Life Cycle and Environmentally Induced Semelparity in the Shore Isopod Ligia cinerascens(Ligiidae) on a Cobble Shore along Tokyo Bay, Central JapanAuthor(s): Toshio Furota and Takeshi ItoReviewed work(s):Source: Journal of Crustacean Biology, Vol. 19, No. 4 (Nov., 1999), pp. 752-761Published by: The Crustacean SocietyStable URL: http://www.jstor.org/stable/1549299 .Accessed: 11/12/2011 10:31

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JOURNAL OF CRUSTACEAN BIOLOGY, 19(4): 752-761, 1999

LIFE CYCLE AND ENVIRONMENTALLY INDUCED SEMELPARITY IN THE SHORE ISOPOD LIGIA CINERASCENS (LIGIIDAE) ON A COBBLE SHORE

ALONG TOKYO BAY, CENTRAL JAPAN

Toshio Furota and Takeshi Ito

ABSTRACT

A 3-year field study and 17-month rearing experiment were conducted on a population of the shore isopod Ligia cinerascens inhabiting a cobble shore in Tokyo Bay, central Japan. The research was designed to clarify aspects of life-cycle and reproductive traits in L. cinerascens. Most males, both in the field and in the rearing experiment, died before the onset of their second winter, but some field males overwintered twice. Most females overwintered once, bred from May through Septem- ber, then died before the next winter. A small group of females, however, began breeding late in the season of the year of their birth, then most likely died without overwintering. Females in the field produced mostly 1 brood or at most 2 broods before dying, but those in the rearing experi- ment lived longer, producing up to 3 broods and possibly more. The results of this study indicate that the typical life cycle of L. cinerascens is annual with a 5-month breeding season, but includ- ing a shortened life cycle completed within a single breeding season. The data from the rearing ex-

periment, however, suggest that the number of broods produced by a female may be limited by en- vironmental factors rather than by genetic characteristics.

Shore isopods of the genus Ligia are com- monly distributed in coastal environments around the world. Variability in life-cycle characteristics have been observed not only among different species, but also among lo- cally separated populations of the same spe- cies. For example, the longevity of L. ocean- ica (L.) varies from 1 year to 2.5 years in Europe (Jons, 1965; Willows, 1984, 1987), while that of L. pallasii Brandt in British Co- lumbia is up to 1.5 years (Carefoot, 1973a). The total number of broods produced by a fe- male also varies, from 1 in L. dilatata Brandt in South Africa (Koop and Field, 1980) to 3 or more in L. oceanica in England (Nicholls, 1931). These data indicate plasticity of the life-cycle pattern in Ligia in response to en- vironmental conditions. It is still unclear, however, if this plasticity arises from geno- typic and/or phenotypic variabilities.

Ligia is abundant along the eastern Asian seaboard, but the life histories of Ligia in this region have not been studied. This study was conducted to clarify the life-cycle character- istics of a population of L. cinerascens Budde-Lund living on a cobble shore along northern Tokyo Bay, central Japan. The life- cycle characteristics of the local field popu- lation of L. cinerascens and those reared un- der laboratory conditions are contrasted, and the results are compared to data from other species of Ligia in other parts of the world.

MATERIALS AND METHODS

Four species of Ligia have been recognized along Japa- nese coasts, and the distribution of each species has been shown to be clearly separated (Nunomura, 1983). Tokyo Bay is located on central Honshu, in the distribution area of L. exotica Roux, but L. cinerascens, which is basi- cally distributed in Hokkaido, northern Japan (Nunomura, 1983), is common. The reason for this segregated distri- bution of L. cinerascens is not clear, but unintentional introduction is suspected (Itani, personal communication).

Study Site.-Shinhama, a man-made lagoon of about 30 ha, is located along the northernmost shore of Tokyo Bay, on the central Pacific coast of Honshu (35?40'N, 139?56'E) (Fig. 1). The lagoon is connected with Tokyo Bay through a 0.5-km long channel. A large population of L. cinerascens is found on a cobble shore bordering the lagoon. The intertidal zone consists of 5-30-cm di- ameter cobble stones on the surface, with gravel and muddy sediment underneath. The horizontal distance be- tween the highest and lowest tide marks is about 9 m with a maximum range of tidal level of approximately 1.5 m. Distribution of L. cinerascens is restricted to an area be- tween the highest tide mark and the middle of the inter- tidal zone.

Field Study.-Two transect lines (A and B) were estab- lished across the intertidal zone from the highest tide mark to the middle intertidal at points A and B in Fig. 1. Five stations (plus a sixth only during the warmer season) were established along each line at 1-m intervals. The tran- sect lines covered almost the entire width of the local dis- tribution of L. cinerascens.

To begin, quantitative samples were collected at each station in March and April 1989. All cobbles and stranded matter in a 25 x 25-cm quadrat were collected along with the surface sediment, using a shovel. The sediment was placed in a plastic box and all isopods in the box were collected.

752

FUROTA AND ITO: LIFE CYCLE OF LIGIA

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Mesh basket sampling was then implemented from May 1989 to September 1991. A plastic mesh basket (30 x 40 cm wide, 10 cm deep, with about 2-mm mesh) was buried at each station. The tops of the baskets were set level with the surface. All baskets were filled with sedi- ment, and cobbles and stranded material (if present) were added to provide hiding spaces for L. cinerascens. The habitat structure in the basket was thus similar to the nat- ural habitat. During winter, an additional basket was buried at the highest station where overwintering L. cin- erascens aggregated under stranded fragments of vege- tation.

At each sampling, the basket was removed without dis- turbing the contents and placed in a plastic container. All L. cinerascens were then collected by hand or with an insect aspirator, and fixed in 70% ethyl alcohol. Samples were collected monthly for most of the period, but more frequently during warmer seasons. Sampling was not im- plemented during January and February 1991.

In the laboratory, the isopods collected were placed on a 1-mm scaled plastic film. Body length (BL) (distance between the top of the head and the end of the telson) was estimated to the nearest 0.1 mm under a stereomicroscope. Since a preliminary observation showed that the maxi- mum error of BL was 1.23% from a mean of 10 repli- cate estimations among 5 individuals, estimation error caused by handling was considered negligible. Sex was determined only for individuals of 10.0-mm BL or more, by inspecting for the presence of the penis. All over- wintered individuals, however, were sexed regardless of size. In gravid females, the number of eggs or juveniles in the brood pouch were counted.

Rearing Experiment.-The container utilized for rearing isopods is shown in Fig. 2. Two sets of this apparatus

Fig. 2. Rearing system used in the experiment. A 5-cm thick layer of sand was placed in a 35-cm long x 25-cm wide x 30-cm deep plastic container, with holes in the bottom to drain water. This container was placed on a shallow tray which held brackish water sprayed regu- larly over the system.

were used for the experiment. Ten females and 12 males collected at the study site on 16 May 1990 were placed in one container, and 10 females and 11 males in the other. None of the females were gravid when introduced. The experiment was continued to October 1991 without ad- dition of new individuals.

The rearing containers were set outside without pro- tection from rain and sunlight. Every 3 or 4 days, the con- tainers were showered with 0.5 1 of brackish water (1:1 fresh and sea water). The water was allowed to remain in the tray, keeping the rearing habitat wet. Goldfish food (consisting mainly of fish powder) and vegetables, such as pear, kiwi, cucumber, and lettuce, were used as food items instead of their natural diet, which consists mainly of intertidal diatoms and algae (Nicholls, 1931; Koop and Field, 1980, 1981; Willows, 1987).

The pouches of the females were checked for the pres- ence of eggs or juveniles every 2-4 days during the breed- ing season (May to September) of 1990. All gravid fe- males were marked with individual color patterns. Maxi- mum and minimum temperatures during each observation interval were recorded with a maximum/minimum ther- mometer placed on the sand surface in the containers.

RESULTS

Field Observations

Gravid females occurred from early May to early September in 1989, late April to mid- September in 1990, and mid-May to late Au- gust in 1991. Mean size of manca-stage young was 3.0 ? 0.1-mm BL (SD, N = 122). Recruitment of newly released young (less than 4-mm BL) was observed at the site from June to September of all three years. This in- dicates that the breeding season, as demon- strated by the presence of gravid females, usually lasted from early May to mid-Sep- tember, and that recruitment began about one month after the onset of gravidity.

The three yearly cohorts (1990, 1991, 1992) showed single-size patterns, and the size overlap between yearly cohorts was lim- ited (Fig. 3). This permits estimation of

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Fig. 3. Seasonal changes in size distribution of the shore isopod Ligia cinerascens in Shinhama Lagoon, 1989-1991. Left, male; right, female (gravid individuals are shown by black bars). Shaded bars indicate nonsexed young, which are divided equally on the male and female sides.

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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 19, NO. 4, 1999

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Fig. 5. Yearly change of mean density in cohorts of the lines in Shinhama Lagoon. Vertical bars show range.

growth (Fig. 4) and change in density (Fig. 5) for each cohort by size-histogram analy- sis. Growth rate of the 0+ (before first over- winter) isopods differed among the 3 yearly cohorts. Size of the 1+ (after first overwinter) isopods measured in March (about 15-mm BL), however, showed no significant differ- ence either among the 3 yearly cohorts of the same sex, or between sexes in the same year (post-hoc Fisher's PLSD, after normalizing by logarithmic transformation, P > 0.05).

During the breeding season, mean size of the 1+ males increased continuously from May (about 18-mm BL) to September (about 30-mm BL). The mean size for females, how- ever, decreased in August (Fig. 4) due to the disappearance of larger females (Fig. 3). All male and female breeders disappeared im- mediately after the breeding season (Figs. 4, 5), except for the 1989 cohort, for which a small number of 1+ males were collected un- til November (about 38-mm BL). The largest males (40-mm BL) were found from March to June 1989. These males could possibly have been born in 1987 and experienced two overwinters (2+).

Prior to the breeding season, in March and April, the sex ratio (female/male) for 1+ in- dividuals varied among observations (Table 1). Female dominance was found in two of six observations. There was, however, no sig- nificant difference in the total ratio for all ob- servations combined. This suggests that the

J 1991

Month shore isopod Ligia cinerascens on two observed transect

sex ratio of L. cinerascens at the study site is basically 1:1.

Densities estimated at each observation sta- tion were converted to the number of L. cin- erascens in a 1-m length of shore line (between the highest and lowest observation stations). The density of each cohort was maximum in early summer (June to July), but then gradu- ally decreased until the beginning of the breeding season. An abrupt decrease was recorded during the breeding season (Fig. 5).

Females become gravid only after reaching an adult body size of 21-mm BL or more. Only a few females, however, had attained

Table 1. Sex ratio in once-overwintered Ligia cineras- cens.

Number of isopods collected

Date Male Female Ratio (male/female)

1989 29 March 75 108 0.69* 15 April 73 74 0.99n.

1990 30 March 185 153 1.21 n

28 April 106 109 0.97n.s

1991 29 March 39 49 0.8Ons 30 April 14 31 0.45**

Total 492 524 0.94n s

Bimodal test: **, P < 0.001; *, P < 0.005; n.s., not significant.

756

FUROTA AND ITO: LIFE CYCLE OF LIGIA

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this adult size by the beginning of the breed- ing season. Most continued to grow, then achieved adult size and became gravid as the breeding season progressed.

At the end of the breeding season (August and September), when most 1+ females had disappeared, some of the largest 0+ females (BL > 20 mm) started gravidity. After the breeding season (late September), however, the number of those 0+ adult-size females,

some of which may have already bred, de- creased sharply (Fig. 3). This could indicate that most of these 0+ breeder females died before their first overwintering.

Short-interval observations on new recruits (BL < 4 mm) and the reproductive condition of adult females were conducted in 1990 (Fig. 6). Density of all 1+ adult females (BL ? 21 mm) showed a peak in late June, then rapidly decreased through July and August. Density

757

JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 19, NO. 4, 1999

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Fig. 7. Relationship between body size (BL3) and brood size for the shore isopod Ligia cinerascens.

of gravid 1+ females, however, showed two peaks, in mid-May and late June. These peaks may be responsible for the two peaks in new recruit density located in mid-June and mid- July. Density of all 0+ adult females (BL > 20 mm) gradually increased after late August. Gravid 0+ females, however, were found only from late August to mid-September. A small peak in new recruit density was observed in late August. Since no gravid 1+ females were found after August, and some of the 0+ fe- males carried fully developed eggs in which eyes had appeared, these late August recruits most likely resulted from release of young by the 0+ females.

Size of brood (number of egg or juveniles in a brood pouch) was found to be positively dependent on BL3 (Fig. 7). No significant dif- ference in the relationship was found between the 0+ and 1+ females (one-way ANCOVA, d.f. = 1, F = 1.498, P = 0.222). Average brood size was 94.5 ? 20.6 SD.

Rearing Experiment

During the breeding season of May through September 1990, the number of gravid fe- males in the first generation (collected at the study shore on 16 May 1990) showed three peaks, in mid-June, mid-July, and mid-August (Fig. 8). Four clear reductions in the number of surviving females were observed, follow- ing the gravid female peaks. The patterns of male mortality from July to September were similar to the female, but the overall male sur- vival ratio was higher. At the end of the breeding season (25 September), four females (27.6-mm BL ? 0.5 SD) and 13 males (31.8- mm BL ?+ 1.0 SD) of the first generation sur- vived. All of these survivors were recon- firmed on 19 October, but none overwintered successfully.

During the 1990 breeding season, a total of 39 gravidity cases were found among the 20 introduced females (some of the females be-

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FUROTA AND ITO: LIFE CYCLE OF LIGIA

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came gravid more than once). In all of these, except for one in which the female died be- fore brood hatch, young were released. Gravid time (egg deposition to young release) decreased with increase in temperature, and varied from about one month in the early breeding season to about two weeks in the late season (Table 2).

Since paint marks were lost when the fe- males molted during the interbrood period, the interbrood time was estimated for only 17 females that were remarked during the ecdy- sis. The interbrood time was 17.4 d ? 1.5 SD (N = 9) between the first and second gravid- ity peaks (June-July), and 12.8 d ? 1.3 SD (N = 8) between the second and third gravidity peaks (July-August). Two females produced three broods between mid-May and late July, but the total number of broods produced over the entire season could not be determined, and may have even exceeded three.

About half of the 0+ second generation young (334 males and 309 females) were re- moved from the rearing systems on 19 July

Table 2. Gravid period (days) of Ligia cinerascens.

Month of Gravid Mean of medium Number egg deposition period (?SD) temperature (+SE) observed

May 29.6 + 1.8 21.3 + 0.8 6 June 22.4 +? 1.1 23.3 + 0.4 8 July 15.9 ?3.9 26.9 ?0.7 15 August 13.6 ? 5.1 26.9 ?+ 0.4 6

and 15 August 1990. No gravid females were found among this group. After this, no ob- servations were made regarding the gravid condition of 0+ second generation young in the rearing systems. On 26 April 1991, about 300 overwintered (1+) second generation in- dividuals, which had reached 15-20-mm BL, were confirmed in the rearing systems. Fe- males of this 1+ second generation started gravidity from late May. The mean BL at midbreeding season (17 June) was 22.3 mm ? 3.3 SD (N = 133) for males, and 21.4 mm ? 2.7 SD (N = 127) for females. These sizes were almost equal to those observed at the field study site (Fig. 4). The first occurrence of third generation young was observed on 11 June 1991. During the following month, about 500 of these young were removed.

At the end of the rearing experiment (18 October 1991), 23 females (27.0 mm ?+ 1.1 SD) and 37 males (32.6 mm ? 2.0 SD) of the 1+ second generation born in 1990 were found in the rearing systems. Mean size of the 0+ third generation young (not sexed) was 15.3-mm BL ? 5.5 SD (N = 248), which was almost equal to that of the 0+ field young as measured during the previous two years (Fig. 4). These results suggest that growth rate and life cycle in the rearing systems were essen- tially similar to those in the natural popula- tions, but that the reared L. cinerascens sur- vived and reproduced longer.

759

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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 19, NO. 4, 1999

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Fig. 9. Life cycle of the shore isopod Ligia cinerascens in northern Tokyo Bay.

DISCUSSION

Some of the largest 0+ females of Ligia cinerascens, which were born at the study shore at the beginning of the breeding sea- son (early June), started their first gravidity at the end of the same breeding season, about 2.5 months after birth, but then died before overwintering (Fig. 3). Most females, how- ever, started gravidity after the first overwin- tering, then disappeared during their first breeding season. Females at the study shore can thus be assumed to experience only one breeding season before dying.

Most 1+ females reached adult size (BL > 21 mm) one month after the start of the breed- ing season (June). The density of the adult fe- males then rapidly decreased in July, and all had disappeared by August (Figs. 3, 6). Most of the largest adult females that started breed- ing from May died during June (Fig. 3). Fur- thermore, the 0+ breeders died about one month later (Fig. 6). Adult life time for both the 0+ and 1+ females can be estimated at about one month, during which the female can reproduce only once (Table 2). This sug-

gests that most field females may produce only one brood during their life time. Some long-lived females, however, may live long enough to produce a second brood.

A great reduction in field population, as well as high mortality among reared females, were observed during the breeding season (Figs. 3, 5, 8). After the breeding season, mean body size of the surviving females in the rearing experiment was smaller than that of males, despite the fact that sizes of both sexes were similar before the breeding sea- son (Fig. 4). These data suggest that the fe- males invest a great amount of energy in egg production and brood care, causing critical exhaustion which may induce mortality.

The life cycle of L. cinerascens at the study shore is portrayed in Fig. 9. The most typi- cal pattern is that the population is maintained by yearly generational replacement. A small number of females, however, show a short- ened life cycle involving rapid growth and re- production at the end of the breeding season in which they were born. Since these 0+ breeding females release young only at the very end of the breeding season, their young

760

FUROTA AND ITO: LIFE CYCLE OF LIGIA

are unable to reach adult size (21-mm BL) by the beginning of the next year's breeding sea- son. These offspring thus wait at least to the midbreeding season (July) to release their own young. These young, however, in turn do not have enough time to grow into 0+ breed- ers themselves. This pattern is similar to the reproduction slips between 1+ and 2+ gener- ations observed in L. oceanica (Willows, 1984, 1987).

The one-year life cycle for L. cinerascens in this study is similar to that reported for L. oceanica (L.) in the western Baltic (Jons, 1965), L. pallasii Brandt in British Colum- bia (Carefoot, 1973a), and L. dilatata Brandt in South Africa (Koop and Field, 1980), but is shorter than that reported for L. oceanica in England (Nicholls, 1931; Willows, 1984). The shortened life cycle observed in this study, in which females breed and die dur- ing a single breeding season, is the first re- ported for species of Ligia. The study site is at a lower latitude than previous studies (ex- cept for South Africa), and higher summer temperatures may account for the fast growth required for the shortened life cycle.

Female L. cinerascens at the study site showed semelparous (one brood production through a life) reproduction, most likely ne- cessitated by their short adult life. The rear- ing experiment, however, showed that fe- males of L. cinerascens are capable of a longer adult life and consequently able to pro- duce up to three or even more broods during a breeding season. European L. oceanica are also essentially semelparous, but some fe- males produce a second brood (Jons, 1965; Willows, 1984, 1987). In addition, reared L. oceanica produce two, three, or more broods (Nicholls, 1931). A similar increase in brood production has also been reported for semel- parous terrestrial isopods when they were reared (reviewed by Sutton et al., 1984). This iteroparous reproduction seen in reared fe- males of Ligia suggests that the semelparous reproduction pattern observed for most fe- males of Ligia in the field may be necessi- tated by external biological and/or physio- chemical conditions, rather than genetic re- productive characteristics.

ACKNOWLEDGEMENTS

We are grateful to Drs. T. Udagawa, A. Asakura, and M. Hasegawa for their helpful suggestions. Dr. N. Nuno- mura kindly identified the isopod studied. Ms. M. Itani is thanked for her comments. Dr. A. lijima assisted in the field observations. Dr. Y. Hasuo and Ms. S. Hasuo, superintendents of the Gyotoku Wild-bird Sanctuary, are thanked for providing the opportunity to use the study site. We also thank Dr. K. Short for editing the English.

LITERATURE CITED

Carefoot, T. H. 1973a. Studies on the growth, repro- duction, and life cycle of the supralittoral isopod Ligia pallasii.-Marine Biology 18: 302-311.

. 1973b. Feeding, food preference, and the up- take of food energy by the supralittoral isopod Ligia pallasii.-Marine Biology 18: 228-236.

Jons, D. 1965. Zur Biologie und Okologie von Ligia oceanica (L.) in der westlichen Ostsee.-Kieler Meeresforschungen 21: 203-207.

Koop, K., and J. G. Field. 1980. The influence of food availability on population dynamics of a supralittoral isopod, Ligia dilatata Brandt.-Journal of Experimen- tal Marine Biology and Ecology 48: 61-72.

, and . 1981. Energy transformation by the supralittoral isopod Ligia ditatata Brandt.-Journal of Experimental Marine Biology and Ecology 53: 221-233.

Nicholls, A. G. 1931. Studies on Ligia oceanica I. A. Habitat and effect of change of environment on respi- ration. B. Observation on moulting and breeding.- Journal of the Biological Association of the United Kingdom 17: 655-673.

Nunomura, N. 1983. Studies on the terrestrial isopod crustaceans in Japan I. Taxonomy of the Family Ligi- idae, Trichoniscidae and Olbrinidae.-Bulletin of the Toyama Science Museum 5: 23-68.

Sutton, S. L., M. Hassall, R. Willows, R. C. Davis, A. Grundy, and K. D. Sunderland. 1984. Life histories of terrestrial isopods: a study of intra- and inter-specific variation.-Symposia of the Zoological Society of Lon- don 53: 269-294.

Willows, R. 1984. Breeding phenology of woodlice and oostegite development in Ligia oceanica (L.) (Crus- tacea).-Symposia of the Zoological Society of Lon- don 53: 469-485.

. 1987. Population dynamics and life history of two contrasting populations of Ligia oceanica (Crus- tacea: Oniscidea) in the rocky supralittoral.-Journal of Animal Ecology 56: 315-330.

RECEIVED: 5 June 1998. ACCEPTED: 29 April 1999.

Address: Department of Biology, Faculty of Science, Toho University, Miyama 2-2-1, Funabashi, Chiba 274-8510, Japan. (e-mail: furota@bio.sci.toho-u.ac.jp)

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