomentum. Gastric and cardiacre- dactylus lunate-digitiform are two longitudinal sulci on the carapace. gions separatedfrom branchiohepaticarea These sulci are in Tumidotheres all these tumid. lacking and, by depressions, regions as was noted above, its dactylusis spatulate. Third maxilliped with ischium indistin- In males of Tumidotheres fused with with 3 ar- addition, possess guishably merus;palp seven free abdominal somites, instead of ticles, carpus shorterthan spatulate propo- two or more fused as observed in males of dus, latter about twice as long as wide; Fabia in in (Campos, preparation). dactylus narrowlyspatulate, inserted an- A of adult and larval mor- of comparison gular notch in middle of ventral margin is more of phologyindicates that Tumidotheres propodus, not extending beyond tip than to Abdomen in both sexes with 7 closely related to Pinnaxodes any propodus. As free somites. othergenus in the Pinnotheridae. adults, both generashow a similar carapaceshape, Type Species. -Pinnotheres margarita an abdominal configurationthat is almost Smith, 1869, by present designation. Gen- identical,and walkinglegs that are of a sim- der masculine. ilar relativelength. Differences are observed Etymology.-From Latin tumidus,swollen, in the outermaxilliped. The ischium of Pin- and theres, to emphasize the possession of naxodes is generally separated from the gastric, cardiac, and branchiohepatic re- merus, while these articles are indistin- gions of the tumid carapace. guishably fused in Tumidotheres.Further- Taxonomic Remarks.-In addition to the more, in the former genus the dactylus ex- 674 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 9, NO. 4, 1989

tends beyond the tip of the propodus,while suggestdivergent evolutionary trends, gives this article in Tumidotheresreaches almost additional support to the establishment of to the tip of the propodus. Larval mor- the genus Tumidotheres. phologyhas been comparedby Hong (1974), who found that the larvae of Pinnaxodes Tumidotheres margarita (Smith, 1869), major and T. maculatusare almost identi- new combination cal. The shape and number of carapace Figs. 1-3 spines,abdominal somites, telson shape,and Synonymy.-Pinnotheres margarita Smith, 1869: the antennaeare very similarin both species. 245.-Smith, 1870: 166-169.-Lockington, 1877: Furthermore,the number of articles of the 154.-Miers, 1886: 276.-Holmes, 1894: 564.- Rathbun, 1910: 587, 1918: 91-93.-Tesch, 1918: maxillule,maxilla, maxillipeds,the setation 285-286.-Glassell, 1934: 301.-Silas and Ala- on these appendages, and the number of garswami, 1967: 1178, 1202, 1223, 1225.- zoeal stagesare exactly the same. This close Schmitt, McCain, and Davidson, 1973: 5, 9, 56, similarity in adult and larval morphology 57.-Wicksten, 1982: 221-225, fig. 1.-Campos- the that Tumidotheres Gonzfilez, 1988: 385.-Campos-Gonzalez and supports hypothesis Campoy-Favela,1988: 221-225, figs. 1, 2. is phylogeneticallyallied to Pinnaxodes,and Cryptophryspubescens Holmes, 1894: 564, 565, pl. similar arguments also can be used to es- 20, figs. 6, 7. tablish that both genera are not closely re- Pinnotherespubescens (Holmes, 1894): Rathbun, lated to any other known generain the Pin- 1918: 63, 65, 66, 87, 88, fig. 43.-Glassell, 1934: notheridae. 301.-Schmitt, McCain,and Davidson, 1973: 82. Material Examined.-GULF OF CALIFORNIA.- Life History Remarks. -Based on a review LagunaPercebu, about 23 km southof San Felipe, Baja of the availableinformation on life histories California, 1 young 9, 9 October 1984, E. Campos, on collector,host Lima pacificaOrbigny, 1846; 2 66 and of pinnotherid species and my unpub- 2 youngQ9, 20 November 1985, E. Campos,coll., host lished observations,I can recognizetwo pat- Barbatia reeveana (Orbigny, 1846). Puertecitos, km terns of reproductivebehavior. In the first 72, roadSan Felipe-San Luis Gonzaga,Baja California, pattern(Christensen and McDermott, 1959; 2 young 6, 13 September1985, G. Lopezand E. Cam- males and females in the hard- pos, coll., host L. pacifica.Playa Kino Viejo, Sonora, Jones, 1977) 2 QQ(1 ovigerous), 24 January 1985, J. R. Campoy- stage live and copulate within the first and Favela, coll., from Argopectencircularis (Sowerby, definitive host. The female molts and de- 1835). Punta San Pedro, Bahia Concepci6n,Baja Cal- velops from the masculineform (hard-stage) ifornia Sur, 1 ovigerousQ, May 1983, P. A. Ramirez, to the feminine form (posthard-stage).The coll., host Pinctada mazatlanica(Hanley, 1855); 1 2, in 18 May 1984, P. A. Ramirez,coll., host P. mazatlan- male also molts but remains the hard- ica; 3 Q2(2 ovigerous),4 November 1984, J. L. Bello- stage. In the second type of reproductive Le6n, coll., host P. mazatlanica. WEST COAST OF behavior (Pearce, 1966, 1969), the crab in- BAJA CALIFORNIA.-Estero El Cardon,Laguna de fects an intermediatehost after completing SanIgnacio, Baja California Sur, 4 $6 and 30 QQ,4 April In this host 1987, EulogioLopez, coll., host Argopecten(?) aequi- postplanktonic development. sulcatus(Carpenter, 1864). Agua Blanca, Bahia del Ro- the crab molts to become either the male or sario,Baja California, 1 Q,4 April 1986, A. Salas,coll., female hard-stage. This stage, which pos- host Hinnitesgiganteus (Gray, 1825). sesses leaves long feathery natatory setae, Distribution.-West coast of BajaCalifornia the intermediatehost and in a participates north to Bahia del Rosario, Baja California; in the sea. Af- copulatory swarming open Golfo de California,from LagunaPercebu, the and the terward, female, eventually male, about 23 km south of San Felipe, Baja Cal- infect the definitive host. The female molts ifornia, to La Paz, Baja CaliforniaSur, and severaltimes and develops to the ovigerous Bahia Kino, Sonora to Bahia de Panama male molts and but remains stage;the grows (Campos-Gonzailez,1988; present study). in hard-stage. This second type of repro- ductive behavior has been documented for Hosts. - : . Argopecten cir- T. maculatus and Fabia subquadrata,and cularis (Sowerby, 1835), Hinnites giganteus preliminaryobservations permit me to infer (Gray, 1825), Argopecten (?) aequisulcatus that T. margarita possesses a similar be- (Carpenter, 1864), Pinctada mazatlanica havior. (Hanley, 1855), Lima pacifica Orbigny, In my opinion the finding of the above 1846, Barbatiareeveana (Orbigny, 1846) (see divergentreproductive behaviors, which are Campos-Gonzalez, 1988; present study). closely relatedto functionalmorphology and SubadultFemale.- Body and legs with short CAMPOS: SYSTEMATICS OF PINNOTHERES MARGARITA AND P. MACULATUS 675

Fig. 1. Female of Tumidotheres margarita (Smith, 1869). Carapace width = 7 mm. a, dorsal view; b, frontal view.

pubescence. Carapace subpentagonal (Fig. cardiac regions, another depression behind 1a) convex, front projected, notched in mid- it. dle; postfrontal ridge extending over full Third maxilliped obliquely placed in buc- width of carapace; gastric and cardiac re- cal cavity (Fig. 1b); ischium and merus in- gions tumid and separated from hepatic and distinguishably fused, inner margin angu- branchial regions by longitudinal depres- late at middle; palp of 3 articles, carpus sion; slight depression between gastric and shorter than propodus, latter subspatulate, 676 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 9, NO. 4, 1989

Fig. 2. Tumidotheresmargarita (Smith, 1869). Female, carapacewidth = 7 mm. a, third maxilliped;c, chela; d, left leg;e, rightleg; f, abdomen.Line aroundfemale abdomen indicates marginal feathery hairs. Male, carapace width = 3.7 mm. b, third maxilliped. CAMPOS: SYSTEMATICS OF PINNOTHERES MARGARITA AND P. MACULATUS 677

C

Fig. 3. Degree of development of the right first pleopod of the male of Tumidotheres margarita (Smith, 1869). a, immature male, carapace width = 3.5 mm, cephalic view; b, immature male, carapace width = 3.7 mm, abdominal view; c, mature male, carapace width = 6.6 mm, abdominal view. 678 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 9, NO. 4, 1989 widest in middle at insertion of dactylus; that the differences noted in the relative latter narrowly spatulate, reaching almost length of the walking legs and the palp of to tip of propodus (Fig. 2a, b). the third maxilliped resulted from misin- Chelipedsstouter than walkinglegs; chela terpretationsof the holotype of P. pubes- slightlyincreasing in height distally (Fig. 2d, cens. Since the two species are similar in all e); palm with subpyramidalelevation on in- other features, I propose that P. pubescens ner face and convex on outer face; fingers is a junior synonym of T. margarita, the shorter than palm, hooked at tip; dactylus older named species. slightly longer than pollex, with triangular tooth and notch proximally placed on cut- SubadultMale. -This is almost identical to ting edge; pollex slightly deflexed, with the adult male figuredby Campos-Gonzalez smaller teeth on cutting edge. and Campoy-Favela (1988). Differences Walkinglegs moderatelystout, each pair were observedin the followingfeatures: car- symmetrical in length except second one, apace with very sparse or without velvety with left dactylus slightly longer than that pubescence, frontal region with medial on right; propodus of leg 1 with feathery notch; walking legs relatively slender, and swimming setae along ventral margin;car- dactyli relativelylonger; abdomen with lat- pus and propodus of legs 2 and 3 with 2 eral margins more parallel; and gonopods fringesof long featherysetae placedon outer similar but undifferentiated(Fig. 3a-c). third ventral on inner face, fringeup margin Morphological and Biological Remarks. - face;dactyli slenderand curved;fourth dac- The of two subadultmales, each liv- and less finding tylus longer curved than preceding with a subadultfemale, was the ones. In ing together decreasingorder, relative length of observation that permitted me to conclude > > 4 > walking legs 2 3 1. that these specimens are Abdomen orbicular postplanktonic (Fig. 2f), slightly stages of T. margarita.As noted above, the longer than broad, laterally not reaching of the male is almost identical coxae of notch morphology walkinglegs, distallyreaching in the subadult and adult stages. However, of firstthoracic sterite; marginclothed with the is differentfrom that of the setae. morphology long feathery postplanktonic female stages. These sub- Pinnotheres pubescens a Junior Synonym adult stages can be recognized as females, ofT. margarita.-The comparisonbetween althoughthey possess severalmasculine fea- the morphology of the subadult females of tures which are lost only when the adult T. margaritaand the description of P. pu- stage is reached.An objective identification bescens noted by Holmes (1864) indicates of T. margarita can be made on the basis that these two putatively different species of the third maxilliped, the carapace re- are almost identical.Discrepancies between gions, and, eventually, the second pair of my description and that of Holmes are in walkinglegs. With respectto the third max- the walking legs and the palp of the third illiped, T. margarita possesses a spatulate maxilliped. Holmes noted that the walking propodus largerthan the carpus and a nar- legs are subequal.However, I found that the row, spatulatedactylus which is inserted in relative length is 2 > 3 > 4 > 1, in de- the middle on the ventral margin of the creasingorder. The second leg is asymmet- propodus. These featuresare otherwise ob- rical, the left dactylus being slightly longer served only in the Atlantic species T. mac- than the right. With respect to the palp of ulatus. With respect to the carapace, T. the third maxilliped, Holmes reportedthat margarita possesses gastric and cardiac re- this consistsof two articles,but I foundthree. gions that are separated from the hepatic The dactylus lies close along the ventral and branchial regions by a depression; all margin of the propodus and may be over- of these regions are tumid (Rathbun, 1918; looked. Wicksten, 1982; Campos-Gonzalez, 1988; I consideredthat the above discrepancies present study). These features are seen ex- concerningthe symmetry/asymmetryof the clusively in T. margarita and T. maculatus. second pair of walking legs arise because Finally, the asymmetryin length of the sec- Holmes studied a hard-stagefemale and my ond pair of walkinglegs is a diagnostic fea- description was based on a late posthard- ture of T. margarita. However, I recom- stage female (perhaps III or IV). I suspect mend caution with the use of this character. CAMPOS:SYSTEMATICS OF PINNOTHERESMARGARITA AND P. MACULATUS 679

A retrospective analysis of the postplank- Lockington, W. N. 1877. Remarks on the Crustacea tonic development of pinnotherid crabs, of the west coast of North America, with a catalogue which included observa- of the species in the museum of the California Acad- my unpublished emy of Sciences.-Proceedings of the California tions for several Mexican species, permits Academy of Sciences, 1876, 7: 145-156. me to infer that very young females of T. Miers, E. J. 1886. Report on the Brachyura collected margarita (prehard- and hard-stage) possess by H.M.S. Challenger during the years 1873-1876.- symmetrical walking legs. This inference is Report on the scientific results ofthe voyage of H.M.S. based on the fact Challenger during the years 1873-1876, Zoology 17: that males and females at i-xli, 1-362. the prehard- and hard-stages are almost Pearce,J. B. 1966. The biology of the crab, identical, differing only in the abdominal Fabia subquadrata,from the watersof the San Juan appendages. The male of T. margarita pos- Archipelago,Washington.-Pacific Science 20: 3-35. 1969. On in Pinnotheresmac- sesses symmetrical reproduction walking legs. ulatus (:Pinnotheridae).-Biological Bul- letin 127: 384. ACKNOWLEDGEMENTS Rathbun, M. J. 1910. The stalk-eyed Crustaceaof I am indebted to my friends and former students Peru and the adjacent coast.-Proceedings of the from the Universidad Autonoma de Baja California United StatesNational Museum 38(1766): 531-620. for collecting and sending specimens of T. margarita 1918. The grapsoid crabs of America.- for examination. My great appreciation is due to Alma United StatesNational MuseumBulletin 97: 1-461. Rosa de Campos, Roger Seapy, and Mike Horn for Schmitt, W. L., J. C. McCain, and E. S. Davidson. their criticism of the manuscript, and to Lon Mc- 1973. DecapodaI. BrachyuraI. Family Pinnotheri- Lanahan for the support given by California State Uni- dae.-In: H. E. Gruner and L. B. Holthuis, eds., versity Fullerton. This work was sponsored by the proj- Crustaceorumcatalogus. W. Junk B.V., Den Haag, ect "Sistematica y bioecologia de los Arthropoda The Netherlands.Pp. 1-160. dominantes en areas selectas del municipio de Ensena- Silas, E. G., and K. Alagarswami. 1967. On an in- da, B.C." of the Escuela Superior de Ciencias, Uni- stanceof parasitisationby the pea-crab(Pinnotheres versidad Aut6noma de Baja California. sp.) on the backwaterclam [Meretrixcasta (Chem- nitz)] from India, with a review of the work on sys- LITERATURECITED tematics,ecology, biology and ethology of pea crabs of the genus PinnotheresLatreille. -Proceedings of Campos-Gonzilez, E. 1988. New molluscan hosts for the Symposium on Crustaceaheld at Ernakulam, two shrimps and two crabs on the coast of Baja 1965, SymposiumSeries 2. MarineBiological Asso- California, with some remarks on distribution.-Ve- ciation of India 3: 1161-1227. liger 30: 384-386. Smith, S. I. 1869. Pinnotheresmargarita Smith, sp. ,and J. R. Campoy-Favela. 1988. Morfologia nov.-In: A. E. Verrill, On the parasitic habits of y distribuci6n de dos cangrejos chicharo del Golfo Crustacea.American Naturalist 3: 245. de California (Crustacea: Pinnotheridae).-Revista 1870. Notes on AmericanCrustacea. No. 1. de Biologia Tropical 35: 221-225. .- Transactions of the Connecticut Christensen, A. M., and J. J. McDermott. 1958. Life- Academy of Sciences 2: 113-176. history and biology of the , Pinnotheres Tesch, J. J. 1918. The Decapoda Brachyuraof the ostreum Say.-Biological Bulletin 114: 146-179. SibogaExpedition. II. Goneplacidaeand Pinnotheri- Glassell, S. A. 1934. Affinities of the brachyuran fau- dae.-Siboga-Expeditie 39c': 149-295. na of the Gulf of Califoria. -Journal of the Wash- Wicksten, M. J. 1982. New records of pinnotherid ington Academy of Sciences 24: 296-302. crabs from the Gulf of California(Brachyura: Pin- Holmes, S. J. 1894. Notes on the west American notheridae).-Proceedingsof the Biological Society Crustacea. -Proceedings of the California Academy of Washington95: 354-357. of Sciences, series 2, 4: 563-588. Hong, S. Y. 1974. The larval development of Pin- RECEIVED:13 April 1989. naxodes major Ortman (Decapoda, Brachyura, Pin- ACCEPTED:30 May 1989. notheridae) under the laboratory conditions.-Pub- lications of the Marine Laboratory, Pusan Fisheries Address: (postal address) Escuela Superior de Cien- College 7: 87-99. cias, Universidad Aut6noma de Baja California, Apar- Jones, J. B. 1977. Post-planktonic stages of Pinnothe- tado Postal 2300, Ensenada, Baja California, Mexico; res novaezelandiae Filhol, 1886 (Brachyura: Pin- and Department of Biological Sciences, California State notheridae).-New Zealand Journal of Marine and University Fullerton, Fullerton, California 92634. Freshwater Research 11: 145-158.