The Growth, Reproduction and Body Color Pattern of Cleantiella Isopus (Isopoda: Valvifera) in Hakodate Bay, Japan

CRUSTACEAN RESEARCH, NO. 41: 1–10, 2012

The growth, reproduction and body color pattern of Cleantiella isopus (Isopoda: Valvifera) in Hakodate Bay, Japan

Tomohiro Takahashi and Seiji Goshima

A b s t r a c t . — We studied the growth, cycling in the intertidal and subtidal areas. reproduction and body color pattern of the Most isopod studies focus on the life marine isopod Cleantiella isopus in Hakodate Bay, cycle, feeding habits and mate choice; Japan from May 2009 to July 2010. Individuals almost all are exclusively on European were collected every month and the sex, body species of the genus Idotea (Naylor, 1955a, length, color pattern, number of eggs per clutch b; Jormalainen et al., 1992). The breeding and developmental stage of embryos for ovigerous period and its length differ among species females were recorded. Five body color patterns or conspecific populations that occupy were identified in C. isopus at Hakodate Bay, and different habitats (Naylor, 1955b; Sheader, their composition was maintained throughout 1977; Salemaa, 1979; Healy & O’Neill, the year. Breeding females (guarded by a male 1984). Although about 20 species have been or carrying eggs) were observed in the field from reported in Japan, as far as we know, there February to August. Newly recruited individuals is only one study about the feeding habit of were first observed in July and grew to mature size by the next breeding season, indicating a Idotea ochotensis (Suzuki et al., 2002). Isopod lifespan of 13–15 months. Precopulatory mate species are common in northern Japan and guarding in which a male holds a female using his play an important role in the community of pereopods was observed. There was no correlation the littoral zone, but their basic biology such between body lengths of guarding males and as life cycle, growth, and reproduction are guarded females. The female reproductive cycle almost unknown. Cleantiella isopus, belonging was synchronous, and two defined reproductive to the family Idoteidae, is distributed from events were detected during the breeding periods, Hokkaido to Kyushu in Japan and inhabits indicating that females bred twice or more during spaces under stones or algae in the intertidal- a lifetime. subtidal zone (Nunomura, 1995, 2011). Body shape is rectangular, and the lateral margins are parallel in the male, while in the female Introduction they are slightly curved. There are several Isopods are an important component of body color patterns (e.g. green, white, yellow coastal ecosystems and fish diets (Sywula, and brown). Antennae consist of five scapes 1964; Strong & Daborn, 1979). Four families with a flagellum, and often the tip is white and about 550 species are known in the in color. The posterior edge of the telson world, and three families and 20 species is slightly rounded and triangular in shape have been reported in Japan (Nunomura, (Nunomura, 1995). 1995). Their feeding habits vary among The aim of this study was to clarify the species, and there are species which forage basic biology of growth and reproduction of algae, seagrass, and animal or animal debris C. isopus and compare it with related species (Kjennerud, 1950; Naylor, 1955a). The living in European regions. In addition, feeding behavior of herbivorous species we categorized the body color pattern of promotes fracture and decomposition of dead C. isopus and considered the relationship plants (Robertson & Mann, 1980). Therefore between body color and habitat. they may play an important role in material LIFE HISTORY OF ISOPOD CLEANTIELLA ISOPUS 3 2 T. TAKAHASHI & S. GOSHIMA 2 animals to the laboratory and measured body Materials and Methods length using a caliper and then proceeded Sampling was carried out every month to determine the sex, number of eggs per from May 2009 to July 2010 in Kattoshi (41° clutch and developmental stages of embryos 44’ N, 140° 36’ E), located on the west side for ovigerous females. Body length was of Hakodate Bay, southwestern Hokkaido. measured as the distance from the anterior The sampling site was at the exposed rocky border of the cephalon to the posterior shore during low tide. The bottom of the border of the telson. All animals over 10 tide pools was covered with stones of mm were sexed by presence or absence of 20–50 cm in diameter. Brown algae such as penis because only after a length of about Undaria pinnatifida, Saccharina japonica and 10 mm was the character recognizable. The Sargassum fulvellum and seagrass such as size frequency distribution of individuals Phyllospadix iwatensis lived on the bedrock was observed and cohorts (age-class) were area without stones. The maximum water identified by approximate body length in temperature recorded was 21°C in July 2010, order to follow changes in mean size of each while the minimum water temperature was cohort. 3°C in February 2010 (Fig. 1). We found C. We defined a functional mature male isopus almost exclusively at our sampling as one that guards a female and functional site, however C. strasseni was also found, mature female as the individual that is but only three times throughout the present guarded by the male or the individual having study. Idotea ochotensis, which is distributed a brood pouch. in various regions of Hokkaido (Nunomura, The developmental stages of embryos Fig. 2. Body color patterns of Cleantiella isopus. A: brown, B: brown-white line, C: brown-white spots, D: light 2011), was never found at the present within the brood pouch were defined as brown, and E: green type. sampling site. follows. Stage I: spherical-ovoid egg of Sampling was conducted during every 0.9 mm in diameter surrounded by two spring low tide for two hours. Isopods were membranes called “chorion” and “vitelline found frequently attached to the bottom of membrane”, stage II: elongate embryo of penis appeared then as well. Males reached stones in tide pools. Sampling was conducted 1.2–2.0 mm in length which has molted 14.3 mm in body length, while females during daytime from May 7 to October 1 in from these two membranes and surrounded Results attained 12.8 mm by August; 16.7 mm in 2009 and from March 23 to July 27 in 2010, by a single membrane called “embryonic Growth males and 14.8 mm in females by September and during nighttime from October 20 in membrane”, and stage III: the embryo of 2.5– The size composition of the sample is and finally 21.5 mm in both sexes by 2009 to February 27 in 2010. We brought 4.0 mm in length which has moulted from illustrated in Fig. 3. In both 2009 and 2010, December (Fig. 4). Growth was suspended in embryonic membrane. Stage III embryos the range of male body length was greater February when water temperature dropped to were not included in the number of eggs than that of females throughout the year 3ºC (Fig. 1). because of the possibility that some embryos (Fig. 3). The population was composed of Breeding females appeared in mid- already escaped from the brood pouch. only large males and females in May 2009 February when minimum water temperature Cleantiella isopus showed several body when we started the study. Newly recruited (3ºC) was recorded. Both sexes reached 25 color patterns. These patterns were easily juveniles were first confirmed in July 7 mm in average length, and most females distinguishable and we divided them into five 2009 (9.6 mm in average length), and two carried eggs by mid-March. Release of categories (Fig. 2). “Brown” is an individual distinct cohorts were detected during July juveniles from the brood pouch occurred that has dark brown body color and often to August 2009 and also in July 2010. The from May to July when they were around has a small white spot on the third thoracic sex of these newly recruited individuals was 5 mm in body length. Large individuals segment. “Brown-white line” is a “brown” unknown because sexual organs (appendages) decreased from July and disappeared by individual whose entire third thoracic were not visible. Both larger males and October in 2009. The results obtained segment is white color. “Brown-white spots” females decreased in number from July and indicate that C. isopus has a lifespan of 13–15 is an individual that has irregular white spots disappeared by October. The sex ratio (male months. over a brown background throughout the /female) was greatly biased toward female Reproduction (0.3–0.6, mean = 0.5) from May to August. Fig. 1. Monthly mean surface water temperature at whole body. “Light brown” is an individual Precopulatory mate guarding was Kattoshi area (open squares) and those in the tide pool that has light brown body color. “Green” is The newly recruited juveniles were first observed, in which a male mounts and (filled squares). an individual that has whitish-green body confirmed and grew to more than 10 mm in restrains a female; grasping her body by color and a black head. average length in July 2009 and 2010 (Figs. using his pereopods (Fig. 5A). Females shed 3, 4) and individuals which had a developed the posterior half of the exoskeleton and then LIFE HISTORY OF ISOPOD CLEANTIELLA ISOPUS 3 2 T. TAKAHASHI & S. GOSHIMA 3 animals to the laboratory and measured body Materials and Methods length using a caliper and then proceeded Sampling was carried out every month to determine the sex, number of eggs per from May 2009 to July 2010 in Kattoshi (41° clutch and developmental stages of embryos 44’ N, 140° 36’ E), located on the west side for ovigerous females. Body length was of Hakodate Bay, southwestern Hokkaido. measured as the distance from the anterior The sampling site was at the exposed rocky border of the cephalon to the posterior shore during low tide. The bottom of the border of the telson. All animals over 10 tide pools was covered with stones of mm were sexed by presence or absence of 20–50 cm in diameter. Brown algae such as penis because only after a length of about Undaria pinnatifida, Saccharina japonica and 10 mm was the character recognizable. The Sargassum fulvellum and seagrass such as size frequency distribution of individuals Phyllospadix iwatensis lived on the bedrock was observed and cohorts (age-class) were area without stones. The maximum water identified by approximate body length in temperature recorded was 21°C in July 2010, order to follow changes in mean size of each while the minimum water temperature was cohort. 3°C in February 2010 (Fig. 1). We found C. We defined a functional mature male isopus almost exclusively at our sampling as one that guards a female and functional site, however C. strasseni was also found, mature female as the individual that is but only three times throughout the present guarded by the male or the individual having study. Idotea ochotensis, which is distributed a brood pouch. in various regions of Hokkaido (Nunomura, The developmental stages of embryos Fig. 2. Body color patterns of Cleantiella isopus. A: brown, B: brown-white line, C: brown-white spots, D: light 2011), was never found at the present within the brood pouch were defined as brown, and E: green type. sampling site. follows. Stage I: spherical-ovoid egg of Sampling was conducted during every 0.9 mm in diameter surrounded by two spring low tide for two hours. Isopods were membranes called “chorion” and “vitelline found frequently attached to the bottom of membrane”, stage II: elongate embryo of penis appeared then as well. Males reached stones in tide pools. Sampling was conducted 1.2–2.0 mm in length which has molted 14.3 mm in body length, while females during daytime from May 7 to October 1 in from these two membranes and surrounded Results attained 12.8 mm by August; 16.7 mm in 2009 and from March 23 to July 27 in 2010, by a single membrane called “embryonic Growth males and 14.8 mm in females by September and during nighttime from October 20 in membrane”, and stage III: the embryo of 2.5– The size composition of the sample is and finally 21.5 mm in both sexes by 2009 to February 27 in 2010. We brought 4.0 mm in length which has moulted from illustrated in Fig. 3. In both 2009 and 2010, December (Fig. 4). Growth was suspended in embryonic membrane. Stage III embryos the range of male body length was greater February when water temperature dropped to were not included in the number of eggs than that of females throughout the year 3ºC (Fig. 1). because of the possibility that some embryos (Fig. 3). The population was composed of Breeding females appeared in mid- already escaped from the brood pouch. only large males and females in May 2009 February when minimum water temperature Cleantiella isopus showed several body when we started the study. Newly recruited (3ºC) was recorded. Both sexes reached 25 color patterns. These patterns were easily juveniles were first confirmed in July 7 mm in average length, and most females distinguishable and we divided them into five 2009 (9.6 mm in average length), and two carried eggs by mid-March. Release of categories (Fig. 2). “Brown” is an individual distinct cohorts were detected during July juveniles from the brood pouch occurred that has dark brown body color and often to August 2009 and also in July 2010. The from May to July when they were around has a small white spot on the third thoracic sex of these newly recruited individuals was 5 mm in body length. Large individuals segment. “Brown-white line” is a “brown” unknown because sexual organs (appendages) decreased from July and disappeared by individual whose entire third thoracic were not visible. Both larger males and October in 2009. The results obtained segment is white color. “Brown-white spots” females decreased in number from July and indicate that C. isopus has a lifespan of 13–15 is an individual that has irregular white spots disappeared by October. The sex ratio (male months. over a brown background throughout the /female) was greatly biased toward female Reproduction (0.3–0.6, mean = 0.5) from May to August. Fig. 1. Monthly mean surface water temperature at whole body. “Light brown” is an individual Precopulatory mate guarding was Kattoshi area (open squares) and those in the tide pool that has light brown body color. “Green” is The newly recruited juveniles were first observed, in which a male mounts and (filled squares). an individual that has whitish-green body confirmed and grew to more than 10 mm in restrains a female; grasping her body by color and a black head. average length in July 2009 and 2010 (Figs. using his pereopods (Fig. 5A). Females shed 3, 4) and individuals which had a developed the posterior half of the exoskeleton and then LIFE HISTORY OF ISOPOD CLEANTIELLA ISOPUS 5 4 T. TAKAHASHI & S. GOSHIMA 4

Fig. 4. Growth of males (filled circles) and females (open circles) of Cleantiella isopus born in 2008, and released juveniles (sex unknown, filled triangle), males (filled squares) and females (open squares) born in 2009.

Females that had begun breeding (guarded by male or carried eggs) were found from February to August in Hakodate Bay. Females increased their body width around the third thoracic segment as the breeding period approached as a result of development of the brood pouch. More than 95% of females had begun breeding from March to June. The number of eggs incubated in the brood pouch varied greatly among females (23–239, mean = 106). The number of eggs correlated with female body length (r2 = 0.392, student’s t-test, P < 0.05), but they varied widely among the same body size class (Fig. 7). The maximum size of embryo Fig. 3. Size frequency distributions of males (left, white bar), juveniles (right, sex unknown, white bar), no in the brood pouch was 6.0 mm. breeding females (right, gray bar), and breeding females (right, black bar) of Cleantiella isopus. Female reproductive cycle from guarding to release of juveniles was synchronized, and two well defined cycles were observed. The first cycle was from mid-February to late the anterior portion during guarding. The and 23.9 mm in females. The minimum size May (recorded in 2010) and the second one brood pouch that was covered with oostegites of individuals which mated was 24.7 mm was from late May to early July (recorded was formed after molting, and females laid for males and 19.6 mm for females. There in 2009) (Fig. 8). In this reproductive event eggs into it (Fig. 5B). Guarding males were was no correlation in body length between (2009 and 2010) all guarded females already Fig. 5. A: Precopulatory mate guarding behavior of always larger than females (Fig. 6); their guarding males and guarded females (r2 = had a brood pouch. Thus, it was considered Cleantiella isopus. Upper is a male and lower is a mean body length was 31.7 mm in males 0.0175, student’s t-test, P > 0.05) (Fig. 6). as the second cycle because of the period and female. B: Brood pouch of female. LIFE HISTORY OF ISOPOD CLEANTIELLA ISOPUS 5 4 T. TAKAHASHI & S. GOSHIMA 5

was 113. pattern percentages did not vary greatly A similar trend has been shown for Idotea In the second cycle, guarding pairs among body length classes (Fig. 9). Body species in the northern Baltic Sea (Salemaa, were observed in late May. These females color was confirmed after stage III of embryo 1979), but there are no similar reports for already had a brood pouch before copulation, development even within the brood pouch Idotea species living in other regions. The and some females guarded by males had (approx. 3.5 mm body length). However, sex ratio was greatly biased toward females developing embryos in the brood pouch. The embryo body color pattern was divided into from May in the cohort born in 2008. This females with an empty brood pouch or with only two patterns: brown series and green temporary bias has been also reported in stage I or stage II embryos were observed series, because their body color was light at in early June. The females with stage the time. III embryos or empty brood pouch were No difference in habitat use was observed observed again in late June (Fig. 8). Mean between individuals of different body color. body length of the females which bred in the Individuals of different color pattern were second cycle was 24.9 mm and mean number observed co-habiting the same refuge under Fig. 6. Body length of males and females of Cleantiella isopus performing mate guarding. Broken line means of eggs per female was 113. The number of stones; a heterogeneous distribution of such the same body length of both sexes. individuals decreased dramatically after the color morphs was consistent throughout the second reproductive cycle finished, but some study. surviving individuals started to breed once more in July 2009 and 2010 (Fig. 8). Mean Discussion presence of the brood pouch of females. body length of the females which bred after Guarding pairs were observed from early the second cycle was 24.8 mm, and mean Compared with early studies, the general February to early April in the first cycle, and number of eggs per female was 45.3. Number biology of C. isopus does not differ greatly then all guarded females had a brood pouch of eggs was much smaller than the first and from other species of Idotea. The lifespan after copulation. The beginning period of the second cycles. of C. isopus was estimated at 13–15 months reproduction differed up to a month among The first cycle was longer than the in the present study, while it is known that individuals. All of the embryos in the brood second one even allowing for the difference I. baltica also has a lifespan within 13–15 pouch were stage I until early April. Then in the onset period (first cycle: three and months, and the lifespan of I. chelipes and I. granulosa are about one year in the northern Fig. 8. Reproductive cycle of Cleantiella isopus. stage I and stage II embryos were observed a half months, second cycle: one month). Percentage of females guarded by males (A), females until early May. In late May, most females In addition, there was a difference of one Baltic Sea (Salemaa, 1979). The cessation of carrying stage I (white), stage II (gray) and stage III had stage III embryos or an empty brood and a half months of incubation between growth in C. isopus from February may be embryos (black) (B), and females with empty brood pouch. Eighteen out of the 65 females the females which started to breed in caused by energy investment in reproduction. pouch indicating just after release of juveniles (C). captured in late May were guarded by males early February and in late March of first (Fig. 8). Mean body length of the females cycle. Variation of the developmental rate which bred in the first cycle was 25.1 mm originated mainly at stage I. While the and mean number of eggs in the brood pouch incubation period of the females that joined the second reproductive cycle took about a month, the females which started to breed in the first cycle (early February) spent about two months to transition from oviposition to stage II.

Body color pattern The most frequent pattern was “brown” in both sexes (34.6% males and 24.1% females). While “light brown” (9.3%) and “green” (9.7%) were less frequent in males. On the other hand, these patterns were frequent in females (18.2% and 21.3%, respectively). This composition did not vary greatly throughout the year, although the percentages of “light brown” and “green” Fig. 7. The relationship between body length of females tended to decrease slightly with increasing and number of eggs in Cleantiella isopus. body length in males. The other body color Fig. 9. The composition of body color patterns of Cleantiella isopus collected during the present study period. LIFELIFE HISTORY HISTORY OF OF ISOPOD ISOPOD CLEANTIELLA CLEANTIELLA ISOPUS ISOPUS 77 6 T. TAKAHASHI & S. GOSHIMA 7 LIFE HISTORY OF ISOPOD CLEANTIELLA ISOPUS 7 was 113. patternpattern percentagespercentages diddid notnot varyvary greatlygreatly AA similarsimilar trendtrend hashas beenbeen shownshown forfor IdoteaIdotea In the second cycle, guarding pairs pattern percentages didamongamong not vary bodybody greatly lengthlength classesclassesA similar (Fig.(Fig. trend 9).9). BodyBodyhas been speciesspecies shown inin for thethe Idotea northernnorthern BalticBaltic SeaSea (Salemaa,(Salemaa, were observed in late May. These females among body length classescolorcolor (Fig. was was confirmed 9).confirmed Body afterafterspecies stagestage in IIIIII the ofof northern embryoembryo Baltic1979),1979), Sea butbut (Salemaa, therethere areare nono similarsimilar reportsreports forfor already had a brood pouch before copulation, color was confirmed afterdevelopmentdevelopment stage III of embryo eveneven within within1979), thethe but broodbrood there pouchpouch are no IdoteasimilarIdotea species speciesreports living livingfor inin otherother regions.regions. TheThe and some females guarded by males had development even within(approx.(approx. the brood 3.53.5 pouch mmmm bodybody Idotea length).length). species However,However, living in sexothersex ratioratio regions. waswas greatlygreatly The biasedbiased towardtoward femalesfemales developing embryos in the brood pouch. The (approx. 3.5 mm body embryolength).embryo body bodyHowever, colorcolor patternpatternsex ratio waswas dividedwasdivided greatly intointo biased fromfrom toward MayMay ininfemales thethe cohortcohort bornborn inin 2008.2008. ThisThis females with an empty brood pouch or with embryo body color patternonlyonly was twotwo divided patterns:patterns: into brownbrownfrom series seriesMay inandand the greengreen cohort temporaryborntemporary in 2008. biasbias This hashas beenbeen alsoalso reportedreported inin stage I or stage II embryos were observed only two patterns: brownseries,series, series becausebecause and green theirtheir bodybodytemporary colorcolor waswas bias lightlight has atat been also reported in in early June. The females with stage series, because their bodythethe color time. time. was light at III embryos or empty brood pouch were the time. NoNo differencedifference inin habitathabitat useuse waswas observedobserved observed again in late June (Fig. 8). Mean No difference in habitatbetweenbetween use was individualsindividuals observed ofof differentdifferent bodybody color.color. body length of the females which bred in the between individuals of differentIndividualsIndividuals body ofof color. differentdifferent colorcolor patternpattern werewere second cycle was 24.9 mm and mean number observedobserved co-habitingco-habiting thethe samesame refugerefuge underunder Fig. 6. Body length of males and females of Cleantiella Individuals of different color pattern were isopus performing mate guarding. Broken line means of eggs per female was 113. The number of observed co-habiting thestones; stones;same refuge aa heterogeneousheterogeneous under distributiondistribution ofof suchsuch the same body length of both sexes. individuals decreased dramatically after the stones; a heterogeneous distributioncolorcolor morphsmorphs of was wassuch consistentconsistent throughoutthroughout thethe second reproductive cycle finished, but some color morphs was consistentstudy.study. throughout the surviving individuals started to breed once study. more in July 2009 and 2010 (Fig. 8). Mean DiscussionDiscussion presence of the brood pouch of females. body length of the females which bred after Guarding pairs were observed from early the second cycle was 24.8 mm, and mean Discussion ComparedCompared withwith earlyearly studies,studies, thethe generalgeneral February to early April in the first cycle, and number of eggs per female was 45.3. Number Compared with early biologystudies,biology oftheof C. C.general isopusisopus doesdoes notnot differdiffer greatlygreatly then all guarded females had a brood pouch of eggs was much smaller than the first and biology of C. isopus doesfromfrom not otherdifferother speciesspeciesgreatly ofof IdoteaIdotea.. TheThe lifespanlifespan after copulation. The beginning period of the second cycles. from other species of Idoteaofof C.C. . isopusisopusThe lifespan waswas estimatedestimated atat 13–1513–15 monthsmonths reproduction differed up to a month among The first cycle was longer than the of C. isopus was estimatedinin atthethe 13–15 presentpresent months study,study, whilewhile itit isis knownknown thatthat individuals. All of the embryos in the brood second one even allowing for the difference in the present study, whileI.I. baltica balticait is known alsoalso hashasthat a a lifespanlifespan withinwithin 13–1513–15 pouch were stage I until early April. Then in the onset period (first cycle: three and I. baltica also has a lifespanmonths,months, within andand the13–15the lifespanlifespan ofof I.I. chelipeschelipes andand I.I. granulosagranulosa areare aboutabout oneone yearyear inin thethe northernnorthern Fig.Fig. 8.8. ReproductiveReproductive cyclecycle ofof CleantiellaCleantiella isopusisopus. . stage I and stage II embryos were observed a half months, second cycle: one month). months, and the lifespan of I. chelipes and I. PercentagePercentage ofof femalesfemales guardedguarded byby malesmales (A),(A), femalesfemales until early May. In late May, most females In addition, there was a difference of one granulosa are about one yearBalticBaltic in Sea Seathe (Salemaa,northern(Salemaa, 1979).1979).Fig. 8. TheThe Reproductive cessationcessation ofcycleof carryingofcarrying Cleantiella stagestage I I isopus (white),(white),. stagestage IIII (gray)(gray) andand stagestage IIIIII had stage III embryos or an empty brood and a half months of incubation between Baltic Sea (Salemaa, 1979).growthgrowth The cessationinin C.C. isopusisopus of fromfromPercentage FebruaryFebruary of females maymay guardedbebe embryos embryosby males (black)(black) (A), females (B),(B), andand femalesfemales withwith emptyempty broodbrood causedcaused by by energy energy investment investmentcarrying in in stage reproduction. reproduction. I (white), stage pouch pouchII (gray) indicating indicating and stage just just after IIIafter release release of of juveniles juveniles (C). (C). pouch. Eighteen out of the 65 females the females which started to breed in growth in C. isopus from February may be embryos (black) (B), and females with empty brood captured in late May were guarded by males early February and in late March of first caused by energy investment in reproduction. pouch indicating just after release of juveniles (C). (Fig. 8). Mean body length of the females cycle. Variation of the developmental rate which bred in the first cycle was 25.1 mm originated mainly at stage I. While the and mean number of eggs in the brood pouch incubation period of the females that joined the second reproductive cycle took about a month, the females which started to breed in the first cycle (early February) spent about two months to transition from oviposition to stage II.

Idotea species (Sheader, 1977; Salemaa, However, it was confirmed for C. isopus around 3°C and it was the lowest throughout 1979; Healy & O’Neill, 1984). Healy & that there was a defined breeding period in the year. Water temperatures during the O’Neill (1984) reported that males died soon Hakodate Bay, which is located at far lower breeding period of European species are after copulation, which might contribute to latitude than the European regions mentioned often over 6°C, while it was very low, about the sex ratio shift in the population. Variation earlier; although C. isopus belongs to a 3°C, in Hakodate Bay. The development of of male’s size distribution was also observed different genus of Valvifera, and there is a embryos was suppressed or even stopped in other Idotea species (Sheader, 1977; regional difference between the Atlantic and by the low water temperature in the first Healy & O’Neill, 1984), but the cause and the Pacific Oceans. cycle, thus the duration of the first cycle was present study Sheader (1977) Naylor (1955) Healy & O’Neill (1984) Healy & O’Neill (1984) Salemaa (1979) Reference significance were unknown. The difference in breeding period and extended. Stage II embryos were observed Precopulatory mate guarding is widely lifetime breeding times may be caused by only after water temperature started to known within Valvifera (Sheader, 1977; the difference in water temperature. Water increase in April. Salemaa, 1979; Jormalainen et al., 1992). temperature, day length and salinity are It is possible that single lifetime breeding 2 2 2 1 Mean number of eggs per female in C. isopus important factors which determine the in I. baltica from the Baltic Sea, where 2 or more 1 or more was similar to that of other isopod species breeding period of animals, and they are minimum water temperature is similar to that Breeding time (Salemaa, 1979), and the positive correlation intricately linked with each other (Orton, of Hakodate Bay, is caused by an extended between number of eggs and female body 1920). Above all, water temperature is low water temperature period that restricts length is also reported for other isopod considered as the major factor mediating juvenile’s growth. While C. isopus grew species (Sheader, 1977; Salemaa, 1979). In reproductive strategies. Water temperature continually throughout a long winter, the C. isopus, guarding males were always larger affects the amount of food resources such growth of I. baltica stops from November to than females, and there was no correlation as phytoplankton, and in turn availability of March and then they grow rapidly; breeding

April-August in body length between guarding males and food resources affects animal growth and with increasing water temperature (Salemaa, June-August throughout year throughout year throughout year February-August Breeding period guarded females (Fig. 6) indicating non size- reproduction. The availability of plankton is 1979). Offspring born in July grow rapidly assortative mating; a similar trend was also especially important for the animals living in until September when water temperature reported in I. pelagica (Healy & O’Neill, high latitude, and their growth and breeding starts to decrease. So it is difficult for them 1984). cycle are coincident with the period from to store energy to produce several broods. – 16°C 14°C 14°C 23°C 17°C

(Max) Habitat environments and reproductive spring to summer when phytoplankton The ability of C. isopus to sustain continuous characters of European Idotea species and bloom occurs (Johnson et al., 2001). The growth throughout winter, in Hakodate C. isopus revealed in the present study lowest water temperatures of middle England Bay, is the main source of the difference in are shown in Table 1. The northernmost and southeastern Ireland where isopods lifetime reproductive potential between these distribution region was the northern Baltic breed throughout the year are 8°C and 6°C, isopod species. – 8°C 6°C 6°C 3°C Water temperature Water 0°C (Min) Sea (northern latitude of 59°50’) and the respectively. The related species I. baltica Cleantiella isopus has several body southernmost region was southeastern living in the Baltic Sea starts to breed after color patterns in Hakodate Bay. Lee (1966) the temperature reaches 10°C (Salemaa, Ireland (northern latitude of 52°10’). There reported I. montereyensis change their body are large differences in latitude between 1979). In Hakodate Bay, the maximum water color to match the background color of their these regions and Hakodate Bay (latitude 41° temperature (21°C) was higher. In contrast, habitat. However in C. isopus, individuals Latitude 54°05’N 52°10’N 52°10’N 41°44’N 59°50’N 55°02’N 44’ N). There is a distinct breeding period the lowest water temperature (3°C) matched of each body color pattern attached to the in the northern Baltic Sea and northeastern the lowest water temperature of the Baltic same rocks and seaweeds, and no clear England, and breeding occurs throughout Sea (Salemaa, 1979). Healy & O’Neill (1984) relationship between body color pattern and the year in middle England and southeastern have shown that low temperature is critical living substrate was found. In addition, the Ireland although there are some peaks. If we for isopods and their activity drops when the composition of their color pattern did not look at the lifetime breeding of isopods in water temperature falls below 6°C. Therefore vary greatly throughout a year. Therefore, each region, it occurs once in the Baltic Sea the defined breeding periods of isopods living the body color patterns may not change and twice in other regions. In northeastern in the Baltic Sea and Hakodate Bay are likely with growth of an individual. The adaptive

Locality England, about one third of the individuals caused by low temperature which suppresses significance of several body color patterns Isle of Man southeastern Ireland southeastern Ireland Hakodate Bay northern Baltic Sea northeastern England produced a second brood (Sheader, 1977). growth and breeding. in this species remains unknown. Further This suggests that defined breeding periods Water temperature also affects embryo studies are needed to clarify its function and disappear as the latitude of habitat decreases. development and juvenile growth. Most significance. In this respect, mate choice This trend is also observed in many species, likely, the difference in embryonic studies as a function of body color pattern for example, loliginid squids Alloteuthis development rate among the two reproductive could prove rewarding as well as studies subulata living in low latitude (Europe) have cycles in C. isopus can be attributed to water on the survival of juveniles from different a longer breeding period than those living in temperature. The water temperature at the color patterns across annual changes in Species I. emarginata I. pelagica I. granulosa Cleantiella isopus Table 1. Habitat features and reproductive characteristics of some Idotea species Cleantiella isopus Table Idotea baltica I. pelagica higher latitude regions (Hastie et al., 2009). beginning of the first reproductive cycle was environment conditions. CRUSTACEAN RESEARCH, NO. 41: 11–18, 2012 10 T. TAKAHASHI & S. GOSHIMA 10 This study concentrated on the basic 355. biology of C. isopus in Hakodate Bay, but ———, 1955b. The life cycle of the isopod Idotea Further record of the shallow water mysid Heteromysis this species is distributed widely throughout emarginata (Fabricius). Journal of Animal proxima W. M. Tattersall, 1922 (Mysida) from the Malacca Japan (Nunomura, 1995, 2011), and it is Ecology, 24: 270–281. Nunomura, N., 1995. Isopoda. In: S. Nishimura (ed.), Strait known that the breeding period and its Guide to Seashore Animals of Japan with Color extension are different among habitats. Pictures and Keys. Vol. II, Hoikusha, Osaka, Similar studies in different regions and in 205–233. (In Japanese) other related species are necessary to reveal ———, 2011. Crustaceans No. 2, Isopoda. Special Yukio Hanamura, Ryon Siow, Alias Man and Faizul Mohd Kassim the factors that affect the particularly plastic Publication of the Toyama Science Museum, No. life history traits of isopods. Such plasticity 24. Toyama Science Museum. (In Japanese) may well be the key to the success of this Orton, J.H., 1920. Sea-temperature, breeding and distribution in marine animals. Journal of the Abstract.—Heteromysis proxima W.M. species across its latitudinal range. O.S. Tattersall, 1967; H. singaporensis O.S. Marine Biological Association of the United Tattersall, 1922 (Mysida) was first reported from Tattersall, 1967; H. (Olivemysis) thailandica Kingdom, 12: 339–366. the Gulf of Manaar, off the south-eastern coast of Fukuoka & Murano, 2002; and Heteromysis Acknowledgments Robertson, A.I. & Mann, K.H., 1980. The role India. A recent sledge net survey conducted on the sp. sensu O.S. Tattersall, 1967 (Müller, 1993; of isopods and amphipods in the initial We would like to express our appreciation north-western coast of Malaysia yielded several Fukuoka & Murano, 2002; Sawamoto & fragmentation of eelgrass detritus in Nova specimens of this little-known mysid from a to the members of the Laboratory of Scotia, Canada. Marine Biology, 59: 63–69. Fukuoka, 2005). This gives the impression sandy beach located in the mouth area of Merbok Benthology, Faculty of Fisheries, Hokkaido Salemaa, H., 1979. Ecology of Idotea species of comparatively poor heteromysid diversity University, for their advice and cooperation (Isopoda) in the northern Baltic. Ophelia, 18: River, facing the Malacca Strait. Although the in South-East Asian waters compared with during this study. We are thankful to the 133–150. Malaysian specimens have a comparatively more than 20 species that have been found anonymous reviewers and Roberto C. Sheader, M., 1977. The breeding biology of Idotea smaller body size than those recorded from in the northern part of Australia (Băcescu India, the morphological features of these Lombardo for their reviews and comments pelagica (Isopoda: Valvifera) with notes on & Bruce, 1980; Băcescu, 1983; Murano, the occurrence and biology of its parasite specimens essentially agree with the typical ones. 1988, 1998b). The fewer recorded species, that helped to improve the manuscript. Clypeoniscus hanseni (Isopoda: Epicaridea). This paper provides further information on the however, may be due to the paucity of Journal of the Marine Biological Association of morphological characteristics of H. proxima on surveys, and this region is still considered to Literature Cited the United Kingdom, 57: 659–674. the basis of newly obtained specimens and extends Strong, K.W. & Daborn G.R., 1979. Growth and be an intriguing and unstudied field for many its geographical range to the Malacca Strait. Hastie, L.C., Nyegaard, M., Collins, M.A., Moreno, energy utilization of the intertidal isopod Idotea coastal marine life forms, including mysid A., Pereira, J.M.F., Piatkowski, U., & Pierce, baltica (Pallas) (Crustacea: Isopoda). Journal of G.J., 2009. Reproductive biology of the loliginid crustaceans. Experimental Marine Biology and Ecology, 41: During the hyperbenthic crustacean squid, Alloteuthis subulata, in the north-east 101–123. Introduction Atlantic and adjacent waters. Aquatic Living Suzuki, M., Watanabe, K., & Mukai, H., 2002. The genus Heteromysis S.I. Smith, 1874 surveys conducted in the coastal waters of Resources, 22: 35–44. Feeding habits and growth of an isopod, Idotea includes a large group of mysid crustaceans north-western Malaysia since 2004, several Healy, B. & O’Neill, M., 1984. The life cycle ochotensis Brandt, in Akkeshi Bay, Hokkaido, (Mysida), currently numbering some 80 specimens of the little-known heteromysid and population dynamics of Idotea pelagica northern Japan. Japanese Journal of Benthology, species world-wide (Anderson, 2010; Price H. proxima W.M. Tattersall, 1922 were found and I. granulosa (Isopoda: Valvifera) in south- 57: 13–20. (In Japanese with English abstract) & Heard, 2011). Heteromysis is regarded as at a shallow depth in the mouth of Merbok east Ireland. Journal of the Marine Biological Sywula, T., 1964. A study of the taxonomy, ecology Association of the United Kingdom, 64: 21–33. a highly adaptable group which is able to River, north-western Peninsular Malaysia. and geographical distribution of species of the thrive in diverse habitats, from open waters This rare heteromysid species is re-described Johnson, W.S., Stevens, M., & Watling, L., 2001. genus Idotea Fabricius (Isopoda, Crustacea) in the Reproduction and development of marine Polish Baltic. Ecological and zoogeographical to cryptic environments such as submarine on the basis of newly captured material, peracaridans. Advances in Marine Biology, 39: part. Bulletin de la Société des amis des sciences caves; some are even known to live in a providing supplementary information on 105–260. et des letters de Poznań (série B), 4: 173–199. commensal lifestyle with a variety of marine their morphology and as a new distribution Jormalainen, V., Tuomi, J. & Merilaita, S., 1992. invertebrates (Tattersall, 1967; Müller, 1993; record. Mate choice for male and female size in aquatic Fukuoka, 2005). Morphologically, this genus The body length (BL) was measured isopod Idotea baltica. Annales Zoologici Fennici, Addresses: (TT, SG) Graduate School of 29: 161–167. is remarkable among the mysids, as they from the anterior end of the rostral plate to Kjennerud, J., 1950. Ecological observations on Fisheries Sciences, Hokkaido University, 3-1-1 normally have a sub-chelate endopod, similar the posterior end of the telson excluding the Idotea neglecta G.O. Sars. Universiteteti Bergen. Minato-cho, Hakodate 041-8611, Japan. to those found in amphipods, in the third apical spines. The terminology in the setal/ Årbok (Naturvitenskapelig rekke), 7: 5–47. E-mails: (TT) tomohiro-takahashi@ thoracic limb. spine system followed Watling (1989). Lee, W.L., 1966. Color change and the ecology of the support99.com; (SG) [email protected]. To date, four species of Heteromysis, The specimens dealt with here have been marine isopod Idotea (Pentidotea) montereyensis ac.jp including one yet undetermined species, deposited in the National Museum of Nature Maloney, 1933. Ecology, 47: 930–941. Naylor, E., 1955a. The diet and feeding mechanism have been recorded from the Malacca Strait and Science, Tokyo (NSMT), and Fisheries Received: 17 February 2011. of Idotea. Journal of the Marine Biological and its neighbouring region: H. minuta Research Institute, Penang (FRI) Association of the United Kingdom, 34: 347– Accepted: 29 March 2012.