- Email: [email protected]
Effects of increasing temperature on social behaviour in territorial groups of pumpkinseed sunfish, Lepomis gibbosus
EFFECTS OF INCREASING TEMPERATURE ON SOCIAL BEHAVIOUR IN TERRITORIAL GROUPS OF PUMPKINSEED SUNFISH, LEPOMIS GIBBOSUS MAaY E. POWER Boston University Marine Program, Marine Biological Laboratory, Woods Hole, Mass. 02543, USA
& JOHN H. TODD New Alchemy Institute, PO Box 432, Woods Hole, Mass. 02543, USA ABSTRACT
To study the effect of thermal stress on their social behaviour, ten territorial groups of pumpkinseed sunfish, Lepomis gibbosus, were subjected to a 1 °C temperature increase every other day until they succumbed. Social behaviour remained remarkably unchanged by thermal stress until nearly lethal levels. As temperature rose, ritualised behaviours increased infrequency, then fell off, probably reflecting changes in general activity. Behavioural and physiological signs of stress appeared from 31 to 38 ° C. Events during these social breakdowns are described and compared with the response of two other freshwater fishes with different social organisations subjected to the same thermal regime.
INTRODUCTION
Todd et al. (1972) have postulated that behaviourally complex fish may be less resistant to stress than fishes with simpler social behaviours. Based on the number of behaviours human observers could distinguish (similar, cross-class comparisons of the number of displays shown by vertebrates have been made in a discussion of the evolution of displays by Moynihan (1970)), Todd et al. designated the following hierarchy of behavioural complexity for three fishes which live in temperate freshwater ponds. (1) Theyellowbullhead, Ictalurus natalis, was the most complex. Todd (1968) has shown this species to exhibit many complex behaviours, non-parental co-operation and individual recognition. His group has described 64 units of bullhead social behaviour. 217 Environ. Pollut. (10) (1976)--© Applied Science Publishers Ltd, England, 1976 Printed in Great Britain
218
MARY E. POWER, JOHN H. TODD
(2) The pumpkinseed sunfish, Lepomis gibbosus, was intermediate in complexity. Miller (1964) first described this species' behaviour, which seems more stereotyped than the bullhead's. Using methods and criteria similar to those employed in bullhead observations, we distinguished 30 units of pumpkinseed social behaviour. (3) The golden shiner, Notemigonus crysoleucas,was designated the simplest fish. Interactions between individuals were uncommon in this schooling minnow and, when they did occur, took eleven forms. Units which describe group activity are necessary in order to record shiner social behaviour, and eleven such units were described (Power, 1974). In the first of a series of comparative studies of these fishes, the social behaviour of groups of yellow bullheads was seriously disrupted by sublethal thermal stress (McLarney et al., 1974). To test the predicted correlation between stressvulnerability and social behaviour, groups of pumpkinseed sunfish and golden shiners were studied under the same schedule of increasing temperature as was used in the bullhead study. This paper reports behavioural changes observed in the pumpkinseed sunfish.
METHODS AND MATERIALS Thirteen groups of pumpkinseed sunfish (Lepomis gibbosus), six with three individuals and seven with two, were studied iduring the.summer and,autumn~ of 1972 and 1973. Members of each group were size-matched and interchanged until each resident could defend a territory. Individuals were distinguished by small, naturally-occurring imperfections like fin notches. Each group was housed in a 190litre aquarium. All aquaria were held in rooms where ambient disturbances were minimal. In 1972 a 10-on/14-off light cycle Was imposed to inhibit reproductive behaviour. This proved unnecessary, and in 1973 all groups were held under natural lighting. A 3-holed concrete block was placed off-centre in each tank. Ammonia levels were kept below 0.1 ppm by subsand filtration and water replacement. Only materials not expected to give off harmful by-products within the temperature range of the study (20-40 °C) were used in aquaria: oyster shell, well-leached concrete, silicone rubber cement, glass, fibreglass, and polyethylene tubing for air delivery. Supplementary air piped into the tanks kept oxygen levels near saturation. Fish were fed daily, to satiation, on freshwater mussels, earthworms and trout chow. Three groups--two with three fish and one with two--were kept as controls at 22-24°C. After several weeks of observation at this temperature, the remaining groups were subjected to a temperature increase of 1 °C every other day until the fish succumbed. (Adjusting the heaters upwards usually effeeted this temperature increase within 5 h). Immediately before temperatures were raised in a tank, the social behaviour of its residents was recorded in coded units for 15 rain (see Miller, 1964 and Power, 1974 for complete descriptions of the behavioural units).
TEMPERATURE EFFECTS ON SOCIAL BEHAVIOUR OF SUNFISH
219
RESULTS
Pumpkinseed social behaviour before thermal stress--22-24 °C Once all residents could defend a territory, each of the thirteen sunfish groups remained relatively stable over time with respect to social behaviour and territory patterns. After the behaviour in each social group was stabilised, the residents' social behaviour was classified as: (i) ritualised; (ii) intense aggressive and (iii) infractive. Ritualised interactions were most common and occurred between fish of nearly equal status, each within its own territory. 'Thrusts' occurred near territorial borders, as fish advanced a short distance directly at a tankmate, then quickly retreated. Residents often oriented towards each other at territorial boundaries in slightly tilted postures called face-offs. If they thrust while in such a posture, the compound unit was recorded as a tilt-thrust. Intense aggressive behaviour broke out on occasions when Such ritual interactions accelerated until one or both of the participants charged. Charges (called 'rushes' by Miller, 1964) were short, rapid bursts of swimming directly at a target fish. If charges culminated in mouth contact, a nip was recorded. During these intensified aggressive encounters, sunfish briefly violated territorial borders, expended more energy and may have increased the risk of inflicting damage (although physically damaged living fish were never seen in, territorial groups before they were thermally stressed). The least frequent category was infractive behavfour: Chases and flees occurred only on the rare occasions when one fish intruded-deeply into the territory of another. The resident would chase the intruder, swimming rapidly after it for as long as was necessary in order to expel it. The intruder would flee, swimming and dodging rapidly until it evaded its pursuer. This fast prolonged swimming cost much energy, and often culminated in potentially damaging nips.
Pumpkinseed social behaviour during increasing temperature 25-39 °C No dramatic changes in pumpkinseed groups occurred--until tanks were above 31 °C. Ritualised behaviour increased after 27 °C, and fell off when tanks were within a few degrees of lethal temperatures, around 34 °C (Fig. 1). Comparison of averaged frequencies of ritualised behaviours in the low, middle and high temperature ranges by the sign test showed this trend to be significant at the 0-05 level. Neither intense aggressive behaviour nor infractive behaviour showed significant trends over all groups with temperature (Fig. 1). However, striking social changes did occur in certain groups. Table 1 summarises events which began in certain experimental tanks one or two centigrade degrees below the temperatures at which the first resident died. In five out of the eight tanks in which status differences could be detected, fish judged to be subordinate because of their smaller territories were the first to show stress. Physiological signs of stress included 'stress pumping' (increased frequency and amplitude of respiratory gill cover movements); loss of pitch control so that
MARY E. POWER, JOHN H. TODD
220
heads dipped down as much as 90 °; and loss of opercle spot control so that spots blanched and darkened erratically with no apparent social significance. (Opercle blanching is normally a submissive signal in pumpkinseeds.) In four of the ten experimental tanks, stressed fish were unusually inactive and
30 ¸
20
6.
10
I
...
N" I0
I0
IO
IO
!
( 2 3 TO 2 4 ) 2 4
!
_~ lo r
'J o
9
7
9
8
I0
"1" ++ t t8 t t6
I0
9
I
I
I
I
1
26
2B
30
32
34
1NTENSE AGGRESSIVE BEHAVIORS
'
I
(z3 To 2 , ) 24
"
~
.
26
28
30
32
34
I
I
I
26
28
30
32
34
. . . . . . . . .
1
( 2 3 TO 2 4 )
24
TEMPERATURE (0 C) Fig. 1. Behaviouraltrends in pumpkinseed sunfish from 23 to 34~'C.
TEMPERATURE EFFECTS ON SOCIAL BEHAVIOUR OF SUNFISH
221
rested o n the b o t t o m of c o m p a r t m e n t s of the concrete block, or o n the substrate. (Normally, sunfish hovered above the substrate except when sleeping.) A n o t h e r behavioural change was'stress swimming'. Fish would swim tremulously in rapid spurts, then stop abruptly, sometimes within the territories of their tankmates. There (if the resident still behaved normally) they suffered nips a n d h a r a s s m e n t for several seconds before leaving. Such obliviousness to previously respected territorial borders was in m a r k e d contrast to the immediate flight of detected intruders at lower temperatures. N e a r lethal temperatures, t a n k m a t e s sometimes harassed stressed fish even when the latter were n o t in their territories. U n u s u a l h a r a s s m e n t was observed in two tanks, a n d was inferred from newly frayed fins on a fish f o u n d dead in a third ( T a n k 1). TABLE 1 BEHAVIOURAL AND PHYSIOLOGICAL EVENTS OBSERVED IN FISH DURING SOCIAL BREAKDOWNS, ONE OR TWO DEGREES BELOW LETHAL TEMPERATURES (d)
Event
2S 4S
1
4
5
6
7
8
9
10
Subordinate stressed first Stress pumping Loss of pitch control Loss of opercle spot control Inactivity Stress swimming Social oblivion Unusual harassment d(lethal temperatures for first resident(s))
-
+ +
+ +
+ +
+ + +
+ -
+ +
-
+
-
+ + + + 36
+
0 -
+ + + 39
+ + + + 33
0 + + + +
32
+
+
+ +
-
+
-
36
35
35
34
35
34
+ = event occurred. - = event not observed. 0 = event irrelevant (no dominance in these tanks). W i t h i n a given t a n k the period between the onset of obvious social changes a n d the first mortality was very short, being often only a m a t t e r of hours. Breakdowns were n o t observed in three of the ten experimental groups (Tanks 2S, 8 a n d 10) b u t m a y have occurred undetected. While sunfish behaviour during social b r e a k d o w n s seemed very different from behaviour in groups at lower temperatures, the frequencies of events recorded d u r i n g these periods were too low to reveal statistically significant trends. Nevertheless, these low frequency behavioural changes were critical in terms o f the fate o f the groups as they a p p r o a c h e d their lethal temperatures.
DISCUSSION T h e r m a l stress had little obvious effect o n p u m p k i n s e e d sunfish social behaviour until lethal levels were approached. The trend in ritualised behaviour closely
222
MARY E. POWER,JOHN H. TODD
resembles the curve drawn by Sylvester (1972) for the effect of temperature on the general activity offish. Movement brought fish to each other's attention, stimulating thrusting. Thus, the increase and decline of ritualised behaviour probably reflects only the activity-temperature relationship to be expected in poikilotherms. More significant biologically (but not statistically) were the events observed over a total range of 31-38 °C, in some social groups one or two degrees below their lethal temperatures. Some of the behavioural and physiological signs of stress appearing at these temperatures resembled events described by other workers studying fish under sublethal stress. 'Stress pumping' in heated pumpkinseeds may be similar to the rapi6 mouth movements which Sparks et ad. (1972a) have observed in bluegills (Lepomis macrochirus) exposed to sublethal zinc poisoning. These workers have also noted social factors in zinc-stresse6 bluegill groups causing subordinate individuals to succumb first (Sparks etal., 1972b). Suchf~ctors were indicated in five out of eight pumpkinseed groups with individuals o f different-status, and might have been more obvious if we had not size-matched the fiskat the outset of the study. The harassment of physiologically stressed individuals by t ~ ' r unaffected tankmates illustrates the interaction of social and-physiologicalfactors contributing to the breakdown of heat stressed pumpkinseed groups. In this respect, tlt¢ pumpkinseed response to thermal stress is intermediate between that of the yellow butllaeadLandthg golderfshitler (Power, 1974). In the latter stu6y, shiner groups showed no changes in social behaviour attributable to thermal stress; but only physiological symptoms (sphaatdeformations, oedema) at 34-35 °C, one or two degrees below lethal, temperatures. In yellow bullhead groups, aggressive behaviours and the ratio of damaging to non-damaging aggressive acts rose markedly at 30 °C, nine degrees below lethal temperatures and four to five degrees below the onset of any signs of physiological stress (Todd et aL, 1972; McLarney et aL, 1974). While shiners succumbed-to individual physiological failures, and deaths in the bullhead groups resulted primarily from social factors, pumpkinseed deaths resulted from an interaction of soefal~and'physiol0gical factors in at least seven out of ten groups. The responses o f these three species, of which the pumpkinseed is intermediate in social complexity, suggest that social factors may become more important in responses to stress as social complexity increases.
ACKNOWLEDGEMENTS
The authors are indebted to Stewart Jacobson, who provided advice and criticism throughout the study. Ivan Valiela and Woollcott Smith made helpful suggestions regarding data analysis, and Robert Jeanne criticised the manuscript. This work was carried out while the authors were at the Woods Hole Oceanographic Institution, under support by Atomic Energy Commission Grant 11-1/3567 to J.H.T.
TEMPERATURE EFFECTS ON SOCIAL BEHAVIOUR OF SUNFISH
223
REFERENCES MCLARNEY, W. O., ENGSTROM, D. & TODD, J. H. (1974). Effects of increasing temperature on social behaviour in groups of yellow bullheads (Ictalurus natalis). Environ. Pollut., 7, 111-19. MILLER, H. C. (1964). The behavior of the pumpkinseed sunfish, Lepomis gibbosus (Linneaus) with notes on the behavior of other species of Lepomis and the pigmy sunfish, Elassoma evergladei. Behaviour, 22, 88-151. MOYNIHAN, M. (1970). Control, suppression, decay, disappearance and replacement of displays. J. theor. Biol., 29, 85-112. POWER, M. E. (1974). Social behavior in pumpkinseed sunfish, Lepomis gibbosus, and golden shiners, Notemigonus crysoleucas, subjected to increasing temperature. M.A. Thesis, Boston University. SPARKS, R. E., CAIRNE J. JR. ~ HEATH, A. G. (1972a). The use of bluegill breathing rates to detect zinc. War. Res., 6, 895-911. SPARKS,R. E., WALLER,W. T. & CAIRNS,J. JR. (1972b). Effects of shelters on the resistance of dominant and submissive bluegills (Lepomis macrochirus) to a lethal concentration of zinc. J. Fish. Res. Bd Can., 29, 1356-8. SYLVESTER,J. R. (1972). Possible effects of thermal effluents on fish: A review. Environ. Pollut., 3, 205-15. TODD, J. H., ENGSTROM,D., JACOaSON, S. & MCLARNEY,W. O. (1972). An introduction to environmental ethology." A preliminary comparison of sublethal thermal and oil stresses on the social behavior of lobsters, and fishes from a freshwater and a marine ecosystem. Progress Report to the United States Atomic Energy Commission. AT (11-1)-3567 (unpublished manuscript). TODD, J. H. (1968). The social behavior of the yellow bullhead(Ictalurus natalis). Ph.D. Thesis, University of Michigan, Ann Arbor, Michigan.
& JOHN H. TODD New Alchemy Institute, PO Box 432, Woods Hole, Mass. 02543, USA ABSTRACT
To study the effect of thermal stress on their social behaviour, ten territorial groups of pumpkinseed sunfish, Lepomis gibbosus, were subjected to a 1 °C temperature increase every other day until they succumbed. Social behaviour remained remarkably unchanged by thermal stress until nearly lethal levels. As temperature rose, ritualised behaviours increased infrequency, then fell off, probably reflecting changes in general activity. Behavioural and physiological signs of stress appeared from 31 to 38 ° C. Events during these social breakdowns are described and compared with the response of two other freshwater fishes with different social organisations subjected to the same thermal regime.
INTRODUCTION
Todd et al. (1972) have postulated that behaviourally complex fish may be less resistant to stress than fishes with simpler social behaviours. Based on the number of behaviours human observers could distinguish (similar, cross-class comparisons of the number of displays shown by vertebrates have been made in a discussion of the evolution of displays by Moynihan (1970)), Todd et al. designated the following hierarchy of behavioural complexity for three fishes which live in temperate freshwater ponds. (1) Theyellowbullhead, Ictalurus natalis, was the most complex. Todd (1968) has shown this species to exhibit many complex behaviours, non-parental co-operation and individual recognition. His group has described 64 units of bullhead social behaviour. 217 Environ. Pollut. (10) (1976)--© Applied Science Publishers Ltd, England, 1976 Printed in Great Britain
218
MARY E. POWER, JOHN H. TODD
(2) The pumpkinseed sunfish, Lepomis gibbosus, was intermediate in complexity. Miller (1964) first described this species' behaviour, which seems more stereotyped than the bullhead's. Using methods and criteria similar to those employed in bullhead observations, we distinguished 30 units of pumpkinseed social behaviour. (3) The golden shiner, Notemigonus crysoleucas,was designated the simplest fish. Interactions between individuals were uncommon in this schooling minnow and, when they did occur, took eleven forms. Units which describe group activity are necessary in order to record shiner social behaviour, and eleven such units were described (Power, 1974). In the first of a series of comparative studies of these fishes, the social behaviour of groups of yellow bullheads was seriously disrupted by sublethal thermal stress (McLarney et al., 1974). To test the predicted correlation between stressvulnerability and social behaviour, groups of pumpkinseed sunfish and golden shiners were studied under the same schedule of increasing temperature as was used in the bullhead study. This paper reports behavioural changes observed in the pumpkinseed sunfish.
METHODS AND MATERIALS Thirteen groups of pumpkinseed sunfish (Lepomis gibbosus), six with three individuals and seven with two, were studied iduring the.summer and,autumn~ of 1972 and 1973. Members of each group were size-matched and interchanged until each resident could defend a territory. Individuals were distinguished by small, naturally-occurring imperfections like fin notches. Each group was housed in a 190litre aquarium. All aquaria were held in rooms where ambient disturbances were minimal. In 1972 a 10-on/14-off light cycle Was imposed to inhibit reproductive behaviour. This proved unnecessary, and in 1973 all groups were held under natural lighting. A 3-holed concrete block was placed off-centre in each tank. Ammonia levels were kept below 0.1 ppm by subsand filtration and water replacement. Only materials not expected to give off harmful by-products within the temperature range of the study (20-40 °C) were used in aquaria: oyster shell, well-leached concrete, silicone rubber cement, glass, fibreglass, and polyethylene tubing for air delivery. Supplementary air piped into the tanks kept oxygen levels near saturation. Fish were fed daily, to satiation, on freshwater mussels, earthworms and trout chow. Three groups--two with three fish and one with two--were kept as controls at 22-24°C. After several weeks of observation at this temperature, the remaining groups were subjected to a temperature increase of 1 °C every other day until the fish succumbed. (Adjusting the heaters upwards usually effeeted this temperature increase within 5 h). Immediately before temperatures were raised in a tank, the social behaviour of its residents was recorded in coded units for 15 rain (see Miller, 1964 and Power, 1974 for complete descriptions of the behavioural units).
TEMPERATURE EFFECTS ON SOCIAL BEHAVIOUR OF SUNFISH
219
RESULTS
Pumpkinseed social behaviour before thermal stress--22-24 °C Once all residents could defend a territory, each of the thirteen sunfish groups remained relatively stable over time with respect to social behaviour and territory patterns. After the behaviour in each social group was stabilised, the residents' social behaviour was classified as: (i) ritualised; (ii) intense aggressive and (iii) infractive. Ritualised interactions were most common and occurred between fish of nearly equal status, each within its own territory. 'Thrusts' occurred near territorial borders, as fish advanced a short distance directly at a tankmate, then quickly retreated. Residents often oriented towards each other at territorial boundaries in slightly tilted postures called face-offs. If they thrust while in such a posture, the compound unit was recorded as a tilt-thrust. Intense aggressive behaviour broke out on occasions when Such ritual interactions accelerated until one or both of the participants charged. Charges (called 'rushes' by Miller, 1964) were short, rapid bursts of swimming directly at a target fish. If charges culminated in mouth contact, a nip was recorded. During these intensified aggressive encounters, sunfish briefly violated territorial borders, expended more energy and may have increased the risk of inflicting damage (although physically damaged living fish were never seen in, territorial groups before they were thermally stressed). The least frequent category was infractive behavfour: Chases and flees occurred only on the rare occasions when one fish intruded-deeply into the territory of another. The resident would chase the intruder, swimming rapidly after it for as long as was necessary in order to expel it. The intruder would flee, swimming and dodging rapidly until it evaded its pursuer. This fast prolonged swimming cost much energy, and often culminated in potentially damaging nips.
Pumpkinseed social behaviour during increasing temperature 25-39 °C No dramatic changes in pumpkinseed groups occurred--until tanks were above 31 °C. Ritualised behaviour increased after 27 °C, and fell off when tanks were within a few degrees of lethal temperatures, around 34 °C (Fig. 1). Comparison of averaged frequencies of ritualised behaviours in the low, middle and high temperature ranges by the sign test showed this trend to be significant at the 0-05 level. Neither intense aggressive behaviour nor infractive behaviour showed significant trends over all groups with temperature (Fig. 1). However, striking social changes did occur in certain groups. Table 1 summarises events which began in certain experimental tanks one or two centigrade degrees below the temperatures at which the first resident died. In five out of the eight tanks in which status differences could be detected, fish judged to be subordinate because of their smaller territories were the first to show stress. Physiological signs of stress included 'stress pumping' (increased frequency and amplitude of respiratory gill cover movements); loss of pitch control so that
MARY E. POWER, JOHN H. TODD
220
heads dipped down as much as 90 °; and loss of opercle spot control so that spots blanched and darkened erratically with no apparent social significance. (Opercle blanching is normally a submissive signal in pumpkinseeds.) In four of the ten experimental tanks, stressed fish were unusually inactive and
30 ¸
20
6.
10
I
...
N" I0
I0
IO
IO
!
( 2 3 TO 2 4 ) 2 4
!
_~ lo r
'J o
9
7
9
8
I0
"1" ++ t t8 t t6
I0
9
I
I
I
I
1
26
2B
30
32
34
1NTENSE AGGRESSIVE BEHAVIORS
'
I
(z3 To 2 , ) 24
"
~
.
26
28
30
32
34
I
I
I
26
28
30
32
34
. . . . . . . . .
1
( 2 3 TO 2 4 )
24
TEMPERATURE (0 C) Fig. 1. Behaviouraltrends in pumpkinseed sunfish from 23 to 34~'C.
TEMPERATURE EFFECTS ON SOCIAL BEHAVIOUR OF SUNFISH
221
rested o n the b o t t o m of c o m p a r t m e n t s of the concrete block, or o n the substrate. (Normally, sunfish hovered above the substrate except when sleeping.) A n o t h e r behavioural change was'stress swimming'. Fish would swim tremulously in rapid spurts, then stop abruptly, sometimes within the territories of their tankmates. There (if the resident still behaved normally) they suffered nips a n d h a r a s s m e n t for several seconds before leaving. Such obliviousness to previously respected territorial borders was in m a r k e d contrast to the immediate flight of detected intruders at lower temperatures. N e a r lethal temperatures, t a n k m a t e s sometimes harassed stressed fish even when the latter were n o t in their territories. U n u s u a l h a r a s s m e n t was observed in two tanks, a n d was inferred from newly frayed fins on a fish f o u n d dead in a third ( T a n k 1). TABLE 1 BEHAVIOURAL AND PHYSIOLOGICAL EVENTS OBSERVED IN FISH DURING SOCIAL BREAKDOWNS, ONE OR TWO DEGREES BELOW LETHAL TEMPERATURES (d)
Event
2S 4S
1
4
5
6
7
8
9
10
Subordinate stressed first Stress pumping Loss of pitch control Loss of opercle spot control Inactivity Stress swimming Social oblivion Unusual harassment d(lethal temperatures for first resident(s))
-
+ +
+ +
+ +
+ + +
+ -
+ +
-
+
-
+ + + + 36
+
0 -
+ + + 39
+ + + + 33
0 + + + +
32
+
+
+ +
-
+
-
36
35
35
34
35
34
+ = event occurred. - = event not observed. 0 = event irrelevant (no dominance in these tanks). W i t h i n a given t a n k the period between the onset of obvious social changes a n d the first mortality was very short, being often only a m a t t e r of hours. Breakdowns were n o t observed in three of the ten experimental groups (Tanks 2S, 8 a n d 10) b u t m a y have occurred undetected. While sunfish behaviour during social b r e a k d o w n s seemed very different from behaviour in groups at lower temperatures, the frequencies of events recorded d u r i n g these periods were too low to reveal statistically significant trends. Nevertheless, these low frequency behavioural changes were critical in terms o f the fate o f the groups as they a p p r o a c h e d their lethal temperatures.
DISCUSSION T h e r m a l stress had little obvious effect o n p u m p k i n s e e d sunfish social behaviour until lethal levels were approached. The trend in ritualised behaviour closely
222
MARY E. POWER,JOHN H. TODD
resembles the curve drawn by Sylvester (1972) for the effect of temperature on the general activity offish. Movement brought fish to each other's attention, stimulating thrusting. Thus, the increase and decline of ritualised behaviour probably reflects only the activity-temperature relationship to be expected in poikilotherms. More significant biologically (but not statistically) were the events observed over a total range of 31-38 °C, in some social groups one or two degrees below their lethal temperatures. Some of the behavioural and physiological signs of stress appearing at these temperatures resembled events described by other workers studying fish under sublethal stress. 'Stress pumping' in heated pumpkinseeds may be similar to the rapi6 mouth movements which Sparks et ad. (1972a) have observed in bluegills (Lepomis macrochirus) exposed to sublethal zinc poisoning. These workers have also noted social factors in zinc-stresse6 bluegill groups causing subordinate individuals to succumb first (Sparks etal., 1972b). Suchf~ctors were indicated in five out of eight pumpkinseed groups with individuals o f different-status, and might have been more obvious if we had not size-matched the fiskat the outset of the study. The harassment of physiologically stressed individuals by t ~ ' r unaffected tankmates illustrates the interaction of social and-physiologicalfactors contributing to the breakdown of heat stressed pumpkinseed groups. In this respect, tlt¢ pumpkinseed response to thermal stress is intermediate between that of the yellow butllaeadLandthg golderfshitler (Power, 1974). In the latter stu6y, shiner groups showed no changes in social behaviour attributable to thermal stress; but only physiological symptoms (sphaatdeformations, oedema) at 34-35 °C, one or two degrees below lethal, temperatures. In yellow bullhead groups, aggressive behaviours and the ratio of damaging to non-damaging aggressive acts rose markedly at 30 °C, nine degrees below lethal temperatures and four to five degrees below the onset of any signs of physiological stress (Todd et aL, 1972; McLarney et aL, 1974). While shiners succumbed-to individual physiological failures, and deaths in the bullhead groups resulted primarily from social factors, pumpkinseed deaths resulted from an interaction of soefal~and'physiol0gical factors in at least seven out of ten groups. The responses o f these three species, of which the pumpkinseed is intermediate in social complexity, suggest that social factors may become more important in responses to stress as social complexity increases.
ACKNOWLEDGEMENTS
The authors are indebted to Stewart Jacobson, who provided advice and criticism throughout the study. Ivan Valiela and Woollcott Smith made helpful suggestions regarding data analysis, and Robert Jeanne criticised the manuscript. This work was carried out while the authors were at the Woods Hole Oceanographic Institution, under support by Atomic Energy Commission Grant 11-1/3567 to J.H.T.
TEMPERATURE EFFECTS ON SOCIAL BEHAVIOUR OF SUNFISH
223
REFERENCES MCLARNEY, W. O., ENGSTROM, D. & TODD, J. H. (1974). Effects of increasing temperature on social behaviour in groups of yellow bullheads (Ictalurus natalis). Environ. Pollut., 7, 111-19. MILLER, H. C. (1964). The behavior of the pumpkinseed sunfish, Lepomis gibbosus (Linneaus) with notes on the behavior of other species of Lepomis and the pigmy sunfish, Elassoma evergladei. Behaviour, 22, 88-151. MOYNIHAN, M. (1970). Control, suppression, decay, disappearance and replacement of displays. J. theor. Biol., 29, 85-112. POWER, M. E. (1974). Social behavior in pumpkinseed sunfish, Lepomis gibbosus, and golden shiners, Notemigonus crysoleucas, subjected to increasing temperature. M.A. Thesis, Boston University. SPARKS, R. E., CAIRNE J. JR. ~ HEATH, A. G. (1972a). The use of bluegill breathing rates to detect zinc. War. Res., 6, 895-911. SPARKS,R. E., WALLER,W. T. & CAIRNS,J. JR. (1972b). Effects of shelters on the resistance of dominant and submissive bluegills (Lepomis macrochirus) to a lethal concentration of zinc. J. Fish. Res. Bd Can., 29, 1356-8. SYLVESTER,J. R. (1972). Possible effects of thermal effluents on fish: A review. Environ. Pollut., 3, 205-15. TODD, J. H., ENGSTROM,D., JACOaSON, S. & MCLARNEY,W. O. (1972). An introduction to environmental ethology." A preliminary comparison of sublethal thermal and oil stresses on the social behavior of lobsters, and fishes from a freshwater and a marine ecosystem. Progress Report to the United States Atomic Energy Commission. AT (11-1)-3567 (unpublished manuscript). TODD, J. H. (1968). The social behavior of the yellow bullhead(Ictalurus natalis). Ph.D. Thesis, University of Michigan, Ann Arbor, Michigan.