In situ studies of the swimming behaviour of Corophium volutator in the estuary of the. River Stour, Suffolk, have shown that swimming has a rhythmicity with ...
J. mar. biol. Ass. U.K. (1988), 68, 565-579 Printed in Great Britain
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DISPERSAL BY BENTHIC INVERTEBRATES: THE IN SITU SWIMMING BEHAVIOUR OF THE AMPHIPOD COROPHIUM VOLUTATOR R.G.HUGHES Centre for Research in Aquatic Biology, School of Biological Sciences, Queen Mary College, University of London, London El 4NS (Figs. 1-3)
In situ studies of the swimming behaviour of Corophium volutator in the estuary of the River Stour, Suffolk, have shown that swimming has a rhythmicity with circadian, semilunar and seasonal components. C. volutator swim only at night, around the times of spring tides, and between May and August. Amphipods of all sizes swim, but mature animals and, on most occasions, the smallest animals were relatively more abundant in the plankton than in the sediment. The possible reasons for C. volutator swimming are discussed, particularly in relation to the role of dispersal in their life-history. It is concluded that a typical individual born between May and August swims once, on its first spring tide, and perhaps once or twice later in its life. Swimming could be prompted by several factors unrelated to reproductive behaviour. The differences between the results of this study and those of others, which indicate swimming to occur in daylight and throughout the year, could point to differences in behaviour between different populations. INTRODUCTION
Studies of the dispersal behaviour of marine and estuarine benthic invertebrates have concentrated on the majority of species where the individuals disperse as a planktonic larva. The view that seems to be prevalent, summarised by Crisp (1974, 1976), is that larvae are an adaptation to allow species to colonise transient habitats and for species with adults of limited mobility to colonise distant habitats. The spreading of the species over wide areas has the advantages of reducing competition and facilitating greater genetic diversity, leaving the species more adaptable to subsequent environmental changes. These advantages are greater with longer distances travelled, and are an explanation for larvae spending up to several weeks drifting in the plankton, despite the acknowledged high mortality rates associated with the pelagic existence. This view may be challenged for at least two reasons. Firstly, in most species the larva represents a swimming stage which in evolution preceded what is now the adult and it is improper to refer to the larva as an adaptation which benefits the adult (e.g. barnacles do not have larvae because they are sessile, rather adult barnacles can be sessile because of their early pelagic life). Secondly, species are not subject to natural selection, the immediate units of selection are individuals (in evolutionary time it is the gene). Consequently the perceived selective advantages of dispersal behaviour are more properly related to the individuals
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and not to the species. The claim that the function of a planktonic larval phase is to disseminate the species is untenable therefore. This paper addresses the hypothesis that for individuals of benthic species there is an optimum compromise in the time spent in pelagic dispersal between very short periods, where individuals would live close to their parent, and the few weeks typical of most planktotrophic larvae. The hypothesis
The basis of the hypothesis is the axiom that there is no selective advantage to the individual in long-term dispersal unless its fitness in a distant site is predictably greater than that in a site somewhat closer to its parent. Further, the advantage must be sufficient to compensate for the increased disadvantages inherent in prolonged dispersal; the higher risks of mortality, of not finding a suitable habitat, and of not being close to a potential reproductive partner. Consequently there is doubt over the advantage to the individual in searching for and colonizing remote habitats, since the chances of success and the rewards are small. Dispersal over very short distances will reduce the mortality rate but also has disadvantages, notably increased intraspecific (and intra-sib) competition, in-breeding, and vulnerability of the 'line of descent' to local catastrophe (Crisp, 1974, 1976). An optimum period of dispersal between these extremes will be different for different species according to other features of their biology, notably their relative mortality risks and the rarity of their habitat - organisms with rare or dispersed habitats (e.g. ectoparasites and commensals) might need a longer pelagic existence to enhance the probability of finding a suitable habitat. Logically, the best compromise for an individual to maximise distance travelled while minimizing its risk of mortality would be a pelagic life of less than 6 h, the usual maximum duration of a tidal current. A longer planktonic existence, with drift on the ebb and flood tide, would markedly increase the mortality risk but could result in shorter net transport and any increase in net transport would only result from the relatively weak residual currents (Crisp, 1976). If the hypothesis is correct and there is no selective advantage to prolonged dispersal, why do larvae swim for much longer periods of up to several weeks ? Planktotrophic larvae are produced with relatively little parental investment in each individual, compared to lecithotrophic (non-feeding) larvae or individuals with direct development, and therefore may have to swim in the plankton at least until they have accumulated sufficient energy to undergo settlement and metamorphosis (see Lucas et al. 1979). Natural selection will only act to reduce the length of larval pelagic life if endowing the egg with more resources increases the relative fitness of the parent. The duration of planktonic life of a larva is not influenced by natural selection acting on that individual (except perhaps by increasing maximum feeding rate or reducing the size at metamorphosis), but on the previous generation, and this is a crucial difference between planktotrophic individuals and those that pass through a non-feeding larval stage or have direct development. Most individuals that grow through a lecithotrophic larval stage
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disperse for less than 6 h (Crisp, 1976), providing support for this hypothesis. However, because of their phylogenetic history they have to disperse early in their lives. Consequently, the benefits and disadvantages of dispersal per se may be better understood by studying dispersal behaviour in those species where natural selection has acted to remove the free-living larval stage. In these species dispersal behaviour (timing and duration) has evolved more directly under the influence of natural selection and unconstrained by their phylogenetic history. The amphipod Corophium volutator was chosen for these reasons, and because, in contrast to other aspects of its biology, its dispersal behaviour was unknown. Corophium volutator (Pallas) C. volutator is widespread and often very abundant in intertidal marine and estuarine muds of northern Europe and north-eastern North America and, like all amphipods, has no larval stage; small amphipods hatch from eggs retained in a ventral thoracic brood pouch. Several aspects of the biology of C. volutator have been studied, particularly its life-cycle (Hart, 1930; Watkin, 1941; Fish & Mills, 1979) and feeding behaviour. C. volutator feeds on suspended material, by filtering particles from the current generated through the U-shaped burrow by the beating pleopods, and on surface deposits, by using the antennae to scrape material into this current (Meadows & Reid, 1966). C. volutator seemingly have little need to leave their burrow, except to find a mate, and in laboratory studies this has rarely been seen. Several authors have observed C. volutator crawling on the surface of the sediment in situ and Fish & Mills (1979) concluded that these were probably males searching for receptive females in their burrows. C. volutator have been found in plankton samples, but no detailed in situ study of swimming behaviour has been undertaken. Beanland (1940) reported C. volutator swimming under 'certain conditions of light and salinity' and Morgan (1965) caught animals swimming above the sediment. Meadows & Reid (1966) presumed that dispersal was accomplished by adults, on the basis of Hart's (1930) observation that juveniles burrow into the sediment close to the parental burrow. The swimming behaviour of C. volutator has been studied in the laboratory by Holmstrom & Morgan (1983a, b, c) who demonstrated a rhythm of swimming activity with three components; a circa-tidal rhythm of 12-13 h, with the maximum occurring on the ebb tide; a semi-lunar rhythm, where swimming was more pronounced at the time of spring tides; and a seasonal rhythm with swimming throughout the year but more pronounced in the summer. This study reports an in situ study of the swimming behaviour of C. volutator which, in addressing the hypothesis outlined above, sought to discover which individuals swam, when they swam, how often they swam, and for how long; and to consider possible explanations for the observed behaviour.
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R.G.HUGHES METHODS The study site
The study site is on the estuarine mud flat of the River Stour at Cattawade, Suffolk, at the northeastern end of the road bridge (Grid Ref. TM 101328). Adjacent to the seaward side of the bridge are sluice gates for controlling the upstream level of the river and which may prevent significant incursion of estuarine water upstream. There is often no downstream flow through the gates at low tide and this part of the estuary dries at low spring tides, apart from a small pool adjacent to the sluice gates. A tide-protection wall slopes down to a concrete ledge, 0-5 m wide, adjacent to, and at the same level as, the mud flat. A number of concrete blocks are embedded in the mud close to this ledge. The study was conducted by standing on the ledge and these blocks to avoid disturbing the C. voiutator in the sediment. The study area is approximately 2-75 m above CD., 1-5 m below M.H.W.S.T. and 0-65 m below M.H.W.N.T. level. The site is first immersed approximately 1 h 45 min before high water. High water at spring tides occurs around 01.00 and 13.00 h and high water at neap tides at 07.00 and 19.00 h. Laboratory observations
To facilitate observations of the behaviour of adult and recently hatched C. voiutator in their burrows, a circular crystallising dish 121 mm external diameter and 50 mm tall was placed inside another of 127 mm internal diameter. The resulting 3 mm wide space between the sides of the two dishes wasfilledwith natural substrata, previously sieved to remove C. voiutator and other infauna, to within 5 mm of the rims of the dishes. The remaining space was filled with sea water diluted to a salinity of 30%,,. Several female C. voiutator carrying eggs or embryos were placed in the water and these soon burrowed in the mud. The apparatus was placed in a glass aquarium adjacent to one of the sides and the aquarium filled with sea water to 5 cm above the rims of the dishes. As the tops of the burrows were close to the rims of the dishes, confinement was not considered a significant deterrent to swimming. The aquarium was kept in a constant temperature room at 18 °C in subdued light of natural daylength duration. Many of the burrows were constructed against the outer of the two dishes and the behaviour of these amphipods, and their broods, were observed (through the aquarium and outer dish) by use of a horizontally mounted stereomicroscope and microscope light by simply turning the dishes to view different animals. Observations of juvenile C. voiutator from twelve broods were made up to 3 days after their release from the brood pouch. In situ observations Swimming C. voiutator were routinely sampled by means of simple traps each consisting of a jar (7 cm diameter and 12 cm tall) onto which was placed a glass filter funnel (8 cm rim diameter) from which the stem had been removed. Each trap was inserted into a 7 cm diameter hole in the mud, to a depth of 8 cm, so that the rim of the trap was 5 cm above the mud to prevent capture of crawling animals. Preliminary plankton samples had indicated that swimming activity was concentrated at the times of spring tides and in 1980 two traps were placed only at these times, but were left in position continuously from June 1981 until December 1982. The traps were examined for trapped C. voiutator, which were collected, at intervals ranging from 12 h, during summer spring tide periods, to one week, during the winter. To estimate the abundance and size-frequency distribution of C. voiutator in the sediment, core samples were taken, usually at the times of significant catches in the traps, by taking 50 samples with a corer of 1-5 cm diameter to a depth of 10 cm. The amphipods were then collected by sieving the mud through a 0-25 mm mesh. Plankton samples were taken at regular intervals on the night of 21/22 June 1982 with a handheld pole net, of 20 cm diameter and mesh size 0-25 mm. Each sample consisted of a number of 2 m long sweeps parallel to the wall and different distances from it. Some sub-samples were taken at the surface and some just above the mud. Emergence traps were deployed during three spring tide periods in June and July 1982 in order to estimate the proportion of C. voiutator that leave the sediment and swim. Each emergence trap was similar in principle to that described by AUdredge & King (1980) and consisted of a glass cylinder (8 cm diameter) the bottom end of which was inverted to form a funnel shape (3 cm max. depth) with a central opening 7 mm wide. The open (top) end of the cylinder was covered with net (0-25 mm mesh). Each trap was taped to three thin wire legs which were thrust into the sediment
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VOLUTATOR
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so that the basal rim of the trap was 1 cm above the mud. The space between the base of the trap and the mud was surrounded by netting attached to the three wire legs to prevent the escape of C. volutator. On the rising tide water filtered through the net around the legs of the trap and into the trap replacing the air which escaped through the netting at the top. As the tide receded captured C. volutator were retained in the reservoir of water in the base of the trap from where they were collected (if present) at both low tides each day. At the end of each series of observations the traps were removed and the mud enclosed by the traps, identified by the marks made by the netting, collected and sieved for the remaining C. volutator that either did not swim or were not caught. All the amphipods collected from the traps, plankton and mud were preserved immediately in 70 % ethanol and returned to the laboratory where they were counted and their length, from the rostrum to the tip of the telson, measured. Animals longer than 5 mm were sexed on the basis of the morphology and size of the second antenna and the presence or absence of oostegites (Lincoln, 1979). RESULTS
Laboratory observations
The adult female C. volutator remained in their burrows between the crystallising dishes periodically turning around, in the way described by Meadows & Reid (1966). The newly hatched amphipods remained in the brood pouch for 1-3 days. After their escape from the brood pouch they remained in the parental burrow for a few hours before constructing their own burrow off that of their parent. Their subsequent behaviour was difficult to observe because of their small size (1 mm long) and only rarely was a juvenile burrow excavated against the side of the outer dish. However, from this short study there is no evidence that juveniles swim or crawl from the parental burrow immediately after release from the brood pouch. No C. volutator were found elsewhere in the aquarium. In situ observations Trap data
The numbers of C. volutator caught in the traps placed from June 1981 to December 1982 are shown in Fig. 1. C. volutator leave their burrows to swim only between late May and early August, a result similar to that of 1980, when traps placed at the times of spring tides caught amphipods only between May and late July. There is a clear semi-lunar rhythm of swimming activity with a marked increase in the number of animals caught at the times of new and full moon. Few or no animals were caught during neap tide periods. There was also a clear circadian rhythm of swimming activity; no C. volutator were caught in the traps immersed during the day, nor were any found in daylight plankton samples taken during summer spring tide periods. Comparisons of the size-frequency distributions of C. volutator from the traps and from sediment samples are shown in Fig. 2. Amphipods of all sizes were found in the traps but mature animals (those longer than 5 mm) were relatively more abundant than in the sediment, as were the smallest amphipods (< 1-5 mm long) on most occasions. (However, there is some evidence from the plankton data (see below) to indicate that these traps may have undersampled the smallest individuals.) Amphipods 1 •5—4*0 mm long were consistently less abundant in the trap samples.
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The numbers of C. volutator caught in the traps in 1980 (Fig. 2) were higher than in the subsequent two years (Fig. 1). This difference probably reflects a decline in abundance of C. volutator; on 3 June 1980 the abundance was estimated at 107000 (±52000 s.D.) m~2, and on 22 June 1982 33125 ( + 20500 S.D.). The large standard deviations reflect the highly contagious (aggregated) dispersion of the amphipods.
No.
12
16
20
24
28
July 1982 Fig. 1. The number of C. volutator caught in traps that were in place continuously from 16 July 1981 until December 1982. The graphs cover only the periods when C. volutator were caught and only show data for days when amphipods were captured. The times of full moon (open circle) and new moon (closed circle) are indicated.
Plankton samples
The samples taken at different heights in the water column on each occasion have been combined as there was no apparent difference in the abundance and size-frequency of swimming C. volutator immediately above the mud and at the water surface, up to 1-5 m above the mud. C. volutator were first detected in the plankton 30 min after immersion of the mud (Table 1). The smallest individuals (< 1-5 mm) formed over two-thirds of the swimming population early in the night, compared to 23 % in the whole population, but this dominance by small animals progressively declined during the night. The relative abundance of adult animals in the net samples was
SWIMMING BEHAVIOUR IN COROPHIUM
VOLUTATOR
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12-,
0 1 2 3 4 5 6 7 0 1 2 Length (mm) Fig. 2. The size frequency distribution of C. volutator taken during seven periods. (A) Sediment samples. (B) Trap samples. (C) The differences between the trap samples (observed) and the sediment samples (expected). The number of animals from the sediment and trap samples is shown in each
Table 1. The abundance of swimming C. volutator caught in plankton samples on the night of 21/22 June 1982 The estimated density of animals in the sediment was 33 125 (s.D. = +20500). * denotes a sample containing many praniza larvae (see text). Time after immersion (min)
Depth of water (m) (approx.)
15 30 45 75 105* 135 165 195 225
0-2 0-3 0-5 0-8 12 1-2 0-7 0-4
No. above each m2
< 1-5 mm long (%)
> 5 mm long (%)
0 57 63 324 68 931 49 672* 49 47 2004 2259 22 691 35 Water too shallow to take a sam Die
12 6 13 10 12 26 11
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correspondingly less than the 17-5 % they comprised of the whole population. In only one sample (165 minutes after immersion) were mature animals relatively more abundant in the plankton than in the sediment. The number of C. volutator swimming above 1 m2 of substratum increased progressively from 30 min after immersion until 45 min after high water (165 min after immersion) and subsequently declined as the tide receded. The
Series 1
Series 2
Series 3 (Trap A)
Series 3 (Trap B)
Length (mm)
Fig. 3. The emergence trap data for the three series of observations. Series 1, 21-23 June 1982 (two traps over two nights); Series 2, 8-12 July 1982 (three traps over four nights); Series 3, 21-24 July 1982 (two traps over three nights, the data from which are given separately). (A) The size frequency distributions of the C. volutator under the emergence traps at the beginning of each series of observations (solid line), calculated by adding the data for animals recovered from the mud under the traps at the end of each series of observations with those for animals caught in the traps (stippled area). The numbers of amphipods under the traps at the beginning of each series of observations are given. (B) The proportion of each size class under the traps at the beginning of the observations and subsequently caught in the traps.
exception to this trend was the sample taken 105 min after immersion in which the relatively low numbers of C. volutator coincided with large numbers of praniza larvae of a gnathiid isopod. (Curiously this was the only sample to contain praniza larvae.) Observations of individual amphipods, made with the aid of red light from a torch as the tide receded, confirmed that the decline in abundance of swimming animals was due to their re-burrowing. Many animals, of all sizes and both sexes, were stranded on the mud by the ebbing tide but most burrowed within about 15 min. The estimated density of the benthic population at this time was 33125
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( + 20500 s.D.) m"2. The maximum density of swimming animals (at 45 min after high water) represented only about 7% of the population. However the tenuous nature of this estimate should be stressed, because it is based on the estimated density (with large standard deviations) of animals only in the small study area; the density of C. volutator elsewhere on the mud fiat is unknown. Emergence trap data
The emergence trap data indicate that the smallest C. volutator (< 1-5 mm) are more likely to swim than larger animals (Fig. 3). The two series of samples that Table 2. The percentage of C. volutator remaining under the emergence traps that were caught TV, number enclosed when the traps were first placed. Series 1 Series 2
Series 3
21/22 June 22/23 7/8 July 8/9 9/10 10/11 21/22 July 22/23 23/24
8% 16% 6° 0 19% 19°0 8% 9° 0 8° 0 9° 0
TV =143 TV = 178
TV = 210
covered three and four nights both caught all of the smallest amphipods, while the series that lasted only two nights caught 78 %. The first two series of samples also indicate that a relatively high proportion of adult C. volutator swim, confirming the conclusions drawn from the trapping of swimming animals, but these observations were not confirmed in the third series later in July when only approximately 25 % of the mature animals in the mud enclosed by the traps were caught. Only a small proportion, between 6 and 19%, of the animals remaining under the traps were caught on any one night (Table 2). The efficiency of the traps in catching swimming animals has not been tested but it is likely that most of the C. volutator that swim were caught, given the 100% catch of the smallest animals and the indication of prolonged swimming from the plankton samples. DISCUSSION
Swimming activity rhythms The data from the traps indicate a rhythmicity with three components; a circadian component, with C. volutator swimming only at night; a semi-lunar component, with swimming activity more obvious around the times of full and new moon; and a seasonal component, with swimming only occurring from May to August inclusive. That no animals were caught in daylight is in-keeping with most previous observation that swimming by benthic amphipods is a nocturnal activity, presumably to avoid predators (e.g. Marzolf, 1965; Jansson & Kallander,
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1968; Fincham, 1970 a, b, 1972, 1974; Preece, 1971; Alldredge & King, 1980). However, Morgan (1965) found C. volutator in daylight plankton samples and recorded swimming in daylight in the laboratory. Holmstrom & Morgan (1983 a) observed a circa-tidal rhythm, with a free running period of approximately 125 h, in which swimming C. volutator were present in daylight but more abundant in darkness. This circa-tidal rhythm was present throughout the year, although less obvious in winter. A semi-lunar rhythm of swimming by benthic amphipods, with peak activity around the times of spring tides, has been reported for most species studied (Watkin, 1939; Preece, 1971; Sheader, 1978; Fincham 1970 a, b). Fincham (1972) reported swimming of Marinogammarus on every day, but, unusually, with a peak of activity around the times of neap tides. Holmstrom & Morgan (1983 a) observed that the circa-tidal swimming of C. volutator in the laboratory had peaks of greatest amplitude around the times of spring tides. The two significant differences between the results of this study and those of Holmstrom & Morgan (they observed C. volutator swimming with a circa-tidal rhythm and throughout the year) may reflect the absence of substrata in their laboratory observations. Fincham (19706) and Lindstrom & Lindstrom (1980) demonstrated that without sediment Bathyporeia pelagica and Pontoporeia affinis respectively readily swam in daylight but only swam in darkness when natural substrata were present. Holmstrom & Morgan (1983 a) also observed that when presented with mud C. volutator tended to remain in their burrows. Perhaps in the absence of substrata C. volutator are stimulated to swim, overriding any natural diurnal and seasonal rhythms and making a normally suppressed circatidal rhythm more apparent. Lindstrom & Lindstrom (1980) concluded that the activity pattern revealed in conditions without a natural substratum was not to be recommended as a basis for behavioural studies. An alternative explanation for the differences between the present study and that of Holmstrom & Morgan is that C. volutator in the Stour behave differently from those in west Wales. Morgan's record (1965) of daylight swimming of C. volutator in west Wales, which contrasts with the exclusively nocturnal swimming reported in this study, offers some support for this view. Timing of swimming
Swimming C. volutator were first detected about 30 min after the substratum was covered with water and they were present until the mud was emersed more than 3 h later. Swimming C. volutator were abundant before the time of high water but the highest density was recorded after high water. In the laboratory Holmstrom & Morgan (1983 a) observed swimming to begin at, or just after, the time of high water, an observation consistent with previous studies on other species, which have shown swimming predominantly on the ebb tide to be common (e.g. Fincham, 1970a, b; 1972; Preece, 1971). Morgan (1965) recorded C. volutator swimming predominantly after high water, but also caught large numbers before high water, which contrasted with his laboratory
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observations of swimming only on the ebb tide. Logically, the effect of swimming predominantly on the ebb tide would be a progressive overall movement of C. volutator downshore and downriver. Clearly, to reduce such tidal transport any ebb tide swimming would either have to be of very short duration, contrary to the observations of extensive swimming in this study, or compensated by flood tide swimming also. The swimming of C. volutator in the River Stour before high water, as well as on the ebb tide, would seem to be essential for the establishment and maintenance of this population 15 km from the sea. Duration of swimming
In the laboratory C. volutator swim only in short bursts and rarely swim higher than about 25 cm from the bottom of the container (Meadows & Reid, 1966; personal observation). The duration of in situ swimming of individuals would be difficult, if not impossible, to determine directly. However, there is some evidence, both direct and deductive, that individuals swim continuously for periods much longer than usually observed in the laboratory. Direct evidence of more prolonged swimming is the similarity of the abundance of amphipods swimming up to 1-5 m above the mud and close to the sediment. The deductive evidence is derived from the emergence trap data, which indicate that on any one night during a spring-tide period only 6-19% of C. volutator leave the mud to swim. A comparison between the density of animals in the plankton with that in the mud also indicates that a similarly low proportion of C. volutator are in the water at any one time. Consideration of these two pieces of evidence leads to the conclusion that the abundance of C. volutator in the plankton throughout the night is due to a small proportion of amphipods swimming for most of the time that water covers the sediment (up to about 3 h). The alternative explanation, that more animals swim but each for only a short period, is not supported by the emergence trap data. This conclusion that amphipods swim for a relatively long period, up to 3 h, is supported by Morgan's (1965) capture of swimming C. volutator in a tow-net while wading 'waist deep'. However, he found animals swimming only in the water above their normal position on the shore, which indicates only a short period of swimming. A similar comparison of the horizontal distribution of amphipods in the plankton with that in the mud, to confirm the extent of swimming, was not possible in this study because all the mud in this part of the estuary is inhabited by C. volutator. Frequency of swimming
The data from the emergence traps and plankton samples indicate that all C. volutator hatched between May and August swim at least once, on their first spring tide. Animals hatched at other times in the reproductive season (March-October) do not swim on their first spring tide but survivors may do so later in their life. The plankton and emergence trap data show that the smallest animals were the most abundant category of swimming animals, but in this
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respect the data from the trapping of swimming animals were less convincing. However, a comparison of the trap data with the plankton samples for 21/22 July 1982 (Fig. 2; Table 1 respectively) indicate that the traps may have undercollected the smallest animals, perhaps because the small animals are more likely to escape from the trap given their small size and their tendency to swim earlier in the night which gives them more time to escape to find more suitable substrata. (In retrospect perhaps it would have been advisable to put sieved sediment in each trap.) All the data indicate that mature C. volutator are more likely to swim than medium-sized animals. However, the small number of nights in which swimming C. volutator were detected and the small proportion of animals detected swimming on any one night, make it likely that some mature individuals do not swim during any one spring-tide period. It is not known how many times an individual that survives the full life-span, from one summer to the next, will swim. The theoretical maximum is six times (depending on the exact life-span) but an estimate based on the low proportion captured in the emergence traps is once or twice. There has been no previous attempt to estimate the number of times individual amphipods swim during their life but the conclusion that only a small proportion of animals swim at any one time is in agreement with two previous estimates. Marzolf (1965) calculated that up to 7-4 % of Pontoporeia affinis in Lake Michigan swam at any one time (where there are no tides to help concentrate swimming activity to a few days in each month) and Edgar (1983), working with algal dwelling amphipods, recorded approximately 3 % swimming on any one night. Why do C. volutator swim? The conclusion that a typical individual that survives the maximum life-span (from one summer to the next) will swim once when young, for less than 3 h, lends some support to the hypothesis that the pelagic dispersal of marine invertebrates from their parent has an optimum duration, for individual fitness, of less than about 6 h. There is no indication in this study that there is any significant advantage in wider dispersal that could, for example, be achieved by young C. volutator swimming on several nights. However, it is clear that swimming is not restricted to one specific stage in the life of an individual and may therefore be stimulated by several factors. Dispersal promotes gene flow, thereby reducing the probability of in-breeding which would lead to an increase in homozygosity. Marzolf (1965) considered that this was one advantage to the otherwise unexplained swimming of Pontoporeia affinis and these advantages undoubtedly hold for C. volutator. The swimming of the smallest C. volutator would alleviate the risks of a local catastrophe which could terminate a hereditary lineage characterized by limited or late dispersal. In this respect Crisp (1974, 1976) stressed the effects of density independent mortality factors, but density dependent mortality may also be significant. Shore birds are important predators of C. volutator (Hawkins, 1985),
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individual birds may consume many thousands of amphipods during one low tide period (Peer, Linkletter & Hicklin, 1986). Redshank (Tringa tringa) have been shown to forage optimally in areas of the highest density of their prey, whereupon the mortality rate of C. volutator was strongly density dependent (Goss-Custard, 1977). In these circumstances natural selection would favour dispersal by young C. volutator, which would prevent the formation of high density aggregations of related individuals and the associated increased mortality risk. Dispersal early in life (as a larva) has often been associated with reducing intraspecific competition. C. volutator feed mainly on diatoms and other small organic particles, both in suspension and in the surface deposits, which are caught on the setose gnathopods and passed to the mouth by the maxillipeds (Meadows & Reid, 1966; Fenchel, Kofoed & Lappalainen, 1975; Neilsen & Kofoed, 1982; Miller, 1984; Icely & Nott, 1986). Hawkins (1985) found that the chlorophyll concentrations on the mud surface declined in early summer, concurrent with the rapid increase in density of C. volutator, and later increased when the amphipod population was reduced by predation by birds. It is possible that early in the summer there is intraspecific competition between amphipods for surface diatoms, and food depletion may be a stimulus for C. volutator, of all sizes, to swim. It is perhaps significant that in the Stour swimming occurs only from May-August, when their densities are highest. Dispersal by the smallest C. volutator would prevent competition between related individuals. The significance of this is greatest, in evolutionary terms, where sibs share a trait that confers some competitive advantage greater than the mean in the rest of the population, where competition between siblings is more deleterious to individual fitness than competition with unrelated individuals and would retard the rate of adaptation. The possible advantages of swimming detailed above argue for dispersal once, early in their life, for subsequent swimming would not increase the benefits. The possible effects of intraspecific competition offer an explanation for swimming by only some larger animals and for a limited part of the year, but does not account for the regularly observed differences in size frequencies between amphipods in pelagic and benthic samples and does not explain why swimming only occurs on a small number of nights. The activity of other infaunal species, for example Cerastoderma edule (Jensen, 1985) and Neries diversicolor (Olaffson & Persson,
1986), may stimulate C. volutator to swim. However, if such disturbance was a significant factor swimming activity may be expected to show less rhythmicity and to affect all sizes equally. The swimming of other benthic amphipods at restricted times (usually at spring tides) has often been related to reproductive activity, particularly searching for a mate (Watkin, 1939; Fincham, 1970 a, b, 1972, 1974; Preece, 1971). Watkin (1941) considered that C. volutator swam to mate in the water column but Fish & Mills (1979) observed males and females sharing burrows for mating, the co-habitation being brought about by the males crawling across the 21
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mud in search of burrowed females. Preece (1971) considered that the swimming of Bathporeia pilosa may be related to the release of young (as had been previously postulated for cumaceans) because the night plankton was dominated by ovigerous females. However, this observation was in contrast to those of Watkin (1939) who had previously recorded more male than female B. pilosa in plankton samples that were occasionally dominated by immature animals. Preece also noted that the release of young coincided with peaks of swimming activity by adults, at the times of spring tides. Fish & Mills (1979) recorded semi-lunar increases in the number of female C. volutator carrying stage 1 embryos and a possible link between swimming and release of young was indicated by the relatively high proportion of mature female C. volutator in the first trap sample that were carrying ova or juveniles, (39 and 29 % respectively compared to 11 and 5 % respectively in the whole population). However, the relationship between the female reproductive cycle and swimming could not be considered further because none of the subsequent trap samples contained a sufficient number of mature females to allow such an analysis, a fact that in itself indicates that such a hypothesis would be misfounded. That the swimming of C. volutator in the Stour occurs over only a portion of the breeding season, and not all mature animals swim during each spring tide period, surely indicates that swimming is not an integral part of reproductive behaviour. REFERENCES ALLDREDGE, A. L. & KING, J. M., 1980. Effects of moonlight on the vertical migration patterns of demersal zooplankton. Journal of Experimental Marine Biology and Ecology, 44, 133-156. BEANLAND, F. L., 1940. Sand and mud communities in the Dovey estuary. Journal of the Marine Biological Association of the United Kingdom, 24, 589-611. CRISP, D. J., 1974. Energy relations of marine invertebrate larvae. Thalassia jugoslavica, 10, 103-120. CRISP, D. J., 1976. The role of the pelagic larva. In Perspectives in Experimental Biology, vol. 1. Zoology (ed. P. Spencer-Davies), pp. 145-155. Oxford: Pergamon Press. EDGAR, G. J., 1983. The ecology of south-east Tasmanian phytal animal communities. IV. Factors affecting the distribution of ampithoid amphipods among algae. Journal of Experimental Marine Biology and Ecology, 70, 205-225. FENCHEL, T. L., KOFOED, L. H. & LAPPALAINEN, A. 1975. Particle size-selection of two deposit feeders: the amphipod Corophium volutator and the prosobranch Hydrobia ulvae. Marine Biology, 30, 119-128. FlNCHAM, A. A., 1970a. Amphipods in the surf plankton. Journal of the Marine Biological Association of the United Kingdom, 50, 177-198. FINCHAM, A. A., 1970i. Rhythmic behaviour of the intertidal amphipod Bathyporeia pelagica. Journal of the Marine Biological Association of the United Kingdom, 50, 1057-1068. FINCHAM, A. A., 1972. Rhythmic swimming and rheotropism in the amphipod Marinogammarus marinus (Leach). Journal of Experimental Marine Biology and Ecology, 8, 19-26. FINCHAM, A. A., 1974. Periodic swimming behaviour of amphipods in Wellington harbour. New Zealand Journal of Marine and Freshwater Research, 8, 505-521. FISH, J. D. & MILLS, A., 1979. The reproductive biology of Corophium volutator and C. arenarium (Crustacea: Amphipoda). Journal of the Marine Biological Association of the United Kingdom, 59, 355-368. GOSS-CUSTARD, J. D., 1977. Predator responses and prey mortality in redshank Tringa totanus (L.) and a preferred prey Corophium volutator (Pallas). Journal of Animal Ecology, 46, 21-35.
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HART, T. J., 1930. Preliminary notes on the bionomics of the amphipod Corophium volutator Pallas. Journal of the Marine Biological Association of the United Kingdom, 16, 761-789. HAWKINS, C. M., 1985. Population carbon budgets and the importance of the amphipod Corophium volutator in the carbon transfer on a Cumberland Basin mudflat, Upper Bay of Fundy, Canada. Netherlands Journal of Sea Research, 19, 165-176. HOLMSTROM, W. F. & MORGAN, E., 1983 a. Variation in the naturally occurring rhythm of the estuarine amphipod Corophium volutator (Pallas). Journal of the Marine Biological Association of the United Kingdom, 63, 833-850. HOLMSTROM, W. F. & MORGAN, E., 19836. The effects of low temperature pulses in rephasing the endogenous activity rhythm of Corophium volutator (Pallas). Journal of the Marine Biological Association of the United Kingdom, 63, 851-860. HOLMSTROM, W. F. & MORGAN, E., 1983 C. Laboratory entrainment of the rhythmic swimming activity of Corophium volutator (Pallas) to cycles of temperature and periodic inundation. Journal of the Marine Biological Association of the United Kingdom, 63, 861-870. ICELY, J. D. & NOTT, J. A. 1985. Feeding and digestion in Corophium volutator (Crustacea: Amphipoda). Marine Biology, 89, 183-195. JANSSON, B.-O. & KALLANDER, C , 1968. On the diurnal activity of some littoral peracarid crustaceans in the Baltic Sea. Journal of Experimental Marine Biology and Ecology, 2, 24-36. JENSEN, K. T., 1985. The presence of the bivalve Cerastoderma edule affects migration, survival and reproduction of the amphipod Corophium volutator. Marine Ecology - Progress Series, 25, 269-277. LINCOLN, R. J., 1979. British Marine Amphipoda: Gammaridae. London: British Museum (Natural History). LINDSTROM, M. & LINDSTROM, A. 1980. Swimming activity of Pontoporeia affinis (Crustacea, Amphipoda) - seasonal variations and usefulness for environmental studies. Annales zoologici fennici, 17, 213-220. LUCAS, M. I., WALKER, G., HOLLAND, D. L. & CRISP, D. J., 1979. An energy budget for metamorphosis of the cypris larva of Balanus balanoides. Marine Biology, 55, 221-229. MARZOLF, G. R., 1965. Vertical migration of Pontoporeia affinis (Amphipoda) in Lake Michigan. Publications. Great Lakes Research Division, no. 13, 133-140. MEADOWS, P. S. & REID, A., 1966. The behaviour of Corophium volutator (Crustacea: Amphipoda). Journal of Zoology, 150, 387-399. MILLER, D. C., 1984. Mechanical post-capture particle selection by suspension- and depositfeeding Corophium. Journal of Experimental Marine Biology and Ecology, 82, 59-76. MORGAN, E., 1965. The activity rhythm of the amphipod Corophium volutator (Pallas) and its possible relationship to changes in hydrostatic pressure associated with the tides. Journal of Animal Ecology, 34, 731-746. NIELSEN, M. V. & KOFOED, L. H., 1982. Selective feeding and epipsammic browsing by the deposit feeding amphipod Corophium volutator. Marine Ecology - Progress Series, 10, 81-88. OLAFSSON, E. B. & PERSSON, L.-E., 1986. The interaction between Nereis diversicolor O. F. Miiller and Corophium volutator (Pallas) as a structuring force in a shallow brackish sediment. Journal of Experimental Marine Biology and Ecology, 103, 103—117. PEER, D. L., LINKLETTER, L. E. & HICKLIN, P. W., 1986. Life history and reproductive biology of Corophium volutator (Crustacea: Amphipoda) and the influence of shorebird predation on population structure in Chignecto Bay, Bay of Fundy, Canada. Netherlands Journal of Sea Research, 20, 359-373. PREECE, G. S., 1971. The swimming rhythm of Bathyporeia pilosa (Crustacea: Amphipoda). Journal of the Marine Biological Association of the United Kingdom, 51, 777-791. SHEADER, M., 1978. Distribution and reproductive biology of Corophium insidiosum (Amphipoda) on the north-east coast of England. Journal of the Marine Biological Association of the United Kingdom, 58, 585-596. WATKIN, E. E., 1939. The pelagic phase in the life history of the amphipod genus Bathyporeia. Journal of the Marine Biological Association of the United Kingdom, 23, 467-481. WATKIN, E. E., 1941. The yearly life-cycle of the amphipod Corophium volutator. Journal of Animal Ecology, 10, 77-93.
