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Reproductive Biology ofThree Land Hennit Crabs (~ecapoda: Anomura: Coenobitidae) in Okinawa, Japan!
Yukio Nakasone 2
Abstract: Reproductive ecological research on three land hermit crabs, Coeno bita rngosus, C. purpureus, and C. cavipes, was conducted in the southern part of Okinawa-jima island in 1985, 1986, 1987, and for a short period in 1999. Size (carapace length) of the smallest ovigerous female was 3.93 mm for C. rngosus, 3.83 mm for C. purpureus, and 9.49 mm for C. cavipes. Breeding season is late May to November for C. rngosus, late May to mid-September for C. purpureus, and mid-May to late August for C. cavipes. Some females of all three species probably produced at least two broods during the breeding season. The smallest males in which spermatophores were present in dissected vas deferens were 4.24 mm for C. rngosus and 4.94 mm for C. purpureus. Coenobita cavipes females produced more, smaller eggs in comparison with C. purpureus. My observations suggest that coenobitid crabs living in areas with a low supply of shells or with poor shells reproduce at smaller sizes, as is the case in marine hermit crabs. Time of onset oflarval release by C. rngosus, with its protracted breeding season, varied according to the seasonal shift in time ofsunset. The period during which females of C. rngosus released larvae was about 2 hr in spring tides but was much longer (3 to 5 hr) during neap tides. Larger females of C. purpureus occupied shells derived from the land snail Achatina fulica; smaller ones used shells from the marine snail Lunella granulata. Use of mutually exclusive larval release sites by the larger and smaller females of C. purpureus remained unchanged over 13 yr, from 1986 to 1999. This behavioral difference may be related to the dif ferences in their habitats (i.e., inland versus shore) and to the route traveled by the larger crabs in reaching the sea from inland sites.
SIX COENOBITID CRAB species, Coenobita vio gaki-jima Island and Iriomote-jima Island lascens Heller, C. brevimanus Dana, C. perlatus (Nakasone 1988a). Three species are widely H. Milne Edwards, C. cavipes Stimpson, C. distributed on the islands of Okinawa Pre purpureus Stimpson, and C. rngosus H. Milne fecture, namely the small species Coenobita Edwards, have been reported from the Ryu rngosus and the larger species, C. purpureus kyu Islands, Japan. Of these, C. violascens, and C. cavipes. Coenobita rngosus usually in C. brevimanus, and C. perlatus are restricted habits the shore, whereas C. purpureus and to the southern Ryukyus, including Ishi- C. cavipes both live from the shore to 600 m or more inland. Small individuals of C. purpureus are commonly found at the shore, but the 1 This research was supported by the Agency for larger ones are less common there. Both C. Culture Affairs, Ministry of Education, Science, Sports, rngosus and small C. purpureus occur sympa and Culture of Japan. Manuscript accepted 28 August trically on most islands of the Ryukyus, but 2000. 2 Biological Laboratory, Faculty of Education, Uni little work has been done on their ecology versity of the Ryukyus, 1 Senbaru, Nishihara-cho, because of the confusion of their taxonomy. Okinawa 903-0213, Japan (E-mail: [email protected] It is well known that land hermit crab fe kyu.ac.jp). males migrate to the shore to release their larvae in the sea, but ecological information Pacific Science (2001), vol. 55, no. 2:157-169 on their reproduction is scanty or fragmen © 2001 by University of Hawai'i Press. tary for the coenobitid species (Yamaguchi All rights reserved 1938, Degener and Gillaspy 1955, Vogel and
157 158 PACIFIC SCIENCE· April 2001
Kent 1971, Ball 1972, De Wilde 1973, Page tiliaceus L., Ipomoea pes-caprae (L.) Br. subsp. and Willason 1982, Wolcott 1988, Brodie brasiliensis (L.) Ooststr., Scaevola taccada 1999). (Gaertn.) Roxb., Argusia argentea (L. fil) G. In Japan, coenobitid crabs have been used Murata, and Pandanus odoratissimus L. fil, al as pets for children, having been introduced though the composition of the vegetation to the mainland from the Bonin Islands. Be differed at individual sites. Because larger cause of their endangerment in the Bonin crabs were rarely caught in the pitfall traps, Islands, all coenobitid crabs in Japan were additional random sampling in the study area recognized as a natural monument on 12 was done by hand. The specimens of C. November 1970, to promote their conserva cavipes examined for breeding season studies tion. This study was carried out to obtain were provided by a pet trader who had per ecological data for conservation under the mission from the Agency for Culture Affairs permission of the Agency for Culture Affairs, to collect land hermit crabs. Ministry of Education, Science, Sports, and The sample specimens were all frozen for Culture ofJapan. later examination. After thawing, the species Extensive observations on the reproductive of shells inhabited by the crabs were deter behavioral ecology of C. cavipes, C. purpureus, mined. The crabs were then removed by and C. rugosus have been made in the south hand or forceps from their shells (the shell ern part of Okinawa during the course of was cracked with a hammer if necessary), and ecological and distributional st:p.dies of land the species and sex of the crabs were deter hermit crabs in Okinawa Prefecture. The mined. Intact shells were returned to suitable purpose of this paper is to clarify the follow habitat for potential reuse by other crabs. ing aspects of these three species: (1) popula Carapace length (anterior calcified part) was tion structure and breeding season; (2) measured to the nearest 0.01 mm with ver changes in time at onset of larval release and nier calipers. All females and some males seasonal changes in the number of larval re caught in 1987 were dissected to determine lease females (i.e., females with eggs ready to the presence of mature ooeytes and sperma be released); (3) body size at sexual maturity; tophores, respectively. and (4) egg size. It was difficult to identify the species or sex of some crabs less than 2.50 mm in length, but for most specimens it was possible to de MATERIALS AND METHODS termine species and sex by means of the exis Monthly samples were taken on the shore of tence of a black band or stripe on the lower Hyakuna and Shimoda, located on the east surfaces of the eyestalks (see Nakasone side ofTamagusuku village; the southern part 1988a) and gonopores on the coxae of the of Okinawa-jima island; and on the shore third pereiopods. The smaller individuals of of Kudaka-jima island about 5.3 km distant C. purpureus lacked a black band, but those from the coast of Azama, Chinen Cape. The of C. rugosus generally had the black band. monthly samples were acquired during the Adults of both species are easy to distinguish periods December 1985 to November 1986 by color differences. and April to November 1987, using two pit Egg sizes were determined based on ocular fall traps (21 by 13.5 by 14 cm) buried to the micrometer measurements of 10 non-eyed same level as the substratum. Chicken feed and 10 eyed eggs from individual pleopods of (ca. 80 g) was put in each trap to attract the each sampled female. The sample for non hermit crabs. The traps were set by 1800 eyed eggs consisted of pleopods from five in hours at the same site every month, and the dividuals of C. rugosus (body length 5.81 crabs trapped were gathered not later than 8.65 mm), seven of C. purpureus (body length 0830 hours the next day. These traps were set 8.08-18.25 mm), and three of C. cavipes twice a month, in the first part and the latter (body length 11.37-15.29 mm). Sizes of eyed part of each month. They were placed in eggs were determined from six individuals vegetation communities that included Hibiscus of C. rugosus (body length 6.82-12.58 mm), Reproductive Biology of Three Land Hermit Crabs . Nakasone 159
six of C. purpureus (body length 10.83 May to October at Kudaka-jima and from 17.03 nun), and four of C. cavipes (body June to October at Hyakuna. The minimum length 12.87-17.23 nun). The t-test and size of ovigerous C. rugosus females was Welch's test (t') were used to analyze the data 4.77 nun at Hyakuna and 4.96 nun at Shi for differences in egg size (length) between moda in 1986, and 5.32 nun at Hyakuna in species. 1987. The maximum size was 8.75 nun at For the study of reproductive behavior, Hyakuna and 9.20 nun at Shimoda in 1986, two sites on the Hyakuna coast at which lar and 12.81 nun at Hyakuna in 1987. In the val release females (females with eggs ready to Kudaka-jima population of C. rugosus both be released) were frequently seen were se sexes ranged mostly from 3 to 7 nun (for lected as study sites A and B. Observations females see Figure 1). Ovigerous females were carried out at these sites to determine were found from early June, although they the time of larval release and the variation in may appear from late Mayas in the 1987 Hya number of larval release females of each spe kuna population samples. Ovigerous females cies. Females returning from the shore after ranged in size from 3.93 to 12.58 mm. releasing their larvae were collected every 5 Because of the small sample size of C. min at these sites. The species and numbers purpureus from Hyakuna, those crabs were of females collected were recorded before not included in the analysis of population release of the specimens. This procedure was structure. In the Shimoda population most repeated from sunset until larval release fe individuals of both sexes ranged from 3 to males became scarce. The sites were about 7 nun. Crabs less than 5 nun appeared mostly 52 m apart, located about midway between from April to October. Ovigerous females the Shimoda and Hyakuna sampling areas. were 6.21-18.26 nun in length in the Hya The survey at sites A and B was conducted by kuna population and 6.20-15.95 nun long in two or three persons with electric flashlights the Shimoda population. The Kudaka-jima during the spring tide, semimonthly from population of C. purpureus consisted mostly of early June through early December 1987. males 4-6 nun long and females 3.5-7.0 nun Additional work at sites A and B was done for long (Figure 2); ovigerous females were 3.83 a short period during the breeding season in 17.29 nun long. Crabs less than 5 nun were 1999 to extend the observations of differential found mostly from April to October. use of sites A and B by large and small fe Based on specimens of C. cavipes collected males of C. purpureus females. in 1986 and 1987 from Hyakuna, ovigerous females range from 9.49 to 19.14 nun in length. Sample sizes for this species were in RESULTS sufficient to warrant further analysis of the Population Size Structure data.
Ceonobita rugosus was much more abundant Breeding Season than C. purpureus at Hyakuna, but both spe cies were abundant at Shimoda and Kuda Ovigerous individuals of C. rugosus were ka-jima. The size-frequency distributions of found from 9 June to 27 November 1986, but females of C. rugosus and C. purpureus from were also observed from 27 May in the 1987 the Kudaka-jima populations are presented in samples. Therefore, the breeding season Figures 1 and 2, respectively. The decline in ranges from at least late May to late Novem number of individuals trapped during winter ber (Figure 3), but may vary from year to was due to the inactivity of the crabs. Both year. Most C. rugosus females were ovigerous sexes of C. rugosus of6-8 nun carapace length from July to August. Of 45 nonovigerous fe were found in large numbers throughout the males captured on 19 May 1987, 15 (33.3 %) year in the Shimoda and the Hyakuna pop had mature ooeytes. Ovigerous females ulations. Individuals of both sexes less than (10.8%, 9 of 83) were first found in the sam 5 nun in length were most frequent from ples on 27 May, of which five had eyed eggs. 160 PACIFIC SCIENCE· April 2001
100r.___.J....J_l r:;: C~ 3 4 r=-J"] 0 1 Jann N-5
01 0 Feb N=1 0 1 [L, r,~r ~1-10 10~ ~71 O~OO 40
30 May N=121 Aug ~ 10 N=254 o 20
10
0'--'=--'- ::f sLS:P=S3
30 July N=229 20 ::1 AnO~~79 10
~t n 0 Nov N=17 Ot-=--- )), 1 5 10 13 1 5 10 13 Carapace Length (mm)
FIGURE 1. Size-frequency distribution of C. rugosus females sampled from December 1985 to November 1986 on Kudaka-jima Island; data for ovigerous females in black.
Of 65 females collected randomly at site B on found from 9 June to 16 September 1986 and 14 June, three had just released their larvae, from 27 May 1987 in the Shimoda popula as suggested by the presence of membranes tion, and from 25 May 1986 in the Kudaka from hatched zoeae still attached to the well jima population. Thus, the breeding season developed pleopodal hairs. ranges from late May to mid-September Ovigerous females of C. purpureus were (Figure 3). Although ovigerous females were Reproductive Biology ofThree Land Hermit Crabs . Nakasone 161
~ [ __.c:~~.=~M.LJLJ~c:L-J::~===2::L5.c:C',---__.r=C', j-J::~~ __.__A_p_r--==-:L=_1_0_2__-:..._
40
30 May N=226 rn ~ 20 aO':l ~ 10 40 "I-
10 10 July25 N=59 Jun14
N=2 10 N=58
20 N=104 20 Jun 25 Aug10 N=66
20
N=170 N=200 ...... 040 40
N=20 July11 60 or------c=~_rr~r_rf"l-l"'I-n~_rr_l"'l__ Aug24 • N=4 o1-----.-..~U~~'"T"1~",..----
20 N=139 N=59
20r- _.l-I__...L..__.l.1__--l..__...lI__-.l... _ ....' __--'-__.....1__--'-__....1__--'- 19 20 21 19 20 21 Time of Day
FIGURE 4. Variation in the number of larval release females with time of day and month ofyear at study site A during spring tides in 1987. Closed bars, C. purpureus; open bars, C. cavipes.
Body Size at Sexual Maturity and Number of C. purpureus bearing eggs were 4.77 and Broods 6.21 mm long, respectively, in the samples from Hyakuna, 4.96 and 6.20 mm from Shi Mature females were determined by the moda, and 3.93 and 3.83 mm from Kudaka presence of embryos deposited on pleopods. jima. Thus, the smallest ovigerous females of The smallest individuals of C. rugosus and both species on Kudaka-jima were smaller .I 20 Jun14 N=508
30 oI--_...... L.&...... L-- Aug10
60 10
40
20 N=124 20 Jun 26 N=238 Vl 11) 10 ('(l Aug25 N=26 E & 0 1---~H"\-MH"t-,o,-l!!~f'rl.,...-&-i'.,...- O~------l"r-,'lrf'H'rTTf"l-ft'1P't-n~T'TT---
11) Vl N=73 ('(l ~ 20 20 11) 0::: ~ 10 JUly11 N=64 N=402 c: 40 j 0 r--1"H'\-~~~~5-&,:r--
N=66 ... 60 11) 20 90 .D E ::l Z 1:[ N =31 60 o1----rTT""rTT1"TTTTTT"T'TTTTT1nT"-----
July 25 40 20 Sept25 N =297
N=284 20 40
o~ UOO~OO N=80 N=52 10 Oct25 10 19 20 21 22 18 19 20 21 22 Time of Day
FIGURE 5. Variation in the number of larval release females with time of day and month ofyear at study site B during spring tides in 1987. Closed bars, C. purpureus; open bars, C. rugosus. Reproductive Biology of Three Land Hermit Crabs . Nakasone 165
110 winter the vas deferens contained spermato phores arranged in a band. In C. rugosus, the smallest male that had spermatophores was 90 18
~--: 4.24 mm long; in C. purpureus the smallest '" ] N=242 N=77 mature male was 4.94 mm. "0 f-" :~ 70 :_.J 14 ~ Dissected females of all three species of "0 "-, .s "0"' crabs studied often had both brooded em .... 'S:" o :0 bryos and mature ooeytes. The percentages ~ 50 10 ~ .D .... of females with both embryos and ooeytes 8 0 ~ varied throughout the reproductive season, Z" .D" 30 6 8 but reached 15.8% in late June in C. purpur Z" eus, 28.6% in early June in C. cavipes, and B " A 83.3% in late July in C. rugosus. Furthermore, 10 Co, 2 of the crabs collected randomly after releas o4--....l....+----,---'---,,....J0 ing larvae at sites A and B, the frequency of 5 10 15 20 Carapace Length (mm) females with mature ooeytes reached at least 80% at some time during the reproductive FIGURE 6. Size-frequency distribution of larval release period of each species. Mature ooeytes were females of C. purpureus at study sites A (broken lines, found from early June to early October in C. right y-axis) and B (solid lines, left y-axis). rugosus, late June to late July in C. purpureus, and earlyJune to late June in C. cavipes. These observations suggest that some females of all than those at both Hyakuna and Shimoda. three species produce more than one brood The smallest female C. cavipes releasing larvae during the breeding season. at site A was 9.49 mm. Mature males were determined by the presence of spermatophores in dissected vas Egg Size deferens. The vas deferens was thick and The mean egg sizes on the first pleopod in large for the period from spring to autumn, each species are presented in Table 1. Data but was thin and small in winter. However, in for the other pleopods are not presented be cause preliminary analysis and testing failed to reveal significant variation in egg size among pieopods of the same species. There 70 were significant differences between species ,,l--~ in the mean length of non-eyed eggs (C. CIl 60 L, <;l rugosus versus C. purpureus: t' = 76.395, ;::l I, ~ 50 df = 13, P < 0.001; C. rugosus versus C. cav > N=150 I : N=243 , I ipes: t' = 8.721, df = 14, P < 0.001; C. pur :.e ,I L_, .E 40 , , pureus versus C. cavipes: t' = 7.539, df = 10, ...... I , P < 0.001), but there were no significant dif 0 r _J , .... 30 , , ferences between species in the mean length 0 I ,I I I of eyed eggs (c. rugosus versus C. purpureus: 8 20 _J L _, ;::l I t' = 2.051, df = 11, P > 0.05; C. rugosus ver I Z 10 B A I sus C. cavipes: t = 0.411, df = 18, P> 0.05; ,. I , I C. purpureus versus C. cavipes: t' = 1.732, L_ ... 0 df = 12, P > 0.05). Thus, when non-eyed 5 10 15 20 eggs became eyed eggs they attained nearly Carapace Length (mm) the same size in all three species. There were no significant differences between non-eyed FIGURE 7. Size-frequency distribution of larval release females of C. cavipes at study site A (broken lines) and of and eyed eggs in mean length in C. purpureus C. rugosus at site B (solid lines). (t = 1.444, df = 18, P > 0.05), whereas there 166 PACIFIC SCIENCE· April 2001
r.n A 12~J1-~LJ1-:'-1c;n (l) N ,= ...... 1:t 29 I:'tI S (l) 30 ~
(l) r.n 20 B N=282 Jun 29 I:'tI ...... (l) (l) 0::; 1 0 ...... I:'tI 0 >l-l I:'tI 40 .....:l
~ 0 30 B N=419 Aug14 l-l (l) .0 20 S Z=10
0 19 20 21 22 23 24 1 Time of Day
FIGURE 8. Variation in the number oflarval release females ofcoenobitid crabs at study sites A and B during neap tides in 1986. Top, data for C. cavipes and C. purpureus at site A, pooled for 29 June; middle, data for C. purpureus and C. rugosus at site B, pooled for 29 June; bottom, data for C. purpureus and C. rugosus at site B, pooled for 14 August. were significant differences between non may be found into mid-September. By com eyed and eyed eggs in mean length in C. parison, the breeding season of C. rugosus is rugosus (t = 3.881, df = 18, P < 0.002) and somewhat longer, extending from late May to C. cavipes (t' = 12.324, df = 12, P < 0.001). November. The difference between length and width was Females of all three crab species in this larger in eyed eggs than in non-eyed eggs. study released their larvae directly into the Thus, the eggs tended to become longer and seawater. However, according to De Wilde more slender in shape as their development (1973), females of C. clypeatus do not enter the progressed. water; they drop or fling their eggs onto the wet rocks and the larvae are washed into the sea during high tide. Brodie (1999) DISCUSSION showed that females of C. compressus release Considering both the chronology of larval hatching larvae into the swash zone and the release and the occurrence of ovigerous zoeal larvae are washed by the receding tide females, it appears that the basic breeding from the swash zone. Thus, it appears that season is similar for C. purpureus and C. the larval release behavior of C. clypeatus and cavipes (i.e., from late May to late August), C. compressus differs from that of the three although ovigerous females of C. purpureus species included in my study, but these dif- Reproductive Biology of Three Land Hermit Crabs . Nakasone 167
tina futica. Thus, it seems likely that they traveled from inland to site A to release their larvae. The use of different larval release sites by larger and smaller females of C. purpureus remained unchanged over 13 yr from 1986 to 1999; this may be related to the differences of inland and shore habitats, and to the route traveled by larger crabs from inland. It was found that onset of larval release by C. rugosus, a species with a long breeding season, varied according to time of sunset (Figure 5). The period during which larval release females were observed was about 2 hr in spring tides, but was much longer (3 to 5 hr) during neap tides (Figure 8). Thus, it appears that the period of time during which larval release females are observed is related to tide level. As described earlier, the smallest ovigerous females of C. rugosus and C. purpureus on Kudaka-jima (3.93 and 3.83 mm, respec tively) were smaller than those at Hyakuna (4.77 and 6.21 mm) and Shimoda (4.96 and 6.20 mm). Hermit crabs on Kudaka-jima were FIGURE 9. Seasonal variation in the number of larval often found occupying old shells with broken release females ofcoenobitid crabs at study sites A and B. apertures, high degrees of abrasion, and with For study site A: solid line, C. purpureus; broken line, C. cavipes; for study site B: solid line, C. purpureus; broken one or more holes, and some crabs also oc line, C. rugosus. cupied plastic bottle caps instead of shells (Nakasone 1987). Thus, the hermit crabs on Kudaka-jima were inhabiting poor shells or ferences in behavior may be related to topo substitutes for shells. My observations suggest graphical differences at the larval release sites. that coenobitid crabs living in areas with a Sites A and B of this study agree with the low supply of shells or with shells of poor general observation that larval release sites quality reproduce at smaller sizes, as is the are protected by rocks and/or reefs from wave case in marine hermit crabs (Markham 1968, action (Yamaguchi 1938). Fotheringham 1976a,b, Bertness 1981a,b). All large females of both C. cavipes and C. The smallest ovigerous females collected purpureus observed at study site A occupied in this study were 3.93 mm long for C. rugo shells derived from the terrestrial snail Acha- sus and 3.83 mm for C. purpureus from
TABLE 1 Comparison of Non-Eyed and Eyed Egg Sizes (Mean ± SD in mm) on the First Pleopod among Three Species of Coenobita
Size of Non-eyed Eggs Size of Eyed Eggs
Species Length Width Length Width
C. rugosus 0.658 ± 0.045 0.616 ± 0.041 0.736 ± 0.040 0.641 ± 0.040 C. purpureus 0.747 ± 0.092 0.715 ± 0.098 0.816 ± 0.110 0.699 ± 0.121 C. cavipes 0.508 ± 0.025 0.473 ± 0.028 0.745 ± 0.052 0.659 ± 0.043 168 PACIFIC SCIENCE· April 2001
Kudaka-jima, compared with 3.98 mm for C. bination of small egg size and large numbers rugosus and 3.05 mm for C. purpureus from of eggs). Yaeyama (Shimamura 1987). The smallest C. As mentioned in the Results, the large cavipes ovigerous female collected at site A females of both C. cavipes and C. purpureus was 9.49 mm, but Shimamura (1987) found that released their larvae at site A occupied ovigerous females of this species as small as the shells of the giant land snail Achatina fut 8.84 mm in samples from Yaeyama. It seems ica. The shells of this land snail are light and likely that most C. rugosus and C. purpureus large, very suitable for large crabs inhabiting females do not reach sexual maturity until inland sites. It is known that the growth and they are more than 4 mm in length. Some egg production of marine and especially land females of both C. rugosus and C. purpureus hermit crabs are affected by the weight of the may lay eggs during their second year of shell occupied (Bertness 1981b, Osorno et al. life, judging from the size-frequency distri 1998). The large but light shells of A. futica butions (Figures 1, 2) and sizes of glaucothoes have a high internal volume/weight ratio (see (Nakasone 1988b). This conclusion was also Osorno et aI. 1998). By occupying these light reached by Shimamura (1987). Similarly, De shells, large females of both C. purpureus and Wilde (1973) reported that C. clypeatus ma C. cavipes may reduce the energetic cost of tures in the second year oflife. Because ofthe carrying a shell (Herreid and Full 1986), and small sample size, it was uncertain whether its large size provides sufficient space for females of C. cavipes reach sexual maturity at larger clutch sizes. According to the Energy sizes less than 8.84 mm. The results of ob Savings Hypothesis proposed by Osorno et aI. servations on spermatophores show that C. (1998), the large females of C. cavipes and C. rugosus and C. purpureus males may not reach purpureus may be able to compensate for the sexual maturity until they attain sizes over energy expended during locomotion from in 4.30 and 5.00 mm, respectively. land sites to the seashore by utilizing large The percentage of females with both but lightweight shells such as those provided brooded embryos and mature ooeytes was by A. futica. 83.3% in late July for C. rugosus, about 80% in July for C. purpureus, and 85.7% in late June for C. cavipes. These observations indi ACKNOWLEDGMENTS cate that some females of these three species I thank M. Tohyama, M. Zaitsu, E. Matsu may produce at least two broods during the moto, N. Miyazato, T. Taira, T. Kohno, and breeding season. Moreover, some females of M. Shimoda for assistance in the field and T. C. rugosus, a species with a protracted breed Kohatsu for C. cavipes samples. Thanks also to ing season, may even produce a third brood, Peter K. L. Ng, National University of Sin as is also the case with C. clypeatus (De Wilde gapore, for his helpful comments on an early 1973). draft. I am also grateful to anonymous re Non-eyed eggs of C. cavipes were the viewers for valuable comments and help with smallest among the three species. The eyed English grammar. eggs in C. rugosus were not significantly dif ferent in size from those of C. cavipes. How C. ever, the larval size at hatch in rugosus was Literature Cited significantly larger than that in C. cavipes (Nakasone 1987). This suggests that egg size Ball, E. E. 1972. Observations on the biology may increase more rapidly in C. rugosus than of the hermit crab, Coenobita compressus H. in C. cavipes just before hatching. Coenobita Milne Edwards (Decapoda; Anomura) on cavipes produced more, smaller eggs com the west coast of the Americas. Rev. BioI. pared with C. purpureus, and the size of larvae Trop.20:265-273. at hatch was the smallest among the three Bertness, M. D. 1981a. Pattern and plasticity species studied (Nakasone 1987, 1988b), a in tropical hermit crab growth and repro common reproductive strategy (i.e., the com- duction. Am. Nat. 117:754-773. Reproductive Biology of Three Land Hermit Crabs Nakasone 169
---. 1981b. The influence ofshell-type on ---. 1988a. Land hermit crabs from the hermit crab growth rate and clutch size Ryukyus, Japan, with a new species from (Decapoda, Anomura). Crustaceana (Lei the Philippines (Crustacea, Decapoda, den) 40:197-205. Coenobitidae). Zool. Sci. (Tokyo) 5:165 Brodie, R. J. 1999. Ontogeny of shell-related 178. behaviors and transition to land in the ---. 1988b. Larval stages of Coenobita terrestrial hermit crab Coenobita compressus purpureus Stimpson and C. cavipes Stimp H. Milne Edwards. J. Exp. Mar. BioI. EcoI. son reared in the laboratory and survival 241:67-80. rates and growth factors of three land Degener, 0., and E. Gillaspy. 1955. Canton hermit crab larvae (Crustacea: Anomura). Island, South Pacific. Atoll Res. Bull. 41: l ZooI. Sci. (Tokyo) 5:1105-1120. SI. Osorno, J. L., L. Fernandez-Casillas, and C. De Wilde, P. A. W. J. 1973. On the ecology Rodriguez-Juarez. 1998. Are hermit crabs of Coenobita clypeatus in Curacao with ref looking for light and large shells?: Evi erence to reproduction, water economy dence from natural and field induced shell and osmoregulation in terrestrial hermit exchanges. J. Exp. Mar. BioI. Ecol. 222: crabs. Stud. Fauna Curacao Other Car 163-173. ribb. lsI. 44:1-138. Page, H. M., and S. W. Willason. 1982. Dis Fotheringham, N. 1976a. Effects of shell tribution patterns of terrestrial hermit stress on the growth of hermit crabs. J. crabs at Eniwetok Atoll, Marshall Islands. Exp. Mar. BioI. Ecol. 23:299-305. Pac. Sci. 36:107-117. ---. 1976b. Population consequences of Shimamura, K. 1987. Ecological studies of shell utilization by hermit crabs. Ecology land hermit crabs in the Yaeyama Islands. 57:570-578. Pages 61-118 in AMAN, a report on the Herreid, C. F., II, and R. J. Full. 1986. En distribution and ecology of land hermit ergetics of hermit crabs during locomo crabs in Okinawa Prefecture. Okinawa tion: The cost of carrying a shell. J. Exp. Prefectural School Board. [in Japanese.] BioI. 120:297-308. Vogel, H. H., and J. R. Kent. 1971. A curious Markham, J. C. 1968. Notes on growth case: The coconut crab. Fauna (Oslo) 2:4 patterns and shell-utilization of the hermit 11. crab Pagurus bernhardus (L.). Ophelia Wolcott, T. G. 1988.3: Ecology. Pages 55 5:189-205. 96 in W. W. Burggren and B. R. Mc Nakasone, Y. 1987. Ecological studies of land Mahon, eds. Biology of the land crabs. hermit crabs in the southern part of Oki Cambridge University Press, Cambridge. nawa Island. Pages 16-60 in AMAN, a Yamaguchi, S. 1938. Spawning and develop report on the distribution and ecology of ment of Coenobita rugosus. Bulteno Scienca land hermit crabs in Okinawa Prefecture. 8:163-177, pIs. 2,3. Imperial University of Okinawa Prefectural School Board. [in Kyushu. [in Japanese with English sum Japanese.] mary.]