A quantitative description of the behaviour of wild juvenile plaice (Pleuronectes platessa L.)

Anim. Behav., 1980,28, 1202-1216

A QUANTITATIVE DESCRIPTION OF THE BEHAVIOUR OF WILD JUVENILE PLAICE (PLEURONECTES PLATESSA L.) BY R. N. GIBSON

Dunstaffnage Marine Research Laboratory, Oban, Scotland Abstract. The behaviour of young plaice (Pleuronectes platessa L.) as they migrate up and down sandy beaches with the tide is described. Their behaviour during this migration consists mainly of swimming and feeding interspersed with rarer behavioural acts. Over short periods swimming behaviour can be described by a random model in which the probability of a swim occurring remains constant. This probability varies markedly, however, from hour to hour. Two types of swimming movement are recognized: one of very short duration represents searching for food and the other, longer, category serves to transport the fish up and down the shore. Variations in the feeding rate and in the frequency, duration, and direction of swimming movements over the tidal cycle are described and related to the changing physical and biological conditions that the fish experience during their intertidal movements. Young plaice spend at least their first summer of life in shallow water on sandy beaches. Their ecology during this period has been studied intensively, most investigations dealing with feeding habits and the role of plaice as predators in the overall ecology of such 'nursery areas' (Bregneballe 1961; Macer 1967; Edwards & Steele 1968; Kuipers 1973, 1977). Because the fish are restricted to water rarely more than a few metres deep, their movements and distribution are governed largely by the tides. In most areas the fish move up and down the beach in synchrony with the ebb and flow of the tide (Edwards & Steele 1968; Gibson 1973a; Kuipers 1973). During these tidal migrations the young fish feed on benthic invertebrates living in the sand although their diet and temporal pattern of feeding varies considerably from beach to beach (Edwards & Steele 1968; Gibson 1973a; Kuipers 1973; Thijssen et al. 1974). Knowledge of the behaviour of the fish in shallow water comes mainly from indirect obselwation either by sampling the population at different states of the tide or times of year (Macer 1967; Gibson 1973a; Kuipers 1973; Lockwood 1974) or from the recapture of marked individuals (Macer 1967; Riley 1973; Lockwood 1974). The possible factors controlling the tidal and seasonal movements have been discussed by Gibson (1973a). The clarity of the water and sheltered nature of many of the beaches on the west coast of Scotland has enabled the fish's behaviour to be observed directly, and by comparing laboratory and field activity patterns, an attempt has been made to assess the function of the juvenile plaiee's endogenous activity rhythm (Gibson 1973b) in controlling its movements in the natural habitat (Gibson 1975). This paper gives

a detailed description of the behaviour of young plaice in the wild and tries to elucidate some of the environmental factors which control their activity and movements. Methods The Study Area The observations were made on two beaches of different aspect and exposure to wave action situated close to the Dunstaffnage Laboratory near Oban on the west coast of Scotland. They were Camas Nathais and Dunstaffnage Bay, which for the sake of brevity will be referred to as Bay C and Bay D respectively. Beach profiles obtained by standard levelling techniques are given in Fig. 1. Bay C has a uniform steeply sloping beach of clean sand facing south west and is bordered on both sides by steep rocks.

Boyc

"

.

100

.

.

.

.

.

200

.

.

.

.

.

.

500

.

.

.

.

HWMNT

400 ft

@

~5

50 75 Horizon~o!dis~once

100

125_m

Fig. 1. Profilesof the two beacheswhere the behaviom-al observations were made. The vertical marks indicate the upper and lower limits of the observations.Approximate levelsof high water mark of neap tides (HWMNT), low water mark of neap tides (LWMNT)and low water mark of spring tides (LWMST) are shown by the horizontal broken lines. 1202

GIBSON: BEHAVIOUR OF WILD JUVENILE PLAICE Bay D has a much gentler gradient over most of the intertidal zone and the slope is about half that of Bay C. Above low water mark of neap tides, the beach consists of a steep bank of coarse stones and gravel, which was never inhabited by plaice. Over the rest of the beach the sediment consists of muddy sand and scattered rocks. It faces north east and is consequently sheltered from the prevailing south-westerly winds. Both beaches have a large population of young plaice throughout the summer and autumn, with fish ranging in size from 3 to 10 cm depending on the season, although those in Bay C were noticeably smaller than those in Bay D at equivalent times of year. The behaviour of the fish was recorded over the period July to September.

Observations and Recording Techniques Providing the water is clear, it is relatively easy to observe plaice in the sea because they are generally most abundant in depths of 1 to 3 m (Gibson 1973a). The method used to watch the fish was developed for an earlier study (Gibson 1975) and the apparatus consisted of a large metal cylinder with a transparent Perspex base. The cylinder was attached to the transom of a small rubber dinghy by means of a universal joint. The dinghy was loosely moored to a floating rope anchored at one end to the shore and at the other to a buoy below low water mark. Observations were made through the base of the cylinder in depths of 1-2 m. Once a fish had been sighted, a spoken commentary of its behaviour was recorded on tape using a portable cassette recorder. Each recording was accompanied by a note of the date, time, and in most cases the depth of water to the nearest 10 cm in which the observation was made. In conjuction with tide charts from a tide gauge situated in Dunstaffnage Bay, a knowledge of the depth of water and slope of the beach enabled the approximate position of the observation on the beach to be calculated. Observations were made only during the day between 0800 and 1800 hours BST, with the majority falling between 1000 and 1600 hours BST. They were timed to cover the whole tidal cycle and most were made in calm sea conditions. The duration of each observation was dependent upon the level of activity and direction of movement of the fish being observed; highly active fish moving parallel to the shore line, for example, could not be followed for as long as those moving directly up or downshore. Great care was taken to avoid disturbing the fish.

1203

Sudden movements, casting shadows and moving the boat over the fish before observations started were all avoided as far as possible. In only six cases, none of which are included in the results, was it obvious that the fish had been disturbed. All other fish were not overtly affected by the presence of the boat and appeared to swim and feed normally. In the laboratory the recorded commentary was played back and transcribed via a keyboard and 10-channel event recorder onto paper charts moving at 6" (15.2 cm)/min. The charts were then analysed for the type and duration of each behavioural act and the sequence of performance of the acts. The acts themselves were defined by a series of preliminary observations and are described in detail in the results section.

Results Over the observation period more than 70 h were spent looking for and watching fish. Of this time, approximately 31 h of useful recordings were made of the behaviour of 385 fish. Durations of recordings varied from approximately 1.5 rain up to 11 rain with a mean of 5.0 for Bay C and 4.7 rain for Bay D. The short duration of the recordings was for the most part due to the difficulty of keeping the fish in sight for longer periods and is one of the drawbacks of working in the field. It is hoped, .however, that this drawback is compensated for by the large number of individuals in the sample. An attempt was made to distribute the observations as evenly as possible throughout the tidal cycle because one of the primary objects of the investigation was to describe the changes in behaviour that took place during this period.

General Description of Behaviour Although three dimensions are theoretically available to flatfish for their movements, the observations showed that young plaice, at least during the day, rarely swim more than a few millimetres off the bottom, so that their activity is essentially two-dimensional. Another feature of flatfish behaviour, allied to their benthic mode of life and cryptic coloration, is the fact that they spend most of their time motionless. When they do move it is in a series of well defined actions each of which is almost always separated from the preceding one by a pause. The pause may last only a fraction of a second or up to several minutes. This sequence of action-pauseaction makes each act easy to recognize and define. Most of the behaviour observed in the sea

1204

ANIMAL

BEHAVIOUR,

consisted of swimming in short bursts and feeding, occasionally interspersed with other much rarer behavioural acts. Each of these behavioural acts is referred to below as an element of the total behavioural repertoire. Qualitative Description of Behavioural Elements The fish spend so much time motionless on the bottom that it is necessary to describe this resting position. The unpigmented under surface of the body lies in contact with the sand and the head is slightly raised. The fish is supported in this position by the left pectoral fin and the anterior rays of the median fins. The eyes are usually protruded and move frequently and independently giving the fish a wide field of vision, up to 215 ~ for one eye in the horizontal (morphologically sagittal) plane (Scheuring 1921). A similar resting position or 'alert posture' has been described for other flatfish (Steven 1930; Olla et al. 1969; Olla et al. 1972; Stickney et al. 1973; Holmes & Gibson, in preparation). Swim. The most common of all the behavioural elements, swimming movements consist basically of two types. In the first, the fish 'shambles' (Verheijen & de Groot 1967) or 'shuffles' (Holmes & Gibson, in preparation) slowly over the bottom, propelling itself forward on the tips of the median fin rays. When moving at higher speeds the whole body leaves the substratum and propulsion is effected by vertical strokes of the caudal fin and posterior half of the body. Between these two types of swimming are various intermediate forms all of which, together with shambling and high speed swimming are classified as a swim. Shift. A shift consisted of a change in position of the fish without moving more than about half a body length from its original position. It also includes turning on the spot. Shifting may occur forwards or backwards and was effected by 'rowing' a few strokes with the anterior rays of the median fins. It was always rapid and it appeared to be a movement which enabled the fish to take a closer look at an object, to change its field of vision, or to orientate its body towards a prey organism. Bite. The act of capturing, or attempting to capture, a prey. A bite consists of a very rapid short lunge forwards and downwards onto the sea bed usually from the alert resting position. The object at which the bite was directed could only rarely be seen by the observer before the bite was performed and equally rarely was the

28, 4

prey captured visible afterwards. This was mainly because the fish feed on small amphipods, copepods and polychaete tentacles which are well camouflaged and too small to see from a distance. Chew. A bite was frequently followed by an action, called chewing, which consisted of vigorous movement of the jaws and opercula. It was assumed to be an action which prepared the captured prey for swallowing. Bury. On occasions the fish would rapidly raise its head and tail simultaneously several times in a fluttering action. This movement resulted in the fish digging itself into the sand. The depth to which the fish buried itself depended on the vigour and duration of the burying action; occasionally the fish would be completely covered with only the eyes visible, but in most cases it only covered itself with a fine layer of sand and remained easily discernible. Yawn. The term yawning was applied to an action in which the fish slowly opened the mouth wide and spread its opercula, often raising its head at the same time. U-bend. During a U-bend the fish slowly raised its head and tail off the bottom so that the body formed a shallow U-shape. Both head and tail were then lowered again to the resting position. The reverse action was occasionally observed. The fish raised only the central portion of its body off the sand, the head and tail remaining in contact with the bottom. Roll. A roll was recorded when the fish rolled on its back ventral side first, and then righted itself again. The action was performed in one smooth forwardly directed action and resulted in the fish scraping its pigmented side on the sand. Another action, analogous to a roll and apparently performed for the same purpose, i.e. to scrape the body on the sand, was also seen on rare occasions. The fish first swam off the bottom. It then darted downwards in a rapid movement scraping the unpigmented (left) side on the sand then swam up again and eventually came to rest. In both cases the contact of the body with the sand was vigorous as it always disturbed a cloud of sand grains. Quantitative Description of Behavioural Elements In this section a more detailed analysis of the frequency of performance of the elements will be given, together with a description of the variations in their frequency over the tidal cycle. The length of the observation period varied con-

GIBSON: BEHAVIOUR OF WILD JUVENILE PLAICE siderably from fish to fish and consequently it was necessary to use a standard measure of frequency. This standard was taken as the number of each element performed per minute and was calculated by dividing the total number of each element recorded for each fish by the duration of the observation period for that fish. The mean frequency of each element was then calculated for each hour of the tidal cycle by averaging the mean frequencies for all fish observed in that hour. Swim. The hourly variation in the mean frequency of swimming movements over the tidal cycle is illustrated in Fig. 2. There was a clear difference in the pattern between the two bays. In Bay C, the frequency of swimming movements decreased as the tide came in and then increased again as it ebbed, with the low tide frequency being approximately double that at high tide. In Bay D there was a general increase in frequency over the whole tidal cycle but there is a clear peak at about mid-ebb and possibly a less welldefined one just before high water. Changes in the mean duration of swims over the tidal cycle were also examined. Swim differs from all other elements recorded in that it can vary markedly in duration from < 1 s up to > 10 s. Swim durations were measured from the pen recorder charts to the nearest second below, and in the descriptions that follow, therefore, durations are grouped into 1-s categories of 0, 1, 2, 3 s, etc. The mean duration of swimming movements for each fish was then calculated by dividing the total time swimming by the number of movements, assigning a value of 0.5 s to those in the 0 s category, 1.5 s to those in the 1 s category and so on. The results are plotted in Fig. 3. It will be noticed from this figure that in both 15

(a)

1205

bays the mean duration changes over the tidal cycle and that there is a different pattern of change in the two bays. In Bay C the mean duration increases to a maximum at high water and then declines again on the ebb tide, whereas in Bay D the mean duration is greatest on the flood tide and more or less constant on the ebb. Comparison of the data presented in Figs 2 and 3 gives some idea of the time the fish actually spend in motion. Multiplying the mean frequency in any one hour by the mean duration in that hour gives the mean time (in seconds) spent swimming per minute during that hour. This variable does not remain constant but varies from approximately 4 to 10 s/min, its pattern of change closely following that of the change in swim frequency (Fig. 2). The results presented so far describe the gross changes in swimming behaviour over a tidal cycle, but it is also possible to examine such behaviour in greater detail in order to determine how it is organized on a shorter time scale. The simplest hypothesis that can be proposed for the short-term organization of swimming behaviour is that the movements are performed at random, that is they are temporally independent of one another. If this is so then the frequency distribution of intervals between each movement when plotted cumulatively as a semi-logarithmic survivorship curve should produce a straight line. As a consequence of temporal independence, a semi-logarithmic plot of the cumulative frequency distributions of bout lengths (a bout is defined below) also results in a straight line and the frequency distributions of intervals and bout lengths can be described as geometric series (Slater 1974). The possibility that the swimming behaviour could be described by such a random model was

'~

(b)

'~

~10

~ hO1

~5 0 -6

-4

-2

0

-4 -2 +2 +4 .+6 " 7irne relative to hi, =hwater (hours)

0

+2

+4

+6

Fig.. 2. Variation in the mean frequency of the elements swim (above), shift (centre), and bite (below) over the tidal cycle in (a) Bay C and (b) Bay D.

-6

-4

-2

0

+2 +4 +6 -6 -4 -2 Time relative to high woler (hours)

0

+2

+4

+6

Fig. 3. Variation in the mean duration of swims over the tidal cycle in (a) Bay C and (b) Bay D.

1206

ANIMAL

BEHAVIOUR,

examined by comparing the frequency distributions of intervals between swims for each hour of the tidal cycle with expected geometric series calculated in the manner descrfbed by Lemon & Chatfield (1971). In the initial analysis it became clear that there were fewer intervals of < 1 s than expected. This is best illustrated by plotting histograms of the actual (rather than cumulative) frequency distributions of intervals and two examples are given in Fig. 4. They are both from Bay C and represent interval distributions at the highest (5-4 h before high water) and lowest (0-1 h after high water) swim frequencies (Fig. 2a). Although the interval frequency distribution in the former hour is not significantly different from a geometric series ( ~ 6 -----24.0, P > 0.05), its form is clearly analogous to that of the latter hour (0-1 h after high water) whose distribution is significantly different from a geometric series ( ~ 6 = 28.8, P < 0.05). The fact that there are fewer intervals < 1 s than expected in both samples suggests that there may be a refractory period of < 1 s during which another swim is unlikely to occur, and that this refractory period is inversely proportional to the overall frequency. If this hypothesis is accepted, then once this refractory period is exceeded, do the remaining intervals, i.e. those ~ 1 s, conform to a geometric series ? It seems they do because calculation of expected frequency distributions on this basis and comparison of these with the observed distributions excluding the first term, showed that they were not significantly different. For 5-4 h before high water, ~ 5 = 21.8, P > 0.10, and for 0-1 h after high water ;(~5 = 11.3, P > 0.70. The biological significance of the refractory period may be to

28,

4

allow the fish to scan its environment visually before making the next move, because swimming forms part of the behaviour performed whilst searching for food. The cumulative frequency distributions of bout lengths for these two hours are plotted in Fig. 5. A bout is defined here as a succession of swimming movements which ends when another behavioural element is performed. This is Slater's (1974) 'common sense' definition and its use was necessary because there were no sharp changes in slope of the log survivorship curves of intervals which would have enabled a bout to be defined according to a critical time limit. As expected, the cumulative frequency distributions of bout lengths lie very close to straight lines except at the lower ends where the presence or absence of a long bout affects the curve considerably. These distributions are not significantly different from geometric series (P > 0.95 in both cases). Examination of the other 22 hourly frequency dis500-

9 5 - 4 h before H.W. o 0-1 h after H~V.

\

\ o\\ \\ \\

g

&

"6

\\

25-

3

\

20o-

o

\

\2

15-

10-

r--~

1

'0. 0

5

~176176

3o

9_--- J

10 Intervol duration (secs)

15 ~ 16 1

Fig. 4. Frequency distribution of the duration of intervals between swims for two hours of the tidal cycle in Bay C. Continuous line, 5-4 h before high water; dashed line, 0-1 h after high water.

5

10 No. swims / bout

15

20

Fig. 5. Survivorship curves f o r bouts o f swims f o r the

same two hours of the tidal cycle as Fig. 4.

GIBSON: BEHAVIOUR OF WILD JUVENILE PLAICE

1207

two categories were that the short duration swims were associated with feeding and possibly represented searching movements, whereas the swims of longer duration served to transport the fish up and down the shore. It was predicted on this basis that the frequency of short swims would be positively correlated with feeding intensity and that the frequency of the longer swims would not. The larger body of data resulting from the present investigation enabled this hypothesis to be re-examined, and correlation coefficients for the relationship between the frequency o f the different swim durations and the frequencies of other behavioural elements and physical variables were calculated. The results of these calculations are given in Table I. Examining the results of the correlations from Bay C first, it will be seen from Table IA that the prediction that short swims ( < 1 s) are significantly correlated with feeding rate (bites/min) is verified (P < 0.001). The correlation of long ( / > 1 s) swim frequency with feeding rate is, however, not significant (P ~ 0.05), also as predicted. In addition, the correlation between short swim frequency and the frequency of the element 'shift', which is also considered to be associated with feeding (see above), is also significant at P < 0.001. In Bay D the situation is somewhat different. Short swim frequency is significantly correlated with shift frequency (P < 0.001), but long swim frequency is not (P > 0.05), as in Bay C. Both short and long swim frequencies, however, are

tributions of bout lengths produced similar results in that all but one were not significantly different from geometric series (P > 0.3 in all but the one case and P > 0.95 in 20 cases). The same type of analysis was applied to the frequency distributions of swim durations in order to determine whether the probability of continuing a swim remained constant from one second to the next. If this were so then the frequency distributions of swim durations would also be similar to geometric series. In 21 of the 24 comparisons (2 bays x 12 11) the hourly frequency distributions were not significantly different (P > 0.05) from geometric series. These results indicate that swimming behaviour can adequately be described as a random process and that within each hour of the t i d a l cycle the probability of a swim occurring within a given interval, or of continuing for further increments of a second once started, remains relatively constant. The changing frequency and duration of swimming movements (see Figs 2 and 3) means, however, that these probabilities vary considerably from hour to hour. Although swimming has the obvious function of getting a fish from one place to another, it was suggested in an earlier paper (Gibson 1975) that swims of short duration ( < 1 s) may have a different function from those of longer ( ~> 1 s) duration. This distinction was an arbitrary one and based on subjective criteria, but further observation only served to strengthen this impression. The functions originally ascribed to the

Table I. Results of Correlations between the Mean Frequency of Swims of Different Types and Other Behavioural and Environmental Variables

A. Correlation of frequency of swims with:

Swim type Bay

Long

N

Frequency ofbites(No./min)

C D

0.592*** 0.522***

--0.065 0.286***

203 182

Frequency of shifts (No./min)

C D

0.562*** 0.825***

--0.106 0.055

203 182

Rate of change in tidal height (m/h)

C D

0.277*** 0.004

Position on beach (m relative to chart datum) C D B.

Short

Correlation of directionality of movement (Yomovements directed upshore) with rate of change of tidal height

*P < 0.05, **P < 0.01, ***P < 0.001.

--0.433*** 0.118

0.131 0.214"* --0.123 0.042

C

0.372***

0.426***

D

0.180"

0.230***

203 182 172 84 157 ~hor0 147 0ong) 164(shot0 160 0on~

1208

ANIMAL BEHAVIOUR,

correlated with bite frequency, but the correlation is not as good for the long swim frequencies, and if swims of only >~ 3 s are considered, the correlation is no longer significant (r = 0.135, P > 0.05). This difference between the two bays may be caused by the fact that there were relatively fewer short and relatively more long swims in Bay D than Bay C (%~ = 70.8, P < 0.001). A second prediction arising from the hypothesis that long and short swims have different functions is that if long swims serve to transport the fish up and down the beach in synchrony with the tide then their frequency should be correlated with the rate of change in the height of the tide. In other words, frequency of the longer swimming movements should be greatest when the tide is ebbing and flooding fastest and vice versa. To test this prediction the correlation coefficients for the relationship between the frequency of swims of the different durations and the rate of change in the tidal height (as m/h for each hour of the tidal cycle) were calculated. The rate of change in tidal height was estimated from the appropriate tide tables. The prediction was confirmed for Bay D because the frequency of long swims was correlated with the rate of change of tidal height (P < 0.01, Table I) and when the long swim category included only those >~ 3 s, the correlation was even more significant (r = 0.265, P < 0.001). The frequency of short swims was not significantly correlated with change in tidal height (P > 0.05). In Bay C, however, the prediction was not confirmed. Here it was the frequency of short swims that was significantly correlated with changes in tidal height. Although this finding conflicts with the original hypothesis, one explanation for the conflict is possible. It has already been mentioned that in Bay C long swims were significantly rarer and that the beach in this Bay is approximately twice as steep as in Bay D (see Fig. 1). Consequently, the distance a fish has to move to compensate for a given change in tidal height in Bay C is about half of that required in Bay D. The necessity of making longer duration migratory movements is thus not as great. Migration may be effected by short movements. Even so, the pattern of change in the frequency of movements >~ 1 s in the two bays is similar, with the higher frequency of long swims being generally associated with the greatest rates of change in tidal height (Fig. 6). The pattern of change of these longer swims over the tidal cycle is different from that of the shorter swims. The

28, 4

difference may be seen by comparing Fig. 6 with Fig. 2. Figure 2 may be taken as representative of the pattern of change in frequency of the shorter swims, because of the relative rarity of the longer swims. The position of a fish on the beach may also have a considerable effect upon the nature of its swimming behaviour. In general, organisms on sandy beaches are more abundant in numbers and biomass at lower levels (see for example, Eleftheriou & McIntyre 1976). The prey density available to a fish is thus, generally speaking, a function of its position on the beach. It seems reasonable to assume that feeding rate (bites/ min) will be dependent on prey density as it is in the closely related flounder, Platichthys flesus (Kiorboe 1978), and indirectly, therefore, on the position of the fish on the beach. Furthermore, because feeding rate and the frequency of short swims are correlated, it can be predicted that short (but not long) swim frequency will also be a function of a fish's position. This prediction is true for Bay C (Table IA) but not for Bay D although it is noticeable that in Bay D the correlation coefficient for short swim frequency versus beach height is much greater than that for long swim frequency and beach height. Again, the beach gradient in Bay D may affect this relationship because its shallower slope means that any differential distribution of prey organisms will be greatly reduced. Also, reference to Fig. 1 will show that the observations in Bay D were made over a more restricted area (LWMNT to LWMST) than in Bay C (HWMNT to LWMST), further reducing the possible differences in prey abundance to which the fish observed in Bay D were exposed. The relationships between short swim frequency and beach position in the two bays are illustrated in Fig. 7. 3~

(o)

3

(b)

' O. -6

-4

-2

O

0 +2 4-4 4-6 -6 -4 -2 Time relotive to high wafer (hours)

0.5

~o

0 0

4-2 4-4

+6

Fig. 6. Variation in the mean frequencyof long swims (~> 1 s in duration) (upper histogram) over the tidal cycle in (a) Bay C and (b) BayD. The lower histograms show the meanrate of changein tidalheight.

GIBSON: BEHAVIOUR OF WILD JUVENILE PLAICE There is thus some supporting evidence for the hypothesis that long and short swims have different functions and this evidence confirms the subjective impression that while feeding the fish make numerous short swimming movements over the bottom, occasionally interspersed with longer movements. Olla et al. (1969) describe similar long and short movements in the winter flounder. It should be emphasized that in this paper the terms 'short' and 'long' refer to duration and not to distance because distance could not be measured during the observations, although, in general, duration and distance are closely related. One further aspect of swimming behaviour has to be considered, and that is the direction of each movement that the fish make. An index of direction (I.D.) was devised on the basis of the percentage of movements directed upshore, left and right movements being excluded. This index could vary from 0, when all movements a fish made were directed downshore, to 100, when all movements were upshore. A mean value of this index was calculated for each hour of the tidal cycle and the results are given in Fig. 8 which shows that upshore movements predominated on the flood tide (I.D. > 50%), downshore movements on the ebb tide (I.D. < 50 %), and that directionality was greatest (maximum and minimum I.D. values) when the tide was ebbing and flooding fastest. It is also noticeable that there was a much more regular change in this index on the ebb than on the flood tide, indicating that downshore migration is more synchronized with the tidal cycle than upshore migration. In both bays directionality was correlated with the rate of change in the tidal height, decreases 14 .

.(Q)

410-12~L

1209

in height in this case being taken as negative (Table IB). The significant correlation between directionality and change in tidal height suggests that the direction of a fish's movement is controlled by the rate and sign (increase or decrease) of the change in tidal height and that this control is exerted on all movements whatever their duration. Shift. The behavioural element shift was the second most common element observed. Its variation in frequency over the tidal cycle closely paralleled that of swim in Bay C, but in Bay D the frequency remained more or less constant (see Fig. 2). The relationship between shift frequency and the frequency of swims of different durations has already been discussed. Shift frequency was also negatively correlated with position on the beach in Bay C (P < 0.01) but not in Bay D (P > 0.1). If shifts represent orientation movements totowards prey as suggested above (see p. 1204), then it would be expected that shift frequency would be dependent upon prey density. Now, because it is likely that prey density is dependent upon level on the beach and because the behaviour of the fish was recorded over a wider range of levels in Bay C, then the fish observed in Bay C would have experienced a greater range of prey densities than the fish in Bay D. If this suggestion is true, it would explain the difference in the pattern in the change of shift frequency over the tidal cycle in the two bays (see Fig. 2) and the fact that shift frequency was correlated with position on the beach in Bay C but not in Bay D. Bite. Feeding rate as measured by the mean number of bites/min varied widely from fish to fish but was similar in its pattern of variation over the tidal cycle to that of both the elements swim and shift (see Fig. 2). The actual act of biting was readily observed and easily distinguished from all other actions, but only rarely

(b)

1001(a)

(b)

m

~4 N

2 9

i

ol

-2 -05

0 0

+2 +4 +1

+6 +8 +~o +1 - 2 ~- 0 ' + 2 ' + 4 +2 +5 - 0 5 0 +1 Height above chart datum

' +6

+2 m,

Fig. 7. Variation in the mean frequency of short swims (< 1 s in duration) with height on the beach above chart datum in (a) Bay C and (b) Bay D.

-6 -4

-2

0 Time +2 +4 +6 -G -4 -2 0 relativeto high water(hours)

+2 +4, +6

Fig. 8. Variation in the mean index of direction over the tidal cycle in (a) Bay C and (b) Bay D.

1210

ANIMAL

BEHAVIOUR,

could the observer see what the fish had attacked. This was particularly true in Bay D. in Bay C, fish were seen to feed on small amphipods, the tentacles of the tubicolous polychaete Lanice conchilega and, higher on the beach, to be strongly attracted to emerging casts of the lugworm Arenicola marina. On many occasions the fish bit at these casts but it could not be ascertained whether they succeeded in capturing the worm. Analysis of stomach contents from the two bays showed that the fish fed mainly on small amphipods, copepods, and polychaete tentacles. It became clear over the observation period that the behaviour of fish before and after performing a bite was often different, fish usually making a longer swimming movement after a bite than before it. The difference in behaviour was analysed quantitatively by comparing the duration of swims preceding and succeeding each bite. The results of this comparison are given in Table II, and the frequency distribution of swim duration before and after bites is clearly different in both bays (P < 0.001). The reason for this difference in behaviour before and after a bite is not clear, because studies on other animals have shown that they tend to alter their behaviour after a successful capture in such a way as to remain in the vicinity of the last captured prey i t e m - - ' a r e a restricted search' (Curio 1976; Zach & Falls 1977). One possible explanation for the longer swim after a bite may be connected with the nature of the food. All prey items live in the sand or on its surface and their response to disturbance is to retract into tubes (polychaetes) or shells (molluscs) or to burrow into the sand. Having been stimulated to do so by the vigorous biting action of the fish, they will be no longer accessible. The biting action of the fish causes considerable localized disturbance and the longer swimming movement after a bite may

28,

4

serve to move the fish out of a disturbed area and into one where prey are undisturbed and more accessible. Alternatively, the longer swim after a bite may be a similar phenomenon to that observed in the stickleback, where rejection of a prey item results in an increased tendency to move away from the site of the rejected prey 'area avoided search' (Thomas 1974). In the present case, however, overt rejection after a bite was rarely seen. The possibility that unsuccessful captures have the same effect on subsequent swimming behaviour as rejection in the stickleback was also examined by comparing the durations of swims performed after those bites which were followed by chewing with the durations of swims after bites not followed by chewing. The hypothesis being tested here was that unsuccessful bites are followed by longer swims than successful ones, using chewing as an indication of success. The two swim duration frequency distributions were not significantly different, however, (%2, p > 0.10) and the hypothesis had to be rejected. Chew. Bites were frequently followed by 'chewing' movements. If chewing indicates a successful capture of a prey item, and observation of fish in aquaria suggests that it does, then the fish are successful in approximately one out of every two capture attempts (bites), because the mean value for the ratio chews/bites was 0.45 in Bay C and 0.42 in Bay D. These values must be regarded as minimum estimates, because it could not always be seen whether a bite was successful or not, or whether every successful bite was followed by overt chewing. The ratio of chews/bites was very variable from fish to fish and from hour to hour over the tidal cycle, but no obvious pattern in the variation could be discerned. Bury. Burying is a typical behaviour pattern of flatfish living on sand and was easily recog-

Table II. Comparison of Swim Durations Before and After a Bite

Frequency of Location swims Bay C Bay D

Swim duration (s)

0

1

2

3

Before bite

599

40

5

4

3

0.6

After bite

412

166

45

21

7

1.0

Before bite

217

23

4

0

1

0.6

After bite

111

61

42

15

16

1.6

>/4

2

x~

P

156.8

< 0.001

111.1

< 0.001

GIBSON: BEHAVIOUR OF WILD JUVENILE PLAICE

1211

tivity. Rasa (1971), who reviewed the occurrence of yawning in fish and studied the yawning behaviour of Microspathodon chrysurus in detail, states that in this species it can be initiated by high levels of excitement and low levels of activity. She suggests that 'its performance would result in an increase in muscle tonus and therefore aids in preparing the animal for action' (Rasa 1971, page 53). U - b e n d . A U-bend was also a rare event and was recorded only 16 times during the whole observation period. Its function is unknown, but it m a y be analogous to yawning (or stretching in other animals) in that it too increases muscle tonus and prepares the animal for action after a period of inactivity. Comparison of the interval durations before and after U-bending showed that there was no significant difference between them (P > 0.05, X 2 test), although one interesting point did emerge when the comparison was being made: it was that U-bending was frequently preceded by yawning (five out o f 16 times or 31 70, see Table V) and was always followed almost immediately by a swim or a shift. This figure of 31 70 is greater than would be expected on a random basis and suggests that the two elements of behaviour may be similar in their causation and function.

nized but only occurred rarely. It was most frequently seen when the fish were least active. Burying was often followed by a long period of inactivity and the time intervals between burying and the elements immediately preceding and following it were markedly different ( P < 0.001, X2 test, Table III). Yawn. Yawning was a relatively rare occurrence and did not change greatly in frequency over the tidal cycle. Yawns were usually preceded by periods of inactivity and succeeded by the almost immediate performance of another element of behaviour, usually swimming. This is in contrast to the act of burying, which was preceded by short periods of inactivity and succeeded by long ones. Table IV compares the frequency distribution of intervals before and after yawns and demonstrates the difference between them. They are highly significantly different (P < 0.001, Z 2 test). The difference in the pre- and post-yawn intervals suggests that yawning prepares the fish in some way for a bout of activity. It has been recorded in several other species o f flatfish (Holmes 1979), and Olla et al. (1972) found that in the summer flounder (Paralichthys dentatus) yawns were generally associated with changes in ac-

Table IlI. Comparison of Durations of Intervals Before and After Burying

Location Bay C

Bay D

Interval duration (s)

Interval frequency

~ 4

5-9

10-19

I> 20

Before bury

57

4

0

1

2.3

After bury

24

9

10

19

17.2

Before bury

81

5

3

0

1.9

After bury

33

15

13

28

21.1

~

X~

P

41.6

< 0.001

59.5

< 0.001

Table IV. Comparison of Duration of Intervals Before and After Yawning

Interval duration (s) Location Bay C

Bay D

Interval

frequency

~< 4

5-9

10-19

i> 20

.~

Before yawn

17

11

9

13

15.2

After yawn

40

7

3

0

2.1

Before yawn

17

7*

6*

11

19.3

After yawn

40

0

1

0

1.3

*These two categories combined in calculating X2.

X2

df

P

26.1

3

< 0.001

30.6

2

< 0.001

1212

ANIMAL BEHAVIOUR,

Roll. Rolling was the rarest behavioural element observed, (nine times) but when it did occur it was very conspicuous. The object of the action seemed to be to rub the upper pigmented surface of the body on the sand and it may therefore be regarded as a 'comfort movement'. Its function may be to reduce irritation caused by, or to dislodge, skin parasites. The action by which the fish scraped its lower unpigmented surface on the sea bed probably serves the same purpose. Interrdatiouships Between the Elements So far the description of the results has mainly been concerned with the variation in the overall frequency of performance of individual elements over the tidal cycle. This section describes the interrelationships between different elements. There are several methods available for examining the interrelationships between the elements constituting a behavioural sequence (for a review see Slater 1973). The method employed here is that of simple transition analysis in which a transition matrix is constructed to demonstrate the frequency with which each element is followed or preceded by another. The massing of data obtained from many animals observed at different times presents a problem, because construction of a valid transition matrix assumes that the probability of transitions between elements does not change greatly with time and that such transition probabilities do not vary markedly between individuals (Cane 1978). In the present case neither of these conditions is likely to be met, but as a general guide to the relative frequencies of, and transitions between, elements, such a matrix is a convenient method of presenting the data. Table V, which presents the data from Bays C and D, should thus only be regarded as a summary of element frequencies and transitions, bearing in mind that the transition probabilities are average values and vary from hour to hour over the tidal cycle. The variations in the transition probabilities between the most common elements (swim, S, shift, SH, and bite, B) over the tidal cycle are illustrated in Fig. 9. The points in this Figure are derived from transition matrices compiled for each hour of the tidal cycle. Figure 9 demonstrates that there is considerable variation in the transition probabilities over the tidal cycle, particularly in the SH-S, SH-SH, and SH-B transitions. Correlation analysis of the relationship between the transition probabilities of the two main elements S and SH and time of the tidal cycle showed that in both bays the probability

28, 4

of S being followed by another S (Ps.s) increased gradually over the tidal cycle (P < 0.02 for Bay C and P < 0.05 for Bay D). In Bay C, Pzmsa decreased from low tide to high tide (P < 0.05) and increased again on the ebb tide (P < 0.01). Conversely, Ps.sa decreased over the tidal cycle (P < 0.05) and Psa.s increased from low to high tide (P < 0.02) and then decreased to low tide (P < 0.05). There was no significant (P > 0.10) change in the SH-SH, SH-S, and S-SH transition probabilities in Bay D. Even though the hourly changes in transition probabilites are considerable, it is still possible to use Table V as a guide to the relative frequencies and interrelationships of all the elements. The elements S, SH and B are clearly the most common, accounting for about 95 ~ of the total and even if the elements S and SH are combined into bouts they still account for > 90 of the total. Combining elements into bouts, i.e. removing all homogeneous transitions from the matrix, will obviously increase the values of the probabilities for heterogeneous transitions. It does not, however, markedly affect the pattern of change of these heterogeneous transitions over the tidal cycle. It is not considered useful to take this analysis any further because of the obvious non-stationary nature of the data, but it is clear from Table V that the elements are not performed at random, several of the off-diagonal entries in the Table being much greater than would be expected on this basis, with the bite-chew transition being the most obvious, but not unexpected, example. Instead, an attempt will be made in the Discussion to explain the observed pattern of variation in some of the transition probabilities over the tidal cycle. Discussion The behaviour of the young plaice described in this paper is relatively simple and consists predominantly of swimming and feeding. Feeding involves searching for, orientating to, and capture of prey. These three phases of the feeding process are effected by the elements swim, shift, and bite respectively. The feeding behaviour has been analysed in greater detail in the laboratory by Holmes & Gibson (in preparation). Swimming behaviour, at least on a short term basis, can be described by a random model in which the probability of a swimming movement being performed remains relatively constant. The much lower probability of a swim continuing for further increments of a second, once started, also

1213

GIBSON: BEHAVIOUR OF WILD JUVENILE PLAICE Table V. Transition Frequencies and Probabilities (in Parentheses) for All Elements for Bay C and Bay D Following element Bay C

Swim

Shift

Bite

Preceding element Swim 6173 (0.74)

1819 (0.22)

315 (0.04)

Chew

Bury

Yawn

U-bend

--

55 (0.01)

24 (0.004)

4 (0.0005)

Roll 3 (0.0004)

Row totals 8393

Shift

1616 (0.45)

1514 (0.42)

414 (0.12)

3 (0.001)

17 (0.005)

22 (0.006)

2 (0.001)

--

3588

Bite

294 (0.39)

106 (0.14)

8 (0.01)

336 (0.45)

--

--

1 (0.001)

--

745

Chew

249 (0.73)

88 (0.26)

3 (0.01)

.

Bury

44 (0.63)

19 (0.27)

3 (0.04)

1 (0.01)

1 (0.01)

2 (0.03)

--

--

70

Yawn

42 (0.76)

10 (0.18)

--

--

--

2 (0.04)

1 (0.02)

--

55

U-bend

5 (0.63)

2 (0.25)

1 (0.13)

.

.

.

.

.

8

Roll

2 (0.67)

--

1 (0.33)

.

.

.

.

.

3

745

340

Column totals

8425

3558

.

.

.

73

.

340

50

8

3

13 202

Following element Bay D

Swim

Shift

Bite

Chew

Bury

Yawn

U-bend

Roll

R o w totals

Preceding element Swim 4901 (0.76)

1151 (0.18)

283 (0.04)

1 (0.0001)

83 (0.01)

19 (0.002)

--

2 (0.0003)

6440

1 (0.0005)

1094

Shift

1078 (0.51)

762 (0.36)

210 (0.10)

--

19 (0.009)

22 (0.01)

2 (0.001)

Bite

224 (0.44)

63 (0.12)

3 (0.006)

213 (0.42)

3 (0.006)

--

--

1 0.002)

507

Chew

144 (0.65)

66 (0.31)

--

--

2 (0.009)

--

1 (0.005)

--

213

Bury

61 (0.58)

25 (0.24)

I (0.01)

--

11 (0.10)

5 (0.05)

1 (0.01)

1 (0.01)

105

Yawn

30 (0.56)

19 (0.35)

--

--

--

1 (0.02)

4 (0.07)

--

54

U-bend

7 (0.88)

1 (0.12)

.

Roll

4 (0.67)

--

Column totals

6449

--

.

. ~

. 1

.

. --

8 --

1

(0.17) 2087

497

214

119

6

(0.17) 47

8

6

9427

1214

ANIMAL

BEHAVIOUR,

remains constant over short periods. These probabilities can be affected in two ways. First, by the performance of other elements: yawning, for example, increases the probability of a swim being performed within a given time, whereas burying has the reverse effect, and attempts at prey capture tend to increase the probability of a subsequent swim continuing. Secondly, and more importantly, these probabilities are affected by environmental factors and the changes in probability are manifested in the variation of the frequency and duration of the swimming movements. This random swimming behaviour may reflect small-scale random distribution of prey, because most swimming movements probably represent searching for food. Unfortunately, as far as could be ascertained, there have been no studies of the microdistribution of the numerous organisms that the fish use as food. The data used in constructing the random model consisted of a combination of results from several individuals observed in any one hour of

28,

4

the tidal cycle with the assumption that the probabilities were equal and constant over that limited time period. Such an assumption may not be strictly valid for animals living in a rhythmically fluctuating environment, but the fact that each hourly set of results does conform to the expectations of a random process suggests that the assumption is not too inaccurate. Some mention of the possible environmental factors which affect the frequency of swimming and other common behavioural elements has already been made, and it was suggested that the pattern of changes in the frequency of the elements swim, shift and bite is a result of the changing physical and biological conditions that the fish experience during their migration up and down the beach. In Bay C the observations that the feeding rate declined as the fish moved up the beach and vice versa were interpreted as resulting from a possible decrease in prey density at higher levels. In addition, there seemed to be a change in feeding tactics as the fish moved up-

(a)

0.8,

\/_.,--'-",/V

e - ~ ~' S-S

0.8-

zx

0.6

0'6

J \ "1

V\I

i

/

~,0.4 -E o,

~'

'\

V\./-

t / A ''-'~'f

SH-SH

s /s :sH

.

0.4

o

o/\

~

0.2

o~o~.

/\ o k 0 o ',/" \..os f~o

--~

0'2

--~SH-B ....

II

im- - m

...... o\=

/

/

\,,--=./~

--,-_.: ":;__: ><

0 -6

-4

-2

-'-,,

0

+2

"r176 O-~D

0 -4 -6 +4 -t6 Time relative to high water (hours)

-2

0

"'--.sHB o

4-P.

Fig. 9. Variation in the transition probabilities between the elements swim (S), shift (SH) and bite (B) over the tidal cycle in (a) Bay C and (b) Bay D.

+4

+6

GIBSON: BEHAVIOUR OF WILD JUVENILE PLAICE shore. At lower shore levels the fish were very active, apparently feeding on small crustaceans and polychaete tentacles, and they made numerous short swimming movements, shifts, and bites. At the higher levels the fish were less active in terms of their swimming frequency. They seemed to be employing a 'sit and wait' tactic whereby they remained stationary until a food organism, often an emerging lugworm cast, appeared and then orientated and swam towards it. The pattern of change in the transition probabilities of S, SH, and B illustrated in Fig. 9a can be explained in the light of this gradual change in feeding tactics. Low down on the beach, where prey density is assumed to be highest, the fish encounter prey frequently and therefore make many orientation (shift) movements and capture attempts (bite) resulting in high values for the S H - S H and SH-B transitions (Fig. 9a). Towards high tide, as the fish move up the beach, prey density decreases and shifts are more frequently followed by swims than by shifts or bites (Fig. 9a), even though the frequency of all three elements has greatly decreased (Fig. 2a). The absence of any significant changes in these transition probabilities in Bay D may again be related to the more restricted area in which the fish were observed in this bay. The gradual increase in Ps.s over the tidal cycle in both bays perhaps represents an increase in food selectivity with decreasing hunger (Ivlev 1961; Chiszar & Windell 1973). Superimposed on their feeding activity is the need for the fish to synchronize their movements with the tide. Such synchronization is particularly important on the ebb so that the fish may avoid being stranded by the receding tide. Synchronization can be effected by varying the frequency, duration, speed, and direction of swimming movements in response to changing tidal conditions. Alteration of the first three of these variables will not be sufficient, however, unless the direction of each movement is appropriate. The results indicate that the fish synchronize their activity with the tide mainly by altering the frequency and direction, but not the duration, of their swimming movements, because both frequency and direction are correlated with change in tidal height (P < 0.01) but duration is not (P > 0.20 for Bay C and P > 0.05 for Bay D). The speed of each movement could not be determined. Figure 8 suggests that direction is particularly well synchronized on the ebb tide. This suggestion is strengthened by the results of an analysis of the relationship between the rate of tidal change and directionality in which the data

1215

for the flood and ebb tides were treated separately, In both bays the positive correlation between these two variables was significant on the ebb tide (P < 0.01), but not on the flood

(P > 0.05). The factors governing the behaviour described here are thus complex and vary in their importance from place to place. It is likely, however, that migration is controlled mainly by physical factors such as currents or changes in hydrostatic pressure, particularly as it has been shown experimentally that young plaice respond to pressure changes by altering their level of activity (Gibson et al. 1978). Feeding behaviour, on the other hand, seems to be dependent to a greater extent on biological factors, particularly the nature of available prey and its density. Acknowledgments

The author gratefully acknowledges the indispensable help of Mr I. Ezzi in the collection and analysis of the data presented in this paper. Dr R. Holmes kindly made several helpful comments on an early draft of the manuscript. REFERENCES

Bregneballe, F. 1961. Plaice and flounder as consumers of the microscopic bottom fauna. Meddr. Danm. Fisk.-og Havanders., N.S. 3, 133-182. Cane, V. R. 1978. On fitting low-order Markov chains to behaviour sequences.Anita. Behav., 26, 332-338. Chiszar, D. & Windell, J. T. 1973. Predation by bluegill sunfish (Lepomis macrochirus Rafinesque) upon mealworm larvae (Tenebrio molitor). Anim. Behav., 21, 536-543. Curio, E. 1976. The Ethology of Predation. New York: Springer-Verlag. Edwards, R. & Steele, J. H. 1968. The ecology of O-group plaice and common dabs at Lochewe. I. Population and food. J. exp. mar. Biol. Ecol., 2, 215-238. Eleftheriou, A. & McIntyre, A. D. 1976. The intertidal fauna of sandy beaches--a survey of the Scottish coast. Scott. Fish. Res. Rep., No. 6~ 61 pp. Gibson, R. N. 1973a. The intertidal movements and distribution of young fish on a sandy beach with special reference to the plaice (Pleuronectes platessa L.). or. exp. mar. Biol. Ecol., 12, 79-102. Gibson, R. N. 1973b. Tidal and circadian activityrhythms in juvenile plaice, Pleuronectes platessa. Mar. Biol., 22, 379-386. Gibson, R. N. 1975. A comparison of the field and laboratory activity patterns of juvenile plaice. In: Proceedings of the 9th European Marine Biology Symposium (Ed. by H. Barnes), pp. 13-28. Aberdeen University Press. Gibson, R. N., Blaxter, J. H. S. & de Groot, S. J. 1978. Developmental changes in the activity rhythms of the plaice (Pleuronectes platessa). In: Rhythmic Activity of Fishes (Ed. by J. Thorpe), pp. 169-186. London: Academic Press.

1216

ANIMAL

BEHAVIOUR,

Holmes, R. A. 1979. Studies on the feeding behaviour of flatfish. Ph.D. thesis, University of Stifling, Scotland. Ivlev, V. S. 1961. Experimental Ecology of the Feeding of Fishes. New Haven: Yale University Press. Kiorboe, T. 1978. Feeding rate in juvenile flounder in relation to prey density. Kieler Meeresforsch., Sonderheft No. 4, 275-281. Kuipers, B. R. 1973. On the tidal migration of young plaice (Pleuronectes platessa L.) in the Wadden Sea. Neth. J. Sea Res., 6, 376-388. Kuipers, B. R. 1977. On the ecology of juvenile plaice on a tidal flat in the Wadden Sea. Neth. J. Sea Res., 11, 56-91. Lemon, R. E. & Chatfield, C. 1971. Organisation of song in cardinals. Anim. Behav., 19, 1-17. Lockwood, S. J. 1974. The settlement, distribution and movements of O-group plaice Pleuronectesplatessa (L.) in Filey Bay, Yorkshire. J. Fish Biol., 6, 465-471. Macer, C. T. 1967. The food web in Red Wharf Bay (North Wales) with particular reference to young plaice (Pteuronectes platessa). Helgotdnder wiss. Meeresunters., 15, 560-573. Olla, B. L., Wicklund, R. & Wilk, S. 1969. Behaviour of winter flounder in a natural habitat. Trans. Am. Fish. Soc., 98, 717-720. Olla, B. L., Samet, C. E. & Studholme, A. L. 1972. Activity and feeding behaviour of the summer flounder (Paralichthys dentatus) under controlled laboratory conditions. Fishery Bull. NOAA., 70, 1127-1136. Rasa, O. A. E. 1971. The causal factors and function of 'yawning' in Microspathodon chrysurus (Pisces: Pomacentridae). Behaviour, 39, 39-57.

28,

4

Riley, J. D. 1973. Movements of O-group plaice Pleuronectes platessa L. as shown by latex tagging. J. Fish BioL, $, 323-343. Scheuring, L. 1921. Beobachtungen und Betrachtungen tiber die Beziehungen der Augen zum Nahrungserwerb bei Fischen. Zool. Jb. Allgem. ZooL, 38, 113-136. Slater, P. J. B. 1973. Describing sequences of behaviour. In: Perspectives in Ethology (Ed. by P. P. G. Bateson & P. H. Klopfer), pp. 131-153. London: Plenum Press. Slater, P. J. B. 1974. Bouts and gaps in the behaviour of zebra finches, with special reference to preening. Rev. comp. Anita., 8, 47-61. Steven, G. A. 1930. Bottom fauna and the food of fishes. J. mar. Biol. Ass. U.K., 16, 677-705. Stickney, R. R., White, D. B. & Miller, D. 1973. Observations on fin use in relation to feeding and resting behaviour in flatfishes (Pleuronectiformes). Copeia, 1973, 154-156. Thijssen, R., Lever A. J. & Lever, J. 1974. Food composition and feeding periodicity of O group plaice (Pleuronectes platessa) in the tidal area of a sandy beach. Neth. J. Sea Res., 8, 369-377. Thomas, G. 1974. The influences of encountering a food object on subsequent searching behaviour in Gasterosteus aculeatus L. Anim. Behav., 22, 941-952. Verheijen, F. J. & de Groot, S. J. 1967, Diurnal activity of plaice and flounder in aquaria. Neth. J. Sea. Res., 3, 383-390. Zach, R. & Falls, J. B. 1977. Influence of capturing a prey on subsequent search in the ovenbird (Ayes: Parulidae). Can. J. ZooL, 55, 1958-1969.

(Received 22 October 1979; revised 22 November 1979; MS. number: 1954)