Annual mass strandings of pelagic (100-200 m), and probably invades the continental slope (Aurioles­ red crabs, Pleuroncodes planipes Gamboa, 1992). Population with­ drawal is associated with a rise in (Crustacea: Anomura: Galatheidae), bottom temperature above 16°C, and pelagic red crabs remain from in Bahia Magdalena, June through October in waters 100-200 m deep, where bottom Baja California Su~ Mexico temperature is in "the range of 12-16°C (Aurioles-Gamboa, 1992). David Aurioles-Gamboa One of the notable characteris­ Centro de Investigationes Biologicas de Baja California Sur tics in pelagic red crab life history Apartado Postal 128. LA Paz B. C. S.• Mexico are mass strandings, which have been reported for Bahia Magda­ lena and the California Coast Maria Isabel Castro-Gonzalez (Glynn, 1961; Boyd, 1962; Kato, Instituto Nacional de la Nutrici6n "Salvador Zubiran" 1974; Stewart et aI., 1984). The Vasco de Quiroga #15. Col. y Del. Tlalpan. J4000. Mexico D. F. main difference between strand­ ings in California and Baja Cali­ Ricardo Perez-Flores fornia is the frequency of ocur­ Centro de Investigaciones Biologicas de Baja california Sur Apartado Postal J28. La rence. Pelagic red crab beachings Paz B. C. S.• Mexico. in California occur during EI Niiio events, which enable the popula­ tion to move northward in warm water currents originating in the south. In contrast, pelagic red crab Pelagic red crabs (or langostilla in about 17-20 mm standard cara­ strandings in Bahia Magdalena Spanish), Pleuroncodes planipes, pace length (SCL), they become are annual, and apparently recur are very abundant galatheid crus­ benthic, making occasional move­ on the same beaches and during taceans off the west coast of Baja ments to the surface (mostly at the same season ofyear. California. Some studies suggest night) in a circadian migration InBahiaMagdalena, pelagic red that pelagic red crabs are the most (Boyd, 1967). Once the animals crabs were observed in the upper abundant species in the micro­ reach 32-34 mm SCL, they are 50 cm of water of the surf zone neck.ton, one ofthe mostimportant fully benthic as are other galat­ before stranding. Onshore winds consumers of phytoplankton, and heid species (Boyd, 1967;Aurioles­ and receding tides hasten and "the most common prey item for Gamboa, 1992). intensify stranding (Boyd, 1962>. many marine vertebrates in the Pelagic red crabs breed from Kato (1974) proposed that the area (Boyd, 1962, 1967; Black­ December throughApril; the peak presence ofpelagic red crabs near burn, 1969; LonghurstetaI., 1967; of the reproductive season is in shore is primarily due to winds, Kato, 1974; Galvan, 1988; Balart February(Boyd, 1962; Kato, 1974; waves, and currents. and Castrol ). GOmez, 1990). Females about 14­ On 9 May 1991, one ofus (D.A­ Although widely used, the com­ 15 mm SCL, have been found car­ G.) observed a mass stranding of mon name (pelagic red crab) de­ ryingeggs, but most ofthe females pelagic red crabs on a beach of scribes only the planktonic period startto breed when they are about Magdalena Island close to the (about one year) in the life of the 20 mm SCL (Boyd, 1962; Serrano, mouth ofthe Bahia Magdalena on species. Larvae, juveniles, and 1991). the Pacific coast of Baja Caliror­ young adults are planktonic. At The benthic population per­ nia (Fig. 1). About 1100 hours, a forms seasonal bathymetric move­ compact surface swarm of live ments, at least in the area from crabs was seen 1-2 m from the 1 Balart-Pliez, E., and Castro-Aguirre, lat. 24° to 26° N, in which they dis­ beach. Small groups ofcrabs were J. L. 1992. Habitos alimenticios de la merluza Bajacaliforniana Merluccius perse during winter and spring to thrown to the beach by waves, and angustimanus, en la costa occidental de occupy the benthos of the conti­ were unable to return to the sea. Baja California Sur, Mexico. Paper pres. nental shelf (0-200 m depth). M­ at the IX International Symposium of Marine Biology, 1-5 June 1992, La Paz ter the breeding season, the popu­ Manuscript accepted 4 October 1993 Baja California Sur, Mexico. lation moves to deeper waters Fishery Bulletin 92:464-470 (1994) 464 NOTE Aurioles-Gamboa et al.: Mass strandings of Pleuroncodes planipes 465

and may produce, depending on body size,

liZ° from 500 to 5000eggs ineach brood (Serrano, 1991). Basedonthis fact, debilitation caused .' by reproductive investment should be more evident in females. For that reason, the chemical composition ofpelagic red crabs in Bahia Magdalena was determined for both sexes. We were aware that males were over­ represented in samples collected on the con­ b tinental shelf (Boyd, 1962; Serrano, 1991); ~ thus we also wished to determine ifstranded (') animals were female-biased, as an explana­ ... tion for the unbalanced sex ratio recorded on the continental shelf. (')

Materials and methods

o To test whether the strandings were due to

(') weakness caused by starvation or malnutri­ III tion, about 20 kg oflive-stranded pelagic red :. crabs were collected as soon they were z stranded.. From this sample, a total of 1,150 individuals were sexed and measured for SeL to the nearest 1.0 mm. Sex was deter­ ISLA SANTA mined by the presence or absence of modi­ MAReARITA fied pleopods, which males use to fertilize the eggs (Boyd, 1962). Standard carapace length

11° was measured from the antorbital notches of the rostrum to the midpoint of the poste­ riorborderofthe carapace (Kato, 1974). This Figure 1 measurement is usually preferred over total Study area on the west coast of Baja California Sur, Mexico. length because it does not vary with shrink­ Dots inside Bahia Magdalena indicate the location of stations age ofthe abdomen. sampled. The shaded area is the region where pelagic red crabs, Stomach contents were analyzed in order Pleuroncodes planipes, were found as indicated by positive sta­ to determine if1) the animals hadbeenfeed­ tions and visual observations (from Solis, 1991). ing before stranding, and 2) the number of items and composition was similar to stom­ ach contents ofpelagic red crabs collected on The general appearance of these pelagic red crabs the continental shelf(Perez andAurioles-Gamboa2). (color and mobility) suggested that the crustaceans We examined the stomach contents from a subsample were healthy and that the stranding could be con­ of nine individuals after fixing in formalin (4%), re­ sidered accidental (Boyd, 1962). We questioned local moving the cardiac-pyloric stomach from the animal, fishermen about crab strandings and determined dissolving its contents intwo drops ofwater andplac­ that mass strandings 1) occur annually, usually in ing them on a smear slide. Perez and Aurioles­ spring, from April through June, and 2) are common Gamboa2 determined that the average stomach on Santa Margarita and Magdalena Islands but composition in a swarm of crabs does not vary sig­ rarely seen on the peninsular coast. nificantly after a sample of six crabs, Since strandings coincide withthe end ofthebreed­ Food items were identified and counted under the ing season, we addressed the null hypothesis that microscope and relative abundance ofmajor groups stranded pelagic red crabs, particularlyfemales, were in a weakened state because ofenergy expended in 2 Perez, F. R., and D. Aurioles-Gamboa. 1992. Cambios en la reproduction, as reported for many crustaceans alimentaci6n invierno-verano de la langostilla Pleuroncodes planipes, en la costa oeste de Baja California. Paper pres. at (Hartnoll, 1985). It is known that pelagic red crabs the IX International Symposium of Marine Biology, 1-5 June are able to breed twice in a single breeding season 1992. La Paz B. C. S. Mexico. 466 Fishery Bulletin 92/2). 1994 of food items was determined. Following Perez and Pelagic red crabs had been caught from the shelfin Aurioles-Gamboa2, we recorded some of the phyto all seasons, but only during mid-summer (when the and zooplankton components in four major groups: bottom-surface temperature difference is as great as 1) phytoplankton, 2) zooplankton, 3) particulate or­ 17"C) did the crabs show signs of damage as they ganic matter (POM), and 4) inorganic matter (small moved slowly and died rapidly on the deck (Aurioles­ grains of sand, clay or mud). The number of Gamboa, unpubl. data). In contrast, crabs were very diatoms, crustacean parts, foraminifers, and other active in the first minutes after stranding, andmoved components, such as small agglomerations of POM, less frequently later. The crabs were brilliant red, were counted and their numbers converted to rela­ which differentiatedthemfrom thelightercolor ofcrabs tive frequency. collected on thecontinental shelf. Basedontheirvigor­ Proximate analyses was based on 200 g 0 and ous activity, the pelagic red crabs stranded on 200 g 0.05, df=9; t=-o.3082). for the stranded pelagic red crabs (Zar, 1984). Food composition (particulate organic matter, zoop­ lankton, and phytoplankton) was not different be­ tween crabs from the two regions. Inorganic matter Results (grains ofsand, clay, etc.) was more abundant in the stomachs ofthe pelagic red crabs collected from the The stranded crabs formed a long brilliant red line shelf (x=365 versus 60; two sample t-test, P<0.05, of several kilometers on the interior coast of the <;If=9; t=-o.0046). This difference, however, does not northern part of Bahia Magdalena (Fig. 1). In addi­ account for a significant change in the feeding hab­ tion, there were two lines of dried crabs separated its ofcrabs from the two samples. by a few meters, higher on the beach and stranded during the previous days. Proximate composition of stranded red crabs In stranded pelagic red crabs, the sexes were not dif­ Behavior of pelagic red crabs ferent in protein and crude fiber (Table 1), however during stranding they differed significantly in lipids and ash contents (two sample t-test, P<0.05, df=9; t=1.870 and 10.012 Two hours ofobservations on a surface swarm about respectively). Females had higher lipid and lower ash 12 m long and 1 m wide were conducted after 1100 content than males, both by about 1.5%. hours (11 May 1991) during the receding tide. The There were significant differences whenthe chemi­ swarm was propelled to and from the beach by the cal composition ofstranded crabs (sexes combined), waves and was unable to move offshore. When the were compared to crabs from the continental shelf swarm was pushed toward the beach by the wave (Table 1). Crabs from both areas were similarin their action, some animals were thrown onto the sand and protein content, but differed in lipids and ash. The exposed as the water receded. lipid content in Bahia Magdalena crabs was almost During sampling on the beach, the pelagic red nine times higher than that in shelf crabs (t-test, crabs moved their legs and actively used their chelae P<0.05, df=16, t=35.664). Crabs from the continen­ as pincers. This behavior was typical of pelagic red tal shelf were higher in fiber and ash but lower in crabs caught in trawls from the continental shelf. carbohydrate content. NOTE Aurioles-Gamboa et al.: Mass strandings of Pleuroncodes planipes 467

Itwas also noted that during handling ofstranded males and females (Fig. 3); mode and mean were crabs an oily, orange film was left in the containers, 15.82 and 17.02 mm for females and 17.36 and 17.26 a phenomenon not previously observed in crabs col­ mm for males, respectively. Differences in mean size lected in more than 200 bottom trawls on the conti­ of males and females were statistically significant nental shelf(Aurioles-Gamboa, 1992). The substance (two-sample t-test=2.057, P<0.05, df=1,147). In older probably contained carotenoids, which in this species organisms, slight sexual dimorphism is evident in have been identified as astaxanthins (Wilkie, 1972). males which are slightly larger and heavier with longer and wider chelae (Serrano and Aurioles­ Size and sex of stranded pelagic red crabs Gamboa, 1991). Pelagic red crabs collected in Bahia Magdalena were Pelagic red crabs are about 14 mm SCL at the end 12-28 mIll SCL. Size distribution was similar for ofthe first year of life (about February-March) and grow approximately 1 mm per month (Boyd, 1962). Because the crabs were about 17 mm SCL (mode), 2500 they should have been about 14-15 months old. 2250 Some individuals were about 24-28 mm SCL (Fig. 3), which according to Boyd (1962) were about 26­ 2000 en 27 months old. ::E w 1750 The number of females (605) in relation to the !: 1500 number ofmales (544), deviates significantly from LL 0 1250 the expected 1:1 proportion (chi-square P

0 Debilitated pelagic red crabs as 2 3 4 5 6 7 8 9 explanation of strandings NUMBER OF STOMACHS We rejected the null hypothesis that stranded pe­ lagic red crabs represent a debilitated fraction of 2250+------1 the population because 1) the stranded crabs moved ' B vigorously during and just after stranding, 2) the en 2000+------1 ::E stomachs of crabs were full and the contents were w 1750+------1 I- ' similar to those collected on the continental shelf, LL 1500'+------,=...------1 which indicated they were feeding normally, 3) the o chemical composition was generally similar to those a: w 1000 collected on the continental shelf, and when differ­ III ent, did not suggest malnutrition, and 4) timingand ::E 750 ::J area ofstrandings are better explained by physical z 500 phenomena (i.e. by accidental strandingdue to fun­ 250 neling effect, wave action, and receding tide). Our o observations support the observations made by 2 3 4 5 6 7 8 NUMBER OF STOMACHS Boyd (l962), that waves and receding tide playa major role after the animals enter the surf zone. 1_ OAOANIC W.TTER _ INORG. MAneR rrl4I ZOClPlANKTON CJ PHYTOPI.ANKTON Two available stranding reports (Boyd, 1962; Jorge Llinas3 ), indicated that beachings occurred during Figure 2 falling tides. According to local fishermen, the two Total number of items and gross stomach composition higherlines ofstranded crabs we found onthebeach from pelagic red crabs, Pleuroncodes planipes, collected of Isla Magdalena on 9 May 1991, were stranded in Bahia Magdalena (A), and organisms typically found two mornings before our visit, also during receding on the benthos of the continental shelf off Baja Califor­ tides. nia

Differences in pelagic red crab chemical composition Table 1 The lipid content of the younger Mean values for proximate chemical analyses ofPleuroncodes planipes stranded pelagic red crabs was dif­ samples from Bahia Magdalena and the Continental Shelf of Baja California. ferent from that recorded in older specimens caught on the benthos of Bahia Magdalena the continental shelf (Table 1). Dif­ ferences in the proportion of chemi- Males Females Significant cal components between young and % % difference old individuals have been reported n=5 n=6 95% conf. * for many decapod species (Herring, Moisture 4.7 (0.28) 4.73 (O.23) 1973; Morris, 1973). The observed Ash 29.79 {O.361 28.21 (0.66) + differences in lipid concentration and Ether extract 12.79 (0.72) 15.46 (1.39) + apparent pigmentation between Crude fiber 7.91 (O.991 8.70 (0.65) (0.07) young-adult and older-benthic pe­ Crude protein 41.75 <0.141 40.64 Carbohydrates 3.06 2.26 lagic red crabs cannot be considered abnormal or attributable to un­ Bahia Magdalena Continental Shelf healthy specimens. There was no evi- Both sexes Both sexes dence to support the hypothesis of a % % debilitated fraction of pelagic red n= 11 n =12 crabs, and strandings can be ex­ Moisture 4.71 (0.20) 4.12 10.32) plained by mere accident. Ash 29.04 (0.241 40.30 10.03) + The differences in lipid and ash Ether extract 14.12 (1.98) 2.75 (0.007) + content between male and female Crude fiber 8.30 (0.62) 12.83 (0.03) + (0.22) stranded crabs would be attributable Crude protein 41.19 38.61 (0.29) Carbohydrates 2.64 1.39 to metabolic differences in which fe­ males require more lipid to invest in • Two-sample I-test for means; + significant difference. - no difference IAlpha=O.051. egg production (Hartnoll, 1985). Some females still had eggs attached on the pleopods as evidence of their repro­ ductive condition; however, the low numbers 350r------, ofovigerous females in the sample, suggested that we collected them at the end of the 300· ······························ . n =1150 breeding season. 250··············· . ~ Size and sex of pelagic ifi 200 . stranded red crabs ::l @ 150········· . II: The stranded individuals we sampled were u. n = 724 predominantly 13 to 20 mm SCL, although 100 . some larger crabs were also found (Fig. 3), Kato (1974) also reported individuals ofthese 50······················· two size distributions in a mass strandingin Bahia Magdalena. Photos were available of 1214 16 1820 22 24 26 28 30 32 34 36 38 40 a mass stranding in May of 1979, in which STANDARD CARAPACE LENGTH mm pelagic red crabs larger than 25 mm SCL San Diego, 123 p. sex ratioincoastalwaters comes from Serrano(1991), 1987. Benthic and pelagic habitats ofthe red crab Pleuroncodes planipes. Pacific Science 21:394­ who reported higher frequency of females inshore 403. during the breeding season. Similar findings were Boyd, C. M., and M. W. Johnson. obtained by Escoto and Orellana (1981) for pelagic 1983. Variations in the larval stages of a decapod red crabs off the Nicaragua coast, and for a closely crustacean, Pleuroncodes planipes, Stimpson related species, P. monodon, from Chile (Arana and (Galatheidae). BioI. Bull.(Woods Hole) 124:142­ Culquichic6n4). However, several authors have re­ 152. portedthatthe total sex ratio on the continental shelf Castro, G. M. I. is male biased (Boyd, 1962; Boyd and Johnson, 1963; 1993. Proce80S tecnologicos aplicados alalangostilla Serrano, 1991). Boyd (1962), suggested that the sex­ (Pleuroncodes planipes Stimpson) y cambios en su ratio differences on the continental shelfcould be due composici6n quimica a diferentes latitudes para su to one or a combination ofthe following causes: 1) a aprovechamiento en alimentaci6n animal. Tesis de Maestria en producci6n animal, 82 p. deviation in primary sex ratio, 2) lower survival rate Escoto, a, and F. Orellana. offemales, or 3) the fact that plankton nets may not 1981. Segundo crucero de evaluaci6n del recurso sample males and females with equal effectiveness. langostino del Pacifico Nicaraguense. Boletin The hypothesis that females die at a higher rate tecnico del Instituto Nicaraguense de la Pesca than males is supported by the present data, since (Diciembre 1980), 42 p. females were more abundantwhere there was a natu­ Galvan, M. F. ral cause of mass mortality. It has been mentioned 1988. Composici6n y analisis de la dieta del atun that the breeding season of the species is synchro­ aleta amarilla Thunnus albacares, en el oceano nized to the time (winter-spring) when coastal up­ Pacifico Mexicano durante el periodo 1984­ welling is more intense. Pelagic red crabs may be 1985. Tesis de Maestria en Ciencias, CIC.lMAR, more abundant in places where phytoplankton is 86p. Glynn, P. W. more plentiful (Blackburn, 1969). Thus, it can be 1981. The first recorded mass strandings ofpelagic advantageous for pelagic red crab females to move red crabs, Pleuroncodes planipes, at Monterey Bay to shore and release larvae in upwelled water. How­ California since 1959, with notes on their ever, by doing so, females are more likely to enter biology. California Fish and Game 47 (1): 97-101. Bahia Magdalena orothercoastal lagoons and die in G6mez, G.J. accidental strandings. 1990. Variaci6n de la distribuci6n y abundancia de los estadios planct6nicos de Pleuroncodes planipes (Crustacea: Galatheidae) en la costa occidental de Literature cited Baja California Sur, Mexico (1986). Tesis de Licenciatura en Biologia Marina, Universidad A. O.A. C. Autonoma de Baja California Sur, Mexico, 86 p. 1984. Official methods of analyses, 14th Hartnoll, G. R. ed. Association ofAnalytical Chemists, Washing­ 1985. Growth, sexual maturity and reproductive ton D.C. output. In A. M. Wenner (ed.), Crustacean issues Aurioles-Gamboa, D. 3: factors in adult growth, p. 101-128. A. A. 1992. Inshore-offshore movements of pelagic red Balkema, Boston, and Rotterdam, Netherlands, crabs Pleuroncodes planipes (Decapoda, Anomura, Herring, P. J. Galatheidae) off the Pacific coast of Baja Califor­ 1973. Depth distributions of the carotenoid pig­ nia Sur, Mexico. Crustaceana 62(1):71-84. ments and lipids ofsome oceanic animals. 2: Deca­ Blackburn, M. pod crustaceans. J. Mar. BioI. Assoc. U.K. 53:539­ 1989. Conditions related to upwelling which deter­ 562. mine distribution oftropical tunas offwestern Baja Kato, S. California. U. S. Fish Wild. Servo Fish. Bull. 1974. Development of the pelagic red crab (Gala­ 68:147-176. theidae, Pleuroncodes planipes) fishery inthe east­ ern Pacific Ocean. Mar. Fish. Rev. 36 (10):1-9. Longhurst, A. R., C. J. Lorenzen, and 4 Arana, E. P., and Z. M. Culquichic6n. 1990. Estructura poblacio­ W. H. Thomas. nal dellanl{Ostino colorado IPleuroncodes monodonJ en la zona centro-sur de Chile. Estudios y Documentos. Final Rep. No. 7/89 1987. The role ofpelagic red crabs in the grazing of to Universidad Cat6lica de Valparaiso, Facultad de RecuTsos phytoplankton off Baja California. Ecology Naturales, Escuela de Ciencias del Mar, 56 p. 48:190-200. 470 Fishery Bulletin 92(21. 1994

Morris, R. J. Solis, F. 1973. Relationships between the sex and degree of 1991. Composici6n y distribuci6n espacio-temporal maturity of marine crustaceans and their lipid de los macroinvertebrados bent6nicos del complejo compositions. J. Mar. Bio1.Assoc. U.K. 53:27-37. lagunar Magdalena-Almejas de la costa occidental Perez, F. R. de Baja California Sur. Tesis de licenciatura en 1992. Alimentaci6n de la langostilla Pleuroncodes Biologia, Univ. Michoacana de San Nicolas de planipes Stimpson, 1860, durante el periodo Hidalgo, Mexico, 96 p. reproductivo (Marzo, 1990). Tesis de licenciatura Stewart, B. S, P. M. Yochem, and R. W. Schreiber. en Biologia, Universidad Nacional Autonoma de 1984. Pelagic red crabs as food for gulls: a possible Mexico, ENEP, Zaragoza, Mexico, D. F., 53 p. benefit of El Nino. The Condor 86:341-342. Serrano, P. v: Wilkie, D. W. 1991. Aspectos reproductivos de la langostilla 1972~ The carotenoid pigmentation of Pleuroncodes Pleuroncodes planipes (Crustacea: Decapoda: Gala­ planipes Stimpson (Crustacea: Decapoda: Gala­ theidae). Tesis de Maestria en Ciencias Marinas, theidae). Compo Biochem. PhysioI. 42 (B):731-734. CICIMAR, 89 p, La Paz Baja California Sur, Mexico. Zar, J. H. Serrano, P. V:, and D. Aurioles-Gamboa. 1984. Biostatistical analysis. Prentice-Hall, Engle­ 1991. Dimorfismo sexual en la langostilla, wood Gliffs, NJ, 716 p. Pleuroncodes planipes Stimpson, 1860 (Crustacea: Decapoda: Galatheidae). Proc. ofSan Diego Soci­ ety ofNatural History 13:1-5.