CRUSTACEAN RESEARCH，NO. 24: 137-145，1995
Limb loss in the poisonous crab Aterglαtis floridus (Linnaeus) - advantages of possessing to玄ins?
Christopher P. Norman
Abstract. - To determine the effec. 1969; Konosu et α1 . ，1969; Yasumura et tiveness of possessing to玄ins as adefense α1 . ，1986). In Japan，three species，all mechanism in crabs，the level of limb loss xanthids [Atergαtis βoridus (Linnaeus， was examined in a poisonous crab 1767)，Zosimus aeneus (Linnaeus，1758) Atergatis floridus. Crabs were col1 ected and P1αtypodiαgrαnu10sα( R u p p e l l ， individua11yusing SCUBAbetween June 1830)] are reported as highly toxic 1990 and December 1992. The sex ratio (Hashimoto et α1 . ，1967; Konosu et α1 . ， approximated 1: 1. Significant levels of 1969). Thedistribution of Z. aeneus and limb loss were observed in both males P.grα，nu10sαi s largely restricted to coral and females，but limb loss 仕equency d品 habitats，however A. βoridus，a rock reef fered between se玄es. Higher 仕equencies dwelling species，is broadly distributed in of limb loss were found in males (4 1. 3% Japan along the southern (temperate) with limb loss) than females (18.4%). Site coastline of Honshu and Shikoku and of loss also differed between sexes，with Kyushu (Sakai，1976). Atergatis floridus males having ahigher loss of the walking also has abroad geographical range legs 1，3and 4than the chelipeds and leg throughout the Indo-Pacific 企omJapan 2(P
vidual survives. When acrab is attacked， rable to other non司 toxic crabs. The eco 鞠 or perceives the threat of attack，the crab logical advantages to crabs of possessing LIMB LOSS IN ATERGATIS FLORIDUS 139
toxins as adefense mechanism are dis- ischium prior to the regeneration of the cussed. limb，was measured and staged using the developmental stages，G 1 (仕 esh break，no Materials and Methods bud) to G7 (fully pigmented and differen- Over a2 .5year period (June 1990 - tiated limb bud)，of Ary et al. (1985).For December 1992) A. βoridus were sampled ovigerous females，egg and ovarian devel- from approximately 0-8 m via SCUBA opmental stages were determined follow- from rock reefs adjacent to the Banda ing the criteria used by Norman &Jones Marine LaboratoIγ，Tokyo University of (1993). Fisheries (34 0 58'3"N，139 0 46'5"E). This survey was carried out concurrently with Results observations on juvenile spiny lobster Thesex ratio (92M:98F) did not signifi- Pα nulirus jα:ponicus ，and amap of the cantlyvary 企omaratio of 1:1 (χ2 =0.189 ， sampling location，details of seasonal df=1，P>0 .5) . The maximum sizes S出 npling frequency，dive duration，habi- sampled were，male 57.2 and female 52.4 tats examined etc. are given in Norman et mmCW; minimum sizes 12.2 and 10.55 α1. (1994).Over atotal of 330 dives，A. mmCW ，respectively. No obvious peaks βoridus were only in 企equently observed in the size distribution pattem relating to and a total of 190 specimens were year classes were observed in either sex sampled. Atergαtis floridus were sampled (Fig. 1). Small juveniles (10-20 mmCW) during the day，being found under boul- were first observed in AugustlSeptember ders and in holes on the rock surface. In- of each year sampled. In both sexes the dividuals were captured by hand，taking mode was the size class 40-45mm CW care not to damage (remove limbs) the (Fig. 1) .Ovigerous females (n =9) were crab.Crabs were placed，individually in observed from June (2 4/6/90) to Septem- self sealing plastic bags in situ to avoid ber (6/9/90). Minimum size of ovigerous any limb loss post-capture. females was 35.4 mmCW; maximum 52.4 In the laboratory，crabs were exam- mmCW (Fig. 1). Dissection of ovigerous ined 品r sex，c訂 apace width (CW)，molt females revealed 5specimens all with late stage and limb loss pattem. Sex was de- staged，eyed eggs (stages 3or 4) with ova- termined from the external abdominal ries in the maturing or ripe condition. morphology，and for specimens <15 mm This suggests that as ovarian develop- CWfrom the pleopod structure via bin- ment is proceeding whilst the females are ocular microscope. Carapace width was ovigerous，multiple broods in asingle measured with hand-held vemier calipers intermolt period may occur in some speci- across the broadest section of the antero- mens of this species. Molt stages were lateral teeth.Molt stage was determined predominantly intermolt (63.7%) and pre- using the criteria of Drach (1939) [(A) molt (34.7%)，however postmolt，soft postmolt，soft with no calcification of the (0.5%) and papershell (1. 1%) were also exoskeleton; (B) papershell，branchio- observed. stegite region flexible ;(C) intermolt，com- Of the sample of 92 males，only 54 pletely hard exoskeleton;(D) premolt， (58.7%) had acomplete limb complement; exocuticle developed beneath the exoskel- that is 38 (4 1. 3%) had one or more limbs etonl .Limb loss ，both the site and fre- missing (Table 1) .Th epattem of loss sig- quency of limb loss was recorded.For nificantly differed 企omarandom pattern specimens with multiple limb loss ，to as- (χ2 =46.8 ，df =9 ，P<0.01) .Loss of cheli- sess whether limb loss occu汀 ed simulta- peds and walking leg 2was low in males， neously or not，the limb bud which devel- and ahigher percentage frequency loss of ops 仕omthe breakage plane of the basi- legs 1，3 and 4was observed (Fig.2). Of 140 C.P.NORMAN
凋A 守 specimens with multiple limb loss (n =17 ， 内U ‘A ザU male and female combined)，all limbs 。 A 五 今υ 日 'u showed the s田 ne stage limb buds indicat・ 話 回 ing that limb loss occuπed at approxi- O 0 mately the same time，with the exception U凶 S 10 ofone specimen [male 36.7 mmCW (13/9/ E U 20 90)，RL3 ，RL4 with stage G4 buds and H t 30 LL3 showing a企 esh break. age，i. e. ，pre- 40 G1 (Ary et α1 . ，1985) (see figure 2for ter・ 0 10 20 30 40 50 60 minology for limbs)]. C 釘 apace Width (mrn) Discussion Fig. 1. Size- 仕equency distribution in 5mm size classes ofmale (above) and female (below) Due to the relative in仕equency of ob- Atergα， tis βoridus sampled between June 1990 servations of A. βoridus in the field ，the and December 1992. Shaded area indicates total number of specimens sampled over ovigerous females. the 2.5 year period are few.However ， some basic information on the general specimens with missing limbs，only one ecology of the species c但 1 be gleaned. The limb missing 29.3%(n =27) was most 仕e- sex ratio approximates 1:1; Saisho & quent，and 7.6% (n =7) had 2limbs miss- Ushio (1969) similarly found a1:1 sex ra- ing，and 2.2% (n =2) had 3and 4limbs tio for samples tak. en企omvarious sites in missing，respectively (Table 1) .Females SWJapan(χ2=0.046 ，df=l ，P>0.5). Saisho showed adifferent pattem oflimb loss. Of &Ushio (1 969) found asimilar size range the 98 females，81. 6%(n =80) had acom- 旬 this study，mean size 43.8 mmCW and plete limb complement 田 ld only 18.4% (n amaximum size of56.1 mmCW ，although =18) showed limb loss (Table 1). The posi- ofwhich sex is not stated. From gonad ob- tion of limb loss in females showed aless servations of ovigerous females，multiple clear pattem，with ，contrary to males，left broods mayoccur during an intermolt pe- leg 2having ahigh frequency of loss riod.Atergαtis βoridus was only observed (6 .1%) and cheliped loss being more 企e- in cryptic habitats during the daytime quently observed (Fig. 2). The 仕equency (holes in the rock face and underneath of loss of individuallimbs in females was relatively large boulders) with the excep- generally low (< 5% )compared to males tion of 1mating p国rwhich was found out- (Fig.2) .Multiple limb loss OCCtl町 ed in fe- side of acrevice ，which was presumably males，and was marginally higher in fe- too confined to allow copulation inside. males than in males，33% offemales (6 of Very few specimens in soft and papershell 18) as opposed to 29% in males (11 of 38) (recently molted) stages were sampled having multiple limb loss (Table 1). Of (1. 6% of the sample)，although these
!， requency of limb loss in male and female Atergatis floridus .Th epercentage frequency with acom ・ plete limb component，wi 白 limb loss ，and for specimens with limb loss the percentage of the to 凶 with single ， double or multiple losses .
Sex Sample Complete Wi白 limb Single Double Triple Quadruple slze (no limb loss) loss loss loss loss loss Male 92 54 38 27 7 2 2 (58.711も) (4 1.3%) (29.3%) (7 .6%) (2.2%) (2 .2% ) Female 98 80 18 12 5 。 (8 1. 6% ) (18.4%) (1 2.2%) (5 .1%) (1. 0%) LIMB LOSS IN ATERGATIS FLORIDUS 141
Male LChel 1.1 %(且= 1)
LL2 2.2% (n= 2) 見 2 3.3% (n =3)
R lA 5.4% (;旦= 5)
RChel 4.1% (且= 4) Female
LL2 3.1% (且= 3) RL2 0% (旦= 0)
RL3 2.0 %(旦 =2)
UA3.1% (且= 3) RL4 3.1% (且= 3)
Fig. 2. Site 組 d percentage frequency ofloss ofindividuallimbs inAtergα， tis floridus for males (n =92) and females (n =98). LChel indicates left cheliped; LLl，left leg 1etc .N values given on the figure indicate the number of crabs sampled missing the limb. Mean value of limb loss for males is 6.0% and for females 2.6%，that is ，if arandom pattern oflimb loss was shown，alllimbs would approximate the mean value.
stages require approximately 10% of the harbor 田 ld unsaleable items，apa 此仕om total time between molts (Hiatt，1948) ， undersized lobsters ，are normally dis- suggesting that these stages are highly carded on the dockside to die and not re- cηptic. turned to the fishing area (pers. obs.). In- Possible causes oflimb loss，apart 仕om traspecific aggression，either due to com- predation，include damage when dis- petition for mates or territoIγare usually carded from fishing operations and resolved in crabs via ritualized displays through intraspecific aggression. Ater- with injury and limb loss generally not gα tis floridus has been noted to be caught occurring (Jachowski ，1974; SincI air ， in tangle nets used in the spiny lobster 1977; Huber，1987). In certain crab spe- fisheη (Konosuet α1 . ，1969). At Banda al- cies ，however ，with restricted habitat re- though juvenile lobsters occur，adults 訂 e quirements such as obligate symbionts of sc 訂 ce this probably being due to limited specific coral species，intraspecific aggres- habitat availability (Norman et αl. ，1994) sion leading to serious injuries 田 ld limb and subsequently fishing pressure by loss are more common (see Huber，1987). tangle nets is low. Further，catches 合om Limb loss is common in A. floridus and tangle nets are normally sorted in the appears to be more prevalent in males 142 C.P.NORMAN
(4 1. 3%with 1or more limbs missing) than sapidus (Smith & Hines，1991) .For com- females (18.4% with 1or more limbs miss- mercially fished cancrids，Shirley & ing) .The site of limb loss also varied be- Shirley (1988) found 18% of Cα ncer tween males and females，with males mα:gister with limb loss in Alaska，whilst having low cheliped loss. Male chelipeds Durkin et αl. (1984) found for amore have marked progressive allometric southern population ofthe same species a growth post maturity (approximately 30 much higher (62%) 仕equency of limb loss mmCW) and in mature specimens are in [comparative data from this study，30% proportionally larger than the isometri- (mean of male and female sample)]. cally growing chelipeds of females (C. P. Bennett (1973) found for Cα ncer pagurus Norman，unpub l. data). These enlarged apercentage frequency of cheliped loss of chelipeds of males may therefore be more 4.8-13.2%，variation being dependent on difficult to cause to autotomize. However， location (comparative data from this in mature portunids，a higher level of che- study，male 0.5% 出 ld female 3.6%) and a liped loss is recorded than for the walking mean loss of awalking leg of 4.9% for legs，this probably being due to the defen- males and 4.4% for females (this study， sive behavior when attacked of turning males 7.5% and females 2.4%).Th erefore， and facing the predator with raised cheli- A. floridus shows comparable levels of peds (McVean & Findlay，1979; Smith， limb loss frequency to other non-toxic 1990; Norman & Jones，1991). In A. crab species，suggesting that the effec- βoridus defensive behavior appears to be tiveness of locating toxins in appendages more passive，either fleeing or retracting to reduce limb loss may be less e首ective into an oval shape and thereby minimiz- than initially suspected. ing protruding appendages (pers. obs.) ， Of the potential predators of A. hence its common English name of the βoridus clear predatory evidence in the ‘green egg crab'. field was only found for the common octo- Multiple limb loss also regularly oc- pus Octopus vulgαris .This was of abso- curs in A. βoridus. For combined male lute predation，i. e. ，death of the crab. and female data，12 specimens had double Many nests of O. vulgaris were observed limb loss 出 ld in afurther 5specimens ，3 with the carapace remains of A. βoridus or more limbs were missing. Evidence littering the mouth ofthe nest.One speci- from the developmental stages of limb men of O. vulgαris ，with 4A. floridus buds，indicates that the majority of these carapace remains around the entrance of limbs were lost at asimilar time，suggest- its nest，was made to regurgitate its stom- ing that these multiple limb losses may ach contents (by continuous prodding have occurred in asingle attack. There- with asnorke l) and a44.1 mmCW par- fore concentrating to垣ns in limbs to be tially digested (flesh still being attached used an 'w町古血g sign' by gi 吋 ngapreda- to the inner surface ofthe cepthalothorax) 旬Ir ahighly toxic limb (see introduction)， A. βoridus was observed in the disgorged maynot血 all cases deter further attacks material. As O .vulg αris forms amaj or onlimbs. fisherγand is commonly eaten in Jap出 1 Comparative data for crabs oflimb loss (occasionally raw) without 組 y repo此s of in natural populations is sparse. In poisonings，the octopus must be able to po此unids，合equencies of limb loss v訂 y detoxi命 the material in A. βoridus. Due both with crab size，e.g. 12% injuvenile to to the predatory behavior of 0. vulgαns， 38% in large adult Necora puber (N orman wrapping the crab in its arms prior to & Jones，1991) and also spatially and paralyzing its prey，predation tends to re- tempDrally，e.g. differences of 9%to 23% sults in death ofthe crab rather than limb between sites and years in Cα llinectes loss. Of other possible predators which LIMB LOSS IN ATERGATIS FLORIDUS 143 may cause limb loss: fish，crustaceans cies of Japanese toxic crabs Zosimus etc. ，no predatory interactions were ob- aeneus and Platypodia granulo錦町e also served in the field. However，the occur- nocturnal and highly cryptic ，with Z. rence oflimb loss suggests that predatory aeneus showing ahighly developed degree pressure is exerted on A. βoridus. of camouflage (Saisho & Ushio，1969). Saito et al. (1984) found artificially cul- This suggests that unlike some other toxic tured pufferfish (TIαkifugu rubripes) to animal groups，crabs mayutilize toxins as have no natural toxicity，although they an additional defensive mechanism，rely- showed ahigh resistance to interperi- ing on other defense mechanisms，i.e. ， toneal injections and concluded that cryptic behavior，thick carapace，limb pufferfish are toxified exogenously，via loss ，camouflage and short-term rapid the food chain. Most fish and crustacean movements to escape，rather than relying species show minimal or no resistance to solely on being toxic and actively display- Gτ 宝s，S'I宝 s and TTX，however certain ing that they are toxic. As such，the pos- species，particularly those which bio- session of toxins may be seen as an addi- accumulate these toxins have high resis- tional deIEmsive mechanism for crabs but tances (Koyama et αl. ，1983; Saito et al. ， unlike some other animal groups that are 1984，1985; Hwanget al. ，1990). Co-evolu- poisonous，solely the possession of toxins tion may have led to specialist predators may not be su伍 cient to fully protect the on A. βoridus either able to detoxi命 (e.g. crabs 企omspecialist predators. Octopus vulgαris) or bioaccumulate and utilize the toxins. Acknowledgments The accumulation ofthese neurotoxins 1thank T. Yoshimura and M. Mina- in A. βoridus may be purely passive; tox- gawa (Seikai National Fisheries Research ins merely being stored in the body and Institute) for their advice on early drafts not primarily used as adefense mecha- of the paper，Prof. H. Yamakawa (Tokyo nism. Evidence to suggest to the contrary， University of Fisheries) for his supervi- that toxins are actively accumulated and sion and assistance during the sampling used as adefense mechanism include: (1) for this study and the two anonymous ref- the consistent occurrence of toxic mate- erees for their guidance. rial in specimens but often of different principal toxin between geographical area (Shiomietαl. ，1982; Noguchi et αl.，1983a， Literature Cited 1983b)，(2) the ability of A. βoridus to pro- Ary， R. D. ，Bartell ，C. K.， Grisoli ，R. M.，& duce T'I宝 a stronger toxin than the source Poirrier ，M. A. ，1985. Morphological changes in regenerating chelipeds of the material GTXs (Noguchi et αl. ，1986; blue crab Cα llinectes sα:pidus Rathbun as Sugitaet αl .， 1987)，and (3) after bacterial indicators of the progression of the molt PI吋 uction/manipulation in the intestine cycle. Journal of Shellfish Research，5(1): the toxins are then concentrated in the 1-8. muscle of the limbs (Konosu et al. ，1969; Bennett，D. B. ，1973. The effect of limb loss and regeneration on the growth of the ed- Saisho & Ushio，1969; Kotaki et al. ，1985). ible crab ，Cα ncer pα:g urus，L. Journal of From daytime in situ observations of Experimental Marine Biology and Ecology， A. βoridus，however ，its first line of de- 13: 45-53. fense seems to be its cryptic behavior. Davis，R. E. ，& Stuart，A. E. ，1988 .A persis- Atergαtis βoridus also has athick cara- tent，TI'X -sensitive sodium current in an invertebrate neuron with neurosecretory pace，comparable with other sympatric ultrastructure .The Journal of Neuro- but non-toxic xanthids of asimilar size science ，8 (11): 397ι3991. and is capable of relatively rapid，short- Drach，P. ，1939. Mue et cycle d'intermue chez term movements (pers. obs.). Other spe・ les crustaces decapodes. Annales de 144 C.P.NORMAN
l'I nstitute Oceanographique，19: 103-391. Medicine，2(2): 118. Durkin，J. T. ，Buchanan ，K. D .，& Blahm，T. Maruyama，J .，& Noguchi，T. ，1984. Tetrodot・ H .，1984 .Dungeness crab leg loss in the oxin -areview with special reference to Columbia River estuary. Marine Fisheries its distribution in nature. La mer，22 :29 9- Review，46: 22-24. 304. Hall，S. ，1988. PSP and other shellfish 初 xins: McVean，A. R. ，1976 .The incidence of auto- recent outbreaks and research. Journal of tomy in Cα rcinus maenαs(L ふJo旧宮al of Shellfish Research，7(3): 565. Experimental Biology and Ecology，24 : Halstead，B .W. ，1992. Dangerous aquatic ani- 177-187. mals of the world:A color atlas .The Dar- 一一一一 ，1982.Autotomy .In :D .E. Bliss，(ed .)， win Press，Inc .，Pri nceton，New Jersey ，264 The Biology of Crustacea，Volume 4.Aca- pp. demic Press，Inc. ，New York ，107-132 . Hashimoto，Y .，Konosu ，S. ，Yasumoto ，T .， 一一一一 ，& Findlay，1. ，1979. The incidence of Inoue，A. ，& Noguchi，T. ，1967 .Occurrence autotomy in an estuarine population ofthe of toxic crabs in Ryukyu and Amami Is- crab Carcinus maenαs.Journal ofthe Ma- lands.Toxicon ，5: 85-90 . rine Biological Society of the United King- 一一一，一一一， Inoue，A. ，Saisho ，T .，& dom，59 :341-354 . Miyake，S. ，1969 .Screening of toxic crabs Noguchi，T. ，Arakawa ，0. ，Daigo ，K. ，& in the Ryukyu and Amami Islands. Bulle- Hashimoto，K.， 1986.Local differences in tin of the Japanese Society of Scientific toxic composition ofaxanthid crab Fisheries，35(1) :83 -87. Atergαtis floridus inhabiting Ishigaki Is- Hiatt，R. W .，1948. The biology of the lined land，Okinawa .Toxicon ，24(7): 70ι711. shore crab pα，chygrapsus cr， αssipes .Pacific 一一一一， Koyama，K.，Uzu ，A.， & Hashimoto，K. ， Science，2: 135-213. 1983a. Local variations of toxicity and Holthuis，L .B .，1968 .Ar ethere poisonous toxin composition in axanthid crab Ater- crabs? Crustaceana，15(2) :21ι222 . gatis floridus .Bulletin ofthe Japanese So・ Huber，M .E. ，1987 .Aggressive behavior of ciety of Scientific Fisheries，49(12) :1883- Trα:peuαintermediαM i e r s 組 d T.d igitαlis 1886. Latreille (Brach界lra: Xanthidae).Journal 一一一一 ，Uzu，A.， Koy創 na，K. ，Maruyama ，J. ， of Crustacean Biology，7(2) :23ι248 . Nagashima，Y. ，& Hashimoto，K. ，1983b . Hwang，D. F. ，Chueh ，C .H. ，& Jeng，S .S .， Occurrence of tetrodotoxin as the major 1990.Susceptibility offish，crustacean and toxin in axanthid crab Atergα，tis floridus. mollusk句 tetrodotoxin and paralytic shell- Bulletin of the Japanese Society of Scien- fish poison.Bulletin of the Japanese Soci- tific Fisheries，49(12): 1887-1892. ety ofScientific Fisheries，56(2 ): 337-343. Norman，C .P. ，& Jones ，M .B.， 1991. Limb loss Jachowski，R. L .，1974 .Ag onistic behavior of and its effect on handedness and growth in the blue crab，Cα ll inectes sαpidus the velvet swimming crab Necorαpuber Rathbun. Behaviour，50: 232-253. (Brachyura:Portunidae) .Journal ofNatu- Konosu，S. ，Inoue ，A .，Noguchi ，T .，& ral History，25: 639-645. Hashimoto，Y. ，1969 .A further examina- 一一一一 ，&一一一一，1993.Reproduction ecology tion on the toxicity of three species of of the velvet swimming crab，Necora puber xanthid crab. Bulletin of the Japanese So・ (Brachyura:Portunidae) ，at Plymouth. ciety ofScientific Fisheries，35(1): 8ι92. Journal of the Marine Biological Associa- Kotaki，Y .，Oshima ，Y. ，& Yasumoto，T .，1985 . tion ofthe United Kingdom，73: 379-389. Bacterial transformation ofparalytic shell- 一一一， Yamakawa，H. ，& Yoshimura，T .， fish to氾ns in coral reef crabs and amarine 1994.Habitat selection ，growth rate and
snail. Bulletin of the Japanese Society of density of juvenile p α， nulirus jα.p onicus Scientific Fisheries，51(6): 1009-1013. (Von Siebold，1824) (Decapoda，Palinu- Koyama，K.， Noguchi，T .，Uzu ，A. ，& ridae) at Banda，Chiba Prefecture，Japan . H 回 ，himo加， K ，1983 .Re sistibility of toxic Crustaceana，66(3): 366-383. and nontoxic crabs against p町 alytic shell- Saisho，T .，& Ushio，Y. ，1969 .A study on the fish poison and tetrodotoxln.Bulletin of di stribution and ecology of 加xic crabs in the Japanese S∞iety of Scientific Fisher- the Ryukyu and Amami Islands .Memoirs i朗， 49(3): 485-489. of the Faculty of Fisheries，Kagoshima Ll ewellyn ，1. E. ，& Endean ，R.， 199 1. Paralytic University，18: 47-63. (in Japanese with shellfish toxins in the xanthid crab English abstract) Atergatis floridus collected from Austra- Saito，T .，Maruyama ，J. ，Ka noh，S .，Jeon ，J. K. ， lian coral reefs. Journal of Wilderness Noguchi，T. ，Harada ，T. ，Murata ，0. ，& LIMB LOSS IN ATERGATIS FLORIDUS 145
Hashimoto，K.， 1984. Toxicity of the cul- mal Behaviour，25 :19 3-207. tured puffer伍sh Fugu rubripes rubripes Smith，L . D .，1990 .Pattems oflimb loss in the along with their resistibility against tetro ・ blue crab，Callinectes sapidus Rathbun， dotoxin. Bulletin ofthe Japanese Society of and the effects of autotomy on growth. B 叫. Scientific Fisheries，50(9): 1573-1575. (in letin of Marine Science，46(1): 23-36. Japanese with English abstract) 一一一一， & Hines，A. H.，199 1. The effect of che- 一一一一， Noguchi，T. ，Takeuchi ，T. ，Ka mimura， liped loss on blue crabs Cα llinectes sα :pidus S. ，& Hashimoto，K.， 1985. Ic hthyotoxicity Rathbun foraging rate on soft-shell clams ofparalytic shellfish poison. Bulletin ofthe Myαα renαri αL.Joumal of Experimental Japanese Society of Scientific Fisheries， Marine Biology and Ecology，151(2): 245- 51(2):257-260. 256. Sakai，T .，1976. Crabs of Japan and the Adja・ Sugita，H .，Ueda ，R.， No郡lchi ，T .，Ar akawa， cent Se田 . Kodansha，Tokyo [In 3volumes: 0 .，Hashimoto ，K.， & Deguchi，Y. ，1987. (1) English text，xxix +773 pp. (2) Plates Identification of the tetrodoxin-producing volume，16 pp. ，251 pls. (3) Japanese text， bacterium isolated 合omthe xanthid crab 461 pp.J. Atergatis βoridus.Bulletin ofthe Japanese Sekkelsten，G . 1.， 1988.Effect of handicap on Society of Scientific Fisheries，53(9): 1693. mating success in male shore crabs Yasumura，D. ，Oshima ，Y. ，Yasumoto ，T. ， Cα rcinus "ωenas. Oikos，51( 2): 131-134. Alcala，A. C. ，& Alcala，L .C .，1986 .Tetro- Shiomi，K.， Inaoka，H. ，Yamanaka ，H. ，& dotoxin and paralytic shellfish toxins in Kikuchi，T. ，1982. Occurrence of alatge Philippine crabs. Agricultural and Biologi- amount of gonyautoxins in axanthid crab cal Chemistry，50(3): 593-598.
Atergα， tis βoridus 企omChiba. Bulletin of White，A .W .，198 1. Sensitivity of marine the Japanese Society of Scientific Fisher- fishes to toxins from the red-tide di- ies ，48(10): 1407-1410. noflagellate Gonyaulax excavatαa， n d i m p l i - Shirley，S. M.，& Shirley ，T. C. ，1988 .Append- cations for fish kills. Marine Biology，65: age injury in dungeness crabs，Cα ncer 255-260. mαgister，in southeastem Alaska. 日shery Bulletin U.S.，86: 156-160. Seikai National Fisheries Research Insti- Sinclair，M .E .，1977. Agonistic behavior ofthe tute ，49 Kokubu-machi，850 Japan stone crab，Men 伊'[J e mercenαnα(Say). Ani-