Effect of body size, temperature and shore level on aquatic and aerial respiration of Actinia equina (L.) (Anthozoa)

J. esp. yurr. Biol. Ecol., 1981, Vol. 53, pp. 153-162

Elsevier/North-Holland

153

Biomedical Press

EFFECT OF BODY SIZE, TEMPERATURE ON AQUATIC

AND AERIAL

AND SHORE

RESPIRATION

LEVEL

OF ACTZiVZz4

EQUZNA (L.) (ANTHOZOA)

ENRIQUE

NAVARRO,

M. MERTXE

ORTEGA

and JOSI? M. MADARIAGA

Departamenlo de Biologia, Fact&ad de Ciencias, Universidad del Pais Vasco. Aptado. 644, Bilbao. Spain

Abstract: Oxygen consumption of Acrinia eqquina (L.) has been measured at five temperatures (IO, 15, 20. 25, 30°C) in air and in water, in animals from two shore levels, from 20 August to 15 September 1979. A clear dependence of i’o? on body weight has been established, and two single values of the weight exponent, 0.56 and 0.36 for aerial and aquatic respiration, respectively, calculated. In all cases PO2 was found to increase with temperature within the 10~30°C range, although sensitivity to thermal variation differed for each interval. Aerial respiration had a low Q,, (1.0-1.64. mean 1.4) between 15 -30 “C for both shore levels. Aquatic respiration showed a stronger dependence on temperature change as well as on shore level, with a clear low Q,,, plateau between 15-25°C (QIo = 1.55) in lowlevel animals and a gradual decrease of Q10 with temperature rise in high-level animals. Aerial bo,, was found to remain always below aquatic i/o,, regardless of shore level, temperature or body weight, but the relation iJoZa’lr/i’o, water kept noticeably lower in low level. Partly as a consequence of the differences in size-dependence of i/o, in air and water, the difference between aerial and aquatic oxygen consumption diminished with increase in body size. INTRODUCTION

The available

information

and, in most cases, respiration. There are (Shumway, 1978), on Actinia equina (Henze, Mangum,

on the oxygen consumption

in Anthozoa

is very limited

related to the effect of environmental factors on aquatic data on the effect of salinity fluctuations in Metridium senile the respiratory behaviour in relation to oxygen tension in 1910), Haloclavaproducta and Merridium senile (Sassaman &

1972) and Diadumene

leucolena

and

Renilla

kollikeri

(Mangum

& Van

Winkle, 1973) or on the effect of temperature in Actinia equina (Newell & Northcroft, 1967) and Metridium senile, Haliplanella luciae and Diadumene leucolena (Sassaman & Mangum, 1970). Although some of these species are truly intertidal, integrated studies of aerial compared with aquatic metabolism are quite exceptional (Griffiths, 1977a, for Actinia equina and Shick et al., 1978, for Anthopleura elegantissima and Metridium senile). In relation to the species Actinia equina (L.), the information is sparse and in some cases contradictory. Aquatic oxygen consumption was studied by Newell & Northcroft (1967) who put forward the hypothesis of the existence of two levels of metabolism, based upon the observation of different individual oxygen consumption rates. Jones et al. (1977), in a revision of the mentioned work, come to the conclusion that individual differences in oxygen uptake rates are the result of a 0022-0981/81/0000-OOOO/$2.50 0 Elsevier/North-Holland

Biomedical Press

154

ENRIQUENAVARROETAL

respiratory rhythm linked to the water content of the enteron cavity, a possibility which had already been suggested by Newell & Northcroft (1967). The effect of temperature on metabolism has been studied by Newell & Northcroft (1967) and Griffiths (1977a,b). In spite of individual differences, in both cases the conclusion reached is that respiratory rate in A. equina is virtually independent of temperature within a wide range of variation of this factor. Under a perspective which considers respiratory rate as one of the components of energy flow throughout animal communities, this result has been interpreted (Newell, 1979, 1980) as an index of the adoption of a conservationist behaviour in this species. The present work extends this interpretation to include the respiration of A. eqtrina in relation to body weight, temperature, level on shore, and aerial and aquatic conditions.

MATERIALSAND

METHODS

COLLECTIONANDMAINTENANCEOFANIMALS A. equina were collected at low tide from the rocky area of Sopelana beach, an exposed sandy beach in the Basque country on Biscayne Bay, at two specific collection sites characterized by an annual mean air exposure permanence of about 12-16 h/day (high level) and 4-8 h/day (low level), respectively. The animals, colfected immediately prior to the experiments, were carefully detached from the rock with a chisel without inflicting any injury. Once in the laboratory, they were maintained for 12-16 h in an aquarium with re-circulating sea water, where they were allowed to become fixed to the respirometers. From 4-12 h before taking measurements, the water in the aquarium was brought to the experimental temperature, to minimize thermal shock effects. After each experiment, the anemones were removed from the respirometers and dried at I10 “C for 4X h (when constant wt was reached).

Oxygen consumption in water was determined in a closed system. Animals were placed in sealed flasks of 150-ml capacity with a magnetic stirrer system on their base to avoid the occurrence of local conditions of anoxia. Oxygen depletion was measured at the end of 1 h, in samples of 50 ml using the micro-Winkler method (Hoar & Hickman, 1975). AERIALRESPIROMETRY

Aerial oxygen consumption was determined using a constant volume manometric procedure in a Warburg apparatus adapted for 70-ml flasks. Griffiths (1977a,b)

RESPIRATION

employed

this same method

with

OF ACTINIA

llO-ml

EQUINA

155

flasks to study the oxygen

consumption

of A. equina. Readings

were made at intervals

of 15 min for l-2 h for each temperature.

RESULTS

The oxygen consumption of A. equina was measured towards the end of August and beginning of September in 1979. Two shore levels were considered (see p. 154) and measurements made in air and in water at five experimental temperatures (10, 15, 20, 25, 30°C). The relationship between the rate of oxygen consumption (GoIo,= ~10, . h-’ animal-‘) and body wt (W = mg of dry wt) can be described by the equation V,, = aWh which can be written

in its linear form as log pO: = log a + b log W.

TABLE

Summary

Condition Air

of linear regression equations of respiration rate (~1 Oz. h-’ ‘animal-’ against (mg)): N, number of animals; a, intercept; b, slope; Y, correlation coefficient. Shore level High

Low

Water

I

High

Temperature (“C)

N

10 15 20 25 30

12 12 32 30 33

0.876 0.663 0.999 0.534 0.666

0.299 0.504 0.367 0.659 0.607

0.82

10 15 20 25 30

15 15 12 17 14

-0.894 0.144 -0.114 0.219 0.573

0.965 0.593 0.711 0.605 0.491

0.88 0.76 0.77 0.73 0.66

10

20 25 30

26 16 16 18 18

0.780 1.145 1.109 1.442 1.610

0.434 0.358 0.463 0.358 0.304

0.63 0.63 0.74 0.78 0.74

10 15 20 25 30

14 16 18 18 17

0.484 0.908 1.334 1.321 1.793

0.534 0.450 0.283 0.337 0.202

0.82 0.75 0.76 0.72 0.71

15

Low

dry body wt

(I

b

0.69 0.57 0.70 0.76

ENRIQUE

156

NAVARRO

ETAL

For each temperature and set of conditions (in air or water and level on shore) individual values of i/0> are plotted against W on logarithmic paper and a line fitted by the least mean squares procedure. The results are summarized in Table I. Covariance analysis applied to the whole group of slopes (20 values) showed differences to be significant at P = 0.001. Differences were, however, found to be non-significant at P = 0.05 when analysing the aerial and aquatic series separately TABLE II Summary

of analysis

of covariance for testing significance of differences equations of Table I: n.s., not significant.

Air Water Total

FS

d.f.

1.85 1.24 2.40

9,172 9,157 19,329

between

slopes for regression

Significance n.s. (P >0.05) n.s. (P > 0.05) P < 0.001

(Table II). It becomes, therefore, possible to calculate two single regression coefticients for aerial (b = 0.5645) and aquatic (b = 0.3607) respiration. The re-calculated intercept values (a) for the two common slopes are represented in Table III together with the antilog a (oxygen consumption in ~1 of a 1-mg dry wt animal).

TABLE III Re-calculated

values

of a (intercept) sumption

for the established two common slopes: (~1 ‘h-l) for an animal of 1 mg dry wt. Air (h, 0.5645)

Shore level

Temperature

antilog

a. oxygen

con-

Water (h, 0.3607)

_

(“C)

CI

antilog

u

‘1

antilog

High

10 15 20 25 30

0.332 0.535 0.615 0.717 0.749

2.14 3.43 4.12 5.21 5.61

0.926 1.125 1.309 1.439 1.500

8.62 13.34 20.36 27.47 31.62

Low

10 15 20 25 30

-0.046 0.206 0.208 0.308 0.415

0.90 1.60 1.61 2.03 2.60

0.832 1.086 1.184 1.277 1.486

6.80 12.20 15.29 18.92 30.61

0

In Fig. 1, the original regression lines from Table I have been redrawn for the new common slopes defined above. The mean dry wt of the animals used in the experimental work was x 150 mg and so we have used this value in plotting the

RESPIRATION

OF ACTINIA

15-l

EQUINA

metabolic rate (~1 Oz . h-’ . mg-‘) from the calculated regression lines. The corresponding values are presented in Fig. 2.

s-s_

AERIAL

AERIAL HIGH SHORE

LOW’ SHORE

2.0 -

-

1.5-

0" -is E, l.O-

25 20 I.5 10

AQUATIC

AQUATIC

HIGH SHORE

LOW’ SHORE

1.0 -

1.5

2.5

2.0 LOG.

Fig.

I. Regression

DRY

I

I

I

1.5

2.0

2.5

WEIGHT

(MC;

)

to the two common regression lines of ko2 against dry wt re-plotted h = 0.56 for aerial respiration and b = 0.36 for aquatic respiration.

coefficients:

ENRIQUE

158

NAVARRO

1

I

I

10

15

20

TEMPERAT’I’HE

Fig. 2. Oxygen consumption 0, aerial, low shore;

EFFECT

ET AL

I

25

I

30

c:

(~1 O2 mg-’ h-‘) of an animal of 150 mg dry wt at five temperatures: 0, aerial, high shore; A. aquatic, low shore; A, aquatic, high shore.

OF TEMPERATURE

In all cases, PO2 increases with temperature within the l&30°C range; the temperature sensitivity is, however, different for each temperature interval. It is also different in air and in water over comparable temperature intervals. The corresponding Q,, values calculated for 5 “C intervals are given in Table IV. Aerial respiration shows high Q,, values in the lo-15 “C range, but there is a reduction over the 15-30 “C interval to l-l.64 (mean 1.40) in animals from both the shore levels considered. Aquatic respiration is characterized, in general, by a stronger thermal dependence of oxygen consumption. Nevertheless, the rate-temperature curve is different for both shore levels showing, in the lower one, a clear plateau between 15-25 “C (Q = 1.55) which does not occur in the high-level animals where Q,, decreases gradually with temperature increase.

RESPIRATION

OF ACTINIA

EQUINA

159

TABLE IV Qlo values cdkuiated

Condition Air

Water

EFFECT

OF

SHORE

LEVEL

ON

for 5 “C intervals

Shore level

Interval (“C)

PI0

High

lo--l5 15-20 20-25 25-30

2.55 1.44 1.60 1.15

Low

l&15 15-20 2&25 25-30

3.19 1.01 1.58 1.64

High

l&15 15-20 20-25 25-30

2.39 2.33 1.82 1.32

Low

lo-15 15-20 2&25 25-30

3.22 1.57 1.53 2.62

AERIAL

COMPARED

WITH

AQUATIC

RESPIRATION

In the size range considered in this work, the aerial respiratory rate remains below the corresponding aquatic one at every temperature. The low-level anemones show a stronger reduction in the aerial oxygen consumption and, therefore, the relation tiOo,air/PO’,, water for this level is always lower than in individuals from the high-shore level (Table V). In addition, and slope, the difference between aerial and aquatic for animals from both levels on shore.

as a consequence of differences in respiration lessens with size increase

TABLE V Relation

Vo2 air;‘Vo,

water

for three arbitrary animals of 50, 150 and 500 mg dry wt for both levels and for the five experimental temperatures. Temperature

shore

(“C)

Shore level

Dry wt (mg)

10

15

20

25

30

High

50 150 500

0.56 0.68 0.87

0.57 0.70 0.92

0.44 0.55 0.71

0.42 0.52 0.69

0.39 0.49 0.63

Low

50 150 500

0.29 0.37 0.46

0.29 0.37 0.48

0.23 0.29 0.38

0.24 0.30 0.37

0.19 0.23 0.30

160

ENRIQUENAVARROEi-AL. DISCUSSION

It becomes possible from this work to establish a clear dependence of I$, upon body wt. The calculated values for the weight exponents are 0.56 for the aerial oxygen consumption and 0.36 for the aquatic rate. In consequence, as body wt increases differences in oxygen consumption between air and water decrease. A similar behaviour of the body wt exponent was described for four species of the genus Littorina (Toulmond, 1967a,b) and more recently for Patella granatina (Branch, 1979). The same type of results have been obtained in the anthozoan Metridium senile (Shick et al., 1978) for animals between 50-500 mg dry wt. It becomes clear from their work that, during air exposure, the reduction of respiratory surface which comes as a consequence of tentacular retraction, would primarily affect the small anemones. In fact, tentacular surface accounts for 81 ‘L of the total area in animals of 50 mg in M. senile and only 67”/, in animals of 800 mg (Shick c’t al., 1978). In addition, aerial oxygen uptake can be affected by resistance to desiccation, and more in the case of small animals because of the larger surface/ volume ratio. In the Actinia equina communities at the two levels considered, aerial I$‘,?remains below aquatic I& for the entire range of body wt and experimental temperatures studied. The effect of aerial condition upon respiratory rate is, however, greater in animals belonging to the low shore, resulting in lower air/water coefficients (Table V). Differences in the relation between aerial and aquatic oxygen consumption have been widely noted in different molluscs which inhabit the intertidal zone and have generally been interpreted in terms of the limits of their vertical distribution (Sandison, 1966; Micallef, 1967; McMahon & Russell-Hunter, 1977). In A. equina, a sessile animal with a largely non-specific feeding behaviour which takes place during tidal submersion, tidal recession results in a noticeable decrease of activity and, consequently, in a lower respiratory rate in air. This decrease in activity during exposure to air, may be related to the “standard” metabolism level established for the aquatic respiration of this species from a high-shore level on the British coast (Newell & Northcroft, 1967). Certainly, there is good agreement between the values of that minimum aquatic consumption and the ones we have obtained for aerial consumption in the high level. We have also found a wide range of relative independence of the aerial l& with temperature (Q10mean = 1.4 between 15-30 “C), a characteristic which has often been associated with the “standard metabolism” of intertidal organisms (Newell & Northcroft, 1967; Newell, 1969, 1973, 1979). The idea of a reversion towards a low “standard metabolism” in A. equina during tidal ebb as a consequence of decreased activity is similar to that suggested by Branch.,& Newell (1978), Branch (1979) and Newell (1979, 1980) for a number of intertidal molluscs. They proposed that during exposure to air, food shortage and wider temperature fluctuations may be compensated for by a diminution of

RESPIRATION

metabolic temperature.

expense

as well as in a certain 1973) showing

a minimal

EQUINA

independence

Similar results have been described

edulis (Coleman, contrasting Griffiths

OF ACTINIA

161

of respiration

for the aerial respiration

dependence

upon

temperature

rate

on

of M~‘rilus change,

with a Q,, close to 2.0 for its aquatic respiration (Widdows, 1976). (1977a) found aerial and aquatic PC), to be similar in specimens

of

Acliniu rquincr from Natal (South Africa) between 200-300 mg dry wt and, therefore, does not establish a distinction between both respiratory conditions. In the case of the present results, as can be appreciated from Table V, differences decrease with size increase, but the ratio Ijo2 air/p,, water only becomes close to 1.O for high-level animals >500 mg dry wt. On the-other hand, Griftiths’ results show an independence of respiratory rate upon temperature which is, in our data, the characteristic feature of aerial respiration (but not of aquatic) in anemones from the high-shore level. Our values of aerial tic,? of a high-level animal of 300 mg dry wt are a little higher than those of Natal individuals during summer (sea-water temperature 25 “C) (Griffiths 1977a,b) and show higher Q,,, values. This disagreement is probably due to the differences in latitude related to thermal acclimation, since we find a very good agreement when comparing the respiratory behaviour of the same animals acclimated to 20 “C (Griffths, 1977b) which is the mean summer temperature of our coastal waters. If Griffiths’ data can be considered as representative of a “standard rate” for high-shore level animals, then there would be agreement between our results and those previously obtained by Newell & Northcroft (1967) and Griffiths (1977a,b). As would be expected from a condition which shows narrower temperature fluctuations and an activity increase linked to food uptake, aquatic respiration is characterized, in general, by a higher oxygen consumption and a stronger dependence upon temperature. For the low level it is, however, possible to distinguish an interval in the rate-temperature curve, for which temperature dependence diminishes (15-25 “C, Q,, = 1.5) which does not occur for the high level and this results in a noticeable reduction of aquatic metabolic rate over its normal range of water temperatures. It is possible that, as Newell (1979, 1980) points out, food restrictions may appear at low-shore levels as a consequence of the strong competition characteristic of the high-density populations of such levels, and this would specially affect the period of aquatic feeding. On the other hand, variations in the duration of the aquatic period between both levels, are likely to determine

different

patterns

in the utilization

of energy

from

the environment. On the high shore, animals will be characterized during tidal flow by high indexes of food intake to obtain sufficient production rates during the shorter period of time they have to feed. It may thus be possible to interpret the characteristic shape of the rate-temperature curve for the aquatic respiration in A. equinu from upper-shore levels with high feeding activity and Q,,, values which only decrease towards the extreme of higher temperatures.

162

ENRIQUE NAVARRO ETAL ACKNOWLEDGEMENT

The authors are indebted to Professor R. C. Newell for his advice and correction of the manuscript. REFERENCES BRANCH, G. M., 1979. Respiratory adaptations in the limpet PutrIfu grmutina: a comparison with other limpets. Camp. Biochem. Physiol., Vol. 62A, pp. 641-647. BRANCH, G. M. & R. C. NEWELL, 1978. A comparative study of metabolic energy expenditure in the limpets Pu~ellu cochlear, P. oculus and P. granutinu. Mm. Biol., Vol. 49. pp. 351-361. COLEMAN, N.. 1973. The oxygen consumption of izI~,ri/us edulis in air. Comp. Biochem. Physiol., Vol. 45A, pp. 393-402. GRIFFITHS, R. J., 1977a. Thermal stress and the biology of Actik equinct L. (Anthozoa). J. e.up. mnr. Biol. Ecol., Vol. 27,pp. 141-154. GRIFFITH& R. J.. 1977b. Temperature acclimation in Actinicr equinu L. (Anthozoa). J. r.x-p. mur. Biol. Ecol.. Vol. 28, pp. 285-292. HEIUZE, M., 1910. tiber den EinfluR des Sauerstoffdrucks auf den Gaswechsel einiger Meerestiere. Biochem. Z., Vol. 26, pp. 255-278. HOAR, W. S. & C. P. HICKMAN, 1975. A kuborator), companion ,fkw ,ymerrrl und comparative phjxiology. Prentice-Hall, New Jersey, 283 pp. JONES, W. C.. V. J. PICK~HALL & S. P. NESBITT, 1977. A respiratory rhythm in sea anemones. J. e.up. Biol., Vol. 68, pp. 187-198. MANGUM, C. P. & W. VAN WINKLE, 1973. Responses of aquatic invertebrates to declining oxygen conditions. Am. Zoo/., Vol. 13, pp. 529-541. M~M,%~I~N. R. F. & W. D. RUSSELL-H~.NTER, 1977. Temperature relations of aerial and aquatic respiration in six littoral snails in relation to their vertical zonation. Biol. BUN. mar. biol. Lab., Woo& Hole, Vol. 152, pp. 182.-198. MICALL~F, H., 1967. Aerial and aquatic respiration of certain trochids. Experientiu, Vol. 23, p, 52. NEWELL. R. C.. 1969. Effects of fluctuations in temperature on the metabolism of intertidal invertebrates. Am. Zool., Vol. 9, pp. 293-307. NEWELL, R. C., 1973. Factors affecting the respiration of intertidal invertebrates. Am. Zoo/., Vol. 13, pp. 513-528. NEWELL, R. C.. 1979. Biology qf‘inrertidul animals. Marine Ecological Surveys, Faversham Kent, 78 I pp. NLU~LL. R. C., 1980. The maintenance of energy balance in marine invertebrates exposed to changes in environmental temperature. In, Animals and environmental fitness, Vol. I, Proc. 1st. Congr. Europ. Sot. for Comp. Physiol. and Biochem., edited by R. Gilles, Pergamon Press, Oxford, pp. 561-582. NF~ELL. R. C. & H. R. NOKTHCROFT, 1967. A re-interpretation of the effect of temperature on the metabolism of certain marine invertebrates. J. Zoo/., Vol. 151, pp. 277-298. QNDISON, E. E., 1966. The oxygen consumption of some intertidal gastropods in relation to zonation. J. Zoo/., Vol. 149. pp. 163-173. SASSAMAN, C. & C. P. MANGUM, 1970. Patterns of temperature adaptation in North American coastal actinians. Mar. Biol., Vol. 7, pp. 123-130. SASS~MAN. C. & C.P. MANGUM, 1972. Adaptation to environmental oxygen levels in infaunal and epifaunal sea anemones. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 143, pp. 657-678. SHICK, J. M., W. I. BROWN, E.G. DOLLIVER & S. R. KAYAR, 1978. Oxygen uptake in sea anemones: effects of expansion, contraction and exposure to air, and the limitations of diffusion. Phj,siol. Zo61.. Vol. 52, pp. 50-62. SHUMWAL. S. E., 1978. Activity and respiration in the anemone Merridium senile L. exposed to salinity fluctuations. J. exp. mar. Biol. Ecol., Vol. 33, pp. 85-92. TOULMOND, A.. 1967a. Consommation d’oxygtne dans I’air et dans l’eau, chez quatre gasteropodes du genre Li/torina. J. Physiol. Paris, Vol. 59. pp. 303-304. TOUL~~OND, A., 1967b. l?tude de la consommation d’oxyg&ne en fonction du poids. dans I’air et dans I’eau, chez quatre especes du genre Litiorina. C. r. hehd. Shunt. Acud. Sri., Paris. Vol. 264, pp. 636-638. WIDDOWS, J.. 1976. Physiological adaptation of M,,ti/u.y &/i,s to cyclic temperatures. J. camp. Pl?ysiol., Vol. 105, pp. 115-128.