Egg size and clutch size in three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan

Egg size and clutch size in three species of Nihonotrypaea(Decapoda: Thalassinidea: Callianassidae) from western

Kyushu, Japan

K. Kubo, K. Shimoda* and A. Tamaki

Faculty of Fisheries, Nagasaki University, Bunkyo-Machi 1^14, Nagasaki 852-8521, Japan.*Corresponding author, e-mail: [email protected]

Three species of the callianassid genus Nihonotrypaea occur in the Ariake Sound estuarine system,southern Japan; they consist of two tidal-£at species (N. harmandi; N. japonica) and one boulder-beachspecies (N. petalura), with maximum population densities of 1440, 343, and 12 indm72, respectively.Nihonotrypaea harmandi and N. petalura are distributed along the coastline from the outermost part of thesound to the open sea, while N. japonica occurs in the middle part of the sound. Nihonotrypaea japonica hasan extended reproductive period from late winter to autumn, while those of the other species are from latespring or summer to autumn. Interspeci¢c comparisons were made for recently laid egg size (as volume)and clutch size (as number of eggs per female). Only in N. japonica was a seasonal egg size variationobserved, being signi¢cantly larger in winter to spring (mean¼0.106mm3) than in summer (0.080mm3).By contrast, clutch size was signi¢cantly smaller in winter to spring, resulting in nearly the same clutchvolume per female (product of the mean egg volume and clutch size) between the seasons. Among the threespecies, the egg size was ordered as N. japonica (overall mean volume through theseasons¼0.092mm3)44N. petalura (0.057mm3)4N. harmandi (0.054mm3). The clutch size was ordered asN. harmandi4N. petalura&N. japonica. The clutch volume was ordered as N. japonica&N. harmandi4N. petalura. The smallest clutch volume value for N. petalura female showed an opposite trendto the relative size of the major cheliped found in a previous study.

INTRODUCTION

The egg size and clutch size are one of the most impor-tant life history traits that directly determine ¢tness inaquatic invertebrates including estuarine macrobenthoswith planktonic larval development. For freshwater andmarine decapod crustaceans, a number of intraspeci¢ccomparisons of egg and clutch sizes among local popula-tions have been made, and possible e¡ects of local habitatconditions have been discussed as ultimate or proximateagents causing these size variations (E¡ord, 1969;Nishino, 1980; Boddeke, 1982; Mashiko, 1982; King &Butler, 1985; Thessalou-Legaki & Kiortsis, 1997; Hancocket al., 1998; Berkenbusch & Rowden, 2000; Gime¤ nez &Anger, 2001; Lardies & Castilla, 2001; Lardies &Wehrtmann, 2001; Brante et al., 2003; Oh & Hartnoll,2004; Paschke et al., 2004). On the other hand, only afew studies have investigated interspeci¢c di¡erences inegg and clutch sizes among congeneric species (King &Butler, 1985; Mashiko et al., 1991; Mashiko, 1992).

Decapod thalassinidean shrimps of the familyCallianassidae are common macro-invertebrates occur-ring from estuarine intertidal to marine subtidal softsediments (Dworschak, 2000; Felder, 2001). Three speciesof the genus Nihonotrypaea are found in Japanese waters.They consist of two tidal-£at species, N. harmandi

(Bouvier, 1901) and N. japonica (Ortmann, 1891), and oneboulder-beach species, N. petalura (Stimpson, 1860). Notethat in papers by Tamaki and his colleagues published

before 1998, the name Callianassa japonica was incorrectlyapplied to N. harmandi (see Tamaki, 2003). In the AriakeSound estuarine system, western Kyushu (the systemranges from Ariake Sound, via Tachibana Bay, to thecoastal waters of the East China Sea), N. harmandi andN. petalura are distributed in the outermost one-third ofAriake Sound and towards the East China Sea (the rangeof a 10-y averaged salinity at 5-m depth of the watersrecorded during 1972 to 1981, 30.5^34.0), while N. japonica

is mostly found in the middle one-third of Ariake Sound(salinity range, 28.5^30.5) (Figure 1; Tamaki et al., 1999;Wardiatno et al., 2003; Tamaki & Harada, 2005;Yokoyama et al., in press). Thus, using the Venice systemterms for the classi¢cation of saline waters, N. harmandiand N. petalura can be designated as euhaline to mixo-euhaline species, and N. japonica as a mixo-polyhalinespecies (Tamaki, 2003; Tamaki & Harada, 2005;Yokoyama et al., in press). In terms of the local distribu-tion, N. harmandi/petalura inhabit a number of small- tomedium-sized sand£ats/boulder beaches distributedalong the coastline, while N. japonica occupies severalextensive sand£ats located at the mouth of large rivers(Figure 1; Tamaki et al., 1999; Wardiatno et al., 2003;Tamaki & Harada, 2005; Yokoyama et al., in press). Themaximum population densities so far recorded were1440 indm72 for N. harmandi, 343 indm72 for N. japonica,and 12 indm72 for N. petalura (Tamaki et al., 1997; Flach &Tamaki, 2001;Wardiatno et al., 2003; Shimoda & Tamaki,2004). Tamaki & Miyabe (2000) found a good

J. Mar. Biol. Ass. U.K. (2006), 86, 103^111Printed in the United Kingdom

Journal of the Marine Biological Association of the United Kingdom (2006)

correspondence between the distribution of adults of thethree species along the coastline and that of their larvaein the waters of the estuarine system. The main larvalretention ground for N. harmandi and N. petalura waslocated in southern Tachibana Bay, while that forN. japonica was in the southern part of the middle AriakeSound (Figure 1).

Callianassid shrimp are well known for distinct sexualdimorphism in the size of the major cheliped withgrowth, with that of the male becoming larger and more

massive. Recently, Shimoda et al. (2005) found a signi¢-cant di¡erence in the degree of such sexual dimorphismamong the three species of Nihonotrypaea, being ordered asN. harmandi4N. japonica4N. petalura; the major chelipedsize of females is proportionally much larger in N. petalura

than in N. japonica and N. harmandi. It can be hypothesizedthat the enlarged major cheliped in females of N. petaluramight result in less energy allocation to egg production.

The aim of the present paper is to describe the egg andclutch sizes in the three species of Nihonotrypaea as a step to

104 K. Kubo et al. Egg and clutch sizes in congeneric callianassids


Figure 1. Distribution ranges of the three species of Nihonotrypaea as indicated with black arrows in the Ariake Sound estuarinesystem spanning from Ariake Sound, via Tachibana Bay (intermediate waters), to the coastal waters of the East China Sea inwestern Kyushu, Japan. The broken lines seaward of the coastline indicate the extent of the relatively large tidal £ats. Five sand-£ats and four boulder beaches were selected for collecting ovigerous female specimens to measure their egg and clutch sizes; thelocations of collection sites for each species are indicated using the ¢rst letter of the species name in parentheses (h, harmandi; j,japonica; p, petalura). The Takamoku-Jima boulder beach is the study site in Konishi et al. (1990). The main larval retention areasfor N. harmandi/petalura and N. japonica larvae are located in southern Tachibana Bay and in the southern part of the middle AriakeSound, respectively, as shown as lightly shaded areas (adapted from Tamaki & Miyabe, 2000).

further explore their reproductive strategies. The con-generic di¡erences in these sizes are discussed in light ofpossible e¡ects of several environmental conditions as ulti-mate or proximate factors. These environmental para-meters include water temperature and salinity, primaryproductivity, and larval retention/dispersal conditions oftheir respective habitats, which have been described inother studies including our own. The strategies for energyallocation to the major cheliped and eggs in the threespecies are also discussed based on new data.

MATERIALS AND METHODS

The breeding seasons of the three species ofNihonotrypaea in the year are from June to October inN. harmandi (Tamaki et al., 1996, 1997), from the end ofFebruary to early November in N. japonica (Y. Wardiatno& A. Tamaki, unpublished data), and from the end ofApril to early November in N. petalura (K. Kubo & A.Tamaki, unpublished data). Ovigerous females of thethree species were collected and ¢xed separately in 10%neutralized seawater^formalin, as follows (see Figure 1for sampling sites): (1) N. harmandi�on the Tomioka Baysand£at (328310N 1308020E), the Mogine¤ sand£at(328280N 1308120E), and the Okoshiki sand£at (328390N1308310E), from June to July 1998 and from June to July1999; (2) N. japonica�on the Arao sand£at (328570N1308250E), the Shirakawa sand£at (328470N 1308360E),and the Okoshiki sand£at, from April to July 1999 andfrom February to March 2000; and (3) N. petalura�onthe Akaiwa boulder beach (328320N 1308020E), the Tsuji-Shima boulder beach (328330N 1308060E), and the Futae¤boulder beach (328320N 1308080E), from April toNovember 1999.

In the laboratory, the developmental stage of eggs wasidenti¢ed under a light microscope according to thecriterion given in Rodrigues (1976): Stage 1¼recentlyprotruded eggs, unsegmented with uniformly distributedyolk; Stage 2¼segmented eggs, called ‘egg nauplii’; andStage 3¼eyed eggs. Four parameters were determinedonly for the ovigerous females with Stage-1 eggs to avoidthe possibility for egg losses during embryogenesis: (1)total length (TL: along mid-dorsal curvature from tip ofrostrum to posterior margin of telson); (2) egg diameter(longest and shortest diameters); (3) clutch size; and (4)clutch volume. Not all females for egg diameter measure-ments were used for clutch size measurements due to theloss of a portion of pleopods during sampling. Conversely,not all females for clutch size measurements were used foregg diameter measurements. The number of female speci-mens used for each measurement category is summarizedinTable 1. ForTL measurements, the curvature was tracedunder a stereomicroscope using a camera lucida, with amagni¢cation of 6 to 12�. For some of the largest speci-mens, the entire curvature image was divided into twoportions and later combined. The traced length wasmeasured using a computer coordinating digitizer for theactual TL value to the nearest 0.1mm. For egg sizemeasurements, 20 eggs were removed from the ¢rst andsecond pleopods of each female and placed individuallyon a slide glass with a shallow depression with a smallamount of water. The egg diameters were measured undera light microscope mounted with a calibrated ocular

micrometer, with a magni¢cation of 100�. Each eggvolume was calculated from the formula for an ellipsoid,Egg volume (mm3)¼pLS2/6, where L and S are thelongest and shortest diameters of the egg to the nearest0.001mm. The mean egg volume from the 20 measure-ments was adopted as the representative egg volume foreach female. For clutch size measurements, the number ofeggs carried by each female was counted under a stereo-microscope after all the eggs were removed from the ¢rstand second pairs of pleopods. Clutch volume (mm3) wasde¢ned as the product of a mean single egg volume andclutch size. In the calculation for any female specimen forwhich both the egg volume and the clutch size weremeasured, these values were simply multiplied. As theegg volume value for the specimens for which only clutchsize was measured (Table 1), the overall mean egg volumevalue for those specimens used for egg volume measure-ments was adopted. For N. japonica, the egg volume valuesin winter to spring (i.e. February to May) and in summer(i.e. June and July) were treated separately (see alsoTable 1).

For the comparison of clutch size and clutch volume inrelation to female body size between seasons in N. japonica

or among the three species, analysis of covariance(ANCOVA) was performed using the Statistical Packagefor the Social Sciences (SPSS) (2002a).

RESULTS

Egg size

The relationships between egg volume (mm3) andfemale body size (as TL, mm) for the three species ofNihonotrypaea are shown in Figure 2. The range of thesedimensions is given inTable 2. Note that the TL values inTable 2 are for the specimens for clutch size measurements,and di¡er slightly from those for egg size measurements.The di¡erence inTL among the three species was signi¢-cant (Kruskal^Wallis test, P50.001). A signi¢cantlylarger TL of N. japonica (mean�SD¼49.7�8.7mm,N¼61) than those of N. harmandi (36.8�6.0mm, N¼51)and N. petalura (40.3�7.8mm, N¼62) was detected(Sche¡e¤ ’s multiple comparison test, both P50.001), butthe di¡erence between the latter two species was notsigni¢cant (P¼0.12). Thus the TL values were ordered asN. japonica4N. petalura&N. harmandi.

Egg and clutch sizes in congeneric callianassids K. Kubo et al. 105


Table 1. Number of female specimens used for egg size- andclutch size measurements in the three species ofNihonotrypaea. For N. japonica, specimens collected duringwinter to spring (February to May) and in summer (June andJuly) are indicated separately.

Measurement category

SpeciesEgg sizeonly Both

Clutch sizeonly

N. harmandi 3 48 25N. japonica winter to spring 7 20 2

summer 3 31 18N. petalura 0 62 2

For N. japonica, the egg volume in winter to spring(February to May; mean�SD¼0.106�0.009mm3, N¼27)was signi¢cantly larger than that in summer (June andJuly; 0.080�0.007mm3, N¼34) (Mann^Whitney U-test,

P50.0001). The correlation coe⁄cients between eggvolume and TL (r¼0.12 and 70.24 for N. japonica inwinter to spring and in summer, 0.22 for N. harmandi,70.06 for N. petalura) were not signi¢cant (P40.1 or0.055P50.1). The overall mean (�SD) egg volumethrough the year was 0.092�0.015mm3 (N¼61) forN. japonica, 0.057�0.005mm3 (N¼62) for N. petalura, and0.054�0.003mm3 for N. harmandi (N¼51). The di¡erencein egg volume among the three species was signi¢cant(Kruskal^Wallis test, P50.001). The Sche¡e¤ ’s multiplecomparison test detected a signi¢cant di¡erence betweenevery pair of the three species: P50.001 for N. harmandi

and N. japonica; 0.015P50.05 for N. harmandi andN. petalura; and P50.001 for N. japonica and N. petalura.Thus the egg volume values were ordered asN. japonica44N. petalura4N. harmandi.

Clutch size and clutch volume

The range of clutch size and female TL for the threespecies of Nihonotrypaea is also given inTable 2.

The relationships between clutch size and female bodysize (as TL3,mm3) for N. japonica are shown separately forwinter to spring and for summer in Figure 3A. The linearregression equations were ¢tted to these two groups of



Figure 2. Relationships between egg volume (mm3) and bodysize [as TL (¼ total length), mm] for females of the threespecies of Nihonotrypaea. For N. japonica, the eggs collectedduring winter to spring (February to May) and in summer(June and July) are indicated separately.

Table 2. Egg size, clutch size, and related early life history traits in callianassid shrimp. Bars mean no data. Female body size of thethree species of Nihonotrypaea is for specimens used for clutch size measurements.

ED EV FBS DB DZD T SSpecies (mm) (mm3) CS (mm) (d) NZ (d) (oC) (%) Reference

Nihonotrypaea

harmandi

0.458^0.487 0.046^0.060a 104^2856 24.4^48.1(TL)

13^22 5 19 23^25 33.0^33.8 (1), (2),(3), (4)

N. petalura 0.465^0.506 0.043^0.072a 56^2880 25.7^64.2(TL)

16* 5 15^16 22^28 33.0^33.8 (1), (2),(5)

N. japonica 0.540^0.594 0.073^0.123a 139^3731 26.0^67.4(TL)

14** 5 16 22.0^24.7 33.2^33.8 (1), (2),(6)

Callianassa ¢lholi 0.464^0.684 0.052^0.168b 660^1500 37^54 (TL) 38.5 5 150 �9^14 32.3^33.0 (7), (8)C. subterranea 0.5^0.6 0.065^0.113b 7000 47 (TL) 30 4 35 18c � (9), (10)C. bouvieri 0.625^0.800 0.164a 80 18^25 (TL) � � � � � (11)Neotrypaea

californiensis

0.62 0.125b 200^14,000 9^19 (CL) 28^35 5 42^56 �11.5^14.5

432 (12), (13)

Callianassa

kraussi

0.94^1.24 0.435^0.998b 40^193 6^11 (CL) 32^33 2 3^5 20 34^35 (14), (15)

C. kewalramanii 0.7^0.9 0.180^0.382b � � � 2 3^4 18^23 30^33 (16)Callichirus major 0.74^0.88 0.252a 8170 136 (TL) 432 3 14 �23c � (17), (18)Lepidophthalmus

louisianensis

0.9^1.2 0.382^0.905b 598 17 (CL) 425^30 2 3^4 26 15 (19), (20),(21)

L. sinuensis � 0.81 251 11^14 (CL) � 2 2^3 25.5^27.5 10 (21), (22)Pestarella

tyrrhena

1.18 0.86b 56^1128 � � 2 5.9^8.4 19^24 37 (23), (24),(25)

Sergio mirim 1.08^1.17 0.660^0.839b 300^6600 64^98 (TL) 30 2 7^14 22^26 32^34 (26)Glypturus

armatus

0.75^0.85 0.221^0.322b � � 18^21 � � 26c 35c (27)

ED, egg diameter (range); EV, egg volume (a: calculated from shortest and longest egg diameters as an ellipsoid, b: calculated from eggdiameter as a sphere); CS, clutch size per female; FBS, female body size (total length or carapace length); DB, duration of brooding;NZ, number of zoeal stages; DZD, duration of zoeal development; Tand S, temperature and salinity during larval development (c:during brooding). Reference: (1) this study; (2) Tamaki & Miyabe, 2000; (3) Tamaki et al., 1996; (4) Konishi et al., 1999; (5) Konishi etal., 1990; (6) Miyabe et al., 1998; (7) Devine, 1966; (8) Berkenbusch & Rowden, 2000; (9) Lutze, 1938; (10) Dworschak, 1988; (11)Dworschak & Pervesler, 1988; (12) Johnson & Gonor, 1982; (13) Dumbauld et al., 1996; (14) Forbes, 1973; (15) Forbes, 1977; (16) Sankolli& Shenoy, 1975; (17) Pohl, 1946; (18) Rodrigues, 1976; (19) Felder & Lovett, 1989; (20) Felder & Rodrigues, 1993; (21) Nates et al., 1997;(22) Nates & Felder, 1999; (23) Thessalou-Legaki, 1990; (24) Thessalou-Legaki & Kiortsis, 1997; (25) Thessalou-Legaki et al., 1999;(26) Pezzuto, 1998; (27) Vaugelas et al., 1986; *, K. Kubo & A.Tamaki, unpublished data; **,Y.Wardiatno & A.Tamaki, unpublisheddata.

plots to perform ANCOVA for signi¢cant di¡erencesbetween them. The di¡erence in the slope values of theregression lines was not signi¢cant (F1,67¼0.5, P¼0.46),but the di¡erence in the y-intercept values of the regressionlines was signi¢cant (F1,68¼9.6, 0.0015P50.01). Thusclutch size was larger in summer than in winter to spring.The ANCOVA for clutch volume (Figure 3B) indicatedthat the slope values of the regression lines were notsigni¢cantly di¡erent (F1,67¼0.6, P¼0.45) and that they-intercept values of the regression lines were not signi¢-cantly di¡erent (F1,68¼0.8, P¼0.38). Thus clutch volumeswere nearly the same between the seasons.

The relationships between clutch size and female bodysize (asTL3, mm3) for the three species of Nihonotrypaea areshown in Figure 4A.Themean (�SD) clutch size per femalewas 1089�654 (N¼73) for N. harmandi, 1598�847(N¼71) for N. japonica, and 862�736 (N¼64) forN. petalura. To perform ANCOVA, the data for N. japonicawas pooled for all seasons. The di¡erence in the slopevalues of the regression lines among the three species wassigni¢cant (F2,202¼16.7, P50.001). The Bonferroni’smultiple comparison test detected a signi¢cant di¡erence(a¼0.05/3¼0.014) between two pairs of the three speciesbut not between the other one: (1) F1,140¼35.1, P50.001for the N. harmandi and N. japonica pair; (2) F1,133¼21.5,P50.001 for the N. harmandi and N. petalura pair; and (3)F1,131¼2.2, P¼0.14 for the N. japonica and N. petalura pair.

Thus the slope values were ordered as N. harmandi

(0.030)4N. petalura (0.013)&N. japonica (0.011). Inpair (3), the di¡erence in the y-intercept values of theregression lines was not signi¢cant (F1,132¼3.1, P¼0.08).



Figure 3. (A) Linear regression of clutch size (¼ number ofeggs per female) on body size [as TL (¼ total length)3, mm3]for females of Nihonotrypaea japonica. The specimens collectedduring winter to spring (February to May) and in summer(June and July) are indicated separately; and (B) linearregression of clutch volume (¼ product of the mean eggvolume and clutch size per female) on body size (as TL3, mm3)for females of N. japonica. The specimens collected duringwinter to spring and in summer are indicated separately.

Figure 4. (A) Linear regression of clutch size (¼ number ofeggs per female) on body size [as TL (¼ total length)3, mm3]for females of the three species of Nihonotrypaea. The specimensof N. japonica collected during winter to spring (February toMay) and in summer (June and July) are indicated separatelybut the regression is shown for the combined data; and(B) linear regression of clutch volume (¼ product of the meanegg volume and clutch size per female) on body size (asTL3, mm3) for the three species of Nihonotrypaea. The specimensof N. japonica collected during winter to spring and in summerare indicated separately but the regression is shown for thecombined data.

Figure 5. Best ¢t linear or nonlinear regressions of majorcheliped wet weight (mg) on body size [as TL (¼ totallength)3, mm3] for ovigerous females of the three species ofNihonotrypaea (after the original data set for ¢gure 3 in Shimodaet al., 2005; see text). The TL of the smallest ovigerous femalewas 24.5mm in N. harmandi, 26.4mm in N. japonica, and26.0mm in N. petalura.

The mean (�SD) and range of clutch volume was58.7�35.4mm3 and 5.1^154.2mm3 (N¼73) forN. harmandi, 144.4�86.7mm3 and 11.1^388.4mm3

(N¼71) for N. japonica, and 50.0�42.7mm3 and 3.5^175.6mm3 (N¼64) for N. petalura (Figure 4B). To performANCOVA, the data for N. japonica was pooled for allseasons.The di¡erence in the slope values of the regressionlines among the three species was signi¢cant (F2,202¼11.5,P50.001). The Bonferroni’s multiple comparison testdetected a signi¢cant di¡erence (a¼0.05/3¼0.014)between two pairs of the three species but not betweenthe other one: (1) F1,140¼0.07, P¼0.79 for the N. harmandi

and N. japonica pair; (2) F1,133¼16.3, P50.001 for theN. harmandi and N. petalura pair; and (3) F1,131¼16.0,P50.001 for the N. japonica and N. petalura pair. Thus theslope values were ordered as N. japonica (0.0012)&N. harmandi (0.0012)4N. petalura (0.0008). In pair (1), thedi¡erence in the y-intercept values of the regression lineswas not signi¢cant (F1,141¼2.7, P¼0.10).

DISCUSSION

Table 2 summarizes the available information on eggsize, clutch size, and related early life history traits incallianassid shrimp. The egg volumes of Nihonotrypaea

harmandi and N. petalura are the smallest, and that ofN. japonica belongs to the group with the second smallesteggs, including Callianassa ¢lholi, C. subterranea, andNeotrypaea californiensis. These six species have four or ¢veplanktotrophic zoeal stages with relatively long planktonicperiods (515 d). Seven species with the largest eggs(C. kraussi, C. kewalramanii, Callichirus major, Lepidophthalmuslouisianensis, L. sinuensis, Pestarella tyrrhena, and Sergio mirim)have two or three planktotrophic/lecithotrophic zoealstageswith shorter planktonic periods (514 d). Inparticular,larvae of Callianassa kraussi remain in their mother burrowuntil metamorphosis (Forbes, 1973). For each species ofNihonotrypaea, clutch size increased with female body size(Figure 4A). The mean clutch size for N. harmandi (1089)was greater than that recorded for samples from theTomioka Bay sand£at population (337) given inTamaki etal. (1997). This was due to the inclusion of the larger speci-mens derived from other localities sampled in the presentstudy.The increase in clutch size with female body size wasrecorded for N. californiensis (see Dumbauld et al., 1996),P. tyrrhena (as Callianassa tyrrhena: Thessalou-Legaki &Kiortsis, 1997), and C. ¢lholi (see Berkenbusch & Rowden,2000). Thus caution must be used when making inter-speci¢c comparisons of the clutch sizes listed inTable 2.

The larval development of the three species ofNihonotrypaea reared under similar food conditions andwater temperatures (22.0^28.08C) in the laboratory inJune was described previously (Konishi et al. (1999) forN. harmandi; Miyabe et al. (1998) for N. japonica; Konishiet al. (1990) for N. petalura). The duration of time to reachthe decapodid stage was nearly the same among the threespecies (i.e. 16 to 19 d). The results in the above studiescon¢rm that the smaller egg size in N. harmandi than inN. japonica (Figure 2) leads to a smaller ¢rst zoeal size.The mean carapace length of the ¢rst zoeae immediatelyafter release from the pleopods of the female was 0.96mmin N. harmandi (N¼20; females, obtained from theTomioka Bay sand£at) and 1.09mm in N. japonica (N¼61;

females, from the Okoshiki sand£at). Tamaki & Miyabe(2000) also recorded that the total length of the ¢rst zoeaof N. harmandi (mean�SD¼2.75�0.08mm, N¼120) wassigni¢cantly smaller than that of N. japonica

(3.05�0.09mm, N¼120). Although N. petalura produceseggs of an intermediate size (Figure 2), its ¢rst zoeal sizeis the largest, with a mean carapace length of 1.24mm(Konishi et al. (1990); N¼no data given; females, fromthe Takamoku-Jima boulder beach located in the outer-most one-third of Ariake Sound (Figure 1)).

Berkenbusch & Rowden (2000) reported that the eggsize in local populations of the callianassid shrimpCallianassa ¢lholi in New Zealand waters signi¢cantlyincreased with the higher latitude. A similar latitudinalcline has been documented for other decapod crustaceans(e.g. E¡ord, 1969; Nishino, 1980; Lardies & Castilla, 2001;Lardies & Wehrtmann, 2001). In these studies, the latitu-dinal clines in egg size were explained as adaptation towater temperature a¡ecting the duration of embryonicand/or planktonic development. The larger egg size in N.

japonica than in N. harmandi recorded in the present study(Figure 2) is in accordance with the lower winter tempera-ture in Ariake Sound than in the outer waters. A 10-yaveraged water temperature at 5-m depth during 1972 to1981 was from 11.08C (January) to 25.58C (July) in themiddle Ariake Sound, while it was from 16.08C (January)to 26.08C (July) in the coastal waters of the East ChinaSea (Coastal Oceanography Research Committee, theOceanographical Society of Japan, 1985). Based on theirmeasurements made in the 1990s,Wardiatno et al. (2003)described the ranges of pore-water temperature in thesediment inhabited by N. japonica and N. harmandi throughthe year: 7.98C (February)^31.18C (September) on theShirakawa sand£at (Figure 1), in which only N. japonica

occurred, and 11.48C (February)^27.28C (September) onthe Tomioka Bay sand£at (Figure 1), in which only N.

harmandi occurred.In his recent review on ‘summer and winter larvae’ of

decapod crustaceans, Anger (2001: 292^293) cited anexample of the seasonal egg size variation in the brownshrimp Crangon crangon in the southern North Sea(Boddeke, 1982). Eggs produced during winter are up to20% larger than summer eggs. The eggs in the winterperiod contain signi¢cantly higher quantities of proteins,lipids, and energy, bestowing the larvae a greater toler-ance to nutritional stress encountered under the wintersea conditions (Paschke et al., 2004). In the populationoccurring in the central Irish Sea, there was no di¡erencein clutch size between winter and summer, resulting in alarger clutch volume in winter (Oh & Hartnoll, 2004).Anger (2001) anticipated that such seasonal egg size varia-tion should occur also in other species with an extendedreproductive period. This may be the case with the largeregg size produced in winter to spring than in summer inthe population of N. japonica in Ariake Sound (Figure 2).The clutch volume was nearly the same between theseasons (Figure 3B: trade-o¡ pattern). The sound is aproductive water area as compared with the sea areasoutside of the sound (e.g. Coastal Oceanography ResearchCommittee, the Oceanographical Society of Japan, 1985).Our recent measurements on chlorophyll-a concentrationof the waters at 5-m depth in the middle Ariake Soundand southern Tachibana Bay through the four seasons



recorded mean (�SD) values of 7.8 (�2.3, N¼4) and 1.25(�0.9, N¼5) mg l71, respectively (Shimoda et al., inpreparation). The values measured near the Shirakawasand£at (Figure 1) on other occasions in summer rangedfrom 9.5 to 13.8 mg l71 (Yokoyama et al., in press). It couldbe speculated that during their speciation process,N. harmandi and N. japonica have adapted to more oligo-trophic waters a¡ected by the open sea and moreeutrophic estuarine waters, respectively. The higherprimary productivity of the Ariake Sound waters mighthave enabled N. japonica larvae to survive even in latewinter to early spring, which is three months earlier thanthe onset of the reproductive season of N. harmandi at thewater temperature of 208C (Tamaki et al., 1997). If naturalselection for the larger larvae of N. japonica equipped withmore nutritional resources has been exerted primarily onthe ‘winter larvae’, the size of the ‘summer eggs’ might beconstrained by that of the ‘winter eggs’.

Gime¤ nez & Anger (2001) reported that the eggs fromfemales of the estuarine crab, Chasmagnathus granulata,maintained at a lower salinity (15%) had on average ahigher biomass (dry weight, carbon, and nitrogen) and alarger diameter than those at a higher salinity (32%). Theauthors argued that the larger egg size at 15% was aconsequence of the greater di¡erence between internaland external osmolalities, resulting in an increased wateruptake. In the present study, the salinity range experi-enced by N. japonica is wider than that by N. harmandi

(pore-water salinities in the sediment through the year,18.0^33.0 vs 33.0^36.0 (Wardiatno et al., 2003)). Thedi¡erent egg volumes between the two species (Figure 2)might be related to such di¡erent salinity ranges, espe-cially during the rainy season (June^July) in southernJapan. To our knowledge, no study has demonstrated thee¡ect of salinity as an ultimate selective agent causing eggsize variations in decapod crustaceans.

Despite egg volume di¡erence between N. japonica andN. harmandi (Figure 2), the clutch volumes were nearly thesame (Figure 4B: trade-o¡ pattern). This suggests that thecarrying capacity of the ovary in the female has a similarallometric pattern with body growth in the two species.The smaller clutch size in N. japonica (Figure 4A) mightbe compensated for by the e⁄cient larval retentionwithin Ariake Sound (Figure 1; Tamaki & Miyabe, 2000).By contrast, the loss of larvae due to dispersal from theoriginal regional population of N. harmandi, which issituated closer to the open sea, might be compensated forby the larger clutch size and by a number of potentiallycolonizable habitats scattered along the coastline (Figure1; Tamaki et al., 1999; Tamaki & Harada, 2005). The eggvolume of the boulder-beach species, N. petalura, was inter-mediate between those of the two tidal-£at species, closerto that of N. harmandi (Figure 2). This suggests that thesame selective force could have been exerted on N. petalura

and N. harmandi, which occur in the same water area(Tamaki et al., 1999; Shimoda & Tamaki, 2004).However, at present, no hypothesis can be given to thelargest ¢rst zoeal size in N. petalura (the values given inthe second paragraph of the Discussion).

For decapod crustaceans, reproductive output such asclutch volume has often been used as a proxy for reproduc-tive e¡ort. However, the latter comprises other compo-nents such as metabolic costs of brooding (Brante et al.,

2003) and e¡ort for mating (Shimoda et al., 2005). In thepresent study, the clutch volume was signi¢cantly smallerin N. petalura than in the other two species (Figure 4B).This is unlikely to be due to the smaller ovarian carryingcapacity in N. petalura, as several clutch-volume plots forthis species overlapped with those for the other twospecies (Figure 4B). Some factors would exist, restrictingenergy investment into egg production within narrowlimits. One possibility is the di¡erence between specieswhen allocating acquired energy to the e¡ort for matingand egg production (trade-o¡ pattern). Based on theoriginal data set given in Shimoda et al. (2005), the best¢t functions describing the relationship between majorcheliped wet weight and body size (as TL3) in ovigerousfemales of the three species were calculated here (Figure5). The selection of these functions was made based on thesmallest value for Akaike’s Information Criterion (AIC)(1973) among the linear regression equation and severalnonlinear ones including polynomial quadratic/cubic,exponential, logarithm, and power equations determinedusing SPSS (2002b). It is noteworthy for N. petalura thatin its early life history, the regression curve is above theother two curves and most convex (Figure 5) in contrastto the lowest position and most concave pattern in itsclutch-volume data plots (Figure 4B). The major chelipedof callianassid shrimp is used as a weapon for intrasexual¢ghting. Shimoda et al. (2005) found a signi¢cant di¡er-ence in the degree of major cheliped sexual dimorphism(male to female ratio) among the three species, beingordered as N. harmandi4N. japonica4N. petalura. Theauthors have also demonstrated intraspeci¢c antagonisticbehaviours of the three species. Males of all species inter-acted aggressively with each other. Females of the twotidal-£at species were non-aggressive, while those ofN. petalura were as aggressive with each other as weremales. Thus interspeci¢c di¡erence in the behaviours offemales agreed with the di¡erence in the size of theirmajor chelipeds. The enlarged major cheliped in femalesof N. petalura might have evolved as a result of the severestintrasexual competition for mates under the much lowerpopulation density (the values given in the Introduction),enabling less energy investment into egg production. Moreenergy allocated to the enlargement of the major chelipedin the earlier body-growth phase subsequent to maturationmay maximize female lifetime ¢tness.

We wish to thank R. Hirohashi, H. Ueno, Y. Wardiatno, N.Obayashi, K. Harada, and R. Fujiwara for their assistance inthe ¢eld, T.T. Gonzales for comments on an earlier draft, andthe three referees for their constructive comments on the manu-script. This study was partly supported by the Japan Society forthe Promotion of Science (JSPS) Grant-in-Aid for Scienti¢cResearch 09640754 and 13854006 to A.T. and by the FujiwaraNatural History Foundation Grant and the Research Institute ofMarine Invertebrates Grant to K.S.

REFERENCESAkaike, H., 1973. Information theory and an extension of themaximum likelihood principle. In Second International

Symposium on InformationTheory (ed. B.N. Petrov and F. Csa¤ ki),pp. 267^281. Budapest: Akade¤ miai Kiado¤ .

Anger, K., 2001. The biology of decapod crustacean larvae. TheNetherlands: A.A. Balkema Publishers. [Crustacean Issues 14.]



Berkenbusch, K. & Rowden, A.A., 2000. Latitudinal variation inthe reproductive biology of the burrowing ghost shrimpCallianassa ¢lholi (Decapoda: Thalassinidea). Marine Biology,136, 497^504.

Boddeke, R., 1982.The occurrence of winter and summer eggs inthe brown shrimp (Crangon crangon) and the pattern of recruit-ment. NetherlandsJournal of Sea Research, 16, 151^162.

Brante, A., Ferna¤ ndez, M., Eckerle, L., Mark, F., Po« rtner, H.-O.& Arntz,W., 2003. Reproductive investment in the crab Cancer

setosus along a latitudinal cline: egg production, embryolosses and embryo ventilation. Marine Ecology Progress Series,251, 221^232.

Coastal Oceanography Research Committee, the Oceano-graphical Society of Japan, 1985. Chapter 21: Ariake-kai. InCoastal Oceanography of Japanese Islands, pp. 815^878. Tokyo:Tokai University Press. [In Japanese.]

Devine, C.E., 1966. Ecology of Callianassa ¢lholi Milne-Edwards1878 (Crustacea, Thalassinidea).Transactions of the Royal Societyof New Zealand, Zoology, 8, 93^110.

Dumbauld, B.R., Armstrong, D.A. & Feldman, K.L., 1996. Life-history characteristics of two sympatric thalassinideanshrimps, Neotrypaea californiensis and Upogebia pugettensis, withimplications for oyster culture. Journal of Crustacean Biology, 16,689^708.

Dworschak, P.C., 1988. The biology of Upogebia pusilla (Petagna)(Decapoda, Thalassinidea). III. Growth and production.Pubblicazioni della Stazione Zoologica di Napoli: Marine Ecology, 9,51^77.

Dworschak, P.C., 2000. Global diversity in the Thalassinidea(Decapoda). Journal of Crustacean Biology, 20, Special no. 2,238^245.

Dworschak, P.C. & Pervesler, P., 1988. Burrows of Callianassabouvieri Nobili 1904 from Safaga (Egypt, Red Sea) with someremarks on the biology of the species. Senckenbergiana Maritima,20, 1^17.

E¡ord, I.E., 1969. Egg size in the sand crab, Emerita analoga

(Decapoda, Hippidae). Crustaceana, 16, 15^26.Felder, D.L., 2001. Diversity and ecological signi¢cance of deep-burrowing macrocrustaceans in coastal tropical waters ofthe Americas (Decapoda: Thalassinidea). Interciencia, 26,440^449.

Felder, D.L. & Lovett, D.L., 1989. Relative growth and sexualmaturation in the estuarine ghost shrimp Callianassa

louisianensis Schmitt, 1935. Journal of Crustacean Biology, 9,540^553.

Felder, D.L. & Rodrigues, S. de A., 1993. Reexamination of theghost shrimp Lepidophthalmus louisianensis (Schmitt, 1935) fromthe northern Gulf of Mexico and comparison to L. siriboia,new species, from Brazil (Decapoda: Thalassinidea:Callianassidae). Journal of Crustacean Biology, 13, 357^376.

Flach, E. & Tamaki, A., 2001. Competitive bioturbators on inter-tidal sand £ats in the EuropeanWadden Sea and Ariake Soundin Japan. In Ecological Studies. Vol. 151. Ecological comparisons ofsedimentary shores (ed. K. Reise), pp. 149^171. Berlin: Springer.

Forbes, A.T., 1973. An unusual abbreviated larval life in theestuarine burrowing prawn Callianassa kraussi (Crustacea:Decapoda: Thalassinidea). Marine Biology, 22, 361^365.

Forbes, A.T., 1977. Breeding and growth of the burrowingprawn Callianassa kraussi Stebbing (Crustacea: Decapoda:Thalassinidea). Zoologica Africana, 12, 149^161.

Gime¤ nez, L. & Anger, K., 2001. Relationships among salinity,egg size, embryonic development, and larval biomass in theestuarine crab Chasmagnathus granulata Dana, 1851. Journal ofExperimental Marine Biology and Ecology, 260, 241^257.

Hancock, M.A., Hughes, J.M. & Bunn, S.E., 1998. In£uence ofgenetic and environmental factors on egg and clutch sizesamong populations of Paratya australiensis Kemp (Decapoda:Atyidae) in upland rainforest streams, south-east Queensland.Oecologia, 115, 483^491.

Johnson, G.E. & Gonor, J.J., 1982. The tidal exchange ofCallianassa californiensis (Crustacea, Decapoda) larvaebetween the ocean and the Salmon River estuary, Oregon.Estuarine, Coastal and Shelf Science, 14, 501^516.

King, M.G. & Butler, A.J., 1985. Relationship of life-historypatterns to depth in deep-water caridean shrimps (Crustacea:Natantia). Marine Biology, 86, 129^138.

Konishi, K., Fukuda, Y. & Quintana, R.R., 1999. The larvaldevelopment of the mud-burrowing shrimp Callianassa sp.under laboratory conditions (Decapoda, Thalassinidea,Callianassidae). In Proceedings of the Fourth International

Crustacean Congress, 1998, Vol. 1. Crustaceans and the biodiversity

crisis (ed. F.R. Schram and J.C. von Vaupel Klein), pp. 781^804. Leiden: Koninklijke Brill.

Konishi, K., Quintana, R.R. & Fukuda, Y., 1990. A completedescription of larval stages of the ghost shrimp Callianassa

petalura Stimpson (Crustacea: Thalassinidea: Callianassidae)under laboratory conditions. Bulletin of the National Research

Institute of Aquaculture, Nansei, Japan, 17, 27^49.Lardies, M.A. & Castilla, J.C., 2001. Latitudinal variation in thereproductive biology of the commensal crab Pinnaxodes chilensis

(Decapoda: Pinnotheridae) along the Chilean coast. Marine

Biology, 139, 1125^1133.Lardies, M.A. & Wehrtmann, I.S., 2001. Latitudinal varia-tion in the reproductive biology of Betaeus truncatus

(Decapoda: Alpheidae) along the Chilean coast. Ophelia, 55,55^67.

Lutze, J., 1938. Ueber systematic, Entwicklung und Oekologievon Callianassa. Helgola« nder Wissenschaftliche Meeresuntersuch-

ungen, 1, 162^199.Mashiko, K., 1982. Di¡erences in both the egg size and the clutchsize of the freshwater prawn Palaemon paucidens de Haan in theSagami River. JapaneseJournal of Ecology, 32, 445^451.

Mashiko, K., 1992. Laying few large eggs or many small eggs infreshwater prawns of the genus Macrobrachium. The Heredity,Special issue 4, 7^16. [In Japanese.]

Mashiko, K., Kawabata, S. & Okino,T., 1991. Reproductive andpopulational characteristics of a few caridean shrimpscollected from Lake Tanganyika, East Africa. Archiv fu« r

Hydrobiologie, 122, 69^78.Miyabe, S., Konishi, K., Fukuda, Y. & Tamaki, A., 1998. Thecomplete larval development of the ghost shrimp, Callianassajaponica Ortmann, 1891 (Decapoda: Thalassinidea:Callianassidae), reared in the laboratory. Crustacean Research,27, 101^121.

Nates, S.F. & Felder, D.L., 1999. Growth and maturation of theghost shrimp Lepidophthalmus sinuensis Lemaitre andRodrigues, 1991 (Crustacea, Decapoda, Callianassidae), aburrowing pest in penaeid shrimp culture ponds. Fishery

Bulletin, 97, 526^541.Nates, S.F., Felder, D.L. & Lemaitre, R., 1997. Comparativelarval development in two species of the burrowing ghostshrimp genus Lepidophthalmus (Decapoda: Callianassidae).Journal of Crustacean Biology, 17, 497^519.

Nishino, M., 1980. Geographical variations in body size, broodsize and egg size of a freshwater shrimp, Palaemon paucidens deHaan, with some discussion on brood habit. JapaneseJournal ofLimnology, 41, 185^202.

Oh, C.-W. & Hartnoll, R.G., 2004. Reproductive biology of thecommon shrimp Crangon crangon (Decapoda: Crangonidae) inthe central Irish Sea. Marine Biology, 144, 303^316.

Paschke, K.A., Gebauer, P., Buchholz, F. & Anger, K., 2004.Seasonal variation in starvation resistance of early larvalNorth Sea shrimp Crangon crangon (Decapoda: Crangonidae).Marine Ecology Progress Series, 279, 183^191.

Pezzuto, P.R., 1998. Population dynamics of Sergio mirim

(Rodrigues 1971) (Decapoda: Thalassinidea: Callianassidae)in Cassino Beach, southern Brazil. Pubblicazioni della Stazione

Zoologica di Napoli: Marine Ecology, 19, 89^109.



Pohl, M.E., 1946. Ecological observations on Callianassa major

Say at Beaufort, North Carolina. Ecology, 27, 71^80.Rodrigues, S. de A., 1976. Sobre a reproduc� a‹ o, embriologia edesenvolvimento larval de Callichirus major Say, 1818(Crustacea, Decapoda, Thalassinidea). Boletim de Zoologia,

Universidade de Sa‹ o Paulo, 1, 85^104.Sankolli, K.N. & Shenoy, S., 1975. Larval development of mudshrimp Callianassa (Callichirus) kewalramanii Sankolli, in thelaboratory (Crustacea, Decapoda). Bulletin of the Department ofMarine Sciences, University of Cochin, 7, 705^720.

Shimoda, K. & Tamaki, A., 2004. Burrow morphology of theghost shrimp Nihonotrypaea petalura (Decapoda: Thalassinidea:Callianassidae) from western Kyushu, Japan. Marine Biology,144, 723^734.

Shimoda, K., Wardiatno, Y., Kubo, K. & Tamaki, A., 2005.Intraspeci¢c behaviors and major cheliped sexual dimorphismin three congeneric callianassid shrimp. Marine Biology, 146,543^557.

SPSS, 2002a. SPSS Advanced ModelsTM 11.5J. Tokyo: SPSS JapanInc. [In Japanese.]

SPSS, 2002b. SPSS Base 11.5J. Tokyo: SPSS Japan Inc. [InJapanese.]

Tamaki, A., 2003. A rebuttal to Sakai (2001): ‘‘A review of thecommon Japanese callianassid species, Callianassa japonica andC. petalura (Decapoda,Thalassinidea)’’. Crustaceana, 76, 115^124.

Tamaki, A. & Harada, K., 2005. Alongshore con¢guration andsize of local populations of the callianassid shrimpNihonotrypaea harmandi (Bouvier, 1901) (Decapoda:Thalassinidea) in the Ariake-Sound estuarine system,Kyushu, Japan. Crustacean Research, 34, 65^86.

Tamaki, A. & Miyabe, S., 2000. Larval abundance patterns forthree species of Nihonotrypaea (Decapoda: Thalassinidea:Callianassidae) along an estuary-to-open-sea gradient inwestern Kyushu, Japan. Journal of Crustacean Biology, 20,Special no. 2, 182^191.

Tamaki, A., Ingole, B., Ikebe, K., Muramatsu, K., Taka, M. &Tanaka, M., 1997. Life history of the ghost shrimp, Callianassajaponica Ortmann (Decapoda: Thalassinidea), on an intertidalsand£at in western Kyushu, Japan. Journal of Experimental

Marine Biology and Ecology, 210, 223^250.

Tamaki, A., Itoh, J. & Kubo, K., 1999. Distributions of threespecies of Nihonotrypaea (Decapoda: Thalassinidea:Callianassidae) in intertidal habitats along an estuary toopen-sea gradient in western Kyushu, Japan. Crustacean

Research, 28, 37^51.Tamaki, A., Tanoue, H., Itoh, J. & Fukuda, Y., 1996. Broodingand larval developmental periods of the callianassid ghostshrimp, Callianassa japonica (Decapoda: Thalassinidea). Journalof the Marine Biological Association of the United Kingdom, 76, 675^689.

Thessalou-Legaki, M., 1990. Advanced larval development ofCallianassa tyrrhena (Decapoda: Thalassinidea) and the e¡ectof environmental factors. Journal of Crustacean Biology, 10, 659^666.

Thessalou-Legaki, M. & Kiortsis, V., 1997. Estimation of thereproductive output of the burrowing shrimp Callianassa

tyrrhena: a comparison of three di¡erent biometricalapproaches. Marine Biology, 127, 435^442.

Thessalou-Legaki, M., Peppa, A. & Zacharaki, M., 1999.Facultative lecithotrophy during larval development of theburrowing shrimp Callianassa tyrrhena (Decapoda:Callianassidae). Marine Biology, 133, 635^642.

Vaugelas, J. de, Delesalle, B. & Monier, C., 1986. Aspects of thebiology of Callichirus armatus (A. Milne-Edwards, 1870)(Decapoda, Thalassinidea) from French Polynesia.Crustaceana, 50, 204^216.

Wardiatno, Y., Shimoda, K., Koyama, K. & Tamaki, A., 2003.Zonation of congeneric callianassid shrimps, Nihonotrypaea

harmandi (Bouvier, 1901) and N. japonica (Ortmann, 1891)(Decapoda: Thalassinidea), on intertidal sand£ats in theAriake-Sound estuarine system, Kyushu, Japan. Benthos

Research, 58, 51^73.Yokoyama, H.,Tamaki, A., Koyama, K., Ishihi,Y., Shimoda, K.& Harada, K., in press. Isotopic evidence for phytoplankton asa major food source for macrobenthos on an intertidal sand-£at, Ariake Sound, Japan. Marine Ecology Progress Series.

Submitted 26 August 2005. Accepted 17 November 2005.



Documents

Egg size and clutch size in three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan