The respiration of the marine isopod Excirolana natalensis (flabellifera; cirolanidae) from an exposed sandy beach

Camp. Biockem. Physiol. Vol. 75A, No. 4, pp. 625 to 629, 1983 Printed

in Great

Britain

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0300-9629/83 $3.00+0.00 1983 Pergamon Press Ltd

THE RESPIRATION OF THE MARINE ISOPOD EXCZROLANA NATALENSZS (FLABELLIFERA; CIROLANIDAE) FROM AN EXPOSED SANDY BEACH R.

BALLY

Zoology Department, University of Cape Town, Private Bag, Rondebosch 7700, South Africa (Received

2 December

1982)

The active and passive respiration rates of E.xcirolanu natalensis were measured in animals from a coarse-grained. exposed sandy beach on the west coast of South Africa. 2. Weight-specific rates were determined over a range of temperatures. 3. The results obtained indicate a suppression of the rate/temperature curve above 15°C. 4. The reasons for this suppression are discussed in the light of the species’ behaviour and environment. Abstract-l.

INTRODUCTION

Isopods of the genus Excirolana are found on sandy beaches world-wide, although some species have also radiated into estuarine and deep-sea habitats (see Bowman, 1971; Kensley, 1978; Jones & Icely, 1981). Of the 13 species found on sandy shores, three have developed exceptionally wide distribution ranges, these being Excirolana orientalis (Japan to Madagascar), E. braziliensis (Chile to Mexico and Brazil) and E. natalensis (west coast of South Africa to Madagascar). The last two species in particular inhabit waters that range in temperature from those suitable for the formation of coral reefs to cold, upwelled waters with temperatures as low as 8-10°C. The behavioural and physiological adaptations that allow these isopods to inhabit this wide environmental range are therefore of considerable interest. The zonation shown by this species is described in Bally (1983) while physiological particulars of the genus have been noted by Klapow (1970, 1972a,b) and Enright (1972). This paper examines the respiratory metabolism of Exciroha natalensis, one of the three widely-distributed sandy beach species of this genus.

whether the animals were acclimatized at constant or cyclic temperatures prior to respirometry. Active and passive weight-specific respiration rates were obtained at 12.5, 14.0, 15.0, 17.5, 20.0 and 22.5”C using animals with acidized dry body weights ranging from 2.5 to 79.4 mg. This is approximately the weight range found in animals living on west coast beaches. Regressions were calculated for each temperature and predicted data was then used in a stepwise regression programme from the Madison Academic Computing Centre in order to obtain stepwise multiple regression equations for active and passive animals. The same data (i.e. predicted data) was used to produce a response surface using a SACLANT threedimensional plotting programme originally obtained from the NATO SACLANT Anti-Submarine Warfare Research Centre at La Spezia, Italy. On one occasion, a temperature profile was taken of the intertidal zone in which the largest numbers of E. nntalensis were found. For this purpose, a series of temperature probes attached to a thermistor were placed on the sand surface and at depths of I, 2, 5 and 10cm. Temperatures were recorded at 30minute intervals from 1000 hr to 1600 hr on a warm (maximum 28°C) sunny day in May. This coincided with the period between low and high water spring tides.

MATERIALS AND METHODS Isopods were collected from Rocherpan, a sandy beach on the west coast of South Africa some 200 km north of Cape Town. The beach is exposed and relatively coarse-grained with a mean sediment diameter of 1.61 phi. Animals were collected at low tide and removed from the sediment by sieving the sand through a 1 mm mesh sieve. The retained animals were placed in containers that were then filled with damp beach sand from the zone from which they had been collected. In the laboratory, single isopods were placed in flasks containing potassium hydroxide that attached to a Gilson Differential Respirometer.

were

then

It was not thought necessary to acclimatize animals to particular temperatures prior to the experiments, since it was felt that in the field intertidal animals would never experience constant temperatures for longer than a few hours. Dame & Vernberg (1978) have provided quantitative confirmation of this view, showing that respiration rates in two crab species differed significantly depending on 625

RESULTS Regression equations for active and passive animals for each of the temperatures measured, together with their correlation coefficients, are given in Table 1. Using the stepwise regression programme, the following equations were obtained describing the weightspecific respiration rates of E. natalensis over the

weight and temperature ranges measured (where R = weight-specific respiration rate in pl/mg per hr, T = temperature in “C and W = acidized dry weight in milligrams). For active rates: Log R = +327.5374 -625.1482 log T + 44.9607 T - 1.2946 T2 -0.2751 log W3 + 1.6570 x lo-’ T3 +2.8740

x 1O-3 W.

R.

626

BALLY

Table 1. Equations far active and passive weight-specific respiration rates in ~~~~~f~~u~a fla~Q~~~sisOver a range of ~~~~~eratures

Activity

Temperature {“Ci

Active

12.5 14.0 17.5 19.3 25.2 12.s

Weight-specific respiration eqL~ati~l~s R/W R/W R/W R/W R/W Rjcv

zzz5.1722M;-+7s = 0.13301V-0.89 = 0,2323CV*“‘,@’ = 0,1837U’“““.7* = 5.i578cV-0~95 = 0.263bS” o.6s

The multiple correlation coefficient for this equation is 0.9947. For passive rates:

YZ 5.925 0.953 0.986 0.988 0.879 5.949

Log R = +7.4829 - 11.5587 log T + Q.5587 T -0.3812 log W -0.9144 x 1O-4 T2 +0.7652 x 10-410g W*T -0,1208 x 10-4 w. The muIt~pIe correlation coefficient for this equation is 0.9512. Figures 1 and 2 show the response surfaces described by the above equations. The temperature profiles measured In the zone of retention are given in Fig. 3.

Passive

Weight-specific Respiration tur-lmrr‘.hr’l

Weight

(ma>

Weight Fig.

I.

I~$I)

Three~dimsnsional and contour plots of response surface showing the effects of weight and t~rn~erat~~re on the active weight-specific respiration rate in E. mtaknsis.

Respiration in a sandy beach isopod

627

Weight-apecific Respiration (ulw!md’.hi’)

23

Fig. 2. Three-dimensional

2a

43 W8)ght (mg)

se

79.4

and contour plots of response surface for passive weight-specific respiration rate of E. natulensis.

1m

IhO

limo of day (hrd

Fig. 3. The effect of depth on sand temperature in the zone of drying. Arrow indicates time first wave of incoming tide reached zone of drying.

R. BALLY

628 DISCUSSION

The results obtained show several features of interest. Firstly, although slopes of both active and passive weight-specific rates show a decrease in rate with increasing weight in the manner common to all organisms, the values for these slopes differ considerably from the value of -0.25 suggested by Hemmingsen (1960) to be the average for most species. They do agree, however, with values found in other intertidal organisms, such as Littorina littorea (Newell & Roy, 1973), Ligia oceanica (Newell et al., 1976), Ligia dilatutu (Koop & Field, 1981). Bullia melanoides and B. digitalis (Brown ef al., 1978) Donax serra and D. sordidus (Dye, 1979) and the subtidal Cirolana imposita (Shafir & Field, 1980). Secondly, it can be seen from Figs 1 and 2 that the respiration rate rises at a fairly steady rate from 12.5 to 175°C. Above this latter temperature however, there is an equally steady decline in the measured rates. This applies to both the active and the passive rates, although the decline is most marked in the passive rates of small animals. The multiple regression equations also show certain features of interest. In the case of active rates, the logarithm of temperature exerts the greatest influence on respiration, followed by temperature and temperature squared. It is only then that the first of the weight factors appears. The passive rate is also chiefly governed by temperature, although not to the same extent as the active rate. In addition, there is a temperature-weight interaction that also influences respiration. The dominant role of temperature on the respiration of Excirolana natalensis should be viewed in the context of the known behavioural and morphological characteristics employed by this and other members of the genus in order to adapt to the uppermost intertidal zones of sandy beaches. Bally (1983) shows that Excirolana natalensis occupies the highest and driest intertidal zone of any water-breathing macrofauna on west coast beaches. On relatively fine-grained beaches (2.25-2.31 phi), this species is found only in low densities and occupies a narrow band in the zone of drying as defined by Pollock & Hummon (1971). On coarser-grained beaches (1.60phi), this species becomes the dominant isopod and occupies not only the zone of drying but also the zone of retention and, to a lesser extent, the zone of resurgence (see Salvat, 1964 and Pollock & Hummon, 1971 for definitions of these zones). The reasons for this change are that firstly, E. natalensis is larger than the other cirolanid species (Eurydice longicornis and Pontogeloides latipes) that it displaces on coarser-grained beaches and is thus a more effective burrower in coarse sands and better able to maintain zonation. Secondly, its larger size entails a more favourable surface to volume ratio resulting in reduced water loss and therefore reduced desiccation stress during low tide. This is particularly important in view of the fact that water retention by intertidal beach sand declines with increasing grain size. The temperatures recorded in the zone of retention (Fig. 3) give some indication of the buffering effect of sand depths on interstitial temperatures. It can be seen that although the surface temperatures fluctuated considerably throughout the period in which they

were measured, these fluctuations were almost completely dampened out by the first 5 cm of sand. At a depth of 10 cm, there was a virtually constant rate of increase in the interstitial temperature. Interestingly, this increase continued after the first wave had washed over the surface of this area of the intertidal zone. There was even a slightly greater increase for the first 15-30 min, since the cold seawater that had washed over the surface was heated by the warm sand as the water percolated through to the 1Ocm level. During the course of a separate study, it was found that most individuals of E. nutalensis are buried at depths of 5-15 cm at Rocherpan (Bally. unpublished data). This species was too scarce on the finer-grained beaches to determine its depth distribution but Bally (1981) has shown that the macrofauna as a whole tends to burrow to shallower depths in fine-grained sands than in coarser-grained ones. This implies that organisms actively seek sand depths that provide protection from heat and desiccation. Because of the greater drainage of water from coarser sands, it is necessary to burrow deeper in such sands to find an adequate environment. It is of interest to note that where the distributions of E. natulensis and E. orientabs overlap on the south-western coast of Madagascar, E. natalensis continues to occupy the uppermost zone despite the tropical latitude and associated high temperatures (Pichon, 1967). Protection from water loss and heat must be sought prior to every low tide, although it is especially important before low tides occurring during the daytime, when temperatures may fluctuate considerably. One cannot assume that animals are successful every time, however, and digging in unsaturated moist sand is costly in energy since sand hardens as it becomes less moist (Chapman, 1949). It was found, moreover, that captive animals rarely dug to depths greater than 1 cm below the surface if placed on damp sand. It is very likely, therefore, that animals frequently have to survive periods of low tide at sand depths where they encounter unfavourable temperature and humidity regimes. A physiological mechanism for conserving energy under those conditions would therefore be of considerable advantage. It would appear that the suppression of the rate/ temperature curve shown in Fig. 4 represents such a mechanism. Here, respiration rates decline above 17.5”C and it is unlikely that organisms would encounter temperatures higher than this unless they were buried at shallow depths. Under such circumstances, it would be of considerable advantage to reduce their respiration rates, firstly to conserve energy and secondly to reduce the water losses associated with increases in metabolic rates. This latter factor is of especial importance to E. natalensis in view of the high intertidal levels and relatively coarse and well-drained sands that it occupies. Circatidal respiratory rhythms of the type found by Marsh & Branch (1979) in Tylos grunularus were not found. This may have been a consequence of the use of freshly captured animals since endogenous activity rhythms have been recorded in many cirolanid isopods (e.g. Klapow, 1972a,b; Enright, 1972; Fish & Fish, 1972; Shafir & Field, 1980) and one would expect these to be expressed in the respiration rate. King (1951) has shown that sand may be removed to

Respiration in a sandy beach isopod

629

BROWNA. C., ANSELLA. D. & TREVALLJON A. (1978) Oxy-

gen consumption by Bullia (Dorsanum) melanoidrs (Deshayes) and Bullia digitalis Meuschen (Gastropoda, Nassariidae)-an example of non-acclimation. Comp. Biothem. Physial. 61A, 123-125. CHAPMANG. (1949) The thixotropy and dilatancy of a marine soil. J. mar. biol. Ass. U.K. 28, 123-140. DAME R. F. & VERNBERGF. J. (1978) The influence of constant and cyclic acclimation temperatures on the metabolic rates of Panopeus herbstii and Uca pug~iator.

5

Biol. Bull. 154, 188-197. DYE

“Yt

12 13 I’(

13 1% a 11 Tomporaturo (‘C)

t

n

n

R

25

Fig. 4. Comparison of active and passive weight-specific respiration rates over a range of temperatures for a standard animal of 2.5 mg.

depths of 4cm or more by a single wave on exposed shores. This, combined with the sudden presence of cold water and change of temperature in the interstitial environment associated with the incoming tide probably overrides any endogenous rhythms that may be present. Indeed, mechanical and thermal stimulation is often used to entrain tidal rhythms in laboratory studies (Naylor, 1976). It seems likely, therefore, that the experimental conditions in this study overshadowed any endogenous respiratory rhythms that may have been present. In summary, E. natalensis shows respiratory adaptations to its environment that enhance this species’ chances of survival in the most extreme intertidal zone on sandy beaches occupied by water-breathing organisms. Acknowledgements-1 would like to thank Mary Armour for her helpful and constructive criticisms. This work was carried out with the assistance of a grant from the South African National Council for Oceanographic Research. REFERENCES BALLY R.

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SHAFIR