REPRODUCTIVE ASPECTS OF TWO ATYID SHRIMP CARIDINA SAKISHIMENSIS AND CARIDINA

TYPUS IN HEAD WATER STREAMS OF KIKAI-JIMA ISLAND, JAPAN

Anila Naz Soomro, Hiroshi Suzuki, Megumi Kitazaki, and Tomoko Yamamoto

(ANS, anilaalisoomro@yahoo.com) Department of Freshwater Biology and Fisheries, University of Sindh, Jamshoro 76080, Sindh,

Pakistan; and United Graduate School of Agricultural Science, Kagoshima University, Shimoarata 4-50-20, Kagoshima 890-0056, Japan;

(HS, correspondence, suzuki@fish.kagoshima-u.ac.jp; MK) Laboratory of Aquatic Resource Science, Faculty of Fisheries, Kagoshima

University, Shimoarata 4-50-20, Kagoshima 890-0056, Japan;

(TY) Education and Research Center for Marine Environments, Faculty of Fisheries, Kagoshima University, Shimoarata 4-50-20,

Kagoshima 890-0056, Japan

A B S T R A C T

Aspect of reproductive ecology of Caridina typus and Caridina sakishimensis were studied in six headwater streams in Kikai-jima

Island, Southern Japan. Monthly surveys were conducted from June 2005 to June 2008. Shrimp specimens were collected with a hand

scoop net. The population size of C. typus was lowest during high precipitation periods but showed immediate recovery attributed to

successful recruitment and increased following the major spawning activities, while that of C. sakishimensis remained stable throughout

the study period. The breeding season of C. sakishimensis was estimated to extend from March to November, with a main breeding

season lasting from June to September, while that of C. typus lasted from March to December. Overall ovigerous females comprised

50% to 80% of mature females of C. sakishimensis during the main spawning season, which indicated that this species remained and

spawned mainly in the headwaters. Both C. sakishimesis and C. typus carried a large number of small sized eggs. This study revealed that

the spawning season, egg size, and brood size are similar in both species; usage of headwater streams was different between C.

sakishimensis and C. typus. Caridina sakishimensis employed these water bodies as spawning ground while C. typus used them as

nursery ground.

KEY WORDS: Atyidae, Caridina, endangered species, recruitment, reproduction, spawning

DOI: 10.1651/10-3329.1

INTRODUCTION

Atyid shrimp are among the most important bioticcomponents in freshwater habitats. They use their chelae,which bear hairs and setae, for scraping, filtering, andcollecting food (algae, leaf litter, and other organic debris)(Fryer, 1960; von Rintelen et al., 2007), and as a resultinfluence detrital processing (Crowl et al., 2001). Further-more, they are known to manipulate sediment andperiphyton with the help of their setaceous chelae andpereiopods (Molina, 1987). According to Pringle and Blake(1994) atyid shrimp along with water flow play interactingroles in sediment distribution.

Studies on the population ecology of atyids haverevealed that temperature and hydrology are the mainfactors affecting their recruitment, growth, survival, andbreeding patterns (Hancock and Bunn, 1997; Dudgeon,1985; de Silva, 1988a, b). These environmental parametersstimulate and maintain gametogenesis and other reproduc-tive processes in freshwater invertebrates, and are stronglytied to latitude differences (Adiyodi and Subramoniam,1983).

Caridina typus H. Milne Edwards, 1837 has been foundas the most dominant species in Kikai-jima, while Caridinasakishimensis Fujino and Shokita, 1975 also attains asizeable density (Soomro et al., 2010). Caridina typus is acosmopolitan atyid being widely distributed in the Indo-west Pacific from South Africa through Polynesia to Japan(Bouvier, 1925; Johnson, 1960, 1961; Tiwari and Pillai,

1971; Costa, 1972; De Silva, 1982; Soomro et al., 2010). InJapan, this species has been reported in the southern,central, and northern Ryukyu Islands (Shokita, 1979) aswell as Kyushu, in the southern part of Honshu, and in thenortheast region it was found up to the Izu Peninsula. In theJapan Sea, this species is limited to the Oki Islands(Kamita, 1970).

On the other hand C. sakishimensis, an endangeredspecies (Kagoshima Red Data Book, 2003), has a restricteddistribution and is only reported in the southern and cen-tral Ryukyu Islands (Yonaguni-jima, Ishigaki-jima, andMiyako-jima in the south; and Kume-jima, Okinoerabu-jima, and Kikai-jima in the center) (Shokita, 1979; Suzukiand Satoh, 1994; Soomro et al., 2010). Thus, these twoatyid shrimp, which have different geographical distribu-tional patterns, coextensively inhabit in Kikai-jima Islandwhere there are a few surface drainage systems. Thepresent paper reports on the comparative reproductiveaspects including spawning season, fecundity, spawningground, and recruitment of C. sakishimensis and C. typus inKikai-jima Island, southern Japan.

MATERIALS AND METHODS

Kikai-jima is one of the Ryukyu Islands located in the south of Japanesemainland (latitude 28u20900N and longitude 28u20900E). Initial samplingwas conducted bi-monthly from June to November 2005 and regularmonthly sampling was conducted from December 2005 through June 2008at small pools of six stations established at Karimata-no-izumi, Shiomichi,

JOURNAL OF CRUSTACEAN BIOLOGY, 31(1): 41-49, 2011

41

Nagamine, Ooasato, Takigawa, and Urabaru (Fig. 1). Specimens were notcollected in February 2006, April 2007, and March 2008 due tounfavorable weather. Specimens were caught with a scoop net (meshsize; 1 3 1 mm) by sweeping. Generally, in life historical studies, aquaticinvertebrates are mostly killed, preserved, and brought to laboratory foridentification, sex determination, and other examinations. However, it wasillegal to kill the endangered C. sakishimensis, and preliminary studies alsorevealed that the population of C. typus was also likely to be effected byregular monthly killing. Therefore, to minimize sampling stress andmortality, specimens were observed on the spot and released back to thepools soon after identification and measurement of orbital total length(OTL) using a caliper to 0.05 mm accuracy. Due to the difficulty in sexingatyid shrimp, individuals were initially categorized into ovigerous femalesand others which included non-ovigerous females and males. Eggs carriedby females were further categorized according to embryonic stage: i.e.,eyed-egg and non eyed-egg. The preliminary survey was conducted toestimate sex ratio in different size classes of both species. In C.

sakishimensis, all individuals smaller than 8 mm OTL were juvenilesand difficult to sex due to undeveloped sexual appendages. Consequently,only individuals larger than 8 mm OTL were sexed. The maximum lengthof males was about 18 mm OTL, and all specimens above 18 mm OTLwere females. The sex ratio was 0.5 in 8-18 mm OTL size class. Similarly,C. typus individuals smaller than 8 mm OTL were also juveniles. The sexratio in 8-22 mm OTL size class of C. typus was 0.5, and all individualslarger than 22 mm OTL were females. The estimated sex ratios of bothspecies were further used to estimate the percentage of ovigerous femalesin the total samples.

In total, 19 ovigerous females of C. sakshimensis and 20 ovigerousfemales of C. typus were collected during the present study and preservedin 75% alcohol for fecundity analysis. In the laboratory, eggs wereremoved from the pleopods of ovigerous females, counted under abinocular microscope (Nikon SMZ-U), and the length and width of 20eggs from each specimen were measured using a micrometer. The OTL ofeach specimen used for fecundity estimations was measured under a

Fig. 1. Map of Kikai-jima Island with the stations, and number in parentheses indicates the altitude of each station in meters.

42 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 31, NO. 1, 2011

microscope. For the length-frequency analysis, 2 mm size classes wereconstructed. Monthly data from all six stations were pooled for thisanalysis.

Water temperature was measured on stations using a digital handy meter(YSI model 63-10, YSI, USA) in the day-time. Monthly rainfall data wasobtained from the local government office of Kikai town.

RESULTS

Monthly Changes in Water Temperature and Rain Fallin Kikai-jima

Water temperature started to rise from March and then fellafter October, while it was highest from July to Septemberand lowest from December to February during the studyperiod (Fig. 2).

In Kikai-jima a high rainfall was observed in June or Julyin every year; i.e., 527 mm in June 2005, 562 mm June2006, 297 mm July 2007 and 241 mm June 2008 (Fig. 2).

Monthly Changes in Size of Caridina sakishimensisin Kikai-jima

In total, 4485 individuals were examined during the presentstudy. The individuals ranged in size from 5.7 to 29.1 mmwith larger sizes mainly comprised of ovigerous females.However, no individuals were recorded in length class 2and 4 mm. Small individuals in 8 mm length class occurredfrom November 2005 to January 2006, July to September2006, November 2006 to January 2007 and July toSeptember 2007. Individuals in the length classes 24 to30 mm were also abundant throughout the study period(Fig. 3I, II).

Ovigerous females occurred during June to November2005, March to November 2006 and May to November

2007. The number of ovigerous females was lowest duringMarch and April, and all observed ovigerous femalescarried non-eyed eggs. Larger numbers of ovigerousfemales were observed from June to September in both2006 and 2007 and ovigerous females in the 24-30 mmlength classes were most abundant.

Monthly Changes in Size of Caridina typus in Kikai-jima

Caridina typus was the most abundant species in Kikai-jima recording the total 8939 individuals of which only1.43% (128 individuals) was ovigerous. Orbital totallengths of the smallest and largest individuals were 4.4and 34.8 mm, respectively. Small individuals in lengthclass 6-8 mm were observed frequently in August andOctober 2005, in January to March and August toDecember 2006. In 2007, the small individuals were foundin January to March and August to December, and in 2008they occurred in January and February. Numbers ofindividuals were usually high throughout the study period,but they decreased to very low numbers during June andJuly and increased again in September in each year (Fig. 4I,II).

Reproduction and Fecundity of Caridina sakishimensis andC. typus

The OTL of smallest ovigerous C. sakishimensis in Kikia-jima was 16.9 mm (Fig. 3I, II). Females carrying eggsoccurred from June through November 2005, March toNovember 2006, and April to November 2007. During Juneto September 50-80% of mature females were ovigerous(Fig. 5).

The OTL of C. sakishimensis ovigerous females used forthe fecundity analysis ranged from 17.1 to 29.1 mm withaverage of 24.5 6 2.6 (SD) mm. The number of eggs variedfrom 240 to 2942. The average number of eggs was 1502.86 777.4 (SD), and mean egg length and width were 0.49 60.04 (SD) mm and 0.28 6 0.02 (SD) mm, respectively(Table 1).

The OTL of the smallest C. typus female carrying eggswas 11.7 mm. Ovigerous females were found in Juneand August 2005, from April through October 2006, andfrom March through December 2007. The percentage ofovigerous females was less than 20% of the maturefemales, except for July 2007, when the total number ofindividuals captured was remarkably small (N 5 11)(Fig. 6).

The number of eggs in C. typus varied with body size.The smallest ovigerous female (11.7 mm) carried 126 eggs,whereas the largest (34.3 mm) one carried 3542 eggs. Themean number of eggs was 1372 6 775.7 (SD). The eggswere oval in shape and measured 0.46 6 0.03 and 0.27 60.01 mm in length and width, respectively (Table 1).

Fig. 2. Monthly rainfall in Kikai-jima and mean monthly watertemperature with standard deviations in the headwaters of Kikai-jima Island.

Table 1. Mean and standard deviation of orbital total length of ovigerous femles, egg numbers, egg length and egg width (mm) of Caridina sakishimensisand C. typus.

Species Size (OTL mm) Number of eggs Egg length Egg width

Caridina sakishimensis 24.5 6 2.6 1502.8 6 777.4 0.49 6 0.04 0.28 6 0.02Caridina typus 22.8 6 5.1 1372.0 6 775.7 0.46 6 0.03 0.27 6 0.01

SOOMRO ET AL.: REPRODUCTION OF ATYID SHRIMP IN KIKAI-JIMA 43

DISCUSSION

The spawning season of C. sakishimesis and C. typus in theheadwater streams of Kikai-jima was observed from Marchto November and March to December, respectively.Ovigerous females of C. sakishimensis showed seasonal

trends more clearly, i.e., they occurred from March toNovember, and higher percentages of ovigerous femaleswere observed during June to September. Consequently, theearly spawning period of C. sakishimensis can be deducedas lasting from March to May, while the main spawningseason occurs from June to September, when 50% to 80%

Fig. 3. Monthly changes in size frequency distribution of orbital total length of Caridina sakishimensis in Kikai-jima Island.

44 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 31, NO. 1, 2011

of mature females were ovigerous. The October andNovember period is the late spawning season.

The numbers of C. typus fluctuated periodically. Lowestnumbers were recorded during June and July in both 2006and 2007, and highest one was in August. Decline in thenumbers of individuals during June and July might indicatea rapid emigration of shrimp due to high rainfall, and an

increase in population at other times is due to recruitmentof juveniles. However, further studies along the riverstretch will ascertain the emigration or downstreamhatching migration of C. typus.

Both Caridina typus and C. sakishimensis carry largebroods. Atyids carrying small sized eggs are mostlycharacterized by high fecundity and prolonged larval

Fig. 3. Continued.

SOOMRO ET AL.: REPRODUCTION OF ATYID SHRIMP IN KIKAI-JIMA 45

Fig. 4. Monthly changes in size frequency distribution of orbital total length of Caridina typus in Kikai-jima Island.

46 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 31, NO. 1, 2011

development (Shokita, 1981; Hayashi and Hamano, 1984).Caridina zeylanica Arudpragasam and Costa, 1962 andCaridina typus with planktonic larval stages were found tocarry a large number of small sized eggs (Choy andMarshall, 1997; De Silva, 1982). Species with large sized

eggs usually have low fecundities and abbreviated or directlarval development. Caridina pristis Roux, 1931 andCaridina serrata Stimpson, 1860 are reported to havelarger sized and fewer number eggs and show directdevelopment (De Silva, 1988a; Yam and Dudgeon, 2005).

Fig. 4. Continued.

SOOMRO ET AL.: REPRODUCTION OF ATYID SHRIMP IN KIKAI-JIMA 47

High fecundity and small sized egg of both C. saksihi-mensis and C. typus suggest that both species may bediadromous. In fact, Suzuki (2001) reported diadromy in C.typus. However, detailed studies on C. sakishinemnsisalong the river stretch are required to confirm its life cycle.

Although a low number of ovigerous females of C. typusoccurred, they showed similar reproductive period as thatof C. sakishimensis. However, there is a differentiation inthe embryonic stages carried by C. sakishimensis and C.typus. The ovigerous females of the former had both noneyed-eggs and eyed-eggs, while almost all ovigerousfemales of the latter had non eyed-eggs only. Thisdifference leads us to suggest that the ovigerous femalesof C. typus move quickly downstream or into brackishwaters to spawn, using the headwaters only as a nursery,while those of C. sakishimensis stay in the headwaterstreams only until their larvae hatch. Hence, despite thesimilarity in spawning season and egg size, there is adifference between both species in the use of the headwaterstream during the different stages of breeding.

Juveniles of C. typus were found commonly during thespawning and post-spawning season (August to February),indicating continuous recruitment. On the other hand,juveniles of C. sakishimenis were observed only a fewtimes (July 2006, and August to September 2007),indicating that they recruit at a mature age.

Future studies on the detailed life cycle of C.sakishimensis and C. typus along the entire stretch of theriver will provide clearer information concerning the lifecycle and migration of these species.

ACKNOWLEDGEMENTS

We are thankful to students in the laboratory of aquatic resource sciencefor their tireless assistance during fieldwork and sampling. We are alsothank Professor Raymond T. Bauer and all who reviewed the initial draftsof the manuscript for their constructive criticism. Thanks are also due toProfessor Miguel Vazquez Archdale from our faculty for correcting theEnglish.

REFERENCES

Adiyodi, R. G., and T. Subramonium. 1983. Arthropoda-Crustacea, pp.443-495. In, K. G. Adiyodi and R. D. Adiyodi (eds.), ReproductiveBiology of Invertebrates, 1, Oogenesis, oviposition, and oosorption.John Wiley, New York.

Arudpragasam, K. D., and H. H. Costa. 1962. Atyidae of Ceylon - I.Crustaceana 4: 7-24.

Bouvier, E. L. 1925. Recherches Sur la morphlogie, les variations ladistribution geographique des crevettes de la famille des atyidae.Encyclopedia Entomology (A) 4: 1-370.

Costa, H. H. 1972. Decapoda: Caridea. Results of Austrian-Ceylonesehydrobiological mission, 1970. V. Bulletin of Fish Research Station, SriLanka (Ceylon) 23 (1, 2): 127-135.

Choy, S., and J. M. Marshal. 1997. Two new species of atyid shrimp(Crustacea: Decapoda): Atyidae) from northern Queensland anddistributional ecology of Caridina typus species-group in Australia.Memories of Queensland Museum 42: 25-36.

Crowl, T. A., W. H. McDowell, A. P. Covich, and S. L. Johnson. 2001.Freshwater shrimp effects on detrital processing and nutrients in atropical headwater stream. Ecology 82: 775-783.

De Silva, K. H. G. M. 1982. Studies on Atyidae (Decapoda: Caridae) of SriLanka. 1. On a new species a new sub species and two species new toSri Lanka. Crustaceana 43 (2): 127-141.

———. 1988a. Studies on atyidae (Decapoda, Caridea) of Sri Lanka. III.Aspect of the population ecology of Caridina simony Bouvier, 1904.Crustaceana 54: 85-103.

———. 1988b. Studies on Atyidae (Decapoda, Caridea) of Sri Lanka. IV.Aspects of population ecology of the endemic freshwater shrimpCaridina pristis, Roux, 1931. Crustaceana 54: 225-243.

Dudgeon, D. 1985. The population dynamics of some freshwater carideans(Crustacea: Decapoda) in Hong Kong with special reference ofNeocaridina serrata (Atyidae). Hydrobiologia 120: 141-149.

Environmental Conservation Section, Kagoshima Prefecture. 2003.Kagoshima Red Data Book. Top Copy, Inc., Kagoshima. 642 pp. (InJapanese)

Fryer, H. G. 1960. The feeding mechanism of some atyid prawns of genusCaridina. Transaction of the Royal Society of Edinburgh 64: 217-244.

Fujino, T. and S. Shokita. 1975. Report on some new atyid Shrimp(Crustacea, Decapoda, Caridea) from the Ryukyu Islands. Bulletin ofScience and Engineering Division, University of the Ryukyus (Maths &Natural Science) 19: 93-113.

Hancock, M. A., and S. E. Bunn. 1997. Population dynamics and lifehistory of Paratya australiensis Kemp, 1917 (Decapoda: Atyidae) inupland rainforest streams, south-eastern Queensland, Australia. Marineand Freshwater Research 48: 361-369.

Hayashi, K. I., and T. Hamano. 1984. The complete larval development ofCaridina japonica De Man reared in the laboratory. Zoological Science1: 571-589.

Fig. 5. Monthly changes in percentage of ovigerous females of Caridinasakishimensis in Kikai-jima Island.

Fig. 6. Monthly changes in percentage of ovigerous females of Caridinatypus in Kikai-jima Island.

48 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 31, NO. 1, 2011

Johnson, D. S. 1960. Some aspects of the distribution of freshwaterorganisms in Indo-Pacific area, and their relevance to the validity of theconcepts of an Oriental region in zoogeography. Proceedings of theCentennial and Biocentennial Congress of Biology, Singapore. pp.170-181.

———. 1961. Notes on the freshwater crustaceans of Malaya. 1. TheAtyidae. Bulletin Raffles Museum Singapore 26: 120-125.

Kamita, T. 1970. Studies on the fresh-water shrimps, prawns andcrawfishes of Japan. Sonoyama Syoten, Matue. 213 pp. (In Japanese)

Milne Edwards, H. 1837. Histoire naturelle des Crustac’es, comprenant 1’anatomie, la physiologie et la classification de ces animaux. Paris, 2: 1-532, atlas, pls. 1-14 bis, 15-25, 25 bis, 26-42.

Molina, F. M. L. 1987. Biologia de Potimirim brasiliana Villalobos, 1950(Crustacea, Decapoda, Atyidae). Doctoral thesis, Univeridade de SaoPaulo, Sao Paulo, Brazil.

Pringle, C. M., and G. A. Blake 1994. Quantitative effects of atyid shrimp(Decapoda: Atyidae) on the depositional environment in tropical stream:Use of electricity for experimental exclusion. Canadian Journal ofFisheries and Aquatic Science 51: 1443-1450.

Roux, J. C. 1931. Sur une nouvelle caridine de Ceylan. Revue Suisse deZoologie 38(3): 63-66.

Shokita, S. 1979. The distribution and speciation of the Inland WaterShrimp and Prawns from the Ryukyu Islands-II. Bulletin of Science andEngineering Division, University of the Ryukyus 28: 193-278.

———. 1981. Life history of the family atyidae (Decapoda: Caridae).Kaiyo to Seibutsu 3 (1): 15-23. (In Japanese)

Soomro, A. N., H. Suzuki, M. Kitazaki, and T. Kobari. (in press.) Speciescomposition of freshwater shrimp in Kikai-jima Island, Southern Japan.Journal of Crustacean Biology 39: (In Press).

Stimpson, W. 1860. Prodromus descriptionis animalium evertebratorum,quae in Expeditione ad Oceanum Pacificum Septentrionalem, a RepublicaFederata missa, Cadwaladaro Ringgold et Johanne Rodgers Ducibus,observavit et descripsit. Pars VIII. Crustacea Macrura. Proceedings of theAcademy of Natural Sciences of Philadelphia 12: 22-47.

Suzuki, H. 2001. A comment on the geological formation of the MishimaIsland, (Takeshima, Ioujima and Kuroshima) as inferred from theirfreshwater crustacean faunas. 2001. Kagoshima University, ResearchCenter for the Pacific Island, Occasional Papers 34: 137-140.

———, and M. Satoh. 1994. Kagoshima nature guide of freshwatershrimp, crayfish and crabs. Nishi Nippon Newspaper Pub., Fukuoka.137 pp. (In Japanese)

Tiwari, K. K., and R. S. Pillai. 1971. Atyid shrimp of genus Caridina H.Milne. Edwards, 1837, from the Andaman Islands (Decapoda, Caridea).Crustaceana 21: 79-91.

von Rintelen, K., T. von Rintelen, and M. Glaubrecht. 2007. Molecularphylogeny and diversification of freshwater shrimp (Decapoda, Atyidae,Caridina) from ancient Lake Poso (Sulwasi-Indonesia). The importanceof being colorful. Molecular Phylogenetics and Evolution 45: 1033-1041.

Yam, R. S. W., and D. Dudgeon. 2005. Inter and intraspecific differencesin life history and growth of Caridina spp. (Decapoda: Atyidae) in HongKong streams. Freshwater Biology 50: 2114-2128.

SOOMRO ET AL.: REPRODUCTION OF ATYID SHRIMP IN KIKAI-JIMA 49