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Acclimation to temperature in Actinia equina L.: Effects of season and shore level on aquatic oxygen consumption
J. Exp. Mar. Biol. Ecol., 1984, Vol. 16,
pp. 19-81
19
Elsevier
JEM 232
ACCLIMATION
TO TEMPERATURE
IN ACTZNZA EQUZNA L.: EFFECTS
OF SEASON AND SHORE LEVEL ON AQUATIC OXYGEN CONSUMPTION
M. MERTXE ORTEGA, J. I. P. IGLESIAS and E. NAVARRO Departamento de Biologia, Fact&ad de Ciencias, Universidad de1 Pais Vasco/Eusknl Herr&o Unibertsitatea. Apdo. 644. Bilbao, Spain
Abstract: Effect ofseasonal and experimental acclimation to temperature upon aquatic oxygen consumption of the sea anemone Acrinia equina L. has been studied in animals from two shore levels during the summer of 1981 and the winter of 1982. A clear influence of both season and shore level on the weight exponent is registered, higher values occurring during the summer. Seasonally acclimated animals from the upper shore showed perfect winter-summer compensation with lateral translation to the right of the R-T curve in response to warm acclimation while this pattern was coupled with clockwise rotation and partial compensation in specimens collected from the low shore. Experimental acclimation during the summer resulted in partial compensation at T, 15 “C and no acclimation was found at T, 25 “C; during the winter, only high shore specimens exhibited compensatory responses. A significant increase in oxygen consumption, regardless of shore level, occurs in winter in both seasonally and experimentally acclimated animals.
In the littoral area, latitude, season, and tidal rhythm are main sources of regular cyclical temperature fluctuations. Effects of temperature on the metabolism of intertidal invertebrates have been extensively reviewed (Newell, 1969; Newell & Bayne, 1973) and general features of temperature compensation in poikilothermic organisms are detailed in Bullock (1955). The studies concerning acclimation to long-term temperature variations of an environmental or experimental nature, show considerable differences among data which are commonly referred to the classifying models developed by Precht (1958) and Prosser (1958). The number of works dealing with thermal acclimation of respiratory metabolism in anthozoans is small: the species Metridium senile exhibits different responses according to latitude and geographical origin (Sassaman & Mangum, 1970; Walsh & Somero, 1981), while no acclimation was found in Haliplanella luciae and Diadumene leucolena (Sassaman & Mangum, 1970). In the species Actinia equina, a pattern of perfect compensation is obtained in subtropical specimens experimentally acclimated to temperatures within their thermal regime (Grifliths, 1977). Previous work in A. equina (Navarro et al., 198 1) showed a differential effect of shore level when considering aerial and aquatic oxygen consumption. Although influence of vertical distribution upon respiratory metabolism is well established (Newell, 1973), available information on the combined effects of experimental acclimation and zonation 0022-0981/84/%03.00 0 1984 Elsevier Science Publishers B.V.
X0
M.MERTXEORTEGA
ETAL.
is scarce (Anderson, 1978). In the present work, acclimation patterns of the respiratory metabolism in A. equina L. are discussed in relation to season, shore level, and body size. MATERIAL
AND METHODS
Animals were collected at low tide from Sopelana Beach, Biscay, at two different shore levels characterized by an annual mean exposure of about 12 to 16 h/day and 4 to 8 h/day, respectively. Immediately after being carried to the laboratory, the animals were rinsed with sea water, any attached particles carefully removed. and placed into aquaria held at the different acclimation temperatures and containing aerated sea water which was changed daily. Minced, fresh mussel (Mytilus edulis L.) was administered twice a week, feeding being discontinued 4 days prior to respirometric measurements. Animals fed well and remained healthy throughout the experiment. Twelve acclimation experiments, each lasting 4 wk, were set up as follows: (a) summer season: acclimation temperatures (7’,) 15, 20, 25 “C; (b) winter season: T, 10, 15, 20 “C. Both shore levels were considered in each season and z 25 animals from each level were used at each temperature. Environmental temperatures at time of collection were chosen to delimit thermal range in superficial coastal waters in this area: August-September, 1981 (20 “C) and January-February, 1982 (12 ‘C). The acclimation period concluded, anemones were transferred to the respirometers and maintained for 12 to 16 h in the same aquaria. Respiration was measured at live exposure temperatures (T, : 10, 15, 20, 25, 30 “C). From 4 to 12 h before taking measurements the water in the aquaria was brought to the experimental temperature to minimize the effects of thermal shock. In addition to the acclimation experiments, acute measurements of oxygen consumption at the same temperatures used for acclimation (T,) were performed in separate groups of animals at the beginning of each acclimation period, in order to provide seasonal data. These animals were maintained in an aquarium with re-circulating sea water at field temperature and then handled in the same way as the other animals. Aquatic oxygen consumption was determined in a closed system using a microWinkler method (Hoar & Hickman, 1975). Dry weight was obtained after 48 h in an oven at 110 “C. RESULTS
Weight regression analyses of oxygen consumption for the different experimental conditions resulted in 72 equations log. tic,* vs. log. w ( to2 = ~1 OZ. h ’ . animal ’ ; w = mg dry wt). Correlation coefficients lay inside the confidence interval for P < 0.00 1. Covariance analyses of the acclimated series showed differences to be significant at P < 0.001 when applied to the entire group of slopes. Differences remained significant when the test was applied to each season separately. We proceeded until groups could
ACCLIMATION
TO TEMPERATUREIN
ACTINIA
81
be established within which differences were non-significant (P > 0.05). In these cases, a common regression coefficient was calculated for each group: Suer, high shore: b = 0.4455 Summer, low shore: b = 0.3016 Winter, high shore: b = 0.2675 Winter, low shore: T, 10 “C b = 0.2966 T, 15 “C b = 0.2383 T, 20 “C b = 0.1973 In winter, acclimated animals experience a reduction in the b values. Differential effect of T, upon weight exponent occurs only in winter-low shore specimens. Metabolic rate (ml 0, *g- l. h- ‘) for an animal of 100 mg dry wt (mean dry wt of the animals used in the experiment) was calculated from the given common slopes and plotted against exposure temperature to give rate-temperature (R-T) curves (Fig. 1).
A
0
Fig. 1. Oxygen consumption (ml 0, ‘g- ’ . h- ‘) of an animal of 100 mg dry wt at five exposure temperatures (T,): 0, T, 15 “C; 0, T, 20 “C; A, T, 25 “C; A, T, 10 “C; A, summer, high shore; B, summer, low shore; C, winter, high shore; D, winter, low shore; vertical lines represent SD for each point.
M. MERTXE ORTEGA ET AL.
x2
During the summer, m~mum rates of oxygen uptake are recorded for both shore Ievels at T, 25 “C and no acclimation is achieved at this temperature. Referred to T, 20 *C (environmental temperature) R-T curves for T, 15 “C present clockwise rotation - Prosser’s type III - (Fig. 1A and B) resulting in partial compensation - Precht’s type III - of acclimated rates (T, = T,) between 15 to 20 “C. Effect of acclimation temperature during the winter season is less homogeneous, the highest rates appearing for Ta 15 oC in the high shore and T, 20 ‘C in the low shore. No compensation occurs in the low shore population (Fig. 1D) while different degrees of compensation are attained in the high shore based on rotation of the curves (Fig. 1C). A comparison between seasons for the two common acclimation t~~rat~es (T, 1.5, 20 ‘C) shows that R-T curves for T, 20 “C are less steep {Fig. 2), jibing a greater
A
TA
TA
B
15°C
20°C
5.0 -
2.0 -
1.0
-
0.5
-
L
1 10
I ,5
I 20
I
I
I
I
I
I
I
25
30
10
15
20
25
30
TEI”C
I
Fig. 2. Oxygen consumption (ml 0,. g- ’ h I) of an animal of 100 mg dry wt at five exposure temperatures (T,): 0, summer, high shore; 0, summer, low shore; A, winter, high shore; A, winter, low shore: A, T, 15°C; B, T, 20°C.
degree of metabolic Theo-~dependence over the entire range of T, . ~~irnurn thermal dependence appears in the summer, high shore within T, 10 to 20 “C (T, 15 ‘C, Q,<)= 1.47; T., 20°C Qlo = 1.62; T., 25 “C, Qlo = 1.25). Oxygen consumption in the winter increases considerably in relation to summer, irrespective of acclimation temperature. Acute measurements of the metabolic rate in the seasonally acclimated group display the same seasonal trend (Fig. 3) with a translation to the right of the R-T curve from winter to summer at both shore levels, coupled with a slight clockwise rotation in the low shore. The Q,, of the seasonal response to acute temperature change illustrates the effects of both season and shore level (Table I). The region of thermal independence displaces from 10 to 15 “C in the winter to 20 to 25 “C in the summer in the high shore, while it appears restricted to summer (20 to
ACCLIMATION TO TEMPERATURE
83
IN ACTINIA
25 “C, Q,,, = 1.58) in the low shore specimens. Q,, values associated with long-term (winter-summer) temperature changes are close to 1 in both shore levels; seasonal compensation is perfect (slight over-compensation) in the high shore and partial in the low shore (Fig. 3). Acclimated metabolic rates (7’, = 7’,) are shown in Fig. 4. Low-shore animals show a translation to the right of the R-T curve from winter to summer which results in a constancy of metabolic rates over the range 12 to 20 “C which covers the interval of environmental temperatures in this area. Clear over-compensation appears in the highshore population.
A 5.0
B
_
-7 I
‘;* a iu 0
2.0_
1.0 _
i 0.5 _ 1
I
I
I
I
I
I
I
10
1s
20
25
10
15
20
25 TE (‘C
I
Fig. 3. Seasonal against acclimated oxygen consumption (ml 0,. g - ’ h - ‘) for an animal of 100 mg dry wt: 0, summer, seasonal; 0, summer, acclimated; A, winter, seasonal; A, winter, acclimated; A, high shore; B, low shore. TABLE I Q,, values calculated
for 5 “C intervals
of seasonal
acute metabolic
rates (ml 0,.
g- i . h- ‘).
Season
Shore level
Interval (“C)
Summer (20 “C)
High
15-20 20-25
4.57 0.95
LOW
15-20 20-25
2.29 1.58
High
IO-15 15-20
0.91 3.02
Low
10-15 15-20
2.75 2.63
High Low
10-20 10-20
0.85 1.38
Winter (12 “C)
Winter-summer
Q10
M. MERTXE ORTEGA E7’,-1L.
84
I
5.0 t
I
i
I
10
15
1
1
20
26 T&z
1 TA (“C 1
Fig. 4. .Acclimated metaboiic rates (ml 0,. g ^ ’ ‘h _ ‘) - T, = 7, - of an animal of 100 mg dry wt: 0, summer, high shore; A, summer. low shore: 0, winter. high shore; A. winter. low shore.
DISCUSSION
The weight exponent in Actinia equina falls between 0.1973 and 044.55; usual values for intertidal anthozoans include: 0.54 in A~thop~eura elegantissirna (Fitt et al., 19821, a common 0.65 for DiaQumene leucolena, ~al~plane~~aluciae, and ~et~~d~u~ senile (Sassaman & ~~gurn, 1970), and 0.36 in Act&k equine (Navarro et al., 1981). The weight exponent seems to depend on the expe~ment~ situation, as taken from our own data on Actiniu and reported values for Metridium senile which range between 0.41 and 0.89 (Shumway, 1978; Shick et al., 1979; Robbins & Shick, 1980; Walsh & Somero, 1981). In this work a seasonal change in the slope b appears, with higher values in the summer. This fact, along with the remarkable increase of metabolie rate during the winter, suggests different levels of metabolism, probably related to the reproductive cycle. Changes in the weight exponent in ~climation exper~ents have been found in Orconectes nais (Armitage & Wall, 1982), ~etrid~u~ senile (Walsh & Somero, 1981), Ligia mea&z (Newell et al., 1976), and Mytilw edulis (Bayne, 1973) this last following the same seasonal pattern. Seasonally acclimated animals exhibit different types of compensation according to shore level. Upper-shore animals show perfect compensation with lateral translation to the right of the R-T curve in response to temperature increase, whereas partial compensation with translation plus clockwise rotation is found in the low shore. Subtropical Actinia equina show a similar lateral translation (Grifftths, 1977). The winter-summer transition results in a clear shift in the range of thermal insensitivity in the direction of rising temperatures for the high-shore anemones; in the tow shore adaptation to summer tempera~es involves a general decrease in the slope of the R-T curve. increasing temperature independence in this season.
ACCLIMATION
TO TEMPERATURE
IN ACTINIA
85
Experimental acclimation appears influenced by both season and zonation. The summer group shows a compensatory response at T, 15 oC (“cold acclimated”) which results in partial compensation between 15 and 20 “C. Metabolic adjustment occurs at different rates of oxygen consumption for each shore level: 0.96 ml 0, *g- ’ *h- * for the high shore and 1.22 ml O2 - g- ’ *h-‘ 1 for the low shore (animal of 100 mg dry wt). This dilTerence between shore levels is consistent with the seasonal data and agrees with the results of Shick (198 1) for A. equina, who finds a lower i/,, in intertidally accl~atized animals collected from a mid-shore location in September. An expansion of the area of thermal independence appears associated with increasing T, in the low shore (Fig. 1B). Reduction in temperature-dependence towards the higher levels of the shore results in upper-shore animals showing the lowest Q,, for the entire range of T, at any of the acclimation temperatures (mean Q,, at 10 to 30 “C on the high shore = 1.61; and on the low shore = 1.80). There seemed to be no acclimation at T, 25 “C in any of the shore levels and metabolism increased over the period of maintenance at this T, (unpubl. data). In A. equina the ability to acclimate thus appears restricted to temperatures within the annual range, as has also been reported by Grilliths (1977) who found no compensation at temperatures outside the environmental range in South African subtropical and Cal-temperate anemones. Winter high-shore animals exhibit a compensatory pattern between 10 and 20 “C, although no compensation was found in the low shore which shows maintenance of the seasonal response. A significant increase in oxygen consumption, regardless of shore level, occurs in winter in both seasonally and experimentally acclimated animals (Fig. 3). As a result of this, compensator adjus~ents are set at a different point each season, being higher during the winter. This phenomenon could be attributed to changes in metabolic requirements throughout the year, as has been suggested for Myt&.r edulis (Widdows & Bayne, 1971; Bayne, 1973) where perfect acclimation superimpased on a similar seasonal trend of metabolism is also found. Ability to restrict the effects of thermal impact upon metabolic expenditure seems to vary with the degree of temperature fluctuation of a given habitat (Newell, 1973, 1979), upper-shore populations being characterized by more effective homeostatic mechanisms (Barnes & Barnes 1969; McMahon & Russell-Hunter, 1977; Branch & Newell, 1978). Consequently, Actinia equina from the high shore would be expected to show maximum thermal independence and this, more so during the summer, is the case. Influence of zonation can be further demonstrated by ex~ing acclimated metabolic rates in relation to seasonal acute measurements (Fig. 3). In the low shore, failure to produce acclimation to experimental temperatures during the winter, coupled with acclimation during the summer, results in perfect compensation from 12 to 20 ’ C (annual range) for the laboratory acclimated group (Fig. 4) which was not evident from the seasonal results. In upper-shore anemones, however, achieving of experimental acclimation in both seasons superimposed on seasonal compensation (perfect between 12 and 20 “C) contributes to experimental over-compensation, intensifying the seasonal response.
M. MERTX~ORTEGA~~~~
Xh
ACKNOWLEDGEMENT
The authors are indebted to Professor R. C. Newell for help with the revision of the manuscript. REFERENCES ANDERSON,G., 1978. Metabolic rate, temperature acclimation and resistance to high temperature of soft-shell clams,Mya arenariu, as affected by shore level. Camp. Biochem. Physiol., Vol. 6lA, pp. 433-438. ARMITAGE,K. B. & T. J. WALL, 1982. The effects of body size, starvation and temperature acclimation on oxygen consumption of the crayfish Orconecaes nais. Camp. Blochem. Physiol., Vol. 73A, pp. 63-68. BARNES,H. & M. BARNES, 1969. Seasonal changes in the acutely determined oxygen consumption and effect of temperature for three common cirripedes, Bulunus ~lanoides (L.), 8. bakmus (L.) and Chtham~~us steffatus (Poli). J. Exp. Mar. Biol. Ecol., Vol. 4, pp. 36-50. BAYNE,B. L., 1973. Physiologica changes in My&s edr&s (L.) induced by temperature and nutritive stress. J. Mar. Biol. Assoc. U.K., Vol. 53, pp. 39-58. BRANCH,G. M. & R. C. NEWELL,1978. A comparative study of metabolic energy expenditure in the limpets Pateila cochlean, P. oculus and P. granular-k Mar. Biol., Vol. 49, pp. 351-361. BUI,I_OCK, T. H., 1955. Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev., Vol. 30, pp. 3 1l-342. Frrr, W.K., R.L. PARDY & M. M. LITTLER, 1982. Photosynthesis, respiration, and contribution to community productivity of the symbiotic sea anemone Anthopleuru eleguntissima (Brandt, 1835). f. Exp. Mar. Biol. Ecol., Vol. 61, pp. 213-232. GRIIFFITHS,R. J., 1977. Temperature acclimation in Acti& equina L. (Anthozoa). J. Exp. Mar. &al. Ecof.. Voi. 28, pp. 285-292. HOAR, W. S. & C.P. HICKMAN, 1975. A luborurory companjon Jar general and comparative physiolo~. Prentice-Hall, N. J., 283 pp. M&%AHON,R. F. & W. D. RUSSELL-HUNTER,1977.Temperature relations of aerial and aquatic respiration in six littoral snails in relation to their vertical distribution. Biol. Buli. (Woods Ii&, Muss.), Vol. 152. pp. 182-198. NAVARRO,E., M. M. ORTEGA& J.M. MADARIAGA,1981. Effect of body size, temperature and shore level on aquatic and aerial respiration of Actiniu equina (L.) (Anthozoa). J. Exp. Mar. Biol. Ecol., Vol. 53, pp. 153-162. NEW~U., R.C., 1969. Effect of fluctuations in temperature in the metabolism of intertidal invertebrates. Am. Zool., Vol. 9, pp. 293-307. NEWELL, R.C., 1973. Factors affecting the respiration of intertidal invertebrates. Am. Zool., Vol. 13, pp. 513-528. NEWELL, R.C., 1979. Biology of intertidal animals. Marine Ecological Surveys, Faversham, Kent, 781 pp. NEWELL,R.C. & B.L. BAYNE, 1973. A review on temperature and metabolic acclimation in intertidal marine invertebrates. Neth. J. Sea Res., Vol.7,pp. 421-433. NEWELL, R.C., A. ROY 6t K.B. ARMITAGE,1976. An analysis of factors affecting the oxygen consumption of the isopod Ligia oceanica. Physiof. ZooI., Vof. 49, pp. 109-$37. PRECHT,H., 1958. Concepts of temperature adaptation of unchanging reactions systems of cold-blooded animals. In, Physiorogicaf adapt&ion, edited by C. L. Prosser, Am. Physiol. Sot., Washington D.C., pp. 50-77. PROSSER,C. L., 1958. The nature of physiological adaptation. In, Physiological adapt&on, edited by C. L. Prosser, Am. Physiol. Sot., Washington DC., pp. 167-180. ROBBINS,R.E. & J.M. SHICK, 1980. Expansion-contraction behaviour in the sea anemone Metridium senile: environmental cues and energetic consequences. In, Nutrition in the lower Metazoa, edited by D. C. Smith & Y. Tiffon, Pergamon Press, Oxford, pp 101-I 16. SASSAMAN,C. & C.P. MANGUM, 1970. Patterns of temperature adaptation in North Amertcan Atlantic coastal actinians. Mar. Biol., Vol. 7, pp. 123-130. SHICK,J. M., 1981.Heat production and oxygen uptake in intertidal anemones from dif%rent shore heights during exposure to air. &fur. &of. Letters, Vol. 2. pp. 225-236.
ACCLIMATION
TO TEMPERATURE
IN ACTINIA
87
SHICK, J. M., W. I. BROWN,E. G. DOLLIVER& S. R. KAYAR,1979. Oxygen uptake in sea anemones: effects of expansion, contraction and exposure to air, and the limitations of diffusion. Physiol. Zool., Vol. 52,
pp. 50-62. SHUMWAY,S. E., 1978. Activity and respiration in the anemone Metridium senile (L.) exposed to salinity fluctuations. J. Eq. Mar. Biol. Ecol., Vol. 33, pp. 85-92. WALSH,P. J. & G. N. SOMERO,1981.Temperature adaptation in sea anemones: physiological and biochemical variability in geographically separated populations of Menidium senile. Mar. Biol., Vol. 62, pp. 25-34. WIDDOWS,J. dc B. L. BAYNE,1971. Temperature acclimation of Myrirus edulis with reference to its energy budget. J. Mar. Biol. Assoc. U.K., Vol. 5 1, pp. 827-843.
pp. 19-81
19
Elsevier
JEM 232
ACCLIMATION
TO TEMPERATURE
IN ACTZNZA EQUZNA L.: EFFECTS
OF SEASON AND SHORE LEVEL ON AQUATIC OXYGEN CONSUMPTION
M. MERTXE ORTEGA, J. I. P. IGLESIAS and E. NAVARRO Departamento de Biologia, Fact&ad de Ciencias, Universidad de1 Pais Vasco/Eusknl Herr&o Unibertsitatea. Apdo. 644. Bilbao, Spain
Abstract: Effect ofseasonal and experimental acclimation to temperature upon aquatic oxygen consumption of the sea anemone Acrinia equina L. has been studied in animals from two shore levels during the summer of 1981 and the winter of 1982. A clear influence of both season and shore level on the weight exponent is registered, higher values occurring during the summer. Seasonally acclimated animals from the upper shore showed perfect winter-summer compensation with lateral translation to the right of the R-T curve in response to warm acclimation while this pattern was coupled with clockwise rotation and partial compensation in specimens collected from the low shore. Experimental acclimation during the summer resulted in partial compensation at T, 15 “C and no acclimation was found at T, 25 “C; during the winter, only high shore specimens exhibited compensatory responses. A significant increase in oxygen consumption, regardless of shore level, occurs in winter in both seasonally and experimentally acclimated animals.
In the littoral area, latitude, season, and tidal rhythm are main sources of regular cyclical temperature fluctuations. Effects of temperature on the metabolism of intertidal invertebrates have been extensively reviewed (Newell, 1969; Newell & Bayne, 1973) and general features of temperature compensation in poikilothermic organisms are detailed in Bullock (1955). The studies concerning acclimation to long-term temperature variations of an environmental or experimental nature, show considerable differences among data which are commonly referred to the classifying models developed by Precht (1958) and Prosser (1958). The number of works dealing with thermal acclimation of respiratory metabolism in anthozoans is small: the species Metridium senile exhibits different responses according to latitude and geographical origin (Sassaman & Mangum, 1970; Walsh & Somero, 1981), while no acclimation was found in Haliplanella luciae and Diadumene leucolena (Sassaman & Mangum, 1970). In the species Actinia equina, a pattern of perfect compensation is obtained in subtropical specimens experimentally acclimated to temperatures within their thermal regime (Grifliths, 1977). Previous work in A. equina (Navarro et al., 198 1) showed a differential effect of shore level when considering aerial and aquatic oxygen consumption. Although influence of vertical distribution upon respiratory metabolism is well established (Newell, 1973), available information on the combined effects of experimental acclimation and zonation 0022-0981/84/%03.00 0 1984 Elsevier Science Publishers B.V.
X0
M.MERTXEORTEGA
ETAL.
is scarce (Anderson, 1978). In the present work, acclimation patterns of the respiratory metabolism in A. equina L. are discussed in relation to season, shore level, and body size. MATERIAL
AND METHODS
Animals were collected at low tide from Sopelana Beach, Biscay, at two different shore levels characterized by an annual mean exposure of about 12 to 16 h/day and 4 to 8 h/day, respectively. Immediately after being carried to the laboratory, the animals were rinsed with sea water, any attached particles carefully removed. and placed into aquaria held at the different acclimation temperatures and containing aerated sea water which was changed daily. Minced, fresh mussel (Mytilus edulis L.) was administered twice a week, feeding being discontinued 4 days prior to respirometric measurements. Animals fed well and remained healthy throughout the experiment. Twelve acclimation experiments, each lasting 4 wk, were set up as follows: (a) summer season: acclimation temperatures (7’,) 15, 20, 25 “C; (b) winter season: T, 10, 15, 20 “C. Both shore levels were considered in each season and z 25 animals from each level were used at each temperature. Environmental temperatures at time of collection were chosen to delimit thermal range in superficial coastal waters in this area: August-September, 1981 (20 “C) and January-February, 1982 (12 ‘C). The acclimation period concluded, anemones were transferred to the respirometers and maintained for 12 to 16 h in the same aquaria. Respiration was measured at live exposure temperatures (T, : 10, 15, 20, 25, 30 “C). From 4 to 12 h before taking measurements the water in the aquaria was brought to the experimental temperature to minimize the effects of thermal shock. In addition to the acclimation experiments, acute measurements of oxygen consumption at the same temperatures used for acclimation (T,) were performed in separate groups of animals at the beginning of each acclimation period, in order to provide seasonal data. These animals were maintained in an aquarium with re-circulating sea water at field temperature and then handled in the same way as the other animals. Aquatic oxygen consumption was determined in a closed system using a microWinkler method (Hoar & Hickman, 1975). Dry weight was obtained after 48 h in an oven at 110 “C. RESULTS
Weight regression analyses of oxygen consumption for the different experimental conditions resulted in 72 equations log. tic,* vs. log. w ( to2 = ~1 OZ. h ’ . animal ’ ; w = mg dry wt). Correlation coefficients lay inside the confidence interval for P < 0.00 1. Covariance analyses of the acclimated series showed differences to be significant at P < 0.001 when applied to the entire group of slopes. Differences remained significant when the test was applied to each season separately. We proceeded until groups could
ACCLIMATION
TO TEMPERATUREIN
ACTINIA
81
be established within which differences were non-significant (P > 0.05). In these cases, a common regression coefficient was calculated for each group: Suer, high shore: b = 0.4455 Summer, low shore: b = 0.3016 Winter, high shore: b = 0.2675 Winter, low shore: T, 10 “C b = 0.2966 T, 15 “C b = 0.2383 T, 20 “C b = 0.1973 In winter, acclimated animals experience a reduction in the b values. Differential effect of T, upon weight exponent occurs only in winter-low shore specimens. Metabolic rate (ml 0, *g- l. h- ‘) for an animal of 100 mg dry wt (mean dry wt of the animals used in the experiment) was calculated from the given common slopes and plotted against exposure temperature to give rate-temperature (R-T) curves (Fig. 1).
A
0
Fig. 1. Oxygen consumption (ml 0, ‘g- ’ . h- ‘) of an animal of 100 mg dry wt at five exposure temperatures (T,): 0, T, 15 “C; 0, T, 20 “C; A, T, 25 “C; A, T, 10 “C; A, summer, high shore; B, summer, low shore; C, winter, high shore; D, winter, low shore; vertical lines represent SD for each point.
M. MERTXE ORTEGA ET AL.
x2
During the summer, m~mum rates of oxygen uptake are recorded for both shore Ievels at T, 25 “C and no acclimation is achieved at this temperature. Referred to T, 20 *C (environmental temperature) R-T curves for T, 15 “C present clockwise rotation - Prosser’s type III - (Fig. 1A and B) resulting in partial compensation - Precht’s type III - of acclimated rates (T, = T,) between 15 to 20 “C. Effect of acclimation temperature during the winter season is less homogeneous, the highest rates appearing for Ta 15 oC in the high shore and T, 20 ‘C in the low shore. No compensation occurs in the low shore population (Fig. 1D) while different degrees of compensation are attained in the high shore based on rotation of the curves (Fig. 1C). A comparison between seasons for the two common acclimation t~~rat~es (T, 1.5, 20 ‘C) shows that R-T curves for T, 20 “C are less steep {Fig. 2), jibing a greater
A
TA
TA
B
15°C
20°C
5.0 -
2.0 -
1.0
-
0.5
-
L
1 10
I ,5
I 20
I
I
I
I
I
I
I
25
30
10
15
20
25
30
TEI”C
I
Fig. 2. Oxygen consumption (ml 0,. g- ’ h I) of an animal of 100 mg dry wt at five exposure temperatures (T,): 0, summer, high shore; 0, summer, low shore; A, winter, high shore; A, winter, low shore: A, T, 15°C; B, T, 20°C.
degree of metabolic Theo-~dependence over the entire range of T, . ~~irnurn thermal dependence appears in the summer, high shore within T, 10 to 20 “C (T, 15 ‘C, Q,<)= 1.47; T., 20°C Qlo = 1.62; T., 25 “C, Qlo = 1.25). Oxygen consumption in the winter increases considerably in relation to summer, irrespective of acclimation temperature. Acute measurements of the metabolic rate in the seasonally acclimated group display the same seasonal trend (Fig. 3) with a translation to the right of the R-T curve from winter to summer at both shore levels, coupled with a slight clockwise rotation in the low shore. The Q,, of the seasonal response to acute temperature change illustrates the effects of both season and shore level (Table I). The region of thermal independence displaces from 10 to 15 “C in the winter to 20 to 25 “C in the summer in the high shore, while it appears restricted to summer (20 to
ACCLIMATION TO TEMPERATURE
83
IN ACTINIA
25 “C, Q,,, = 1.58) in the low shore specimens. Q,, values associated with long-term (winter-summer) temperature changes are close to 1 in both shore levels; seasonal compensation is perfect (slight over-compensation) in the high shore and partial in the low shore (Fig. 3). Acclimated metabolic rates (7’, = 7’,) are shown in Fig. 4. Low-shore animals show a translation to the right of the R-T curve from winter to summer which results in a constancy of metabolic rates over the range 12 to 20 “C which covers the interval of environmental temperatures in this area. Clear over-compensation appears in the highshore population.
A 5.0
B
_
-7 I
‘;* a iu 0
2.0_
1.0 _
i 0.5 _ 1
I
I
I
I
I
I
I
10
1s
20
25
10
15
20
25 TE (‘C
I
Fig. 3. Seasonal against acclimated oxygen consumption (ml 0,. g - ’ h - ‘) for an animal of 100 mg dry wt: 0, summer, seasonal; 0, summer, acclimated; A, winter, seasonal; A, winter, acclimated; A, high shore; B, low shore. TABLE I Q,, values calculated
for 5 “C intervals
of seasonal
acute metabolic
rates (ml 0,.
g- i . h- ‘).
Season
Shore level
Interval (“C)
Summer (20 “C)
High
15-20 20-25
4.57 0.95
LOW
15-20 20-25
2.29 1.58
High
IO-15 15-20
0.91 3.02
Low
10-15 15-20
2.75 2.63
High Low
10-20 10-20
0.85 1.38
Winter (12 “C)
Winter-summer
Q10
M. MERTXE ORTEGA E7’,-1L.
84
I
5.0 t
I
i
I
10
15
1
1
20
26 T&z
1 TA (“C 1
Fig. 4. .Acclimated metaboiic rates (ml 0,. g ^ ’ ‘h _ ‘) - T, = 7, - of an animal of 100 mg dry wt: 0, summer, high shore; A, summer. low shore: 0, winter. high shore; A. winter. low shore.
DISCUSSION
The weight exponent in Actinia equina falls between 0.1973 and 044.55; usual values for intertidal anthozoans include: 0.54 in A~thop~eura elegantissirna (Fitt et al., 19821, a common 0.65 for DiaQumene leucolena, ~al~plane~~aluciae, and ~et~~d~u~ senile (Sassaman & ~~gurn, 1970), and 0.36 in Act&k equine (Navarro et al., 1981). The weight exponent seems to depend on the expe~ment~ situation, as taken from our own data on Actiniu and reported values for Metridium senile which range between 0.41 and 0.89 (Shumway, 1978; Shick et al., 1979; Robbins & Shick, 1980; Walsh & Somero, 1981). In this work a seasonal change in the slope b appears, with higher values in the summer. This fact, along with the remarkable increase of metabolie rate during the winter, suggests different levels of metabolism, probably related to the reproductive cycle. Changes in the weight exponent in ~climation exper~ents have been found in Orconectes nais (Armitage & Wall, 1982), ~etrid~u~ senile (Walsh & Somero, 1981), Ligia mea&z (Newell et al., 1976), and Mytilw edulis (Bayne, 1973) this last following the same seasonal pattern. Seasonally acclimated animals exhibit different types of compensation according to shore level. Upper-shore animals show perfect compensation with lateral translation to the right of the R-T curve in response to temperature increase, whereas partial compensation with translation plus clockwise rotation is found in the low shore. Subtropical Actinia equina show a similar lateral translation (Grifftths, 1977). The winter-summer transition results in a clear shift in the range of thermal insensitivity in the direction of rising temperatures for the high-shore anemones; in the tow shore adaptation to summer tempera~es involves a general decrease in the slope of the R-T curve. increasing temperature independence in this season.
ACCLIMATION
TO TEMPERATURE
IN ACTINIA
85
Experimental acclimation appears influenced by both season and zonation. The summer group shows a compensatory response at T, 15 oC (“cold acclimated”) which results in partial compensation between 15 and 20 “C. Metabolic adjustment occurs at different rates of oxygen consumption for each shore level: 0.96 ml 0, *g- ’ *h- * for the high shore and 1.22 ml O2 - g- ’ *h-‘ 1 for the low shore (animal of 100 mg dry wt). This dilTerence between shore levels is consistent with the seasonal data and agrees with the results of Shick (198 1) for A. equina, who finds a lower i/,, in intertidally accl~atized animals collected from a mid-shore location in September. An expansion of the area of thermal independence appears associated with increasing T, in the low shore (Fig. 1B). Reduction in temperature-dependence towards the higher levels of the shore results in upper-shore animals showing the lowest Q,, for the entire range of T, at any of the acclimation temperatures (mean Q,, at 10 to 30 “C on the high shore = 1.61; and on the low shore = 1.80). There seemed to be no acclimation at T, 25 “C in any of the shore levels and metabolism increased over the period of maintenance at this T, (unpubl. data). In A. equina the ability to acclimate thus appears restricted to temperatures within the annual range, as has also been reported by Grilliths (1977) who found no compensation at temperatures outside the environmental range in South African subtropical and Cal-temperate anemones. Winter high-shore animals exhibit a compensatory pattern between 10 and 20 “C, although no compensation was found in the low shore which shows maintenance of the seasonal response. A significant increase in oxygen consumption, regardless of shore level, occurs in winter in both seasonally and experimentally acclimated animals (Fig. 3). As a result of this, compensator adjus~ents are set at a different point each season, being higher during the winter. This phenomenon could be attributed to changes in metabolic requirements throughout the year, as has been suggested for Myt&.r edulis (Widdows & Bayne, 1971; Bayne, 1973) where perfect acclimation superimpased on a similar seasonal trend of metabolism is also found. Ability to restrict the effects of thermal impact upon metabolic expenditure seems to vary with the degree of temperature fluctuation of a given habitat (Newell, 1973, 1979), upper-shore populations being characterized by more effective homeostatic mechanisms (Barnes & Barnes 1969; McMahon & Russell-Hunter, 1977; Branch & Newell, 1978). Consequently, Actinia equina from the high shore would be expected to show maximum thermal independence and this, more so during the summer, is the case. Influence of zonation can be further demonstrated by ex~ing acclimated metabolic rates in relation to seasonal acute measurements (Fig. 3). In the low shore, failure to produce acclimation to experimental temperatures during the winter, coupled with acclimation during the summer, results in perfect compensation from 12 to 20 ’ C (annual range) for the laboratory acclimated group (Fig. 4) which was not evident from the seasonal results. In upper-shore anemones, however, achieving of experimental acclimation in both seasons superimposed on seasonal compensation (perfect between 12 and 20 “C) contributes to experimental over-compensation, intensifying the seasonal response.
M. MERTX~ORTEGA~~~~
Xh
ACKNOWLEDGEMENT
The authors are indebted to Professor R. C. Newell for help with the revision of the manuscript. REFERENCES ANDERSON,G., 1978. Metabolic rate, temperature acclimation and resistance to high temperature of soft-shell clams,Mya arenariu, as affected by shore level. Camp. Biochem. Physiol., Vol. 6lA, pp. 433-438. ARMITAGE,K. B. & T. J. WALL, 1982. The effects of body size, starvation and temperature acclimation on oxygen consumption of the crayfish Orconecaes nais. Camp. Blochem. Physiol., Vol. 73A, pp. 63-68. BARNES,H. & M. BARNES, 1969. Seasonal changes in the acutely determined oxygen consumption and effect of temperature for three common cirripedes, Bulunus ~lanoides (L.), 8. bakmus (L.) and Chtham~~us steffatus (Poli). J. Exp. Mar. Biol. Ecol., Vol. 4, pp. 36-50. BAYNE,B. L., 1973. Physiologica changes in My&s edr&s (L.) induced by temperature and nutritive stress. J. Mar. Biol. Assoc. U.K., Vol. 53, pp. 39-58. BRANCH,G. M. & R. C. NEWELL,1978. A comparative study of metabolic energy expenditure in the limpets Pateila cochlean, P. oculus and P. granular-k Mar. Biol., Vol. 49, pp. 351-361. BUI,I_OCK, T. H., 1955. Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev., Vol. 30, pp. 3 1l-342. Frrr, W.K., R.L. PARDY & M. M. LITTLER, 1982. Photosynthesis, respiration, and contribution to community productivity of the symbiotic sea anemone Anthopleuru eleguntissima (Brandt, 1835). f. Exp. Mar. Biol. Ecol., Vol. 61, pp. 213-232. GRIIFFITHS,R. J., 1977. Temperature acclimation in Acti& equina L. (Anthozoa). J. Exp. Mar. &al. Ecof.. Voi. 28, pp. 285-292. HOAR, W. S. & C.P. HICKMAN, 1975. A luborurory companjon Jar general and comparative physiolo~. Prentice-Hall, N. J., 283 pp. M&%AHON,R. F. & W. D. RUSSELL-HUNTER,1977.Temperature relations of aerial and aquatic respiration in six littoral snails in relation to their vertical distribution. Biol. Buli. (Woods Ii&, Muss.), Vol. 152. pp. 182-198. NAVARRO,E., M. M. ORTEGA& J.M. MADARIAGA,1981. Effect of body size, temperature and shore level on aquatic and aerial respiration of Actiniu equina (L.) (Anthozoa). J. Exp. Mar. Biol. Ecol., Vol. 53, pp. 153-162. NEW~U., R.C., 1969. Effect of fluctuations in temperature in the metabolism of intertidal invertebrates. Am. Zool., Vol. 9, pp. 293-307. NEWELL, R.C., 1973. Factors affecting the respiration of intertidal invertebrates. Am. Zool., Vol. 13, pp. 513-528. NEWELL, R.C., 1979. Biology of intertidal animals. Marine Ecological Surveys, Faversham, Kent, 781 pp. NEWELL,R.C. & B.L. BAYNE, 1973. A review on temperature and metabolic acclimation in intertidal marine invertebrates. Neth. J. Sea Res., Vol.7,pp. 421-433. NEWELL, R.C., A. ROY 6t K.B. ARMITAGE,1976. An analysis of factors affecting the oxygen consumption of the isopod Ligia oceanica. Physiof. ZooI., Vof. 49, pp. 109-$37. PRECHT,H., 1958. Concepts of temperature adaptation of unchanging reactions systems of cold-blooded animals. In, Physiorogicaf adapt&ion, edited by C. L. Prosser, Am. Physiol. Sot., Washington D.C., pp. 50-77. PROSSER,C. L., 1958. The nature of physiological adaptation. In, Physiological adapt&on, edited by C. L. Prosser, Am. Physiol. Sot., Washington DC., pp. 167-180. ROBBINS,R.E. & J.M. SHICK, 1980. Expansion-contraction behaviour in the sea anemone Metridium senile: environmental cues and energetic consequences. In, Nutrition in the lower Metazoa, edited by D. C. Smith & Y. Tiffon, Pergamon Press, Oxford, pp 101-I 16. SASSAMAN,C. & C.P. MANGUM, 1970. Patterns of temperature adaptation in North Amertcan Atlantic coastal actinians. Mar. Biol., Vol. 7, pp. 123-130. SHICK,J. M., 1981.Heat production and oxygen uptake in intertidal anemones from dif%rent shore heights during exposure to air. &fur. &of. Letters, Vol. 2. pp. 225-236.
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TO TEMPERATURE
IN ACTINIA
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pp. 50-62. SHUMWAY,S. E., 1978. Activity and respiration in the anemone Metridium senile (L.) exposed to salinity fluctuations. J. Eq. Mar. Biol. Ecol., Vol. 33, pp. 85-92. WALSH,P. J. & G. N. SOMERO,1981.Temperature adaptation in sea anemones: physiological and biochemical variability in geographically separated populations of Menidium senile. Mar. Biol., Vol. 62, pp. 25-34. WIDDOWS,J. dc B. L. BAYNE,1971. Temperature acclimation of Myrirus edulis with reference to its energy budget. J. Mar. Biol. Assoc. U.K., Vol. 5 1, pp. 827-843.