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Orientated swimming by megalopae of several eastern North Pacific crab species and its potential role in their onshore migration
Journal of Experimental Marine Biology and ELSEVIER
Ecology
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
186 (1995) l-16
Orientated swimming by megalopae of several eastern North Pacific crab species and its potential role in their onshore migration Alan L. Shanks University of Oregon, Oregon Institute of Marine Biology, Charleston, OR 97420, USA Received 4 March 1994; revision received 12 September 1994; accepted 13 September 1994
Abstract The megalopal stage of most near shore and intertidal crabs must return to the coast to complete their development. Crab megalopae are strong swimmers and if they swam consistently shoreward they could conceivably swim back to shore. This hypothesis was tested for megalopae of Pachygrapsus crussipes (Randall), Lophopanopeus bellus bellus (Stimpson, 1860), Cancer oregonensis (Dana), and C. gracilis (Dana) by investigating their swimming orientation when housed in a transparent container with a view of the underwater illumination or swimming freely in the sea. In the transparent container, megalopae tended to swim in the direction of the sun’s bearing. Free swimming megalopae swam straight courses and displayed significant preferred swimming directions. Puchygrupsus crassipes and L. bellus bellus megalopae swam at the sea surface and parallel to the current direction. Free swimming C. oregonensis and C. grucilis swam at about 3 to 5 m depth and in the direction of the sun’s bearing. Megalopae of Puchygrupsus crassipes and C. oregonensis were observed on 4 and 3 days respectively and they did not preferentially swim in a shoreward direction. These results suggest that they do not migrate back to shore by swimming. The orientated swimming may, however, assist the megalopae in returning to shore or locating a settlement site. Swimming with the surface current might help megalopae to migrate shoreward in the convergence zone over internal waves or Langmuir circulation cells. Swimming in the direction of the sun’s bearing might represent a search behavior for a benthic settlement site. Keywords: Behavior;
Cancer;
Crab; Dispersal;
Megalopae;
Orientation
1. Introduction Larvae 4 months
of brachyuran to complete
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SSDI
crabs from the eastern North Pacific Ocean require from 2 to their development (Lough, 1974). At the end of the period of
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B.V. All rights reserved
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planktonic development the megalopae must seek out the habitat which they will occupy as juveniles or adults. For coastal crabs this is frequently the intertidal and shallow subtidal environments. In the waters off Oregon, Lough (1974) found that the larvae of many coastal crabs dispersed to about 16 km from shore. Thus, the megalopae of these crabs must make a fairly extensive cross-shelf migration in order to regain the shore. Two possible mechanisms for this shoreward migration can be suggested: the megalopae may actively swim ashore in a well oriented fashion or they may utilize cross-shelf currents and be swept ashore (Shanks, 1987). Researchers have suggested that the larvae of several coastal fishes (Powles, 1981) the puerulus of the Australian rock lobster, Punulirus cygnus, (Phillips, 1981) and postlarval Homarus americanus (Cobb et al., 1989) might migrate ashore by swimming. In the case of the puerulus of Panulirus qgnus and postlarval H. nmericunus, this suggestion was based, at least in part, on their strong swimming ability. Swimming speeds of Punulirus qgnus puerulus range from 15 to 46 cm.s ’ (Phillips & Olsen, 1975) and for H. americnnus from 7 to 13.2 cm s ’ (Rooney & Cobb, 1991). Further, H. americanus postlarvae have been observed to swim oriented straight line courses at the ocean’s surface (Cobb ct al., 1989). These postlarvac are strong swimmers which, if their swimming were directed shoreward, might be capable of making a swim-ashore migration. Could a larval crab make a return migration by swimming? Bainbridge (1957) in one of the earliest uses of diving gear to study zooplankton, observed crab megalopae swimming straight line courses near the ocean’s surface. Many megalopae are strong swimmers (pers. obs.; Shanks, 1985; Luckenbach & Orth, 1992). For example, the megalopae of Pachqgrapsus crussipes are capable of sustained speeds of 9.5 cm.ss’ (Shanks, 1985). If these megalopae were to swim at this speed in a consistent direction for the entire duration of the megalopa stage (at least 10 days, pers. obs.), they could cover distances in excess of 80 km, more than 5 times the distance to which they are, on average, dispersed off shore (Lough, 1974). An onshore migration based on active swimming would be of obvious advantage only to larvae which swam in the correct direction, e.g. eastward along the west coast of North America. The question addressed in this study is whether the megalopae of several coastal crab species from the eastern North Pacific Ocean orient their swimming in an eastward or onshore direction. Daytime observations were made of the swimming orientation of megalopae in containers from which they had a clear view of the underwater illumination and released to swim freely in the ocean.
2. Methods A variety of methods were used to obtain megalopae for the following experiments. Pachygrapsus crussi’es megalopae used in the 198 1 and 1982 experiments were caught in traps consisting of bundles of hemp or cotton rope (Shanks, 1983) hung from the end of the Scripps Institution of Oceanography pier (35” 5’ N, 177” 5’ W). The L. bellus bellus megalopae were not captured, but were observed swimming in the surface waters of Park Bay, San Juan Islands, Washington (48” 40’ N, 123” 0’ W).
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Megalopae of Cancer oregonensis and C. gracilis were attracted to a night light hung from the pier at the Friday Harbor Laboratories, San Juan Islands, Washington, and caught with a dip net. Megalopae of Pachygrapsus crassipes, C. oregonensis, and C. gracilis were held in running seawater systems for t24 h prior to their use in field observations. Observations were made on the swimming direction of contained megalopae which had an unobstructed view of the underwater illumination. Ten megalopae were placed in a sealed transparent Plexiglas cylinder (15 cm diameter x 10 cm height filled with sea water). Using SCUBA, the viewing chamber was carried to ~3 m depth. The cylinder was maintained in a constant compass orientation by lining a reference mark on the cylinder up with north on a compass afhxed to the handle of the apparatus. After about a 5-min wait to allow the animals to adjust to the underwater illumination the megalopae swimming in each 30” sector of the cylinder were counted. On 1, 9, and 15 March 198 1 and 3 June 1982 observations were made on the megalopae of Pachygrapsus crassipes. On 31 July 1992 observations were made on C. oregonensis megalopae. Free release experiments of megalopae were made in the ocean using methods analogous to those used in the study of pigeon orientation (Schmidt-Koenig, 1979). Approximately 20 megalopae were placed in a 50-ml syringe filled with sea water and transported to the release site. Pachygrapsus crassipes megalopae were released on 1, 9, and 15 March 1981 and 3 June 1982. The release site on 1 March was offshore from the Scripps Institution of Oceanography in water about 6 m deep. The releases on 9 and 15 March and 3 June were made z 150 m from shore at Goldfish Point in La Jolla, California, in water about 10 m deep. Observations of swimming orientation of C. oregonensis and C. gracilis were made in Park Bay and West Sound in the San Juan Islands, Washington. Water depth at each of these release sites was about 10 m. All releases were made at depths of from 2 to 5 m. All of the Pachygrapsus cmssipes megalopae which were successfully released (i.e. those which were not lost from sight, eaten by fish, or swam to and settled on the observer) immediately swam to the surface where they began to swim horizontally at depths < 0.1 m (Shanks, 1985). Each megalopa was followed to the surface, maintaining a distance of 1 to 2 m, just keeping the individual within sight. When the animal reached the surface and began swimming horizontally, the vanishing direction of the swimming megalopa was noted to the nearest 5” using a hand held sighting compass. C. oregonensis and C. gracilis megalopae swam upward 1 to 2 m following their release (see below). As with Puchygrapsus crassipes megalopae, each megalopa was followed until it began to swim horizontally at which point the vanishing direction of the swimming megalopa was noted. To see if swimming direction remained constant, following the determination ofthe vanishing direction, the observer swam in the direction in which the just-released megalopa had last been swimming. These observations were attempted on about half of the free releases. For the Pachygrapsus crassipes observations the direction of the brightest underwater illumination, the sun’s bearing at the surface, wind direction, surface wave direction and surface current direction were all noted. Current direction was determined by noting the orientation of strips of plastic bag tied to a buoyed and weighted line set in the center of the release site. A nearly identical set of physical observations were made during the San Juan Islands free releases. During these latter observations, current
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speed and direction were measured with an Inter Oceans S-4 current meter set at the depth at which the released megalopae swam. Lophopanopeus bellus bellus were observed from the deck of a motor boat. They were swimming at the surface within the convergence zone associated with a tidally-forced internal wave (Shanks & Wright, 1987). These observations were made in Park Bay, San Juan Islands, Washington on 6 May 1986. Swimming directions of the megalopae were noted as the boat glided slowly through the convergence. To control for the possibility that the megalopae were simply swimming away from the boat, the boat was steered through the convergence several times and from several different compass headings. The sun’s direction and the direction in which the internal wave convergence was propagating were noted. Winds were too light to produce waves.
3. Results 3. I. Pachygrapsus
crassipes
On 1 and 9 March 1981 the swimming directions of the contained Pachygrupsus were not significantly different from random (Fig. 1, Rayleight Test, p> 0.05). The sky on 1 March was overcast and the sun was not visible. The sky was clear on 9 March. On the remaining two dates (15 March and 3 June), however, the distributions of swimming directions of contained megalopae were significantly oriented (Fig. 2, Rayleigh Test, P-C 0.05). On these latter two dates the mean angle of orientation deviated little from the sun’s bearing (i.e. deviations were 9” and 4” for 15 March and 3 June, respectively). These data suggest that, on the days when the megalopae within the container displayed a statistically preferred swimming direction, they were swimming in the direction of the brightest underwater illumination or toward the sun. Due to a variety of problems, the swimming direction of less than half of the Pachygrapsus crassipes megalopae released was measured. The megalopae are less than a centimeter in total length and some animals were simply lost from view. Releases were made close to shore in an area where there were a number of juvenile fishes. A number of megalopae fell prey to these fishes. The major problem, however, was due to the strong thigmokinesis displayed by Puchygrupsus crussipes megalopae (Shanks, 1985). If the observer approached a megalopa too closely the animal would turn, swim towards him, and climb onto his person. Upon successful release (57 successful releases out of about 240 attempted), Pachygrupsus crassipes megalopae tumbled about for several seconds, oriented to the surface, and then rapidly swam upward (Shanks, 1985). They swam up to the surface until they actually contacted the surface of the ocean (from below they could be seen to dimple the ocean’s surface). At the surface they began to swim horizontally at depths < 10 cm. Without hesitation they adopted a swimming direction and they began to swim steadily in this direction. Swimming directions appeared to be bimodal and with or against the current. More than half of the animals appeared to swim in the direction of the current and these rapidly disappeared from view. About 20”< of the released animals appeared to swim against the current. These individuals often took a long time crussipes megalopae
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1 March 1981 Current
S %Angle = 180” + 74” r=o.l73,n=iO NS
f Angle = 319” ?:22” r = 0.700, n = 10, P = 0.005 9 March 1981
E
Sun’s Bearing
S
X Angle = 278” +-25” r = 0.628, n = 20, PC 0.001
Sun’s Bearing
S
ii Angie = 120” +-77” r = 0.100, n = lo, NS
Fig. 1. Swimming orientation of Puchygrupsus crassipes megalopae swimming freely in the water column (left-hand figures) and housed in a transparent Plexiglas container with a view of the underwater illumination (right-hand figures). . indicate the swimming direction of each megalopa. The labelled arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath each circular figure are the results of the Rayleigh circular statistics test. Due to the behavior of the freely swimming megalopae (see text) the distribution of swimming directions was considered to be bimodal (left-hand figures). The data were analysed following the rules for axially symmetric data (Batschelet, 1981).
to swim out of view. Many, in fact, appeared to be making no forward progress even though they were swimming actively. On a number of the releases the observer swam in the direction in which the animal was seen to be swimming when it vanished. Usually I was able to find the animal and they had in all cases maintained their swimming
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15 March 1981 N
vn*s
Searing
vr+g
S
S
E Angle = 135” ? 35” r = 0.818, n = IO, P~O.001
f Angle = 268” k 30” r z 0.475, n = 13, P~0.05 3 June 1982
E
W
KAngle = 110” + 30” r = 0.452, n = 14, P = 0.0567
W
E
Z Angle = 176” t 33” r = 0.835, n = 10, P = 0.001
Fig. 2. Swimming orientation of Pach~grapsus crassipes megalopae swimming freely in the water column (left-hand figures) and housed in a transparent Plexiglas container with a view of the underwater illumination (right-hand figures). . indicate the swimming direction of each megalopa. The labelled arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath each circular figure are the results of the Rayleigh circular statistics test. Due to the behavior of the freely swimming mcgalopae (see text) the distribution of swimming directions was considered to be bimodal (left-hand figures). The data were analysed following the rules for axially symmetric data (Batschelet, 1981).
direction. Puchygrqsus cmssipes megalopae appeared to be and flat course over distances of at least meters to tens of The behavior of the free swimming megalopae and the directions both suggested that the vanishing angles were
able to maintain a straight meters. distribution of swimming bimodally distributed and
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centrally symmetric. To apply circular statistics to axial data all vanishing angles were doubled (Batschelet, 1981). The Rayleigh test indicated that there was on each date a statistically significant preferred direction to the orientation of the free swimming megalopae (Figs. 1 and 2). There were large deviations between the sun’s bearing and the mean swimming direction (i.e., mean angle in Figs. 1 and 2) of the megalopae on each release date. The differences between the sun’s bearing and the mean swimming direction of the megalopae were 199”, 78”, 151”, and 70” for 1, 9, and 15 March and 3 June, respectively. On 15 March there was a strong offshore wind. The release site was within 150 m of shore and in the lee of coastal hills. The waters at the release site were glassy. On the other three release dates waves were present. The mean swimming direction deviated from the wave direction by 49”, 32”, and 180” on 1 and 9 March and 3 June, respectively. The mean swimming directions of the released megalopae deviated little from the current direction (deviations were 5 O, 12”, 1 O, and 10” on 1, 9, and 15 March and 3 June, respectively). The observed behavior of the free swimming megalopae and the similarity between the mean swimming orientation and the current direction suggest that the megalopae were orientating to the local current direction. 3.2. Lophopanopeus
bellus bellus
Megalopae of L. bellus bellus were observed in Park Bay from the deck of a motor boat. All of the individuals were swimming just below the surface (several centimeters depth) in the convergence zone over an internal wave (Shanks & Wright, 1987). Although the total length of these megalopae is only 0.5 cm they were clearly visible even when standing in the boat. The animals were darkly pigmented, almost black, and there was a reflective green patch in the center of their carapace. Observations were made on the swimming direction of 24 individuals. The distribution of swimming directions was unimodal and the Rayleigh test indicated that there was a statistically significant preferred swimming direction (Fig. 3). The mean swimming direction was 97” and the 95 y0 confidence interval was k 24”. The sun’s bearing (150 “) was outside the 95 y0 confidence interval indicating that the megalopae were not orientated toward the sun. The direction of the internal wave’s propagation was 100”. The mean swimming direction differed by only 3” (well within the 95% confidence interval around the mean angle) from the direction in which the internal wave was propagating. These data suggest that the L. bellus bellus megalopae were swimming in the direction of propagation of the internal wave. 3.3.
Cancer oregonensis
Observations on the behavior of C. oregonensis were made toward the end of the settlement season for this species. Enough animals were caught late in July to make observations on both contained and free swimming animals, but on later dates too few animals were caught for both sets of observations to be made. Observations of the swimming orientation of contained C. oregonensis megalopae were made on 31 July 1992. The Rayleigh test indicated that the contained megalopae had a preferred swim-
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Y Angle = 97” f 49”, 95% Confidence Interval f 24” r = 0.637, n = 24, P< 0.001 Fig. 3. Swimming orientation of L. b&s bellus megalopae swimming at the surfxc in the convergence zone over an internal wave. . indicate the swimming direction of each megalopa. The labelled arrows indicate the direction in which the internal wave was propagating (and, hence the direction of the surface current in the convergence), sun’s bearing, and the mean swimming angle of the megalopae. Beneath the figure are the results of the Rayleigh circular statistics test.
ming direction (Fig. 4). The mean angle of this swimming direction deviated only 2” from the sun’s bearing. Like contained Pachygrapsus crussipes megalopae, contained C. oregonensis megalopae appeared to be swimming toward the brightest sector of the underwater light field or toward the sun. The behavior of free released C. oregonensis megalopae (38 successful released out of 63 attempted) was strikingly different from that of Pachygrapsus crussipes. Following ejection from the syringe, C. oregonensis megalopae tumbled about for a second or two and then, with their legs extended and their body oriented horizontally, they rotated. After several rotations they tucked all or all but the most anterior pair of legs under their body and began to swim upward at a slight angle. Animals were released at 5 m depth and most individuals swam toward the surface for 1 to 2 m before beginning to swim a level course. They maintained a fixed bearing through out this time. Superimposed on this straight-line swimming were vertical and horizontal oscillations with amplitudes of around 5 cm. Occasionally animals would extend all of their legs, rotate again, and then swim off in the same direction in which they had previously been swimming. No matter how closely megalopae were approached none swam toward the observer, who was again able to swim in the vanishing direction and locate some of the megalopae. All had maintained the initial swimming direction. These data suggest that C. oregonensis megalopae were able to maintain a straight and level course over distances of meters to tens of meters while swimming within the water column. Distributions of swimming directions of free swimming C. oregonensis megalopae were unimodal and the Rayleigh test indicated that the megalopae had statistically significant preferred swimming directions (Fig. 4). On none of the three sample dates
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Sun’s Bearing 31 July 1992 a Angle = 176” + 39” r = 0.771, n = 18, Pd 0.001
31 July 1992 X Angle = 150” + 38” r=0.781,n=7,P=0.009
N
W
S 3 August 1992 f Angle = 223” k 52” r = 0.590, n = 14, P = 0.006
27 August 1992 f Angle = 107” f 27” r = 0.891, n = 6, P< 0.004
Fig. 4. Swimming orientation of C. oregonensis megalopae swimming freely in the water column (A, C and D) and housed in a transparent Plexiglas container with a view of the underwater illumination (B). . indicate the swimming direction of each megalopa. Arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath each circular figure are the results of the Rayleigh circular statistics test.
was the current direction within the 95% confidence interval of the mean swimming direction. On 31 July and 3 August, when surface waves were present, the wave direction was also outside the 95% confidence interval around the mean swimming direction. The three free releases were made at different times of the day and the mean
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swimming direction appeared to change with the direction of the sun’s bearing. On each of the three sample dates the sun’s bearing was well within the 95 7; confidence interval of the mean swimming direction. The average difference between the mean swimming direction and the sun’s bearing was only 10”. These data suggest that C. oregonerzsis megalopae were swimming toward the brightest sector of the underwater illumination. On 27 August the weather was partly cloudy. The sun went behind the clouds during three releases. Interestingly, these three animals swam at about 180” to the sun’s bearing (square data points in Fig. 4, 27 August). These data were excluded from the Rayleigh test analysis. 3.4.
Cancer gracilis
Too few megalopae of this species of crab were caught to make observations on both contained and freely swimming individuals. Only observations on freely swimming megalopae were made. Further, C. gracilis megalopae are small (around 0.5 cm in total length), and were difficult to follow underwater. Upon release many animals were lost from view. This difficulty led to a low number of observations (seven successful released out of 35 attempted). Observations on the swimming behavior of C. grucilis megalopae were made on 27 August 1992. Following their release, the behavior of these megalopae was identical to that of C. ovegonensis. The distribution of swimming directions was unimodal and significantly directed (Fig. 5). Due to the low number of replicate observations it was not possible to determine the 95”/, confidence interval around the mean swimming N
Bearing
f Angle = 82” f 35” r = 0.814, n = 7, P = 0.005 Fig. 5. Swimming orientation of freely swimming C. gradis megalopae released on 27 August 1992. . indicate the swimming direction of each megalopa during the time the sun was visible. The open boxes represent observations made while the sun was behind clouds. The labelled arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath the figure are the results of the Rayleigh circular statistics test. The Rayleigh test was made using only the data collected when the sun was visible.
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direction. The mean swimming direction of C. gracilis deviated 33” from the sun’s bearing, within & one angular deviation of the mean swimming direction. Like C. oregonensis megalopae, C. gracilis megalopae appeared to be directed toward the sun’s bearing.
4. Discussion The megalopae observed in this study displayed the characteristics of organisms which might migrate to shore by swimming. That is, they were found to be (1) strong swimmers that swam straight and oriented paths, (2) they swam steadily and continuously, and (3) they were able to maintain their course over distances of at least several tens of meters. Due to logistical limitations it was impossible to measure in situ swimming speeds, but they were probably on the order of 5 cm*s-‘. Ignoring the effects of currents, if these megalopae swam for 12 h per day for 10 days they could cover about 20 km, a substantial distance. If their swimming was directing them back to the coast (i.e. the west coast of North America for these species) then they should have orientated to the east. Multiple observations were made on two species, C. oregonensis and Pachygrapsus crassipes. Neither swam preferentially to the east. C. oregonensis swam toward the brightest sector of the underwater illumination or toward the sun’s bearing. Thus, in the morning they swam toward the east, but by afternoon they swam westward. Pachygrupsus crussipes megalopae appeared to be swimming relative to the local current direction. About half of the released animals swam to the west. The present data do not support the hypothesis that these two species migrate shoreward by directed swimming. Two species were observed on only one date and the mean swimming direction in both cases was close to eastward. Because of the limited number of observations these data cannot be used to make conclusive generalizations. The mean swimming direction of C. gracilis was 82 ‘, nearly eastward. The sun’s bearing was 115’ so it is quite possible that, like C. oregonensis, C. gracilis was swimming toward the brightest sector of underwater illumination. Lophopanopeus bellus bellus had a mean swimming direction of 97’) also nearly eastward. This swimming direction may be a response to the flow field within the internal-wave convergence in which they were observed (see below). If however, “eastward” is defined as between 45” and 135’ then 29% and 38% of the C. gracilis and L. bellus bellus megalopae respectively were not swimming east. These species have been in existence since at least the Pleistocene (Menzies, 1951) or in excess of a million generations. Given the strong selective advantage of swimming in the correct direction it seems doubtful that such a large percentage of their megalopae would be found swimming in the “wrong” direction. All of the megalopae were released during the day and all remained in the well illuminated surface waters. Cancer oregonensis and C. gracilis swam at depths <5 m while Pachygrapsus crassipes and L. bellus bellus swam within centimeters of the ocean’s surface. All of these megalopae are relatively large for meroplankters, 0.5 to 1 cm in total length, and were visible in the water. Large meroplankton, such as these mega-
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lopae, which remain at or near the surface during the daytime expose themselves to visual predators. In fact, one of the common causes for unsuccessful releases of Pachygrapsus crassipes megalopae was that they were consumed by fishes at the release site. Furthermore, Cancer megalopae are a common component in the diet of silver salmon (Anon., 1949; Brodeur et al., 1987). Swimming at or near the ocean’s surface during daylight would seem to be a maladaptive behavior unless, of course, the behavior serves some additional and compensating purpose within the life cycle of the organisms. One possibility is that the swimming behavior might aid in the onshore migration of the megalopae. They apparently do not actually swim ashore, but by swimming they may somehow increase their chances of returning to shore and finding a suitable habitat in which to settle. The behavior of the organisms observed during this study fall into two categories: those which swam at several meters below the surface and those which swam at the surface. Both C. oregonensis and C. gtmilis swam several meters below the surface. The swimming of C. oregonensis was clearly oriented toward the sun. The swimming orientation of C. grucilis may also have been oriented toward the sun, but too few observations are available for a clear conclusion. During the course of a day C. oregonensis would swim a large arc; toward the east in the morning with a steady shift to the west in the afternoon. If a 5 cm.s -’ swimming speed, a 12-h day, and no current is assumed, then a megalopa could swim an arc about 2 km long. What could be the adaptive advantage to this behavior? Like swimming in the surface waters during daylight, this behavior probably increases the chances that the megalopae will be consumed by predators. A megalopa swimming steadily along in a straight line is, undoubtedly, a more obvious target to a visual predator than one that is holding still (Zaret, 1980). Furthermore, steady orientated swimming by increasing the volumn of water through which the megalopae pass would increase their chances of encountering cnidarian predators (e.g. medusae and siphonophores). In fact, megalopae as well as other meroplankton are a common component in the diet of a number of siphonophores (Purcell, 198 la,b). The directed swimming behavior could represent a search behavior for a patchy food source. However, the carapace of megalopae commonly contains large oil droplets (pers. obs.), which suggests that they possess a substantial energy reserve. Given this energy reserve and the probable increased risk of predation due to directed swimming, it is doubtful whether the directed swimming behavior of C. oregonensis is a search for a patchy food supply. To complete their life cycle, C. oregonensis megalopae must settle in the shallow subtidal or low intertidal zone (Morris et al., 1980). Perhaps the directed swimming behavior is a mechanism for searching for a settlement site. The depth at which the megalopae swam (several meters) would, at low tide, cause them to settle at shallow subtidal depths and, at high tide, at low intertidal depths. The directed swimming would allow them to search a path of the order of z 2 km long per day. During the megalopal stage, which lasts one to several weeks, an individual might be able to search 10 to 30 km of water for a settlement site. It is difficult to see, however, how the swimming behavior of C. oregonensis might
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cause an onshore migration. Despite all of their swimming, megalopae kilometers from shore, in the waters over the continental shelf, would remain kilometers from shore. As they were carried along by a current, the observed swimming behavior would cause them to swim through, and perhaps, search a large volume of water, but they would only encounter the shoreline if the current carried them there. The observations reported in this paper were made close to shore and during daylight. Cancer oregonensis megalopae may express one set of behaviors when they are at a distance from shore and/or during the night. These offshore/nighttime behaviors might aid in the onshore migration of the megalopae. Offshore from Vancouver Island, C. oregonensis megalopae inhabit the neuston at night and migrate down into the water column during the day (Jamieson & Phillips, 1988). While in the neuston these larvae might be transported shoreward by internal waves (Shanks, 1983, 1987; Kingsford & Choat, 1986) or in Langmuir circulation cells generated by westerly winds (Shanks, 1986; Kingsford et al., 1991). The orientated swimming reported here may be a second set of behaviors which are utilized during daylight hours and/or when the organism perceives that it is near the coast. The orientated swimming behavior may represent a visual “search” for a settlement site which in a near shore environment might significantly aid an individual in finding a suitable habitat in which to settle. Pachygvapsus crassipes megalopae swimming freely in the water column did not orient in the direction of the sun’s bearing or wave direction. These megalopae appeared to be orienting with or against the local current direction. On average 73 % (SD = 13, n = 4) of these megalopae swam with or against the current (i.e. within + one angular deviation of the current direction). There was some preference for megalopae to swim with, rather than against, the current (with the current 50%, SD = 20%; against the current 23”/,, SD = 16%). Rheotaxis has been previously observed in surface-swimming postlarval crustaceans. Cancer magister megalopae have been observed swimming at the surface and against a current (MacKay, 1943). Extensive observations have been made on postlarval H. americanus. They have been observed in the field to swim at the surface and with or against the local current, behaviors similar to those displayed by Pachygrupsus crassipes megalopae. In laboratory flume experiments (Ennis, 1986; Rooney and Cobb, 1991) postlarval H. americanus tended to swim against the current. Callinectes sapidus megalopae also display rheotaxis in laboratory flume experiments (Luckenbach & Orth, 1992). Lophopanopeus bellus bellus megalopae also swam at the surface. Shanks & Wright (1987) found L. bellus bellus megalopae concentrated in the convergence zone over internal waves. The significantly higher concentration of megalopae in the convergence zone suggests that they were being transported shoreward by the internal waves (Shanks & Wright, 1987). All of the observations of swimming direction in L. bellus bellus megalopae reported here were made on animals swimming in the convergence zone over an internal wave. Their mean swimming direction was within 4” of the direction in which the internal wave was propagating. The surface flow in the convergence would have been in the direction of internal wave propagation (Osborne & Burch, 1980; pers. obs.) and current speed should have been of the order of tens of centimeters per second (Gargett, 1976; pers. obs.). Nearly 80% of these megalopae were swimming roughly
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Cairns & LaFond, 1966; Sawyer, 1983). If postlarvae swimming in the convergence of an internal wave swam with the converging current then their speed relative to the phase speed of the wave would be the converging current speed (u) plus their own swimming speed (u swimming). Given a non-transporting internal wave (i.e. c > u), a non-swimming animal would not be transported. A larva with positive rheotaxis, however, might be transported by this wave if c < u + u swimming. Due to the swimming behavior of the postlarvae, a non-transporting internal wave could become a transporting internal wave. By swimming with the converging current a postlarva may increase its chances of rapidly migrating onshore in the convergence zone over an internal wave.
Acknowledgements This research was supported in part by NSF Grant No. OCE-9017807. Field assistance was provided by M. Reeder, K. de1 Carmen, and Dr. W.G. Wright. Field work in the San Juan Islands was greatly facilitated by the help of the faculty and staff of the Friday Harbor Laboratories, University of Washington. The manuscript was greatly improved by the advice of two anonymous reviewers.
References Anonymous, 1949. Crab larvae as food for the silver salmon. Fish. Comm. Oregon. Res. BrieA Vol. 2, pp. 1-17. Bainbridge, R., 1953. Studies on the interrelationships of zooplankton and phytoplankton. J. Mar. Biol. Assoc. U.K., Vol. 32, pp. 385-447. Batschelet, E., 1981. Circular statistics in biology. Academic Press, New York, New York, 371 pp. Brodeur, R.D., B.C. Mundy, W.G. Pearcy & R.W. Wisseman, 1987. The neustonic fauna in coastal waters of the northeast Pacific: Abundance, distribution, and utilization by juvenile salmonids. Oregon State University, Sea Grant College Program, Publication No. ORESU-T-87-001. Cairns, J.L. & E.C. LaFond, 1966. Periodic motions of the seasonal thermocline along the southern California coast. J. Geophys. Res., Vol. 71, pp. 3903-3915. Cobb, J.S., D. Wang, D.B. Campbell & P. Rooney, 1989. Speed and direction of swimming by postlarvae of the American lobster. Trans. Am. Fish. Sot., Vol. 118, pp. 82-86. Ennis, G.O., 1986. Swimming ability of larval American lobsters, Homarus americanus, in flowing water. Can. J. Fish. Aquar. Sci., Vol. 43, pp. 2177-2183. Gargett, A.E., 1976. Generation of internal waves in the Strait of Georgia, British Columbia. Deep-Sea Res., Vol. 23, pp. 17-32. Jamieson, G.S. & A.C. Phillips, 1988. Occurrence of Cancer crab (C. magister and C. oregonensis) megalopae off the west coast of Vancouver Island, British Columbia. Fish. Bull., Vol. 86, pp. 525-542. Jillett, J.B. & J.R. Zeldis, 1985. Aerial observations of surface patchiness of a planktonic crustacean. Bull. Mar. Sci., Vol. 37, pp. 609-619. Kingsford, M.J. & J.H. Choat. 1986. The influence of surface slicks on the distribution and onshore movement of small fish. Mar. Biol., Vol. 91, pp. 161-171. Kingsford, M.J., E. Wolanski & J.H. Choat. 1991. Influence of tidally induced fronts and Langmuir circulation on distribution and movements of presettlement fishes around a coral reef. Mar. Biol., Vol. 109, pp. 167-180. Lough, R.G., 1974. Dynamics of crab larvae (Anomura, Brachyura) off the central Oregon Coast, 1969- 197 1. Ph.D. Dissertation, Oregon State University, Corvallis, 298 pp. Luckenbach, M.W. & R.J. Orth, 1992. Swimming velocities and behavior of blue crab (Callinecres sapidus Rathbun) megalopae in still and flowing water. Estuaries, Vol. 15, pp. 186-192.
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MacKay, D.C.G., 1943. The behavior of the Pacific edible crab Cuncer mug&r Dana. J. Camp. Psychol., Vol. 36, pp. 255-268. Menzies, R.J., 195 1. Pleistocene brachyura from the Los Angeles area: Cancridae. J. Puieontol.,Vol 25, pp. i65-170. Morris, R.H., D.P. Abbott & E.C. Haderlie. 1980. Intertidul invertebrates ojCalijb~~ia. Stanford University Press, Stanford, California, 690 pp. Osborne, A.R. & T.L. Burch, 1980. Internal soiitons in the Andaman Sea. Science, Vol. 208, pp. 451460. Phillips, B.F., 1981. The circulation of the southeastern Indian Ocean and the planktonic lift of the wcstcm rock lobster. Oceanogr. Mar. Bioi. Annu. Rev., Vol. 19, pp. 1l-39. Phillips, B.F. & L. Olsen, 1975. Swimming behavior of the puerulus larvae of the Western rock lobster. Aust. J. Mar. Freshwater Res., Vol. 26, pp. 415-417. Pow&, H.. 1981. Distribution and movements of neustonic young of estuarine dependent (Mugil spp., Pomatomu.~ sultutrix) and estuarine independent (Curyphaenu spp.) fishes off the southeastern United States. Rupp. P.-v. Reun. Cons. Irlt. Explor. Mer., Vol. 178, pp. 207-209. Purcell, J.E., I98 1a. Dietary composition and die1 feeding patterns of epipelagic siphonophorcs. Mar. Biol., Vol. 65, pp. 83-90. Purcell, J.E., 1981b. Selective predation and caloric consumption by the siphonophore Rosaceu cymhifirmis in nature. Mar. Biol.. Vol. 63, pp. 283-294. Rooney, P. & J.S. Cobb, 1991. Effects of time of day, water temperature, and water velocity on swimming by postlarvae of the American lobster, Homarus americanus. Gun. J. Fish. Aquot. Sci., Vol. 48, pp. 19441950. Sawyer, C., 1983. A satellite study of ocean internal waves. NOAA Technical Memorandum ERL PMEL-46, 70 PP. Schmidt-Koenig, K., 1979. Aviun orientation and nuvigution. Academic Press, London, 253 pp. Shanks, A.L., 1983. Surface slicks associated with tidally forced internal waves ma) transport pelagic larvat of benthic invertebrates and fishes shoreward. Mar. Ecol. Prog. Ser.. Vol. 13, pp. 31 l-315. Shanks, A.L., 1985. The behavioral basis of internal wave induced shoreward transport of the megalopae of Pachygrapsus crussipes. Mar. Ecol. Prog. Ser. 1Vol. 24, pp. 289-295. Shanks, A.L., 1986. Vertical migration and cross-shelf dispersal of larval Cancer spp. and Rartdallicl ornutu (Crustacea, Brachyura) off the coast of southern California. Mar. B&l., Vol. 92, pp. 189-200. Shanks, A.L., 1987. Mechanisms of cross-shelf larval transport. In, Sig~~posts in the sea, edited by W.F. Hcrrnkind & A.B. Thistle, Dept. of Biological Science, Florida State University, Tallahassee, pp. l528. Shanks, A.L., 1988. Further support for the hypothesis that internal waves can transport larvae of invertebrates and fish onshore. Fish. Bull., Vol. 86, pp. 703-714. Shanks, A.L. & W.G. Wright, 1987. Internal-wave-mediated shoreward transport of cyprids, megalopae, and gammarids and correlated longshore differences in the settling rate of intertidal barnacles. J. Exp. Mur. Biol Ecol., Vol. 114, pp. I-13. Zaret. T.M., 1980, The effect of prey motion on planktivore choice. In, Evolution und erolog~~of zooplur~kfnn cor~mzurzities. edited by U’.C. Kerfoot, University Press of New England, Hanover, New Hampshire, USA. pp. 594-603.
Ecology
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
186 (1995) l-16
Orientated swimming by megalopae of several eastern North Pacific crab species and its potential role in their onshore migration Alan L. Shanks University of Oregon, Oregon Institute of Marine Biology, Charleston, OR 97420, USA Received 4 March 1994; revision received 12 September 1994; accepted 13 September 1994
Abstract The megalopal stage of most near shore and intertidal crabs must return to the coast to complete their development. Crab megalopae are strong swimmers and if they swam consistently shoreward they could conceivably swim back to shore. This hypothesis was tested for megalopae of Pachygrapsus crussipes (Randall), Lophopanopeus bellus bellus (Stimpson, 1860), Cancer oregonensis (Dana), and C. gracilis (Dana) by investigating their swimming orientation when housed in a transparent container with a view of the underwater illumination or swimming freely in the sea. In the transparent container, megalopae tended to swim in the direction of the sun’s bearing. Free swimming megalopae swam straight courses and displayed significant preferred swimming directions. Puchygrupsus crassipes and L. bellus bellus megalopae swam at the sea surface and parallel to the current direction. Free swimming C. oregonensis and C. grucilis swam at about 3 to 5 m depth and in the direction of the sun’s bearing. Megalopae of Puchygrupsus crassipes and C. oregonensis were observed on 4 and 3 days respectively and they did not preferentially swim in a shoreward direction. These results suggest that they do not migrate back to shore by swimming. The orientated swimming may, however, assist the megalopae in returning to shore or locating a settlement site. Swimming with the surface current might help megalopae to migrate shoreward in the convergence zone over internal waves or Langmuir circulation cells. Swimming in the direction of the sun’s bearing might represent a search behavior for a benthic settlement site. Keywords: Behavior;
Cancer;
Crab; Dispersal;
Megalopae;
Orientation
1. Introduction Larvae 4 months
of brachyuran to complete
0022-0981/95/$9.50 0
SSDI
crabs from the eastern North Pacific Ocean require from 2 to their development (Lough, 1974). At the end of the period of
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B.V. All rights reserved
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planktonic development the megalopae must seek out the habitat which they will occupy as juveniles or adults. For coastal crabs this is frequently the intertidal and shallow subtidal environments. In the waters off Oregon, Lough (1974) found that the larvae of many coastal crabs dispersed to about 16 km from shore. Thus, the megalopae of these crabs must make a fairly extensive cross-shelf migration in order to regain the shore. Two possible mechanisms for this shoreward migration can be suggested: the megalopae may actively swim ashore in a well oriented fashion or they may utilize cross-shelf currents and be swept ashore (Shanks, 1987). Researchers have suggested that the larvae of several coastal fishes (Powles, 1981) the puerulus of the Australian rock lobster, Punulirus cygnus, (Phillips, 1981) and postlarval Homarus americanus (Cobb et al., 1989) might migrate ashore by swimming. In the case of the puerulus of Panulirus qgnus and postlarval H. nmericunus, this suggestion was based, at least in part, on their strong swimming ability. Swimming speeds of Punulirus qgnus puerulus range from 15 to 46 cm.s ’ (Phillips & Olsen, 1975) and for H. americnnus from 7 to 13.2 cm s ’ (Rooney & Cobb, 1991). Further, H. americanus postlarvae have been observed to swim oriented straight line courses at the ocean’s surface (Cobb ct al., 1989). These postlarvac are strong swimmers which, if their swimming were directed shoreward, might be capable of making a swim-ashore migration. Could a larval crab make a return migration by swimming? Bainbridge (1957) in one of the earliest uses of diving gear to study zooplankton, observed crab megalopae swimming straight line courses near the ocean’s surface. Many megalopae are strong swimmers (pers. obs.; Shanks, 1985; Luckenbach & Orth, 1992). For example, the megalopae of Pachqgrapsus crussipes are capable of sustained speeds of 9.5 cm.ss’ (Shanks, 1985). If these megalopae were to swim at this speed in a consistent direction for the entire duration of the megalopa stage (at least 10 days, pers. obs.), they could cover distances in excess of 80 km, more than 5 times the distance to which they are, on average, dispersed off shore (Lough, 1974). An onshore migration based on active swimming would be of obvious advantage only to larvae which swam in the correct direction, e.g. eastward along the west coast of North America. The question addressed in this study is whether the megalopae of several coastal crab species from the eastern North Pacific Ocean orient their swimming in an eastward or onshore direction. Daytime observations were made of the swimming orientation of megalopae in containers from which they had a clear view of the underwater illumination and released to swim freely in the ocean.
2. Methods A variety of methods were used to obtain megalopae for the following experiments. Pachygrapsus crussi’es megalopae used in the 198 1 and 1982 experiments were caught in traps consisting of bundles of hemp or cotton rope (Shanks, 1983) hung from the end of the Scripps Institution of Oceanography pier (35” 5’ N, 177” 5’ W). The L. bellus bellus megalopae were not captured, but were observed swimming in the surface waters of Park Bay, San Juan Islands, Washington (48” 40’ N, 123” 0’ W).
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Megalopae of Cancer oregonensis and C. gracilis were attracted to a night light hung from the pier at the Friday Harbor Laboratories, San Juan Islands, Washington, and caught with a dip net. Megalopae of Pachygrapsus crassipes, C. oregonensis, and C. gracilis were held in running seawater systems for t24 h prior to their use in field observations. Observations were made on the swimming direction of contained megalopae which had an unobstructed view of the underwater illumination. Ten megalopae were placed in a sealed transparent Plexiglas cylinder (15 cm diameter x 10 cm height filled with sea water). Using SCUBA, the viewing chamber was carried to ~3 m depth. The cylinder was maintained in a constant compass orientation by lining a reference mark on the cylinder up with north on a compass afhxed to the handle of the apparatus. After about a 5-min wait to allow the animals to adjust to the underwater illumination the megalopae swimming in each 30” sector of the cylinder were counted. On 1, 9, and 15 March 198 1 and 3 June 1982 observations were made on the megalopae of Pachygrapsus crassipes. On 31 July 1992 observations were made on C. oregonensis megalopae. Free release experiments of megalopae were made in the ocean using methods analogous to those used in the study of pigeon orientation (Schmidt-Koenig, 1979). Approximately 20 megalopae were placed in a 50-ml syringe filled with sea water and transported to the release site. Pachygrapsus crassipes megalopae were released on 1, 9, and 15 March 1981 and 3 June 1982. The release site on 1 March was offshore from the Scripps Institution of Oceanography in water about 6 m deep. The releases on 9 and 15 March and 3 June were made z 150 m from shore at Goldfish Point in La Jolla, California, in water about 10 m deep. Observations of swimming orientation of C. oregonensis and C. gracilis were made in Park Bay and West Sound in the San Juan Islands, Washington. Water depth at each of these release sites was about 10 m. All releases were made at depths of from 2 to 5 m. All of the Pachygrapsus cmssipes megalopae which were successfully released (i.e. those which were not lost from sight, eaten by fish, or swam to and settled on the observer) immediately swam to the surface where they began to swim horizontally at depths < 0.1 m (Shanks, 1985). Each megalopa was followed to the surface, maintaining a distance of 1 to 2 m, just keeping the individual within sight. When the animal reached the surface and began swimming horizontally, the vanishing direction of the swimming megalopa was noted to the nearest 5” using a hand held sighting compass. C. oregonensis and C. gracilis megalopae swam upward 1 to 2 m following their release (see below). As with Puchygrapsus crassipes megalopae, each megalopa was followed until it began to swim horizontally at which point the vanishing direction of the swimming megalopa was noted. To see if swimming direction remained constant, following the determination ofthe vanishing direction, the observer swam in the direction in which the just-released megalopa had last been swimming. These observations were attempted on about half of the free releases. For the Pachygrapsus crassipes observations the direction of the brightest underwater illumination, the sun’s bearing at the surface, wind direction, surface wave direction and surface current direction were all noted. Current direction was determined by noting the orientation of strips of plastic bag tied to a buoyed and weighted line set in the center of the release site. A nearly identical set of physical observations were made during the San Juan Islands free releases. During these latter observations, current
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speed and direction were measured with an Inter Oceans S-4 current meter set at the depth at which the released megalopae swam. Lophopanopeus bellus bellus were observed from the deck of a motor boat. They were swimming at the surface within the convergence zone associated with a tidally-forced internal wave (Shanks & Wright, 1987). These observations were made in Park Bay, San Juan Islands, Washington on 6 May 1986. Swimming directions of the megalopae were noted as the boat glided slowly through the convergence. To control for the possibility that the megalopae were simply swimming away from the boat, the boat was steered through the convergence several times and from several different compass headings. The sun’s direction and the direction in which the internal wave convergence was propagating were noted. Winds were too light to produce waves.
3. Results 3. I. Pachygrapsus
crassipes
On 1 and 9 March 1981 the swimming directions of the contained Pachygrupsus were not significantly different from random (Fig. 1, Rayleight Test, p> 0.05). The sky on 1 March was overcast and the sun was not visible. The sky was clear on 9 March. On the remaining two dates (15 March and 3 June), however, the distributions of swimming directions of contained megalopae were significantly oriented (Fig. 2, Rayleigh Test, P-C 0.05). On these latter two dates the mean angle of orientation deviated little from the sun’s bearing (i.e. deviations were 9” and 4” for 15 March and 3 June, respectively). These data suggest that, on the days when the megalopae within the container displayed a statistically preferred swimming direction, they were swimming in the direction of the brightest underwater illumination or toward the sun. Due to a variety of problems, the swimming direction of less than half of the Pachygrapsus crassipes megalopae released was measured. The megalopae are less than a centimeter in total length and some animals were simply lost from view. Releases were made close to shore in an area where there were a number of juvenile fishes. A number of megalopae fell prey to these fishes. The major problem, however, was due to the strong thigmokinesis displayed by Puchygrupsus crussipes megalopae (Shanks, 1985). If the observer approached a megalopa too closely the animal would turn, swim towards him, and climb onto his person. Upon successful release (57 successful releases out of about 240 attempted), Pachygrupsus crassipes megalopae tumbled about for several seconds, oriented to the surface, and then rapidly swam upward (Shanks, 1985). They swam up to the surface until they actually contacted the surface of the ocean (from below they could be seen to dimple the ocean’s surface). At the surface they began to swim horizontally at depths < 10 cm. Without hesitation they adopted a swimming direction and they began to swim steadily in this direction. Swimming directions appeared to be bimodal and with or against the current. More than half of the animals appeared to swim in the direction of the current and these rapidly disappeared from view. About 20”< of the released animals appeared to swim against the current. These individuals often took a long time crussipes megalopae
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1 March 1981 Current
S %Angle = 180” + 74” r=o.l73,n=iO NS
f Angle = 319” ?:22” r = 0.700, n = 10, P = 0.005 9 March 1981
E
Sun’s Bearing
S
X Angle = 278” +-25” r = 0.628, n = 20, PC 0.001
Sun’s Bearing
S
ii Angie = 120” +-77” r = 0.100, n = lo, NS
Fig. 1. Swimming orientation of Puchygrupsus crassipes megalopae swimming freely in the water column (left-hand figures) and housed in a transparent Plexiglas container with a view of the underwater illumination (right-hand figures). . indicate the swimming direction of each megalopa. The labelled arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath each circular figure are the results of the Rayleigh circular statistics test. Due to the behavior of the freely swimming megalopae (see text) the distribution of swimming directions was considered to be bimodal (left-hand figures). The data were analysed following the rules for axially symmetric data (Batschelet, 1981).
to swim out of view. Many, in fact, appeared to be making no forward progress even though they were swimming actively. On a number of the releases the observer swam in the direction in which the animal was seen to be swimming when it vanished. Usually I was able to find the animal and they had in all cases maintained their swimming
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(lC8.YiJ
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15 March 1981 N
vn*s
Searing
vr+g
S
S
E Angle = 135” ? 35” r = 0.818, n = IO, P~O.001
f Angle = 268” k 30” r z 0.475, n = 13, P~0.05 3 June 1982
E
W
KAngle = 110” + 30” r = 0.452, n = 14, P = 0.0567
W
E
Z Angle = 176” t 33” r = 0.835, n = 10, P = 0.001
Fig. 2. Swimming orientation of Pach~grapsus crassipes megalopae swimming freely in the water column (left-hand figures) and housed in a transparent Plexiglas container with a view of the underwater illumination (right-hand figures). . indicate the swimming direction of each megalopa. The labelled arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath each circular figure are the results of the Rayleigh circular statistics test. Due to the behavior of the freely swimming mcgalopae (see text) the distribution of swimming directions was considered to be bimodal (left-hand figures). The data were analysed following the rules for axially symmetric data (Batschelet, 1981).
direction. Puchygrqsus cmssipes megalopae appeared to be and flat course over distances of at least meters to tens of The behavior of the free swimming megalopae and the directions both suggested that the vanishing angles were
able to maintain a straight meters. distribution of swimming bimodally distributed and
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Exp. Mar. Biol. Ecol. I86 (1995) l-16
I
centrally symmetric. To apply circular statistics to axial data all vanishing angles were doubled (Batschelet, 1981). The Rayleigh test indicated that there was on each date a statistically significant preferred direction to the orientation of the free swimming megalopae (Figs. 1 and 2). There were large deviations between the sun’s bearing and the mean swimming direction (i.e., mean angle in Figs. 1 and 2) of the megalopae on each release date. The differences between the sun’s bearing and the mean swimming direction of the megalopae were 199”, 78”, 151”, and 70” for 1, 9, and 15 March and 3 June, respectively. On 15 March there was a strong offshore wind. The release site was within 150 m of shore and in the lee of coastal hills. The waters at the release site were glassy. On the other three release dates waves were present. The mean swimming direction deviated from the wave direction by 49”, 32”, and 180” on 1 and 9 March and 3 June, respectively. The mean swimming directions of the released megalopae deviated little from the current direction (deviations were 5 O, 12”, 1 O, and 10” on 1, 9, and 15 March and 3 June, respectively). The observed behavior of the free swimming megalopae and the similarity between the mean swimming orientation and the current direction suggest that the megalopae were orientating to the local current direction. 3.2. Lophopanopeus
bellus bellus
Megalopae of L. bellus bellus were observed in Park Bay from the deck of a motor boat. All of the individuals were swimming just below the surface (several centimeters depth) in the convergence zone over an internal wave (Shanks & Wright, 1987). Although the total length of these megalopae is only 0.5 cm they were clearly visible even when standing in the boat. The animals were darkly pigmented, almost black, and there was a reflective green patch in the center of their carapace. Observations were made on the swimming direction of 24 individuals. The distribution of swimming directions was unimodal and the Rayleigh test indicated that there was a statistically significant preferred swimming direction (Fig. 3). The mean swimming direction was 97” and the 95 y0 confidence interval was k 24”. The sun’s bearing (150 “) was outside the 95 y0 confidence interval indicating that the megalopae were not orientated toward the sun. The direction of the internal wave’s propagation was 100”. The mean swimming direction differed by only 3” (well within the 95% confidence interval around the mean angle) from the direction in which the internal wave was propagating. These data suggest that the L. bellus bellus megalopae were swimming in the direction of propagation of the internal wave. 3.3.
Cancer oregonensis
Observations on the behavior of C. oregonensis were made toward the end of the settlement season for this species. Enough animals were caught late in July to make observations on both contained and free swimming animals, but on later dates too few animals were caught for both sets of observations to be made. Observations of the swimming orientation of contained C. oregonensis megalopae were made on 31 July 1992. The Rayleigh test indicated that the contained megalopae had a preferred swim-
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Y Angle = 97” f 49”, 95% Confidence Interval f 24” r = 0.637, n = 24, P< 0.001 Fig. 3. Swimming orientation of L. b&s bellus megalopae swimming at the surfxc in the convergence zone over an internal wave. . indicate the swimming direction of each megalopa. The labelled arrows indicate the direction in which the internal wave was propagating (and, hence the direction of the surface current in the convergence), sun’s bearing, and the mean swimming angle of the megalopae. Beneath the figure are the results of the Rayleigh circular statistics test.
ming direction (Fig. 4). The mean angle of this swimming direction deviated only 2” from the sun’s bearing. Like contained Pachygrapsus crussipes megalopae, contained C. oregonensis megalopae appeared to be swimming toward the brightest sector of the underwater light field or toward the sun. The behavior of free released C. oregonensis megalopae (38 successful released out of 63 attempted) was strikingly different from that of Pachygrapsus crussipes. Following ejection from the syringe, C. oregonensis megalopae tumbled about for a second or two and then, with their legs extended and their body oriented horizontally, they rotated. After several rotations they tucked all or all but the most anterior pair of legs under their body and began to swim upward at a slight angle. Animals were released at 5 m depth and most individuals swam toward the surface for 1 to 2 m before beginning to swim a level course. They maintained a fixed bearing through out this time. Superimposed on this straight-line swimming were vertical and horizontal oscillations with amplitudes of around 5 cm. Occasionally animals would extend all of their legs, rotate again, and then swim off in the same direction in which they had previously been swimming. No matter how closely megalopae were approached none swam toward the observer, who was again able to swim in the vanishing direction and locate some of the megalopae. All had maintained the initial swimming direction. These data suggest that C. oregonensis megalopae were able to maintain a straight and level course over distances of meters to tens of meters while swimming within the water column. Distributions of swimming directions of free swimming C. oregonensis megalopae were unimodal and the Rayleigh test indicated that the megalopae had statistically significant preferred swimming directions (Fig. 4). On none of the three sample dates
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9
Sun’s Bearing 31 July 1992 a Angle = 176” + 39” r = 0.771, n = 18, Pd 0.001
31 July 1992 X Angle = 150” + 38” r=0.781,n=7,P=0.009
N
W
S 3 August 1992 f Angle = 223” k 52” r = 0.590, n = 14, P = 0.006
27 August 1992 f Angle = 107” f 27” r = 0.891, n = 6, P< 0.004
Fig. 4. Swimming orientation of C. oregonensis megalopae swimming freely in the water column (A, C and D) and housed in a transparent Plexiglas container with a view of the underwater illumination (B). . indicate the swimming direction of each megalopa. Arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath each circular figure are the results of the Rayleigh circular statistics test.
was the current direction within the 95% confidence interval of the mean swimming direction. On 31 July and 3 August, when surface waves were present, the wave direction was also outside the 95% confidence interval around the mean swimming direction. The three free releases were made at different times of the day and the mean
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swimming direction appeared to change with the direction of the sun’s bearing. On each of the three sample dates the sun’s bearing was well within the 95 7; confidence interval of the mean swimming direction. The average difference between the mean swimming direction and the sun’s bearing was only 10”. These data suggest that C. oregonerzsis megalopae were swimming toward the brightest sector of the underwater illumination. On 27 August the weather was partly cloudy. The sun went behind the clouds during three releases. Interestingly, these three animals swam at about 180” to the sun’s bearing (square data points in Fig. 4, 27 August). These data were excluded from the Rayleigh test analysis. 3.4.
Cancer gracilis
Too few megalopae of this species of crab were caught to make observations on both contained and freely swimming individuals. Only observations on freely swimming megalopae were made. Further, C. gracilis megalopae are small (around 0.5 cm in total length), and were difficult to follow underwater. Upon release many animals were lost from view. This difficulty led to a low number of observations (seven successful released out of 35 attempted). Observations on the swimming behavior of C. grucilis megalopae were made on 27 August 1992. Following their release, the behavior of these megalopae was identical to that of C. ovegonensis. The distribution of swimming directions was unimodal and significantly directed (Fig. 5). Due to the low number of replicate observations it was not possible to determine the 95”/, confidence interval around the mean swimming N
Bearing
f Angle = 82” f 35” r = 0.814, n = 7, P = 0.005 Fig. 5. Swimming orientation of freely swimming C. gradis megalopae released on 27 August 1992. . indicate the swimming direction of each megalopa during the time the sun was visible. The open boxes represent observations made while the sun was behind clouds. The labelled arrows indicate the current direction, sun’s bearing, wave direction, and mean swimming angle of the megalopae. Beneath the figure are the results of the Rayleigh circular statistics test. The Rayleigh test was made using only the data collected when the sun was visible.
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direction. The mean swimming direction of C. gracilis deviated 33” from the sun’s bearing, within & one angular deviation of the mean swimming direction. Like C. oregonensis megalopae, C. gracilis megalopae appeared to be directed toward the sun’s bearing.
4. Discussion The megalopae observed in this study displayed the characteristics of organisms which might migrate to shore by swimming. That is, they were found to be (1) strong swimmers that swam straight and oriented paths, (2) they swam steadily and continuously, and (3) they were able to maintain their course over distances of at least several tens of meters. Due to logistical limitations it was impossible to measure in situ swimming speeds, but they were probably on the order of 5 cm*s-‘. Ignoring the effects of currents, if these megalopae swam for 12 h per day for 10 days they could cover about 20 km, a substantial distance. If their swimming was directing them back to the coast (i.e. the west coast of North America for these species) then they should have orientated to the east. Multiple observations were made on two species, C. oregonensis and Pachygrapsus crassipes. Neither swam preferentially to the east. C. oregonensis swam toward the brightest sector of the underwater illumination or toward the sun’s bearing. Thus, in the morning they swam toward the east, but by afternoon they swam westward. Pachygrupsus crussipes megalopae appeared to be swimming relative to the local current direction. About half of the released animals swam to the west. The present data do not support the hypothesis that these two species migrate shoreward by directed swimming. Two species were observed on only one date and the mean swimming direction in both cases was close to eastward. Because of the limited number of observations these data cannot be used to make conclusive generalizations. The mean swimming direction of C. gracilis was 82 ‘, nearly eastward. The sun’s bearing was 115’ so it is quite possible that, like C. oregonensis, C. gracilis was swimming toward the brightest sector of underwater illumination. Lophopanopeus bellus bellus had a mean swimming direction of 97’) also nearly eastward. This swimming direction may be a response to the flow field within the internal-wave convergence in which they were observed (see below). If however, “eastward” is defined as between 45” and 135’ then 29% and 38% of the C. gracilis and L. bellus bellus megalopae respectively were not swimming east. These species have been in existence since at least the Pleistocene (Menzies, 1951) or in excess of a million generations. Given the strong selective advantage of swimming in the correct direction it seems doubtful that such a large percentage of their megalopae would be found swimming in the “wrong” direction. All of the megalopae were released during the day and all remained in the well illuminated surface waters. Cancer oregonensis and C. gracilis swam at depths <5 m while Pachygrapsus crassipes and L. bellus bellus swam within centimeters of the ocean’s surface. All of these megalopae are relatively large for meroplankters, 0.5 to 1 cm in total length, and were visible in the water. Large meroplankton, such as these mega-
12
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lopae, which remain at or near the surface during the daytime expose themselves to visual predators. In fact, one of the common causes for unsuccessful releases of Pachygrapsus crassipes megalopae was that they were consumed by fishes at the release site. Furthermore, Cancer megalopae are a common component in the diet of silver salmon (Anon., 1949; Brodeur et al., 1987). Swimming at or near the ocean’s surface during daylight would seem to be a maladaptive behavior unless, of course, the behavior serves some additional and compensating purpose within the life cycle of the organisms. One possibility is that the swimming behavior might aid in the onshore migration of the megalopae. They apparently do not actually swim ashore, but by swimming they may somehow increase their chances of returning to shore and finding a suitable habitat in which to settle. The behavior of the organisms observed during this study fall into two categories: those which swam at several meters below the surface and those which swam at the surface. Both C. oregonensis and C. gtmilis swam several meters below the surface. The swimming of C. oregonensis was clearly oriented toward the sun. The swimming orientation of C. grucilis may also have been oriented toward the sun, but too few observations are available for a clear conclusion. During the course of a day C. oregonensis would swim a large arc; toward the east in the morning with a steady shift to the west in the afternoon. If a 5 cm.s -’ swimming speed, a 12-h day, and no current is assumed, then a megalopa could swim an arc about 2 km long. What could be the adaptive advantage to this behavior? Like swimming in the surface waters during daylight, this behavior probably increases the chances that the megalopae will be consumed by predators. A megalopa swimming steadily along in a straight line is, undoubtedly, a more obvious target to a visual predator than one that is holding still (Zaret, 1980). Furthermore, steady orientated swimming by increasing the volumn of water through which the megalopae pass would increase their chances of encountering cnidarian predators (e.g. medusae and siphonophores). In fact, megalopae as well as other meroplankton are a common component in the diet of a number of siphonophores (Purcell, 198 la,b). The directed swimming behavior could represent a search behavior for a patchy food source. However, the carapace of megalopae commonly contains large oil droplets (pers. obs.), which suggests that they possess a substantial energy reserve. Given this energy reserve and the probable increased risk of predation due to directed swimming, it is doubtful whether the directed swimming behavior of C. oregonensis is a search for a patchy food supply. To complete their life cycle, C. oregonensis megalopae must settle in the shallow subtidal or low intertidal zone (Morris et al., 1980). Perhaps the directed swimming behavior is a mechanism for searching for a settlement site. The depth at which the megalopae swam (several meters) would, at low tide, cause them to settle at shallow subtidal depths and, at high tide, at low intertidal depths. The directed swimming would allow them to search a path of the order of z 2 km long per day. During the megalopal stage, which lasts one to several weeks, an individual might be able to search 10 to 30 km of water for a settlement site. It is difficult to see, however, how the swimming behavior of C. oregonensis might
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cause an onshore migration. Despite all of their swimming, megalopae kilometers from shore, in the waters over the continental shelf, would remain kilometers from shore. As they were carried along by a current, the observed swimming behavior would cause them to swim through, and perhaps, search a large volume of water, but they would only encounter the shoreline if the current carried them there. The observations reported in this paper were made close to shore and during daylight. Cancer oregonensis megalopae may express one set of behaviors when they are at a distance from shore and/or during the night. These offshore/nighttime behaviors might aid in the onshore migration of the megalopae. Offshore from Vancouver Island, C. oregonensis megalopae inhabit the neuston at night and migrate down into the water column during the day (Jamieson & Phillips, 1988). While in the neuston these larvae might be transported shoreward by internal waves (Shanks, 1983, 1987; Kingsford & Choat, 1986) or in Langmuir circulation cells generated by westerly winds (Shanks, 1986; Kingsford et al., 1991). The orientated swimming reported here may be a second set of behaviors which are utilized during daylight hours and/or when the organism perceives that it is near the coast. The orientated swimming behavior may represent a visual “search” for a settlement site which in a near shore environment might significantly aid an individual in finding a suitable habitat in which to settle. Pachygvapsus crassipes megalopae swimming freely in the water column did not orient in the direction of the sun’s bearing or wave direction. These megalopae appeared to be orienting with or against the local current direction. On average 73 % (SD = 13, n = 4) of these megalopae swam with or against the current (i.e. within + one angular deviation of the current direction). There was some preference for megalopae to swim with, rather than against, the current (with the current 50%, SD = 20%; against the current 23”/,, SD = 16%). Rheotaxis has been previously observed in surface-swimming postlarval crustaceans. Cancer magister megalopae have been observed swimming at the surface and against a current (MacKay, 1943). Extensive observations have been made on postlarval H. americanus. They have been observed in the field to swim at the surface and with or against the local current, behaviors similar to those displayed by Pachygrupsus crassipes megalopae. In laboratory flume experiments (Ennis, 1986; Rooney and Cobb, 1991) postlarval H. americanus tended to swim against the current. Callinectes sapidus megalopae also display rheotaxis in laboratory flume experiments (Luckenbach & Orth, 1992). Lophopanopeus bellus bellus megalopae also swam at the surface. Shanks & Wright (1987) found L. bellus bellus megalopae concentrated in the convergence zone over internal waves. The significantly higher concentration of megalopae in the convergence zone suggests that they were being transported shoreward by the internal waves (Shanks & Wright, 1987). All of the observations of swimming direction in L. bellus bellus megalopae reported here were made on animals swimming in the convergence zone over an internal wave. Their mean swimming direction was within 4” of the direction in which the internal wave was propagating. The surface flow in the convergence would have been in the direction of internal wave propagation (Osborne & Burch, 1980; pers. obs.) and current speed should have been of the order of tens of centimeters per second (Gargett, 1976; pers. obs.). Nearly 80% of these megalopae were swimming roughly
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Cairns & LaFond, 1966; Sawyer, 1983). If postlarvae swimming in the convergence of an internal wave swam with the converging current then their speed relative to the phase speed of the wave would be the converging current speed (u) plus their own swimming speed (u swimming). Given a non-transporting internal wave (i.e. c > u), a non-swimming animal would not be transported. A larva with positive rheotaxis, however, might be transported by this wave if c < u + u swimming. Due to the swimming behavior of the postlarvae, a non-transporting internal wave could become a transporting internal wave. By swimming with the converging current a postlarva may increase its chances of rapidly migrating onshore in the convergence zone over an internal wave.
Acknowledgements This research was supported in part by NSF Grant No. OCE-9017807. Field assistance was provided by M. Reeder, K. de1 Carmen, and Dr. W.G. Wright. Field work in the San Juan Islands was greatly facilitated by the help of the faculty and staff of the Friday Harbor Laboratories, University of Washington. The manuscript was greatly improved by the advice of two anonymous reviewers.
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