enthos Research Vol. 51, No. 2 : 21- 32 (1996) BENTHOS RESEARCH

The Japanese Association of Benthology

Vertical Distribution and Life Cycle of Two Isopod

within Intertidal Mussel Beds

Keiji Iwasaki Institute for Natural Science, Nara University

ABSTRACT The vertical distribution and life cycle of two isopod crustaceans, dentisinus Shen and Cirolana harf oldi japonica Thielemann, were studied at Shirahama, Wakayama Prefec- ture, central Japan, where two mytilids Septif er virgatus (Wiegmann) and Hormomya mutabilis (Gould) formed vertically contiguous mussel beds. The abundance of the isopods tended to increase downshore within the S. virgatus bed in the upper and middle intertidal zones but decreased abruptly within the H. mutabilis bed in the lower intertidal zone. Very few individuals were found within the H. mutabilis bed throughout the year. The size struc- ture of both species of isopods did not differ greatly among five shore levels within the S. virgatus bed. Multiple linear regression analyses against density of D. dentisinus revealed that the amount of sediment within the mussel beds tended to be negatively correlated while the density and volume of mussels both tended to be positively correlated. Both species re- produced twice a year. However, seasonal changes in size structure suggested that the lon- gevity of the two generations born during the year differed between the species: spring- autumn and autumn-spring generations for D, dentisinus, and spring-next spring and autumn-next autumn generations for C. h. japonica. The association between isopods and mussels is discussed with a focus on the presence or absence of sediment within mussel beds.

Key words: intertidal isopods, life cycle, mussel beds, vertical distribution

INTRODUCTION Salemaa 1979, 1987; Healy & O'Neill 1984; Tuomi et al. 1988; Kroer 1989) and supralittoral Isopod crustaceans are common in a broad isopods of the family Ligiidae (e. g., Willows range of marine habitats, from supralittoral 1987a, b) . However, relatively few studies have shores to deep-sea environments (e.g., been conducted on the ecology of other rocky Harrison 1988; Brown & Odendaal 1994) . Infor- shore species belonging to the Cirolanidae and mation on their biology and the important roles (Wieser 1962, 1963; Glynn they play in demersal communities has been 1965; Holdich 1968, 1970, 1971, 1976; Johnson gathered progressively (e.g., Shafir & Field 1976). 1980; Stepien & Brusca 1985; Brown & Odendaal In Japan, activity rhythms and behaviour 1994) . In particular, on rocky shores there have been investigated for some supralittoral have been a great number of ecological studies isopods of the genera Tylos and Ligia (e. g., on boreal isopods of the Idotea (e. g., Ondo 1958a, b, 1959; Ondo & Mori 1956; Imaf uku 1976) . However, information on the Received November 2, 1995 : Accepted April 10, 1996 distribution and ecology of isopods, par-

21 Vol. 51, No. 2 Benthos Research November, 1996 ticularly cirolanids and sphaeromatids, has bed, and the shore heights of the sampling sites been fragmental and scanty (Sekiguchi 1982, were noted (mean height for the replicates: 1985; Sekiguchi et al. 1981, 1982; Mori & Tanaka +65, +38, + 9 and - 6 cm within the S. virgatus 1989; Iwasaki 1995a), and there have been no bed, - 29 and - 56 cm within the H. mutabilis quantitative studies on the life history or popu- bed) . Mussels, isopods, other invertebrates lation dynamics of intertidal isopods. and sediment within the quadrats were all col- Two isopod crustaceans, lected. In 1994, sampling was conducted at five Shen (Sphaeromatidae) [Japanese name: levels in the S. virgatus bed and two levels in the Shiriken-umisemi] and Cirolana harf ordi ja- H. mutabilis bed. Triplicate samples were ob- ponica Thielemann (Cirolanidae) [Nise- tained at each level (mean height for the repli- sunahorimushi] , are common species on the cates: +67, +48, +26, +7, -10 cm within the S. intertidal shores of Japan and have been re- virgatus bed, - 31 and - 59 cm within the H. ported to occur abundantly within mussel beds mutabilis bed) . In the laboratory the mussels, (Tsuchiya 1979; Tsuchiya & Nishihira 1985, isopods, other invertebrates, and sediment 1986; Iwasaki 1995a) and among barnacles were separated from one another. Surface (Mori & Tanaka 1989) . The present paper re- water was blotted from the mussels, and their ports the vertical distribution and life cycle of volume was measured by putting them into a the two species inhabiting mussel beds graduated cylinder with sea water. All consisting of Septif er virgatus (wiegmann) were counted and weighed, and the size of all [Murasaki-inkogai] and Hormomya mutabilis isopods (width of 1st pereonite) was measured (Gould) [Hibarigai-modoki] . Information on to the nearest 0.05 mm. Accurate and prompt the breeding season and brood size of gravid measurements of body lengths in both isopod females is also given and compared with that species were difficult because specimens fixed for other rocky shore isopods. in formaldehyde solution were rolled up. Since the width of the 1st pereonite was highly corre- STUDY STITE AND METHODS lated with body length for both species (April 1994; D. dentisinus: BL (body length) = 2.152 The study site was a sandstone rocky reef on a Pw (1st pereonite width) -0.045, r - 0.988, p < moderately wave-exposed shore near the Seto 0.001, n = 50, C. h. japonica: BL = 2.977 Pw - Marine Biological Laboratory, Kyoto Univer- 0.139, r = 0.967, p < 0.001, n- 50), the former sity, wakayama Prefecture (33° 42'N,135° 21'E). could represent body size adequately. Addi- The rocky reef had a very smooth, flat surface tionally, males and females were discriminated which sloped gently from the upper intertidal from each other and from juveniles by the pres- (80 cm above mean tide level) to subtidal zones ence of penes and oostegites (or oostegite with ca. 5° inclination. Shore height is hereafter buds), respectively. Males of D. dentisinus expressed in cm preceded by + or -, indicating have a median process on the dorsal surface of above or below mean tide level. The tidal range the pleons, and the lengths of these processes at this site extends from +110 to -110 cm. The were measured because the length relative to mussel S. virgatus formed a bed from the upper body size changed seasonally, supposedly re- to middle intertidal zone, and H. mutabilis in flecting their reproductive maturity. Eggs or the lower intertidal zone. The two mussel beds juveniles within the marsupia of mature females were vertically contiguous with a very narrow were counted. Sediment was dried under the zone of overlap. A detailed map of this study sun for two days and weighed after sifting out site and the zonal distribution of mussels and mussel shell fragments with a sieve with 1 mm other sessile organisms are given in Iwasaki mesh openings. (1994: site B). Monthly sampling was carried out at the Cross-shore sampling was carried out in late middle levels of the respective mussel beds April of 1982 and 1994. In 1982, two quadrats of (+35 cm for S. virgatus, - 40 cm for H. 50 cm2 each were haphazardly tossed onto the mutabilis) from early April, 1982, to early mussel bed at each of four levels in the S. April, 1983, and afterwards, sampling was con- virgatus bed and two levels in the H, mutabilis tinued at four-month intervals until early April,

22 Life cycle of intertidal isopods

1985. The same sampling method as for cross- zone are shown in Table 1. In April, 1982, no shore sampling was employed, and duplicate predictor variable was correlated significantly samples were obtained in each mussel bed. In with the density of D. dentisinus. The coeffi- the laboratory, the same procedures as those in cient of multiple determination was also not the cross-shore samplings were followed. significant. In April, 1994, however, sediment To detect factors affecting the vertical distri- weight was negatively correlated, and density bution of isopods, multiple linear regression and volume of mussels positively correlated, analyses were made for isopod densities in 12 with the density of D. dentisinus. The coeffi- quadrats at six shore levels in April, 1982, and cient of multiple determination was also signifi- in 21 quadrats at seven shore levels in April, cant. The amount of sediment also tended to be 1994. Predictor variables were shore height, negatively correlated with the density of C. h. volume and number of mussels, amount of sedi- japonica, although the correlation was not sig- ment, and density of the predatory polychaetes nificant on either survey date. Arabella iricolor (Montagu) and Nereis To examine the relationship between the den- nichollsi Kott. sities of the two isopod species in April, 1994, residuals of the regressions of the density of D. RESULTS dentisinus on the amount of sediment and den- sity and volume of mussels were calculated (see Vertical change in abundance and size struc- Table 1) , and the correlation between the re- ture siduals and the raw densities for C. h. japonica Figures 1 & 2 show the vertical density pro- were analysed within the S. virgatus bed. No files of D, dentisinus and C. h. japonica. In significant correlation was detected between April, 1982, and April, 1994, densities of both the values ( r = 0.238, n = 15, p > 0.05), so no species tended to increase with decreasing specific association between the distributions shore height within the S. virgatus bed, but a of the two species is indicated. Isopod densities significant negative correlation was detected in April, 1982, could not be analysed in this way only for D, dentisinus in April, 1994 ( r = 0.623, because of the small number of samples. p < 0.05) . Within the H, mutabilis bed, very few The size structure of D. dentisinus in late D. dentisinus and no C. h. japonica were found. April, 1994, did not differ remarkably among Results of multiple linear regression analyses the five levels sampled within the S. virgatus for isopod densities throughout the intertidal bed (Fig. 3a). At the lowest level (-10 cm), two

Fig. 1. Vertical profiles of density of D, dentisinus col- Fig. 2. Vertical profiles of density of C. h. japonica col- lected within the mussel beds in April, 1982 and 1994. lected within the mussel beds in April, 1982 and 1994.

23 Vol. 51, No. 2 Benthos Research November, 1996

Table 1. Results of multiple linear regression analyses for isopod density in April, 1982 ( n =12) and 1994 ( n = 21) . Stan- dard partial regression coefficients and their probability of significance (ns : not significant at 5 % level, * : significant at 5 % level) are shown together with the coefficant of multiple determination ( r2 ). Polychaete density indicates summed density of two predatory polychaetes, Arabella iricolor and Nereis nichollsi. Mussel density and volume denote summed values for S virgatus and H. mutabilis.

a. D. dentisinus b. C. h. japonica

Fig. 3. Size structure (expressed as width of 1st pereonite) of D, dentisinus and C, h. japonica collected at five shore levels (means for triplicate samples) of the S. virgatus bed in April, 1994. Gray, black, cross-hatched, and white Fig. 4. Monthly change in size structure (expressed as parts indicate juveniles or individuals of undetermimate width of 1st pereonite) of D. dentisinus collected at the sex, males, females with oostegite buds, and females middle level (MTL +35 cm) of the S virgatus bed. For brooding eggs or juveniles, respectively. n: number of in- key to shaded patterns see Fig. 3. dividuals.

24 Life cycle of intertidal isopods

1983 1984 1985

Fig. 5. Size structure of D. dentisinus in April, August, and December, 1983-1985. For key to shaded patterns see Fig. 3. peaks in the width of the 1st pereonite were Seasonal change in size structure and density found at 0.6-0.8 mm and 1.6 -1.8 mm, and the Many juvenile D. dentisinus smaller than 1 peak for smaller individuals tended to increase mm wide appeared in May and October, 1982, in size in the higher shore levels. At the three and increased in size until August, 1982 and middle levels, the peak for larger individuals January, 1983, respectively (Fig. 4) . This indi- was obscure. Most individuals larger than 1.4 cates that recruitment of juveniles occurred mm in width were sexed. Males were found at mainly between early April and May and be- all five shore levels, and most individuals wider tween September and October. The spring co- than 2 mm were males. Mature females brood- hort grew quickly in the summer and disap- ing eggs or juveniles, or females with oostegite peared in October. Growth of the autumn buds, were collected at the four lower levels, cohort was slow during the autumn and winter and they ranged from 1.4 to 2.1 mm in width. (Fig. 4), and in the following early April large The size structure of C. h. japonica was simi- individuals reproduced and then disappeared lar among the four lower shore levels in the S. by August (Figs. 4, 5) . The difference in size virgatus bed in April, 1994 (Fig. 3b) . Two co- structure between early or mid-April, 1982 - horts were recognised in each histogram, and 1985 (Figs. 4, 5) , and late April, 1994 (Fig. 3), the modes of the cohorts lay between 1.25-1.75 also indicates that mass recruitment of juve- mm for the smaller cohort and over 3.0 mm for niles occurred during that month. Mature fe- the larger cohort except for those at the +48 cm males brooding their young were found in level. Most individuals larger than 2 mm were April, May, and August 1982 (Fig. 4) . The pro- sexed. Ten mature females brooding young portion of females with oostegite buds de- were collected, and their width ranged from 2.3 creased from April to July but increased in to 3.4 mm. August. From October to December there were The numbers of D. dentisinus and C. h. japon- no females with oostegite buds, but the propor- ica collected in April 1982 were too small to tion increased again in March, 1983 (Fig. 4). compare the size structure among the four Males with visible median process were col- shore levels within the S. virgatus bed. lected almost throughout the year except in Oc- tober and December, 1982 (Fig. 4) . The size structures in April, August, and December, 1983

25 Vol. 51, No. 2 Benthos Research November, 1996

The relative length of the median process on the male pleon, expressed as a proportion of the width of the 1st pereonite, increased in spring, tended to be constant until September, and decreased afterward (Fig. 6) . No male with a visible median process on its pleon was collected in October or December, 1982 (see Fig. 4). The density (100 cm 2) of D. dentisinus at the middle level of the S. virgatus bed showed two peaks in May and October, 1982, and tended to decrease afterwards (Fig. 7) . The two peaks corresponded to the months of juvenile recruit- ment. Very few D. dentisinus were ever col- Fig. 6. Seasonal change in relative length (mean±SD) of lected in the middle level of the H. mutabilis bed median process on pleon of male D, dentisinus expressed throughout the year. as proportion of width of 1st pereonite. Data from males The seasonal change in the size structure of with median processes. C. h. japonica is shown in Fig. 8. In June, 1982,

-1985 , tended always to be uni-modal with the modes ranging between 1.0 -1.8 mm (Fig. 5), similar to those for the respective months in 1982. Mature females brooding young were col- lected in both April and August, and the pro- portion of females with oostegite buds was also high in these months. In December, 1983 and 1984, only one or two males were found. Most individuals larger than 2 mm wide were males throughout the study period.

Fig. 8. Monthly change in size structure (expressed as width of 1st pereonite) of C. h, japonica collected at the Fig. 7. Monthly change in densities of the two isopod spe- middle level (MTL +35 cm) of the S. virgatus bed. For cies from April, 1982, to April, 1983. key to shaded patterns see Fig. 3.

26 Life cycle of intertidal isopods

1983 1984 1985

Fig. 9. Size structure of C. h. japonica in April, August and December 1983-1985. For key to shaded patterns see Fig. 3.

most isopods larger than 2 mm wide disap- of juvenile recruitment. This isopod's density in peared, whereas many juveniles smaller than 1 the middle level of the H. mutabilis bed was very mm appeared and formed a cohort. This juve- low, from 0 to 6 per 100 cm2, throughout the nile cohort increased in size until October. year. From November onward, however, the impor- tance of this cohort decreased because another Number of brood juvenile cohort appeared and constituted more Forty-nine females of D. dentisinus brooding than half of the population. The size of the new eggs or juveniles were collected during the recruits increased progressively, but slowly, study period, ranging from 1.4 to 2.4 mm in during the winter. Mature females brooding width (Fig, l0a) . The number of brooded eggs eggs or juveniles were collected in April - June or juveniles significantly increased with in- and September - October, and they constituted creasing parental size both in spring and sum- 25-100% of the isopods larger than 2.0 mm in mer (Fig. 10a) . Brood size in summer tended to width. Females with oostegite buds were found be greater than in spring, but a statistical com- in April - June and August - September. The parison between them was impossible because size structure in April, 1983-1985, tended to be of the heterogeneity of variances from the re- bimodal with the modes lying between 1.5 - 2.0 gression lines. The size of brooding C. h. japon- mm for the smaller cohort and over 2.5 mm for ica ranged from 2.25 to 3.4 mm wide, and num- the larger cohort (Fig. 9). This pattern resem- ber of brooded juveniles per parent increased bled that of April, 1982 (Fig. 8) and 1994 (Fig. with increasing parental size only in the spring 3b). In August and December, 1983-1984, many brood (Fig. lOb). small (<2 mm) and few large (>2 mm) isopods were collected, and the size structures were DISCUSSION similar to those for the respective months in 1982 (Fig. 8). Distribution within mussel beds Changes in the density of C. h. japonica in the Several workers studying the crevice fauna of middle level of the S. virgatus bed showed two intertidal shores have reported that isopods in- distinct peaks in June - July and November cluding sphaeromatids are abundant in rock (Fig. 7), and these corresponded to the months crevices in the intertidal zone (Morton 1954;

27 Vol. 51, No. 2 Benthos Research November, 1996

a. . dent/sinus b. C. h. japonica

Fig. 10. Number of brooded juveniles (including eggs) as a function of size (width of 1st pereonite) of brooding females. Solid and broken lines indicate regression lines for spring broods of both species and a summer brood for D. dentisinus, respectively. **, * and ns for correlation coefficient (r) denote significance at 1% and 5% level and non-significance at 5% level.

Kensler & Crisp 1965) . Holdich (1970, 1971, throughout the year (Figs. 1, 2, 7). 1976) revealed that juvenile and adult Stepien & Brusca (1985) reported that the isopods of the genus Dynamene (= Naesa, nocturnally active isopod Cirolana Sphaeromatidae) are distributed in different diminuta Menzies forms swarms that sur- habitats: juveniles occur in lower intertidal round, bite and attack live fishes near the algal mats and feed on the algae, and the adult seaf loor off southern Californian shores. In males and females shelter together in crevices Japan, C. h. japonica and another cirolanid and empty barnacle tests during their breeding isopod, Bathynomus do ederleini Ortomann, periods. Mori & Tanaka (1989) reported that D. were caught in fish-baited traps placed on the dentisinus utilizes the secondary space formed seaf loor and within a shark Dalatias licha by barnacle shells. In the present study site, Bonnaterre caught in a gill net, respectively empty tests of the barnacles Tetraclita (Sekiguchi et al. 1981; Sekiguchi 1982) . These squamosa japonica Pilsbry and Chthamalus findings indicate that free-living cirolanid challengeri Hoek occurred abundantly within isopods have a considerable swimming ability gaps formed after mass dislodgements of mus- (Macquart-Moulin 1992) . Mori & Tanaka sels by waves (Iwasaki, unpublished data). (1989) reported the vertical migration of D. Also, algal mats consisting exclusively of dentisinus following fluctuations of the water Gigartina intermedia Suringar and Corallina surface. I also frequently found that C. h. ja- pilurif era Postels et Ruprecht occurred in the ponica and D. dentisinus swim actively in water lowest intertidal zone of the present study site containers in the laboratory. Accordingly, (Iwasaki 1994) . However, very few isopods these two isopod species most likely also swim were found within the empty barnacle tests or actively in the field, and their vertical distribu- algal mats (Iwasaki, unpublished data), and tions within the mussel beds in the present distribution of the two isopod species was re- study (Figs. 1, 2) may be temporary ones lim- stricted to the Septifer virgatus mussel beds ited to daytime emersion. However, the

28 Life cycle of intertidal isopods restriction of the isopod population to the S. because juvenile oligochaetes emerging from virgatus bed during emersion suggests the oc- cocoons escape ingestion by M. edulis. Juvenile currence of some factor affecting the vertical isopods may also be subject to no negative ef- distribution of both species. This distribution fect by mussels because they are brooded pattern differed from that of D. dentisinus re- within female's marsupia, spending their early ported by Mori & Tanaka (1989) in which lives with no planktonic stage. Therefore life isopod density tended to increase downshore on within mussel beds is likely to be advantageous a barnacle-dominated, vertical concrete wall. for these ovoviviparous species; they escape Mussel beds formed by the genus Mytilus are desiccation in emersion, wave action, and well known for their structural complexity in predation by large carnivores such as fish and terms of surface area of shell valves, amount of crabs that cannot intrude into the mussel beds. byssal threads, and presence of organic (faeces However, the arguments presented above and pseudof aeces) and inorganic (sand and cannot explain the scarceness of isopods within silt) particles (Suchanek 1985; Seed & Suchanek the H, mutabilis mussel bed. The amount of 1992) . This complexity provides inf aunal ani- sediment, which was much greater in the H. mals with a variety of micro-habitats, and thus mutabilis bed than in the S. virgatus bed mussel beds harbour a large number of (Iwasaki 1994, 1995a, b), was negatively corre- species (Suchanek 1985; Seed & Suchanek 1992). lated with the densities of both isopod species, Mussel beds formed by S. virgatus and H. and the correlation for D. dentisinus was sig- mutabilis are also inhabited by a large number nificant in April, 1994 (Table 1) . In light of the of animal species, although the f aunal composi- fact that Cirolana harf ordi harf ordi Loc- tion differed markedly between the two species kington is known to dig only minimumly in the of mussels (Iwasaki 1995a) . Both S. virgatus sand (Johnson 1976) , no refuge from wave ac- and H. mutabilis form mono-layered mussel tion and desiccation is available for C. h. japon- beds of a maximum 3.5 - 4.5 cm thickness ica and D. dentisinus in the H. mutabilis bed (Iwasaki 1994) . Although this is much thinner with a great amount of sediment. When the two than the multi-layered mussel beds formed by mussel species were enclosed separately within Mytilus edulis L, and M. calif ornianus Conrad cages set in the middle S. virgatus zone, the (Suchanek 1985; Seed & Suchanek 1992), the hu- amount of sediment within the artificial mussel midity and temperature within beds of the for- clumps and the densities of recruits of the two mer species are higher than in air above them isopod species into the clumps differed little be- (Ohsako et al. 1981). tween the two mussel species (Iwasaki 1995a). The density and volume of mussels tended to This shows that there is no specific association be positively correlated with the density of D. between the isopods and either of the two mus- dentisinus (Table 1) . These variables reflect sel species. Accordingly, the greater amount of the structural complexity within the mussel sediment within the H. mutabilis bed must have beds, and the positive correlation may indicate prevented the isopods from resting in the mus- that the complexity of the S. virgatus bed deter- sel bed during emersion. mines the quantity of resting sites and refuges No significant correlation was detected be- from desiccation during emersion and from tween the densities of the two isopod species wave action during awash conditions. within the S. virgatus bed. This suggests that Woodin (1976) predicted that no inf aunal there is no specific association between the spe- forms should consistently attain their highest cies. densities among densely packed suspension- feeding bivalves because the latter reduce the Seasonal change in breeding period probability of successful larval settlement by In the rocky intertidal zone of the Californian any larvae, including their own. However, coast, brooding females of the sphaeromatid Commito (1987) and Commito & Boncavage Dynamenella glabra (Richardson) and ciro- (1989) reported a positive correlation between lanid Cirolana harf ordi harf ordi Lockington Mytilus edulis density and the abundance of the were present in every month of the year (Glynn oligochaete Tubificoides benedeni (Udekem) 1965; Johnson 1976). In Wales, Dynamene

29 Vol. 51, No. 2 Benthos Research November, 1996 bidentata (Adams) has only one distinctive Considering that only large males of the brooding period from April to June, but the autumn cohort were collected in May - July length of the period increases at more south- 1982, longevity of males may be longer than erly locations (Holdich 1968, 1976). that of females, as reported by Holdich (1968) Cirolana h. japonica has been suggested to for Dynamene bidentata in Wales. Generaliza- have only one short breeding season each year tion of results of the present study and geo- (Bruce & Jones 1981) . This was based on obser- graphical variation in the life cycles of these vations showing that none of the 2000 speci- species remain to be investigated in future re- mens of this species collected in northern and search. southern Kyushu island in July were brooding eggs and that a size frequency plot of the popu- Acknowledgements lation showed a single peak. In the present study site, however, the size structure in July, I am grateful to Noboru Nunomura for his 1982, appeared to comprise two cohorts (Fig. taxonomic advice and to Kensuke Nakata, 8), and over a one-year population survey two Tomoko Yamamoto, Hiroshi Ashiwa, Michael reproductive periods were revealed, April-June Huff man and two referees for their comments and September - October (Fig. 8), followed by and English correction on this draft. abundant juvenile recruit in June and Novem- ber. Furthermore, seasonal changes in size REFERANCES structure (Figs. 8, 9) suggest that this species comprised two generations with a one-year lon- Brown, A. C. and F. J. Odendaal 1994 The biology of gevity in 1982 -1983, a spring to next spring oniscid of the genus Tylos. Advances in Ma- generation and an autumn to next autumn gen- rine Biology, 30: 89-153. eration. Bruce, N. L. and D. A. Jones 1981 The systematics and No information on the life cycle and breeding ecology of some cirolanid isopods from southern season of D. dentisinus has been available to Japan. Journal of Natural History, 15: 67-85. date. The present study revealed that D. Commito, J. A. 1987 Adult-larval interactions: predic- dentisinus had two reproductive periods in 1982 tions, mussels and cocoons. Estuary, Coastal and -1983 , April - May and August - September Shelf Science, 25: 599-606. (Fig. 4), although no brooding females were Commito, J. A. and E. M. Boncavage 1989 Suspension- found in September, 1982. The reproductive pe- feeders and coexisting inf auna : an enhancement coun- riod in April was repeated during the following terexample. Journal of Experimental Marine Biology two years in 1984 to 1985 (Fig. 5) . The differ- and Ecology, 125: 33-42. ence in size structure between early or mid- Glynn, D. W. 1965 Community composition, structure, April, 1982 -1985 (Figs. 4, 5), and late April, and interrelationships in the marine intertidal 1994 (Fig. 3), indicates that mass recruitment Endocladia muricata-Balanus grandula association in of juveniles occurred during that month. Very the Monterey Bay, California. Beaufortia, 12: 1-198. small juveniles (<0.75 mm wide) of the autumn Harrison, K. 1988 Seasonal reproduction in deep-sea cohort were found even 2 - 3 months after the Crustacea (Isopoda: Asellota) . Journal of Natural summer-autumn reproductive period (Fig. 4). History, 22: 175-197. Two possible explanations suggest themselves: Healy, B, and M. O'Neill 1984 The life cycle and popula- 1) juveniles grew more slowly during autumn tion dynamics of Idotea pelagica and I, granulosa and winter than during spring and summer, 2) (Isopoda: Valvifera) in south-east Ireland. Journal juveniles produced by females with a longer re- of the Marine Biological Association of the United productive period were introduced into this Kingdom, 64: 21-33. study site. Holdich, D. M. 1968 Reproduction, growth and The two cohorts produced in these two repro- bionomics of Dynamene bidentata (Crustacea: ductive periods may have had different Isopoda). Journal of Zoology London, 156: 137-153. longevities, 5 - 6 months (April - October) for Holdich, D. M. 1970 The distribution and habitat pref- the spring cohort and 7-10 months (September erences of the Afro-European species of Dynamene - July) for the autumn cohort (Fig . 4). (Crustacea: Isopoda). Journal of Natural History,

30 Life cycle of intertidal isopods

4: 419-438. T. Fukutomi 1981 An example of distribution of Holdich, D. M. 1971 Changes in physiology, structure intertidal organisms in an rocky intertidal zone near and histochemistry occurring during the life-history the Seto Marine Biological Laboratory of Kyoto Uni- of the sexually dimorphic isopod Dynamene versity I. Nanhiseibutsu, 23: 97-102 (in Japanese). bidentata (Crustacea: Peracardia) . Marine Biology, Ondo, Y. 1958a Periodic behavior of the shore isopod, 8 : 35-47. Megaligia exotica (Roux) II. Interrelations of inter- Holdich, D. M. 1976 A comparison of the ecology and nal physiological conditions and tidal rhythmic life cycles of two species of littoral isopod. Journal changes on the periodic journey. Japanese Journal of of Experimental Marine Biology and Ecology, 24: Ecology, 8: 26-34 (in Japanese with English sum- 133-149. mary). Imafuku, M. 1976 On the nocturnal behaviour of Tylos Ondo, Y. 1958b Daily rhythmic activity of Tylos granulatus Miers (Crustacea: Isopoda) . Publications granulatus IV. Characteristic movement of the shore of the Seto Marine Biological Laboratory, 23: 299- sowbug accompanied with the periodic movement of 340. waves (in comparison with Talorchestia brito). Iwasaki, K. 1994 Distribution and bed structure of the Japanese Journal of Ecology, 8: 84-90 (in Japanese two intertidal mussels, Septif er virgatus (Wieg- with English summary). mann) and Hormomya mutabilis (Gould) . Publica- Ondo, Y. 1959 Daily rhythmic activity of Tylos tions of the Seto Marine Biological Laboratory, 36: granulatus V. Studies on the mechanisms of periodic 223-247. behavior accompanied with periodic movement of Iwasaki, K. 1995a Comparison of mussel bed communi- waves. Japanese Journal of Ecology, 9: 159-167 (in ties between two intertidal mytilids Septif er virgatus Japanese with English summary). and Hormomya mutabilis. Marine Biology, 123: 109- Ondo, Y., and S. Mori 1956 Periodic behavior of the 120. shore isopod, Megaligia exotica (Roux) I. Observa- Iwasaki, K. 1995b Factors delimiting the boundary be- tions under natural conditions. Japanese Journal of tween vertically contiguous mussel beds of Septifer Ecology, 5: 161-167 (in Japanese with English sum- virgatus (Wiegmann) and Hormomya mutabilis mary). (Gould). Ecological Research, 10: 307-320. Salemaa, H. 1979 Ecology of Idotea species (Isopoda) in Johnson, W. S. 1976 Biology and population dynamics the northern Baltic. Ophelia, 18: 133-150. of the intertidal isopod Cirolana harf ordi. Marine Salemaa, H. 1987 Herbivory and microhabitat prefer- Biology, 36: 343-350. ence of Idotea spp. (Isopoda) in the northern Baltic Kensler, C. B. and D. J. Crisp 1965 The colonization of Sea. Ophelia, 27: 1-15. artificial crevices by marine invertebrates. Journal Seed R. and T. H. Suchanek 1992 Population and com- of Animal Ecology, 34: 507-516. munity ecology of Mytilus. Development of Kroer, N. 1989 Life cycle characteristics and reproduc- Aquaculture and Fish Sciences, 25: 87-169. tive patterns of Idotea spp. (Isopoda) in the Sekiguchi, H. 1982 Scavenging amphipods and isopods Limf j ord, Denmark. Ophelia, 30: 63-74. attacking the spiny lobster caught in a gill-net. Re- Macquart-Moulin, C. 1992 La migration nocturne de ports on the Fisheries Research Laboratory Mie Uni- Eurydice truncata Norman, 1868 (Isopoda, Ciro- versity, 3: 21-30. lanidae) au dessus du plateau continental et de la Sekiguchi, H. 1985 Note on the burrow of a giant deep- marge. Crustaceana, 62: 201-213 (In French with Eng- sea isopod Bathynomus doederleini (Flabellifera: lish abstract). Cirolanidae) . Proceedings of the Japanese Society of Mori, K and M. Tanaka 1989 Intertidal community Systematic Zoology, 31: 26-29. structure and environmental conditions of exposed Sekiguchi, H., Y. Yamaguchi and H. Kobayashi 1981 and sheltered rocky shores in Amakusa, Japan. Publi- Bathynomus (Isopoda: Cirolanidae) attacking sharks cations from the Amakusa Marine Biological Labo- caught in a gill-net. Bulletin of the Faculty of Fish- ratory, Kyusyu University, 10: 41-64. ery, Mie University, 8: 11-17. Morton, J. E. 1954 The crevice faunas of the upper Sekiguchi, H., Y. Yamaguchi and H. Kobayashi 1982 intertidal zone at Wembury. Journal of the Marine Geographical distribution of scavenging giant Biological Association of the United Kingdom, 33: isopods Bathynomids in the northwestern Pacific. 187-224. Bulletin of the Japanese Society of Scientific Fisher- Ohsako, Y., K. Iwasaki, K. Satake, S. Sakimukai, and ies, 48: 499-504.

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Shafir, A. and J. G. Field 1980 Importance of a small of the aquatic isopod Idotea baltica. Annales carnivorous isopod in energy transfer. Marine Ecol- Zoologici Fennici, 25: 145-151. ogy Progress Series, 3: 203-215. Wieser, W. 1962 Adaptation of two intertidal isopods. Stepien, C. A, and R. C. Brusca 1985 Nocturnal attacks I. Respiration and feeding in Naesa bidentata on nearshore fishes in southern California by crusta- (Adams) (Sphaeromatidae) . Journal of the Marine cean zooplankton. Marine Ecology Progress Series, Biological Association of the United Kingdom, 42: 25: 91-105. 665-682. Suchanek, T. H. 1985 Mussels and their role in structur- Wieser, W. 1963 Adaptation of two intertidal isopods. ing rocky shore communities. In, The Ecology of II. Comparison between Campecopea hirsuta and Rocky Coasts, Moore, P. G. and R. Seed (eds.), Naesa bidentata (Sphaeromatidae) . Journal of the Hodder and Stoughton, London, pp. 70-96. Marine Biological Association of the United King- Tsuchiya, M. 1979 Quantitative survey of intertidal or- dom, 43: 97-112. ganisms on rocky shores in Mutsu Bay, with special Willows, R. I. 1987a Population dynamics and life his- reference to the influence of wave action. Bulletin of tory of two contrasting populations of Ligia oceania the Marine Biological Station of Asamushi, Tohoku (Crustacea: Oniscidea) in the rocky supralittoral. University, 16: 69-86. Journal of Animal Ecology, 56: 315-330. Tsuchiya, M. and M. Nishihira 1985 Islands of Mytilus Willows, R. I. 1987b Intrapopulation variation in the as a habitat for small intertidal animals : Effect of reproductive characteristics of two populations of island size on community structure. Marine Ecology Ligia oceania (Crustacea: Oniscidea) . Journal of Progress Series, 25: 71-81. Animal Ecology, 56: 315-330. Tsuchiya, M. and M. Nishihira 1986 Islands of Mytilus Woodin, S. A. 1976 Adult-larval interactions in dense as a habitat for small intertidal animals : Effect of inf aunal assemblages : patterns of abundance. Jour- Mytilus age structure on the species composition of nal of Marine Research, 34: 24-41. the associated fauna and community organization. Marine Ecology Progress Series, 31: 171-178. Address Tuomi, J., V. Jormalainen and H. Ilvessalo 1988 Keiji Iwasaki : Institute for Natural Science, Nara Uni- Growth, food consumption and reproductive tactics versity, 1500 Misasagi-cho, Nara 631, Japan.

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