Endogenous rhythms of circatidal swimming activity in the estuarine copepod Eurytemora affinis (Poppe)

J. Exp. Mar. Biol. Ecol., 161 (1992) 27-32 © 1992 Elsevier Science Publishers BV. All fights reser ced 0022-0981/92/$05.00

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Endogenous rhythms of circatidal swimming activity in the estuarine copepod Eurytemora affinis (Poppe) A.R. Hough and E. Naylor School of Ocean Sciences, University of Wales, Bangor, Menai Bridge, Gwynedd, UK (Received 18 July 1991; revision received 12 March 1992; accepted 27 March 1992) Abstract: Under constant cortditions in the laboratory the estuarine copepod Eurytemora affinis (Poppe) displays an endogenous circatidal swimming rhythm. The phasing of peak endogenous activity varies with the semilunar (neap-spring) cycle and with position along the estuary. Animals collected on spring tides of increasing amplitude show peak activity during the expected flood tide, while those sampled on spring tides of decreasing amplitude or towards the limit of tidal influence display peak activity during the expected ebb tide. This is apparently the first report of an endogenous circatidal rhythm in a copepod, the phase-lability of which is unusual. These findings also support field observations on tidal abundances and position maintenance behaviour in this species. Key words: Circatidal; Copepod; Estuary; Rhythm; Swimming

INTRODUCTION

Studies of endogenous locomotor rhythmicity in planktonic organisms have hitherto mainly addressed questions concerning circadian vertical migrations (Enright & Hamner, 1987; Sulkin et al., 1979), which are presumed to act as predation or photodamage avoidance mechanisms (Kerfoot, 1985). There is, however, an obvious adaptive advantage to tidal vertical migrations in the estuarine environment where advection by residual seaward flow may be counteracted by tidal transport into the estuary. This is particularly relevant to animals which spend part of the migratory cycle at, or near to, the bottom and migrate upwards into faster-moving water masses on a tidal basis (Hill, 1991). So far the only demonstration of endogenous circatidal swimming rhythms in planktonic crustaceans is in zoea larvae of the crab, Rhithropanopeus harrisii (Cronin & Forward, 1979). These show a rhythm of vertical migration which, although under circadian modulation, is strongly tidal with animals reaching minimum depths at the time of expected high tide and maximum depths at expected low water. Field observations on the tidal abundances of Eurytemora affinis in a tidally mixed estuary (Hough & Nay!or, 1991) have demonstrated vertical migrations on either the flood or ebb tide, depending on both the position of animals along the estuary and the Correspondence address: A.R. Hough, Environmental Advisory Unit, Yorkshire House, Chapel Street, Liverpool L3 9AG, UK.

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time of sampling relative to the semilunar cycle. Animals were consistently flood-tide active at the seaward end of the estuary and ebb-tide active towards the limit of tidal influence, and there was an accumulation of animals in mid-estuary, apparently related to a specific salinity zone. Sampling over a semilunar cycle showed animals moving upstream over spring tides and downstream over neaps, seemingly in response to salinity variation with tidal amplitude. This movement contrasts with the reported behaviour of R. harrisii larvae which appear to maintain station in estuaries of low tidal amplitude by vertical swimming rhythms around the depth of zero net flow (Forward & Cronin, 1980; Cronin & Forward, 1982). The clearly marked differences in tidal amplitudes between the Conwy Estuary here and those inhabited by R. harrisii, prompted the present investigation. It was designed to test for the existence, and extent, of endogenous control over the behavioural mechanism of position maintenance in E. affinis, which field observations (Hough & Naylor, 1991) suggest is more complex than in R. harrisii. MATERIALS AND METHODS

Eurytemora were collected during daytime high tides at a point mid-way along, and also near the limit of tidal influence of, the Conwy Estuary, northern Wales (see Hough & Naylor, 1991), using a hand-held plankton net of 0.2-mm mesh size. They were then immediately transported to the laboratory and placed in an actograph recording system, with approximately the same delay in each case after the time of collection. The external dimensions of the actograph chamber, constructed of 6 mm thick Perspex, were 12 cm high, 15 cm wide and 3 cm deep. Preliminary video-recording of the swimming of Eurytemora in the actograph chamber showed that, on a tidal basis, they were sometimes concentrated near the bottom and at other times dispersed throughout the whole water column, depending upon the intensity of their typical copepod "hop and sink" behaviour. Accordingly, their temporal patterns of swimming upwards in the water column were quantified using an array of eigbt IR transmitters and receivers arranged, respectively, on the front and back of the actograph chamber, hence operating over a distance of 1.8 cm of water. The transmitter/receiver units were arranged in two groups of four, equally spaced across the 15 cm width of the tank, with four placed 3 cm from the top and four 8 cm from the top. The receivers were monitored by a BBC model B microcomputer, beam interruptions being summed every 15 min and recorded on cassette tape. ~ 2000 individuals (adults and copepodites) were used in each experiment and there was consistency in the activity records of the four replicate receivers at each level in the tank, except when obvious malfunctions occurred. Data were therefore plotted as total activity records by all operating receivers over 15-min intervals, plotted as 3-point moving averages to reduce "noise". All experiments were carried out in continuous darkness in water collected at high tide from the sampling site and at 12 ° C, which was within 3 °C of the temperature at the site of collection.

SWIMMING ACTIVITYOF AN ESTUARINE COPEPOD

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RESULTS Fig. 1 shows the activity trace of animals collected from mid-estuary on a tide when tidal amplitudes were increasing, in May, 19~9. Peak activity occurred ~ 1.5 h before the times of expected high water and dropped sharply before the time of high tide to be maintained at low levels throughout the ebb tide. Animals collected from midestuary on a tide later in the same spring-neap cycle when tidal amplitudes were decreasing (Fig. 2), again showed a circatidal pattern of upward swimming. Maximum activity at this time occurred after expected high tide and then decreased slowly over the ebbing tide to a minimum during the time of the expected flood tide. The base level of activity was much higher during late springs than during early springs, but the significance of this difference remains to be evaluated in these experiments. A consistent decrease in height of the activity peaks in Fig. 2, presumed here to be due to the observed mortality of copepods in the recording chamber, was found throughout this experiment, but the rhythm persisted over at least five tidal cycles. Animals collected during early spring tides, but near the limit of tidrl influence, in May, 1990 (Fig. 3), showed maximum swimming shortly after the time of expected high tide and a similar activity pattern to that of animals collected during late spring tides in mid-estuary (Fig. 3). None of the rhythms recorded show any indication of circadian modulation of the circatidal activity.

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Fig. 1. Swimmingactivityof ~ 2000 E. affinis collected from mid-estuaryduring spring tides of increasing amplitude. A three-point moving averagewas applied to the data, * - time of expected high tide.

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DISCUSSION

All three of the experiments carried out in this study demonstrate the existence of an endogenous circatidal rhythm of upward swimming behaviour in E. affinis. Moreover, changes in the timing of the activity maxima of this rhythm over the semilunar 250 7

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S W I M M I N G ACTIVITY OF AN ESTUARINE COPEPOD

31

cycle and with position along the estuary suggests an obvious mechanism underlying the tidal abundances of E. affinis in the field (Hough & Naylor, 199!). Activity before the time of expected high tide, as found in animals collected in mid-estuary on early spring tides and apparently also in animals towards the seaward end of the species range (Hough & Naylor, 1991) would lead to animals rising in the water column on the flood tide and so being transported upstream. The sharp fall in swimming activity in these animals before the scheduled high tide would lead to sinking of animals to the bottom of the water column over the high slack water. Maintained low levels of swimming activity near the bottom over the ebbing tide and the possible intermittent adoption of a benthic habit at times of minimal activity (J. A. Runge & Y. Simard, pers. comm.) would then help to prevent re-suspension of animals and so reduce the possibility of transport downstream. Ebb-tide active animals, found on late spring tides in mid-estuary, and throughout the semilunar cycle at the most upstream site, show peak swimming activity 1.5-3.5 h after the time of expected high water. These patterns of behaviour would result in the concentration of Eurytemora in the middle reaches of the estuary and correlate well with the spring-neap movement of the population upstream and downstream which has been observed in the field (Hough & Naylor, 1991). The semilunar and positional changes in the timing of swimming activity represent a considerable phase lability in the endogenous rhythm of Eurytemora. Apparently the only other example of such a change in the phasing of a circatidal rhythm is in the estuarine amphipod Corophium volutator (Holmstrom & Morgan, 1978; Harris & Morgan, 1986). This shows seasonal and semilunar changes in the timing of peak activity, attributed to seasonal differences in temperature and an interaction of endogenous semilunar and tidal rhythms. In contrast to other examples of semi-lunar modulation of endogenous swimming rhythms, the rhythm in E. affinis appears to be modulated by position along the estuary as well as tidal range. The environmental variable serving as a zeitgeber for this rhythm remains to be determined, but as E. affinis appears to be distributed relative to a preferred salinity zone, salinity probably provides the most reliable cue. For this reason, the present experiments were carried out in water obtained at the site where the animals were collected, to preclude the possibility that any endogenous rhythmicity might be phase-shifted by a transfer to a salinity different from that at the site of collection. This rhythm in E. affinis represents only the second demonstration of endogenous tidal activity patterns in what is essentially a planktonic species, and apparently the first in a copepod. Most other such rhythms have been reported in benthic or benthonic forms (Naylor, 1985), the only other reported example in a planktonic organism being that of zoeal larvae of the crab R. harrisii in which, unlike the rhythm in E. affinis, the phase of the rhythm appears to remain constant relative to the spring-neap cycle (Cronin & Forward, 1979). Field observations on R. harrisii, however, do suggest spring-neap differences in the timing ofthe vertical migration (Forward & Cronin, 1980) and changes in the point of the larval maxima with changing salinity (Cronin, 1982).

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A.R. HOUGH AND E. NAYLOR

The reasons behind these similarities with E. affinis are not clear and present a clear basis for further study. ACKNOWLEDGEMENTS

This work was carried out during a NERC studentship to A.R. Hough.

REFERENCES

Cronin, T.W., 1982. Estuarine retention of the crab Rhithropanopeus harrisii. Estaarine Coastal Shelf Sci., Vol. 15, pp. 207-220. Cronin, T.W. & R.B. Forward, Jr., 1979. Tidal vertical mig~'ation: an endogenous rhythm in estuarine crab larvae. Science, Vol. 205, pp. 1020-1022. Cronin, T.W. & R.B. Forward, Jr., 1982. Tidally timed behaviour: effects on larval distributions in estuaries. In, Estuarine comparisons, edited by V. S. Kennedy, Academic Press, New York, pp. 505-520. Enright, J.T. & W.M. Hamner, 1967. Vertical diurnal migration and endogenous rhythmicity. Science, Vol. 157, pp. 937-941. Forward, R. B. Jr. & T. W. Cronin, 1980. Tidal rhythms of activity and phototaxis of an estuarine crab larva. Biol. Bull., Vol. 158, pp. 295-303. Harris, G.J. & E. Morgan, 1986. Seasonal and semi-lunar modulation of the endogenous swimming rhythm in the estuarine amphipod Corophhml vohaotor (Pallas). Mar. Behav. PhysioL, Vol. 12, pp. 303-314. Hill, A.E., 1991. A mechanism for horizontal zooplankton transport by vertical migration in tidal currents. Mar. Biol., Vol. 111, pp. 485-492. Holmstrom, W. F. & E. Morgan, 1978. Some properties ofthe tidal activity rhythm in the estuarine amphipod Corol,hium vohaator. In, Cyclic phenomena in marine plants and animals. Proc. 13th Eur. Mar. Biol. Syrup., edited by E. Naylor & R.G. Hartnoll, Pergamon Press, Oxford, pp. 355-356. Hough, A.R. & E. Naylor, 1991. Tidal swimming activity and retention of Eurytemora affinis (Crustacea:Copepoda) in a mixed estuary. Mar. Ecol. Prog. Ser., Voi. 76, pp. !15-122. Kerfoot, W.C., 1985. Adaptive value of vertical migration: Comments on the predation hypothesis and some alternatives. In, Migration: mechanisms and adaptive significance, edited by M.A. Rankin, Contrib. Mar. Sci. Suppl., Vol. 27, pp. 91-113. Naylor, E., 1985. Tidally rhythmic behaviour of marine animals. Syrup. Soc. Exp. Biol., Vol. 39, pp. 63-93. Sulkin, S.D., I. Phillips & W. Van Heukelem, 1979. On the locomotor rhythm of brachyuran crab larvae and its significance in vertical migration. Mar. Ecol. Prog. Ser., Vol. 1, pp. 331-335.