VENUS 71 (3–4): 199–207, 2013 ©Ma lacological Society of Japan

Swimming Ability of Juvenile chinensis by Pedal Flapping

Yoshitake Takada1*, Yuko Ito2 and Ikuo Hayashi3 1Japan Sea National Fisheries Research Institute, Fisheries Research Agency Japan, Suido-cho 1-5939-22, Niigata 951-8121, Japan 2Musa 1-28-20, Kushiro, Hokkaido 085-0806, Japan 3Kumano Biological Research Institute, Atashika-cho 1320, Mie 519-4206, Japan

Abstract: Swimming behaviour of juvenile Mactra chinensis was observed in the laboratory. Clams of 7–15 mm shell length swam by pedal flapping after launching from the bottom by leaping. The average swimming speed of 7–9 mm clams was 6.0 cm s–1 and that of 9–15 mm clams was 7.8 cm s–1. The average distance swum reached 17.4 cm. Larger individuals of 31–35 mm shell length class did not show swimming behaviour but they performed leaping. Swimming by pedal flapping extended the range of locomotive distance through the water column at least 4.1 times over that achieved by leaping. Therefore swimming is thought to be an adaptive behaviour to reduce the risk of predation and increase the chance to find a better place to burrow.

Keywords: behaviour, swim, jump, foot flapping, size,

Introduction

Bivalves inhabiting soft sediment areas are not always bound to the seafloor bottom. The occurrence of post-metamorphic bivalves in the water column has often been observed from plankton samples (Williams & Porter, 1971). Some bivalve are known to produce byssus threads and to be dispersed passively by water currents (Sigurdsson et al., 1976; Beukema & de Vlas, 1989). Other groups of bivalves actively propel themselves into the water column by swimming and leaping (Ansell, 1969; Stanley, 1970). According to Stanley (1970), for bivalves swimming is defined as a mode of self-propulsion through the water. Swimming is observed only in a few groups of bivalves (Morton, 1964; Stanley, 1970). Scallops (Pectinidae) and file shells (Limidae) are notable in swimming by expulsion of water (Morton, 1980; Donovan et al., 2004). Propulsion of these groups arises from clapping the shells. Occasional swimming is observed in the Solenidae and Solemyidae (Stanley, 1970), which eject water to propel themselves by rapidly clapping the shell and retracting the foot. On the other hand, leaping is defined as launching the shell by kicking the substratum with the foot (Ansell, 1969; Stanley, 1970) and is not counted as swimming behaviour. This definition stresses the locomotive mechanism. Feder (1967) illustrated the leaping behaviour of Cardium [= Acanthocardia] as an escape response from starfish predation. Another species of Cardiidae, Laevicardium [= Fulvia] laevigatum can swim by pedal movement after leaping (Stanley, 1970), but the behaviour was only briefly described as “Swimming is accomplished by kicking against the water with the foot and simultaneously clapping the thin valves together to expel water ventrally”. Fraser (1967) reported that Tagelus divisus (Solecurtidae) swim by pedal movement after leaping, but the description was also very brief. To our knowledge, swimming by pedal movement has been regarded as a very rare behaviour and only minimal attention has been paid to

* Corresponding author: [email protected] 200 Y. Takada et al. its biological significance. In this study, we observed swimming behaviour of Mactra chinensis Philippi 1846 (Veneroida: Mactridae) by pedal movement. The focus of this study is to evaluate the frequency of the swimming behaviour in the laboratory. This behaviour was recorded by a video camera and the influence of shell size on the behaviour was investigated.

Materials and Methods

Dredge sampling was carried out at 7 m depth on a sandy bottom off Niigata (138°54´E, 37°52´N) on August 25th, 2008. The temperature of the bottom seawater was 25.6°C and the salinity was 33.0. Juvenile Mactra chinensis were sorted into four size classes by their shell length (7≤–<9, 9≤–<11, 11≤–<13, and 13≤–<15 mm, measured to 0.1 mm precision) and kept in a reserve tank (30 L, cylindrical transparent polycarbonate tank) with running natural seawater for 1 to 3 days before the experiments. An additional sampling was carried out at 6 m depth at the same area on October 22nd, 2008. At this time, the seawater temperature was 21.4°C and the salinity was 33.5. Clams of 31–35 mm size class (shell length 31≤–<35 mm, 0.1 mm precision) were sorted out and kept in the same tank as before. Clams of the other size classes were rare and could not be used for the following experiment. Swimming behaviour of the M. chinensis in the reserve tank was recorded by a hand-held video camera. Detailed observation was carried out in small cylindrical PVC experimental tanks (Fig. 1) of 30 cm diameter and 13 cm depth (9.2 L). The experimental tanks were placed in a darkroom with fluorescent lights (13–15 μmol m–2 sec–1, about 1000–1100 lux). Filtered seawater (25°C) flowed into the tank at a rate of 1.0 L min–1 from four tubes at the periphery of the tank and drained from the centre of the tank. Each batch of size sorted clams was placed gently in the experimental tanks: 100 individuals of 7–9, 9–11, 11–13 mm classes, 50 individuals of 13–15 mm class, and 20 individuals of 31–35 mm class. The clams were placed directly on the PVC bottom of the tank with one side of their shell down and they were spaced without contact with one another at the beginning of the experiment. The behaviour of the clams was recorded by a video camera right above the tanks for two hours starting directly after they were introduced into the tanks, and analyzed later. Occurrence of three types of behaviour (Tap, Leap, and Swim; see Results for details) at ten- minute interval was recorded. The duration and the length of each swimming bout were estimated from scanning consecutive frames of the video records that had 0.033 second intervals. The length

Fig. 1. PVC experimental tanks (diameter 30 cm, depth 13 cm) from a view of the video camera. Swimming of Juvenile Clam Mactra 201 of the swim was measured by projection onto the bottom of the tanks. Some of the swimming bouts were terminated when the clams collided with the wall of the tank, but most clams continued swimming after they hit the wall. Data for these clams were included in the following analysis. Effects of size on swim distance and period were analysed by one-way ANOVA. Before the ANOVA, the distance data were square-root transformed and homogeneity of variances was tested by Bartlett’s test (P > 0.05). In order to analyse the size effects on the regression between the period and distance of the swim, the most fitted regression model was obtained by calculating AIC of all the combinations of the size classes.

Results

Three types of behaviour in Mactra chinensis were recognized in the laboratory: Tap, Leap, and Swim. Tap involved rotating or sliding the shell on the bottom by extending and pushing the foot down to the bottom of the experimental tank. Leap involved launching the shell into the water column after a rapid push of the foot onto the bottom. The foot did not flap during the Leap. Swim involved launching the shell by the initial rapid push of the foot just like in the Leap, and then flapping the foot to propel the shell in the water column. During the Swim, the shell valve slightly opened but did not clap (Fig. 2; Supplemental material). The siphons and the foot extended from the shell, and the clam moved in a posterior direction (to the direction of the siphons). The ventral margin of the shell was upward and the shell swung from side to side with the flapping of the foot. In the 48th frame (in Fig. 2), the foot was bent perpendicular to the direction of the movement, and it was straightened in the next frame. The foot was kept straightened for the next three frames (0.1 seconds). Next, the foot was bent slowly to the opposite side of the shell and the shell rotated. It took nine frames (0.3 seconds) from one bend of the foot to the next. In the experimental tank, the clams showed Swim behaviour a number of times during the 2-hour observation period, except those in the 31–35 mm class (Table 1). Among the four size classes (7–9, 9–11, 11–13, and 13–15 mm), the maximum Swim distance was 42.0 cm in the 9–11 mm class, and the maximum Swim period was 4.07 seconds in the 13–15 mm class. Statistically significant differences were detected in the average Swim distance (one-way ANOVA, P < 0.05) and the average Swim period (one-way ANOVA, P < 0.05). Clams of smaller size classes tended to swim for a shorter distance and over a shorter period (Table 1: Tukey- Kramer, P < 0.05). The most fitted regression model between the period (x, second) and distance (y, cm) of the Swim (Fig. 3) was obtained when the four size classes were combined into two size groups. The regression line for the smallest size class (7–9 mm) was y = 3.528 + 5.972x, and that for the other size classes (9–15 mm) was y = 2.915 + 7.848x. These slope parameters demonstrate that the clams in the smallest class swim more slowly than the larger clams. The average Leap period and distance for 13–15 mm clams were 0.69 ± 0.08 sec and 4.20 ± 1.39 cm (± SD, n = 5), respectively. This demonstrates that the Swim distance (17.3 cm, Table 1) was 4.1 times further than the Leap distance. Frequencies of the three behaviours varied with time. Temporal decrease in the frequency was pronounced in the Tap behaviour (Fig. 4). An exponential function (y = a exp [b x]) can be fitted to the frequency (y) of the four classes of M. chinensis (except 31–35 mm class, n = 48) against the time from the beginning of the experiment (x minute) by a nonlinear regression procedure. The parameters of the exponential regression were statistically significant (a = 0.1399 ± 0.0106, b = –0.0335 ± 0.0036; ± SE, P < 0.05). The frequency of the Leap behaviour also appeared to decrease temporally from the beginning of the experiment, but variations between the size classes were large (Fig. 5). The frequency of the Swim behaviour increased at the beginning of the 202 Y. Takada et al.

45 46 47 48 49

50 51 52 53 54

Fig. 2. Swimming behaviour of Mactra chinensis in the reserve tank. Number on the top left corner is the sequential number of the frames (30 frames per second) from the beginning of the Swim.

Table 1. Swimming distance and period of Mactra chinensis in the experimental tanks during two hours observation. Size Distance (cm) Period (s) class Number Number of (mm) of clams Swim bouts Average (± SD) Maximum Average (± SD) Maximum 7– 9 100 72 11.78 ± 5.00a 31.6 1.38 ± 0.58a 2.97 9–11 100 106 14.15 ± 5.77ab 42.0 1.42 ± 0.60a 3.64 11–13 100 57 17.37 ± 8.14c 30.4 1.85 ± 0.75b 2.83 13–15 50 34 17.26 ± 6.12bc 32.0 1.85 ± 0.69b 4.07 31–35 20 0 – – – – Different superscript letters indicate significant difference (Tukey-Kramer, P < 0.05). experiments, then decreased thereafter (Fig. 5). It showed peaks during a period of 10–20 minutes from the start in the 7–9 mm, 9–11 mm, and 13–15 mm classes, and 20–30 minutes in the 11–13 mm class. Then, the frequency decreased gradually, with exception of the 13–15 mm class, which showed a second peak during the period of 40–50 minutes. The peak values were in the range of 0.16–0.32 times (individual–1 minute–1) for the four classes (7–15 mm). In these classes, the Swimming of Juvenile Clam Mactra 203

40

30

20 Distance (cm)

10 7 - 9 mm 9 - 11 mm 11 - 13 mm 13 - 15 mm 0 01234 Period (second) Fig. 3. Relationships between the period (x, second) and distance (y, cm) of the Swim behaviour. Lines show the linear regressions for smallest size class (7–9 mm, the broken line) and for the other size classes com- bined (9–15 mm, the solid line). frequency of the Swim behaviour at the peak was more than that of the Leap behaviour.

Discussion

Swimming and leaping behaviours This study revealed that swimming is not a rare behaviour for juvenile Mactra chinensis in the laboratory. This species swims by pedal flapping after launching from the bottom by leaping, but without clapping the shell valves (Fig. 2). It differs from Fulvia laevigatum, which claps its shells during swimming after leaping using the foot (Stanley, 1970). Although the hydrodynamic mechanisms of swimming are beyond the focus of this study, shell clapping by Fulvia is thought to cause ejection of water that helps to propel the shell. The result of this study suggests that pedal movement is the only propulsive force during the swimming of M. chinensis. Absolute swimming speeds (cm sec–1) of juvenile M. chinensis are 6.0 (7–9 mm shell length) and 7.8 (9–15 mm) on average. This value is much lower than that for Amusium pleuronectes (45 cm sec–1 for 65 mm shell height, Morton, 1980) and other scallops (Brand, 2006), but slightly higher than in Limaria fragilis (4 cm sec–1 for 27 mm shell height, Donovan et al., 2004). Because of the small shell length of juvenile M. chinensis, relative swimming speeds (body length sec–1) are 7.5 (7–9 mm shell length) and 6.5 (9–15 mm), which are comparable to the 6.9 of A. pleuronectes and higher than the 1.5 of L. fragilis. Both A. pleuronectes and L. fragilis swim by water ejection. The results of this study show that pedal flapping creates a fairly effective locomotive force for swimming and is as effective as water ejection. 204 Y. Takada et al.

0.2 y=0.1399 × exp(-0.0335 t) ) -1

0.15 minute

-1 7-9 mm 9-11 mm 11-13 mm 13-15 mm 0.1 31-36 mm

0.05 Frequency of Tap (individual

0 0 10 20 30 40 50 60 70 80 90 100 110 120 Time (minute) Fig. 4. Temporal change in the frequency of the Tap behaviour for the five size classes of Mactra chinensis. The frequencies were counted for 10 minute intervals and the frequency values per individual per minute were calculated. An exponential curve fitted to the data points for the four smallest size classes (7–15 mm in shell length, n = 48) is also shown. The largest size class (31–35 mm in shell length) does not fit the curve and is represented by broken lines.

) 0.25 0.2

-1 7-9mm 11-13mm 0.2 Leap 0.15 Swim 0.15 0.1 minute -1 0.1 0.05

0.05 0

0 0.25 13-15mm 0.35 0.2 9-11mm 0.3 0.15

0.25 0.1

0.2 0.05

0.15 0

0.1 0.1 31-36mm 0.05 0.05

0 0 Frequency of Leap and Swim (individual 0 10 20 30 40 50 60 70 80 90 100 110 120 100 20 30 40 50 60 70 80 90 100 110 120

Time (minute) Fig. 5. Temporal change in the frequency of the Leap and Swim behaviours for the five size classes of Mactra chinensis. The frequencies were counted for 10 minute intervals and the frequency values per individ- ual per minute are shown. Swimming of Juvenile Clam Mactra 205

The leaping behaviour of M. chinensis is the same as that of M. stultorum [= M. coralline] described by Ansell (1969). The foot was extended and bent back under the shell, and then pressed suddenly against the bottom, lifting the shell into the water column. Mactra chinensis launches from the bottom by leaping before it flaps the foot for swimming. The swimming behaviour is a consecutive sequence of combined behaviours of the foot; a kick onto the substratum that enables leaping, and the flapping in the water that enables swimming. Considering that the swimming behaviour follows the leap and that the larger individuals (>31 mm) perform leaping but not swimming, the pedal movement during the swimming may be considered to be a behaviour derived from a modification of the leaping behaviour.

Possible factors for the swimming and leaping behaviours Ansell (1969) summarized three types of stimulus responsible for the occurrence of leaping behaviour: 1) predators, 2) failure of burrowing after disturbance, 3) removal of the from water. In this study, the bottom of the experimental tanks was not covered by sediment. The Tap behaviour in this study can be regarded as a sequence of probing the bottom with the foot but failing to burrow. So in this study, the leap and tap behaviours occurred under the Ansell’s second condition. In addition, the occurrence of peak frequency of swimming after 10–20 minutes suggests the possibility that M. chinensis carried out swimming after its trials of tapping and leaping had failed to find a good place to burrow. In its natural habitat, M. chinensis may avoid benthic predators. Seastars and naticid gastropods are well-known predators that induce leaping (Feder, 1967; Ansell, 1969). At the sampling area of the sandy bottom off Niigata, the seastars Astropecten latespinosus and A. scoparius, and gastropods Neverita didyma and Philine orientalis are potential predators on juvenile M. chinensis. The naticid gastropod N. didyma is known to cause leaping behaviour in the bivalve Ruditapes philippinarum (Rodrigues, 1986), and it is also known that adult M. chinensis leap to escape from N. didyma (Okutani, 2003). The juvenile clams of 13–15 mm shell length travelled 4.2 cm away from the start point by leaping, and 17.3 cm by swimming on average, including some individuals that stopped swimming at the wall of the experimental tank. So swimming can extend the escape distance to at least 4.1 times further than leaping, and this possibly further reduces the risk of predation. Swimming can be concluded to be an adaptive escape behaviour when a predator approaches juvenile M. chinensis. Ansell’s third condition, the removal from water, is thought to be an artificial stimulus and does not fit into the present study. But in this study, the clams experienced handling disturbances before the start of the observations. Temporal decreasing trends of Tap, Leap, and Swim behaviours (Figs. 4, 5) indicate that handling disturbances stimulated these behaviours and the stimulus may decrease with time. However, it is also possible that a decrease in stored energy in the clams may cause the temporal decreasing trends in these behaviours. Flow of water is thought to be one of the cues that initiate the swimming behaviour. The shallow sandy bottoms that M. chinensis inhabits are frequently disturbed by rough waves and currents induced by rough weather, and juveniles are thought to be frequently washed out from the sediment (Sakurai et al., 1996). The maximum burrowing depth of M. chinensis is to 0.4 times the shell length below the surface of the sediment (Kondo, 1987). A clam of 15 mm shell length can be completely washed out by disturbance of only 21 mm of the sediment. When M. chinensis is washed out it tries to actively re-burrow. But, high water flow may affect its ability to align in a burrowing posture and prevent it from burrowing (Sakurai, 2002). In such a case it may be adaptive to find another place where the water flow is low enough to burrow, by leaping and/or swimming during periods of turbulence.. The results of this study showed that M. chinensis of 31–35 mm shell length did not show swimming behaviour, although they did leap. The decrease of the relative swimming speeds (body 206 Y. Takada et al. length sec–1) from 7.5 to 6.5 with the increase in the size of juvenile clams indicates that smaller clams may swim better than larger clams. Larger clams may not generate enough force to swim by pedal flapping. Alternatively, swimming for the larger clams may not be cost effective from hydrodynamic and energy expenditure viewpoints. Considering that the mature size of M. chinensis is about 30 mm (Sakurai et al., 1992), the clams may stop swimming after reproductive maturation. We do not know much about the life history strategies of M. chinensis in their early life stage (Sakurai et al., 1996); however, it may be adaptive for clams to increase investments in reproduction and reduce investments in locomotion after reproductive maturation. In conclusion, the results of this study showed that M. chinensis of 7–15 mm shell length have the ability to swim by pedal flapping, and during laboratory observations this behaviour readily occurred. Larger individuals of 31–35 mm shell length did not show swimming but they still performed leaping. The pedal flapping extends the range of locomotive distance through the water column and is a potentially adaptive behaviour to reduce the risk of predation and increase the chance to find a better place to burrow.

Supplemental Material

Supplemental video of the swimming behaviour of Mactra chinensis in the reserve tank is available at http://www.momo-p.com/index.php?movieid=momo130516mc01b.

Acknowledgments

We wish to thank the faculty and staff of the Japan Sea National Fisheries Research Institute for research space and support. This research received no specific grant from any funding agency, or from the commercial or non-profit sectors.

References

Ansell, A. D. 1969. Leaping movements in the . Proceedings of the Malacological Society of London 38: 387–399. Beukema, J. J. & de Vlas, J. 1989. Tidal-current transport of thread-drifting postlarval juveniles of the bivalve Macoma balthica from the Wadden Sea to the North Sea. Marine Ecology Progress Series 52: 193–200. Brand, A. R. 2006. Scallop ecology: distributions and behaviour. In: Shumway, S. E. & Parsons, G. J. (eds.), Scallops: Biology, Ecology and Aquaculture, pp. 651–744. Elsevier B. V., Amsterdam. Donovan, D. A., Elias, J. P. & Baldwin, J. 2004. Swimming behaviour and morphometry of the file shell Limaria fragilis. Marine and Freshwater Behaviour and Physiology 37: 7–16. Feder, H. M. 1967. Organisms responsive to predatory sea stars. Sarsia 29: 371–394. Fraser, T. H. 1967. Contributions to the biology of Tagelus divisus (Tellinacea: Pelecypoda) in Biscayne Bay, Florida. Bulletin of Marine Science 17: 111–132. Kondo, Y. 1987. Burrowing depth of infaunal bivalves — Observation of living species and its relation to shell morphology. Transactions and Proceedings of the Palaeontological Society of Japan, New series 148: 306–323. Morton, B. 1980. Swimming in Amusium pleuronectes (Bivalvia: Pectinidae). Journal of Zoology, London 190: 375–404. Morton, J. E. 1964. Locomotion. In: Wilbur, K. M. & Yonge, C. M. (eds.), Physiology of , Vol. 1, pp. 383–423. Academic Press, New York. Okutani, T. 2003. Twenty Biological Tales of Mollusks. 172 pp. Tokai University Press, Hadano. (in Japanese) Rodrigues, C. L. 1986. Predation of the naticid gastropod, Neverita didyma (Röding), on the bivalve, Ruditapes philippinarum (Adams & Reeve): evidence for a preference linked functional response. Publi- cations from the Amakusa Marine Biological Laboratory, Kyushu University 8: 125–141. Sakurai, I. 2002. Habitat condition critical of the surf clam Mactra chinensis in relation to bottom disturbance. Fisheries Engineering 39: 155–160. (in Japanese with English abstract) Swimming of Juvenile Clam Mactra 207

Sakurai, I., Kurata, M. & Abe, A. 1996. Age structure and mortality of the sunray surf clam Mactra chinensis off Tomakomai, southwest Hokkaido. Fisheries Science 62: 168–172. Sakurai, I., Kurata, M. & Miyamoto, T. 1992. Breeding season of the sunray surf clam Mactra chinensis in Tomakomai, southwest Hokkaido. Nippon Suisan Gakkaishi 58: 1279–1283. (in Japanese with English abstract) Sigurdsson, J. B., Titman, C. W. & Davies, P. A. 1976. The dispersal of young post-larval bivalve molluscs by byssus threads. Nature 262: 386–387. Stanley, S. M. 1970. Relation of shell form to life habits of the Bivalvia (Mollusca). The Geological Society of America, Memoir 125: 1–296. Williams, A. B. & Porter, H. J. 1971. A ten–year study of meroplankton in North Carolina estuaries: occurrence of postmetamorphal bivalves. Chesapeake Science 12: 26–32.

(Received October 29, 2012 / Accepted March 25, 2013)

バカガイ幼貝の足による遊泳行動

高田宜武・伊藤祐子・林 育夫

要 約

バカガイ Mactra chinensis幼貝の遊泳行動を実験室内で観察した。殻長 7～15 mm の小型のバカガイは 底面から跳躍後に，足を左右に振って遊泳した。遊泳速度は殻長 7～9 mm の個体で毎秒平均 6.0 cm， 9～15 mm の個体で毎秒平均 7.8 cmであった。遊泳距離は平均 17.4 cmであった。殻長 31～35 mm のや や大きい個体は，跳躍はするものの遊泳行動は認められなかった。水塊中でのバカガイの移動距離は，足 を振って遊泳することにより，単なる跳躍よりも 4.1倍増加した。したがって野外での遊泳行動は，捕食 のリスクを低減するとともにより良い生息場所に潜砂できる可能性を増加させる適応的行動だと思われ る。