CRUSTACEAN RESEARCH，NO. 37: 74-79，200 8

Cheliped differentiation and sex ratio of the fiddler Ucαα rcuαta

Takao Yamaguchi and Yasuhisa Henmi

A bstrαct.--We analyzed atotal of male were dominant among the adults 3，784 young fiddler crabs of Ucαα rcuα- with aCW between 15.1 and 20.5 mm. tα(D e Haan，1833) with carapace Johnson suggested that male bias in U. pugi- width s(CW) between 1. 45 and 9.95 lator could be the result of di旺' e rential mor- mm，collected from asite on the Ohno tality rates between sexes. Frith & River in Central Kyush u ，Japan. All Brunenmeister (1980) examined the sex crabs with CW< 3.0 mmpossessed two ratios and distributions of five small symmetrical ch elipeds. Young species at Phuket Island in Thailand and male crabs with aCW between 3.0 and found two to three times more males than 6.0 mmexhibited one of four stages of females (2.35 in Ucα urvillei (Milne- cheliped differentiation: 1) two small Edwards，1852) (94 males/40 females); 2.2 chelipeds; 2) two large chelipeds; 3) in Uca lactea (De Haan， 1835) (396 only one cheliped; and 4) asymmetrical males/181 females)). They concluded that it chelipeds (on elarge and one small). was necessary to know the sex ratio at the Weidentifie d646 male and 632 female hatching stage to understand sex ratio crabs with aCW between 6.0and 9.95 imbalances. mm. No statistical difference from the It is very important to know the sex ratio 1:1 ratio is evident. We conclude that of the fiddler crabs at the earliest possible the basic sex ratio for U. αrcuαt αi s stage. Without knowing such aratio ，it is unity. impossible to discuss and evaluate the sex ratios of adult crabs. However，in the earliest fiddler crab stages secondary sexual charac- Introduction ， teristics are undeveloped. Young Ucαc r a b s Johnson (2003) researched the sex ratios possess two small symmetrical chelipeds of fiddler crabs and published alist of and are impossible to separate sexually results from 25 studies that demonstrated (Morgan， 1923; Yamaguchi， 1977; male bias in most populations. To deterrnine Yamaguchi & Henmi，2001). Morgan (1923) apossible experimental source for this bias ， found agroup of somewhat larger juveniles Johnson compared the sex ratios for crabs of with two large chelipeds and assumed that Uca ρugilator (Bosc，1802) collected using they were males and that males developed pitfall traps (126 males:95 females) and cheliped asymmetry after losing one of their quadrat excavation (179 males: 144 females) . chelipeds (Morgan，1924). Yamaguchi The sex ratio was clearly male-biased for (1977) examined the cheliped condition of a both methods but it was also found to be sig- large numberof young U. lacteα( D e Haan， ni:fi cantly related to crab size. Females were 1835) and confirmed the existence of four dominant among the juvenile crabs with a types of cheliped combinations: 1) two small carapace width 5and 10 mm， chelipeds; 2) two large chelipeds; 3) one the sex ratio was close to unity for crabs cheliped only (either right or left cheliped with aC 羽T between 10.1 and 15 mm，and being lost); and 4) asymmetrical chelipeds SEX RATIO OF UCA ARCUATA 75

200

150

的 門 N =3 784 戸 ， υE ち 」 t E A AA ω u U 3 5 = z

50

。 2 3 4 567 8 9 10 Carapace width (mm)

亡二二コ with two small chelipeds (n =2 ，130) wi 出 two large chelipeds (n =240) ・園田with only one chelipeds (n =182) 園田園with asymmetrical chelipeds (n =1 ，232)

Fig. 1. Cheliped composition of young crabs of Uca arcuata (De Haan，1833) collected at the Ohno Ri ver，Central Kyushu，Ja pan.

(one large and one small). 官le young crabs crabs over the minimum size at which the with only one cheliped regenerated asmall di 宜erentiation of large cheliped is finished， cheliped in place of the lost one.百le remain- we might find atrue ，unbiased sex ratio. It ing cheliped continued to grow and became seems reasonable that no large sex-baised alarge cheliped，and thus the crabs attained di旺'erence in habitat preference or behavior cheliped asymmetry. Yamaguchi & Henmi existed between the two sexes of young (2001) also confirmed the presence of four crabs. The study of Yamaguchi & Henmi types of cheliped combinations in Uca arcua- (2001) dealt with too small sample size (total ta and showed that young males in the tran- n= 645; n= 87 > 5.6mm C"乃to assess sex sitional stages of cheliped development had ratios ，so we performed this quantitative aCW between 3.0 and 5.6 mm. The males sampling study of young U. arcuata to deter- with aCW > 5.6 mmwere fully di旺erentiat- mine reliable sex ratios . ed，with one small and one large cheliped. It is not possible to determine the sex Materials and Methods ratio of young crabs correctly before the di 壬 ferentiation of cheliped asymmetry in males Collection of young Uca arcuata was car- iscomplete. However，by examining young ried out at the Ohno River in Central 76 T. YAMAGUCHI &Y. HENMI

Kyushu (Otani et αl. ，1997; Yamaguchi & Henmi，2001) from late August to mid Discussion October in 1997，2000 ，and 2004 through 2007. Young crabs were collected by exca- In aprevious paper (Yamaguchi & vating randomly selected burrows. After col- Henmi，2001) ，we examined cheliped d出er- lection ，crabs were put in jars containing 80 entiation in Uca arcuαta but could not ana- %alcoho l. Soon after retuming to the labora- lyze sex ratios because of the small sample tory ，we examined the cheliped condition size for the young crabs collected at two di 壬 and determined the sex from the cheliped ferent sites. In the current study，we exam- characteristics. The C 羽T was measured ined amuch larger number of crabs (n = using astereomicroscope equipped with an 3，784) collected at asingle site. From our ocular micrometer. Although the size di 宜er- quantitative study it became clear that the ence between the large and small chelipeds development of two large chelipeds could was not so prominent as in adult crabs，the occurred before the loss of one cheliped，the two chelipeds were distinguishable from smallest crab that developed two large che- each other: the manus of the large cheliped lipeds had aC 羽T of 3.05 mm，and the small- was well developed and broad ry amaguchi， est crab with only one cheliped had aCW of 2001; Yamaguchi & Henmi，2001). There 3.4 mm. However，not all young males devel- was no di 血culty to separate small males that oped two large chelipeds. Approximately 50 just finished cheliped di 旺erentiation from %of the crabs with only one cheliped kept a the crabs with two small or two large che- small cheliped. They dropped one of che- lipeds. lipeds before developing into two large che- lipeds condition. Otani et al. (1997) studied the population Results s甘ucture and growth of U. αrcuata at Ohno Theresults of the various cheliped condi- River. They conducted monthly collection of tions are presented in Fig. 1. Wecollected a the crabs in 1989 and 1990. Ovigerous total of 3，784 young crabs with aCW females were collected on 18 June 1989 and between 1. 45 and 9.95 mm. Of these，2 ，1 30 10 June 1990.τbey obtained small sex-unde- crabs had two small symmetrical chelipeds termined crabs on 17 August 1989 and 18 and were thus undifferentiated (male or August 1990. Wecollected the young crabs female). Two hundred forty crabs exhibited during the period from late August to mid two large symmetrical chelipeds and 182 October. Weestimate the age of young crabs possessed only one cheliped; these crabs obtained by us did not exceed four were males in atransitional stage of develop- months. They were small compared to the ment. The size of the smallest male with adult crabs and the large chelipeds of the completed di 旺erentiation ，reflected by che- males were not so large. Otani et al. (1997) liped asymmetry，had aCW of 3.4 mm. No reported that the minimum size of the young crabs with two large chelipeds or only ovigerous female was 19 .4 mmCW and the one cheliped had aCW of >6.0 mm. largest male and female had aCW of 36.8 Crabs with aCW between 6.0 and 9.95 mmand 33.6 mm，respectively. It is expect- mmconsisted of 646 males and 632 females ed that no large sexual di旺'erences occur in and sex ratio showed no significant devia- the habitat preference and behavior in the tion from unity (p > 0.05 ，Pearson's chi- crabs with aCW between 6.0 and 9.95 mm. square test). 百1 I s result demonstrated that Wedetermined that the basic sex ratio of U. the basic sex ratio of Uca arcuata is 1:1 and arcuαt αi s 1: 1. Furthermore，one of us no sex bias exists in this species of fiddler (Yamaguchi) examined atotal of 13 ，913 crab. young crabs of Ucαlactea (Yamaguchi， 1977) and also confirmed the four types of SEX RATIO OF UCA ARCUATA 77

cheliped conditions for this species. He narrow fronts; the other four，broad-front showed that all young crabs with aCW く 2.3 species. Beinlich & von Hagen (2006) per- mmhad two small chelipeds. The males formed an extensive study of 出e taxonomy with aCW between 2.3 and 5.3mm exhibit- of fiddler crabs. According to them the ed transitional stages with varying propor- genus Uca comprises about 94 species. They tions of undifferentiated males. The males admitted atotal of eight subgenera and four with aCW of >5 .4 mmwere fully differenti- of them contained the species of narrow- ated，with one small and one large cheliped. front and other four consisted of broad-front Yamaguchi (1977) presented the percent- species. Uca arcuatαi s anarrow-front ages for each of the four types in afigure but species included in Deltuca whereas U. did not repo此 the exact numbers of crabs or lactea is abroad-front species placed in the sex ratio .We now report that for U. Celuca in Crane's taxonomy. Beinlich &von lα ctea with aC 羽T between 5.5 and 6.9 mm， Hagen (2006) assigned U. αrcuata to the there were 795 males and 812 females with subgenus Tubuca and U. lactea to amember no significant statistical deviation from unity of the subgenus Paraleptuca. Uca pugnax is (p > 0.05，Pearson's chi-square test). The anarrow-front species and Crane (1975) and basic sex ratio is also 1:1 in U lactea. also Beinlich & von Hagen (2006) included W olf et al. (1975) examined avery large it in Minuca. Uca CU1仰 uanta is abroad-front number of crabs of Uca ρugnαx(Smith ， species and was placed in Celuca by Crane 1870). They divided crabs into three size (1975). However，Beinlich & von Hagen groups; > 1. 0cm ，0.5- 1. 0cm and く 0.5 cm. (2006) separated the subgenus Celuca into Thesex ratio of the crabs above 1. 0cm was two subgenera，Paraleptuca and Leptuca ， 1. 3:1 (1 ，106 males/852 females) and 1. 07:1 and included U. cumulanta in Leptuca. (2 ，862 males/2，683 females) for crabs with a Therefore，taxonomically separated four CWbetween 0.5 and 1. 0cm. Theratio of the species in the genus Uca are common in crabs below 0.5 cm was not treated. They exhibiting 1:1 ratio ，suggesting that the thought that the basic sex ratio of U pugnax basic sex ratio of fiddler crabs is generally was 1:1 and explained the deviation from the 1:1 and therefore an ancestral character. unity in the sex ratio of the crabs of above The cause of biased sex ratios in adult 1. 0cm might be the result，in part，of di 宜er- crabs was explained variously. Johnson ential predation. They suggested that the (2003) admitted that in many species and large cheliped of the male might hinder，or populations，the percentage of males signifi- delay capture. Ahmed (1976) examined a cantly exceeds that of females and it reveals total of 640 young crabs of Uca cumulanta that sex ratio is strongly influenced by (Crane，1943) with aCW く 5.0 mmand species，year ，habitat use and location. reported that many crabs，especially those Montague (1980) discussed the sex of fid ・ withaCWく 2.0 mm，exhibited no secondary dler crabs based upon the studies of other sexual characteristics and it was therefore works and suggested that the predominance impossible to determine sex. He did not of males is an artifact of sample collection. report on young crabs that had lost ache- Ahmed (1976) examined size compositions liped. 百le di宜erence between the sexes (159 of 1，552 Uca rapax (Smith，1870) and 657ι males/150 females) in the young crabs was cumulanta with aCW above 5.0 mm，and not statistically significant and he concluded reported that crabs of the largest size class- that U cumulanta have a1:1 sex ratio at the es were almost exclusively males. The sex time of initial sexual di 宜erentiation. ratios were 1. 54 in ι rapax (941 males/611 Thetwo species，U arcuata and U lactea females) and 1. 16 in U. cumulanta (353 are included in separate subgenera. Crane males/304 females). He explained that the (1975) split the genus Uca into nine subgen- females of the two species had avoided cap- era. Five of these contained the species with ture by burrowing deeper than males and 78 T. YAMAGUCHI &Y. HENMI were represented in lesser number.Otani et pared these sex ratios with those obtained al. (1997) collected 654 males and 482 by other researchers，he did not discuss pos- females of U. αrcuata and obtained amale- sible causes of the strong male bias. Macia biased sex ratio of 1. 36. They rationalized et al .(2001) examined the effects of lunar this deviation from unity as apossible sam- and hourI yvariations on sex ratios in U . pling artifact because the males of U. αrcuα- annuliPes and found that the ratio was 的 possess alarge red claw that make them always biased toward males，with changes in easier to recognize than females during col- female activity affecting the ratio. More lection. However，it was concluded that the females were active during the first and new main causefor the deviation was different moons and the ratios were closer to 1:1 dur- mortality rates between the two sexes. ing these periods.τbis represented asignifi- Genoni (1985) reported that the sex ratio of cant behavioral difference between the U. rapax was 1. 46 (242 males/166 females) sexes. Spivak et αl. (1991) examined the and suggested differential mortality as apos- population structure of Uca uruguayensis sible cause. Valiela et al. (1974) reported Nobili ，1901 and reported that the average that females occupied 42.9 %of 713 speci- percentage of males was 65.1 % (total n= mens of U. ρugnax，and also suggested that 1，310) and the sex ratio increased with size ， greater moはality of smaller females was the from 50 to approximately 90 %.τbey did not cause. discuss the cause of biased sex ratio of the Crane (1975) reported that various kinds speCles. of birds attack fiddler crabs. Bildstein et α l. deRi vera (2003) reported that males of (1989) examined the response of whiteibis ， Uca crenulata (1βc k i n g t o n ，1877) outnum- Eudocimus albus，to U. ρugilator and report- bered females and that males built their bur- ed that the bird chose females or declawed rows higher up on the beach than females males four times as often as intact males. did. At the upper central part of the field ， However，Johnson (2003) thought that pre- there were 684 males and 203 females (46 dation was not an important determinant of quadrats，a sex ratio of 3.37: 1. 00). Over the fiddler crab sex ratios. Thesizes of fiddler entire area，there were 827 males and 521 crab populations are enormous relative to females (83 quadrats，a sex ratio of 1. 59: those of most predators. Johnson argued 1. 00). She suggested that ahigher levels of that the degree to which predation limited predation on females might be acause of the fiddler crab abundance remained an open biased sex ratio ，and explained that amale question.Koga et al. (2001) reported that bias in the adult sex ratio could contribute to the great-tailed grackle Quiscalus mexicanus， polygyny because an abundance of males was acommon and persistent predator of would set the stage for more breeding males Uca beebei (Crane，1941) (Koga et al. ，2001). than breeding females and，consequently ， However，the sex ratio of this species was increased competition among males for mat- noted to be 1:1 (Koga et al. ，1998) . mg. Emmerson (1994) studied the sex ratios Webelieve that detailed studies are of eight species of crabs，including four Uca needed to analyze the process how males species in southern Africa: Uca annulipes outnumber females，and also to know the (Milne- Edwards，1837) ，Uca urvillei (Milne- meaning of the predominance of males in Edwards，1852) ，Uca hesperiae (Crane， the adult crabs，in various species of the 1975) ，and Uca chloroPhthalmus (Milne- genus Uca. Edwards，1837) ，with average sex ratios of 4.51 (2 ，060 males/457 females) ，2.96 (1 ，061 Acknowledgements males/358 females) ，1. 94 (659 males/340 Wewish to express our sincere thanks to females) ，and 1. 87 (2 ，621 males/1，401 two anonymous reviewers for very valuable females) ，respectively. Although he com- suggestions and correction of the manu- SEX RATIO OF UCA ARCUATA 79 scrip t. mating population density of 出e fiddler crab Uca annulipes at Saco ，lnhaca Island (Mozambique). Hydrobiologia，449: Literature Cited 213-219. Montague C. 1980. A natural history of temper- Ahmed，M. ，1976. Astudy of the norrnal and aber- ， ， rant sexual types of the Venezuelan fiddler ate western Atlantic fiddler crabs (g enus Uca) crabs Uca cumulanta and U rapax. Bulletin of with reference to their impact on the salt marsh. Contributions in Marine Science 23: Marine Science，26: 499-505. ， 2 55. Beinlich ，B. ，& von Hagen，H. 0. ，2006. Materials 5-- for amore stable subdivision of the genus Morgan，T. H. ，1923. Thedevelopment of asym- metry in the fiddler crab. American Uca L后ach. Zoologische Mededelingen，80: 57: 269-273. 9-32. Naturalist， 1924. le artificial induction of symmetri- Bildstein ，K L.， McDowell. S. G. ，& Brisbin，1. L.， 一一一一， 百 1989. Consequences of sexual dimorphism in cal claws in male fiddler crabs. American Naturalist 58: 289-295. sand fiddler crab ，Uca ρugilato r. differential ， vulnerability to avian predation. Otani，T. ，Yamaguchi ，T.， & Takahashi，T.， 1997. Population structure growth and reproduc- Behaviour，37: 133-139. ， tion of the fiddler crab ，Uca arcuata (De Crane，].， 1975. Fiddler crabs of the world， Haan). Research，26: 109-124. : genus Uca. xxiii + 736 pp. ， Spivak D. Gavio M. & Navarro C. E. Princeton University Press，Princeton. ，E. ， ， A.， ， ， 1991. Life history and structure of the world's deRi viera ，C. E. ，2003. 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D. ， Christy，]. H. ， & Kumamoto 862-0924 Japan;σH) tsu Marine 1998. Elevated predation risk changes mating ， Ai Station Center for Marine Environmental behaviour and courtship in afiddler crab. ， Studies，Kumamoto University，Matsushima ， Proceeding of the Royal Society，Lo ndon，B ， Kami-Amakusa 861-6102，Japan. 265: 1385-- 1390. E-mails:(TY) [email protected]卯; Macia Quincardete & Paula 200 A ，A.， ， 1.， ， ].， 1. σH ) [email protected] comparison of alternative methods for esti-