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Comparative respiration of tropical echinoids
Comp. Biochem. Physiol., 1968, Vol. 24, pp. 649 to 652. Pergamon Press. Printed in Great Britain
SHORT COMMUNICATION COMPARATIVE RESPIRATION OF TROPICAL ECHINOIDS JOHN B. LEWIS Bellairs Research Institute of McGill University, St. James, Barbados
(Received 25 July 1967) Abstract--1. The rates of oxygen consumption of six species of tropical sea urchins were determined. 2. The oxygen consumption rates of three species of epifaunal, regular urchins were significantly higher than the rates of two infaunal, irregular species. 3. Oxygen consumption rates of a cidarid species which lacks peristomeal gills were intermediate between the other two groups. INTRODUCTION
RECENT review articles by Farmanfarmaian (1966) and by Moore (1966) have underlined the fact that the respiratory physiology of sea urchins is known for only a few species. Such information is restricted to the regular urchins, for example Strongylocentrotus (Farmanfarmaian, 1959; Giese & Farmanfarmaian, 1963; Giese et al., 1966) and Arbacia (Farmanfarmaian, 1966). The irregular urchins, such as the spatangoids and clypeastroids, have not been investigated nor is there information on comparative respiration between infaunal and epifaunal forms. Furthermore, with the exception of Tripneustes (Moore & McPherson, 1965) the respiratory physiology of tropical echinoids has not been investigated. The following study is a contribution to the comparative respiratory physiology of six species of tropical echinoids from varying ecological habitats and diverse taxa. METHODS AND MATERIALS
Freshly caught sea urchins of the following species were used for study: Eucidaris tribuloides (Lamarck), Echinometra lucunter (Linnaeus), Tripneustes esculentus Leske, Diadema antillarum Philippi, Brissus unicolor (Leske) and Mellita sexiesperforata (Leske). Specimens were acclimatized in concrete tanks in running sea water for 1-5 days before being used for experiments. Only active, healthy specimens which responded readily to external stimuli were collected. Twenty-five specimens of each species were placed for study in individual glass or polythene vessels in measured amounts of freshly filtered sea water which was approximately saturated by vigorously bubbling air into it. The water in each experimental vessel was 649
650
JOHN B. LEWIS
gently stirred with a magnetic stirrer. The experimental animal rested on a platform at the bottom of the vessel and a glass tube inserted into the water allowed the withdrawal of water into sample bottles. A layer of paraffin oil was added to the water surface in the vessel after the urchin had been introduced. Experiments were continued for 3-hr periods during daylight, at the same time of day. In order to minimize any effect of seasonal variations in metabolism the experiments were carried out over a period of approximately 2 months. At the end of the test period a 50 cm 3 sample of water was carefully withdrawn, to prevent bubbling, into a Pyrex flask. A control vessel without an urchin was treated in the same manner. Oxygen determinations were carried out immediately on the samples by oxygen electrodes manufactured by the Precision Scientific Co. of Chicago, Illinois. An accuracy of +__0.1 ml O2/I. is claimed by the manufacturers for this instrument. Test volumes, diameters and lengths were measured for each experimental animal. For a series of twelve animals of each species, nitrogen content of whole animals, less the gonad tissue, was determined by Kjeldahl digestions and subsequent ammonia determination by colorimetric titrations.
RESULTS The rates of oxygen consumption of various sizes of the six species of echinoids, at salinity 33~oo to 34~o and temperature 26--27°C, are shown in Fig. I. The regressions of log oxygen consumption on log total nitrogen of urchins show that the rates per unit weight of nitrogen decreased with increased size in all species. This is in agreement with the physiology of other echinoderms reported by Farmanfarmaian (1966) and of other animals (Zuethen, 1953). A comparison of the different oxygen consumption rates suggests that the six species can be divided into three groups. The regular sea urchins, Diadema, Echinometra and Tripneustes which are epifaunal forms, have the highest rates of oxygen consumption. The irregular urchins Mellita and Brissus are burrowing forms, i.e. infaunal in habitat, and have the lowest rates of oxygen consumption. Eucidaris, which unlike other regular sea urchins, lacks peristomeal gills, has a respiratory rate below that of the epifaunal urchins. Pooled group mean oxygen consumptions of the two infaunal forms were significantly different from the pooled group means of the epifaunal forms at the level P = 0-01. Similarly, the mean oxygen consumption of Eucidaris was significantly different from both the infaunal and epifaunal pooled group means. The respiratory rates of the six species are higher than the rates reported from colder water. Farmanfarmaian (1966) has listed the following rates for three coldwater species: Arbacia, 0.024; Strongylocentrotus, O.036;Echinocardium, 0.012 ml 02]hr/g wet wt. By converting these figures to weight of oxygen and allowing 2 per cent nitrogen of the wet weights of the urchins the above rates are equivalent to 0.0014, 0.0025 and 0-0008 mg O2/hour/mg N. The rates for Arbacia and Strongylocentrotus were determined at 20°C and that of Echinocardium at 15°C.
COMPARATIVE RESPIRATION OF TROPICAL ECHINOIDS
651
The lower rates of these species are consistent with the results of other authors' comparisons of cold-water and warm-water forms. Comparisons of respiration and metabolism of tropical and temperate or cold-water animals have been reviewed by Bullock (1955), Prosser (1955) and Scholander et al. (1953). Specific comparisons have been made by Thorson (1936), Sparck (1936), Fox (1939) and Vernberg (1959). 0.020l~
0.009' o.oo7'
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~.
~
~
o
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~,,,,,,.
--°m 0.002
0.00~
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I
I
log
FIG.
I
I
30 40 50 60 weight,
mg
I
I
I I
80 I00
I
200
I I ~) 300 400 5 0
nitrogen
1. Oxygenconsumptionratesofsixspeciesoftropiealseaurchins.Regression lines are fitted by the method of least squares.
The respiratory rate of Tripneustes from Barbados may be compared directly with the respiratory rates reported by Moore & McPherson (1965) from Miami. These authors found respiratory rates between 0.05 and 0.014-cms of O~/hr/test volume for urchins between 25 and 200 ml test volume at 30°C or approximately 0.070-0.020 mg O2/hr/test volume. The oxygen consumption rates of Tripneustes in Barbados, in terms of test volumes, were found to be 0.032-0.008 mg Oz/hr/test volume at 26-27°C. The rates of various sizes of the Miami specimens thus show oxygen consumption rates somewhat higher than the Barbados specimens although they were determined at temperatures 3-4°C higher. However, the growth rates of Tripneustes have been found to be higher in Barbados than in Miami (Lewis, 1958; Moore et al., 1963). The difference in respiratory rates between urchins which are infaunal and epifaunal in habit are consistent with the results for other marine invertebrates. Thorson (1936) found that epifaunal forms had higher oxygen consumption rates than did bottom-living species. The same results were noted by Sparck (1936) for lamellibranchs. A low respiratory rate for the irregular urchin Echinocardium has also been recorded by Montuori (1913).
652
JOHN B. LEWIS
Acknowledgement--I am grateful to the National Research Council of Canada for a grant in aid. REFERENCES BULLOCK T. H. (1955) Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev. 30, 311-342. FARMANFARMAIANA. (1959) T h e respiratory surface of the purple sea urchin (Strongylocentrotus purpuratus). Doctoral Dissertation, Stanford University. FARMANFARMAIANA. (1966) T h e respiratory physiology of echinoderms. In Physiology of Echinoderrnata (Edited by BOOLOOTIAN R. A.), pp. 245-265. Interscience, New York and London. F o x H. M. (1939) T h e activity and metabolism of poikilothermal animals in different latitudes--V. Proc. zool. Soc. Lond. A109, 141-156. GIESE A. C. 8¢ FARMANFARMAIANA. (1963) Resistance of the purple sea urchin to osmotic stress. Biol. Bull. 124, 182-192. GIESE A. C., FARMANFARMAIANA., HILDEN S. & DEOZEMAP. (1966) Respiration during the reproductive cycle in the sea urchin Strongylocentrotus purpuratus. Biol. Bull. 130, 192-201. LEwis J. B. (1958) T h e biology of the tropical sea urchin Tripneustes esculentus Leske in Barbados, British West Indies. Can. J. Zool. 36, 607-621. MONTUORI A. (1913) Les processus oxydatifs chez les animaux marins en rapport avec la loi de superficie. Arch. ital. Biol. 59, 213-234. MooRE H. B. (1966) Ecology of echinoids. In Physiology of Echinodermata (Edited by BOOLOOTXANR. A.), pp. 73-85. Interscience, New York and London. ~/[OORE H. B., JUTARET., JONES J. A., McPHERSON B. F. & ROPER C. F. E. (1963) A contribution to the biology of Tripneustes esculentus. Bull. mar. Sci. GulfCarib. 13 (2), 267-381. MooRE H. B. & McPHERSON B. F. (1965) A contribution to the study of the productivity of the urchins Tripneustes esculentus and Lytechinus variegatus. Bull. mar. Sci. I5, 855-871. PROSSER C. L. (1955) Physiological variation in animals. Biol. Rev. 30, 229-262. SCHOLANDER P. F., FLAGG W., WALTERS V. ~ IRVING L. (1953) Climatic adaptation in Arctic and tropical poikilotherms. Physiol. Zool. 26, 67-92. SPARCK T. (1936) On the relation between metabolism and temperature in some marine lamellibranchs, and its zoogeographical significance. K. danske Vidensh. Selsk., biol. Medd. 13, 1-27. THORSON G. (1936) T h e larval development, growth and metabolism of Arctic marine bottom invertebrates compared with those of other seas. Medd. Gronland 100, 1-155. VERNBERG F. J. (1959) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca--I I. Oxygen consumption of whole organisms. Biol. Bull. 117, 163-184. ZEUTrmN E. (1953) Oxygen uptake as related to body size in organisms. Quart. Rev. Biol. 28, 1-12.
SHORT COMMUNICATION COMPARATIVE RESPIRATION OF TROPICAL ECHINOIDS JOHN B. LEWIS Bellairs Research Institute of McGill University, St. James, Barbados
(Received 25 July 1967) Abstract--1. The rates of oxygen consumption of six species of tropical sea urchins were determined. 2. The oxygen consumption rates of three species of epifaunal, regular urchins were significantly higher than the rates of two infaunal, irregular species. 3. Oxygen consumption rates of a cidarid species which lacks peristomeal gills were intermediate between the other two groups. INTRODUCTION
RECENT review articles by Farmanfarmaian (1966) and by Moore (1966) have underlined the fact that the respiratory physiology of sea urchins is known for only a few species. Such information is restricted to the regular urchins, for example Strongylocentrotus (Farmanfarmaian, 1959; Giese & Farmanfarmaian, 1963; Giese et al., 1966) and Arbacia (Farmanfarmaian, 1966). The irregular urchins, such as the spatangoids and clypeastroids, have not been investigated nor is there information on comparative respiration between infaunal and epifaunal forms. Furthermore, with the exception of Tripneustes (Moore & McPherson, 1965) the respiratory physiology of tropical echinoids has not been investigated. The following study is a contribution to the comparative respiratory physiology of six species of tropical echinoids from varying ecological habitats and diverse taxa. METHODS AND MATERIALS
Freshly caught sea urchins of the following species were used for study: Eucidaris tribuloides (Lamarck), Echinometra lucunter (Linnaeus), Tripneustes esculentus Leske, Diadema antillarum Philippi, Brissus unicolor (Leske) and Mellita sexiesperforata (Leske). Specimens were acclimatized in concrete tanks in running sea water for 1-5 days before being used for experiments. Only active, healthy specimens which responded readily to external stimuli were collected. Twenty-five specimens of each species were placed for study in individual glass or polythene vessels in measured amounts of freshly filtered sea water which was approximately saturated by vigorously bubbling air into it. The water in each experimental vessel was 649
650
JOHN B. LEWIS
gently stirred with a magnetic stirrer. The experimental animal rested on a platform at the bottom of the vessel and a glass tube inserted into the water allowed the withdrawal of water into sample bottles. A layer of paraffin oil was added to the water surface in the vessel after the urchin had been introduced. Experiments were continued for 3-hr periods during daylight, at the same time of day. In order to minimize any effect of seasonal variations in metabolism the experiments were carried out over a period of approximately 2 months. At the end of the test period a 50 cm 3 sample of water was carefully withdrawn, to prevent bubbling, into a Pyrex flask. A control vessel without an urchin was treated in the same manner. Oxygen determinations were carried out immediately on the samples by oxygen electrodes manufactured by the Precision Scientific Co. of Chicago, Illinois. An accuracy of +__0.1 ml O2/I. is claimed by the manufacturers for this instrument. Test volumes, diameters and lengths were measured for each experimental animal. For a series of twelve animals of each species, nitrogen content of whole animals, less the gonad tissue, was determined by Kjeldahl digestions and subsequent ammonia determination by colorimetric titrations.
RESULTS The rates of oxygen consumption of various sizes of the six species of echinoids, at salinity 33~oo to 34~o and temperature 26--27°C, are shown in Fig. I. The regressions of log oxygen consumption on log total nitrogen of urchins show that the rates per unit weight of nitrogen decreased with increased size in all species. This is in agreement with the physiology of other echinoderms reported by Farmanfarmaian (1966) and of other animals (Zuethen, 1953). A comparison of the different oxygen consumption rates suggests that the six species can be divided into three groups. The regular sea urchins, Diadema, Echinometra and Tripneustes which are epifaunal forms, have the highest rates of oxygen consumption. The irregular urchins Mellita and Brissus are burrowing forms, i.e. infaunal in habitat, and have the lowest rates of oxygen consumption. Eucidaris, which unlike other regular sea urchins, lacks peristomeal gills, has a respiratory rate below that of the epifaunal urchins. Pooled group mean oxygen consumptions of the two infaunal forms were significantly different from the pooled group means of the epifaunal forms at the level P = 0-01. Similarly, the mean oxygen consumption of Eucidaris was significantly different from both the infaunal and epifaunal pooled group means. The respiratory rates of the six species are higher than the rates reported from colder water. Farmanfarmaian (1966) has listed the following rates for three coldwater species: Arbacia, 0.024; Strongylocentrotus, O.036;Echinocardium, 0.012 ml 02]hr/g wet wt. By converting these figures to weight of oxygen and allowing 2 per cent nitrogen of the wet weights of the urchins the above rates are equivalent to 0.0014, 0.0025 and 0-0008 mg O2/hour/mg N. The rates for Arbacia and Strongylocentrotus were determined at 20°C and that of Echinocardium at 15°C.
COMPARATIVE RESPIRATION OF TROPICAL ECHINOIDS
651
The lower rates of these species are consistent with the results of other authors' comparisons of cold-water and warm-water forms. Comparisons of respiration and metabolism of tropical and temperate or cold-water animals have been reviewed by Bullock (1955), Prosser (1955) and Scholander et al. (1953). Specific comparisons have been made by Thorson (1936), Sparck (1936), Fox (1939) and Vernberg (1959). 0.020l~
0.009' o.oo7'
riDne u
~
"~
~.
~
~
o
o 003
~,,,,,,.
--°m 0.002
0.00~
I
15
E
20
I
I
log
FIG.
I
I
30 40 50 60 weight,
mg
I
I
I I
80 I00
I
200
I I ~) 300 400 5 0
nitrogen
1. Oxygenconsumptionratesofsixspeciesoftropiealseaurchins.Regression lines are fitted by the method of least squares.
The respiratory rate of Tripneustes from Barbados may be compared directly with the respiratory rates reported by Moore & McPherson (1965) from Miami. These authors found respiratory rates between 0.05 and 0.014-cms of O~/hr/test volume for urchins between 25 and 200 ml test volume at 30°C or approximately 0.070-0.020 mg O2/hr/test volume. The oxygen consumption rates of Tripneustes in Barbados, in terms of test volumes, were found to be 0.032-0.008 mg Oz/hr/test volume at 26-27°C. The rates of various sizes of the Miami specimens thus show oxygen consumption rates somewhat higher than the Barbados specimens although they were determined at temperatures 3-4°C higher. However, the growth rates of Tripneustes have been found to be higher in Barbados than in Miami (Lewis, 1958; Moore et al., 1963). The difference in respiratory rates between urchins which are infaunal and epifaunal in habit are consistent with the results for other marine invertebrates. Thorson (1936) found that epifaunal forms had higher oxygen consumption rates than did bottom-living species. The same results were noted by Sparck (1936) for lamellibranchs. A low respiratory rate for the irregular urchin Echinocardium has also been recorded by Montuori (1913).
652
JOHN B. LEWIS
Acknowledgement--I am grateful to the National Research Council of Canada for a grant in aid. REFERENCES BULLOCK T. H. (1955) Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev. 30, 311-342. FARMANFARMAIANA. (1959) T h e respiratory surface of the purple sea urchin (Strongylocentrotus purpuratus). Doctoral Dissertation, Stanford University. FARMANFARMAIANA. (1966) T h e respiratory physiology of echinoderms. In Physiology of Echinoderrnata (Edited by BOOLOOTIAN R. A.), pp. 245-265. Interscience, New York and London. F o x H. M. (1939) T h e activity and metabolism of poikilothermal animals in different latitudes--V. Proc. zool. Soc. Lond. A109, 141-156. GIESE A. C. 8¢ FARMANFARMAIANA. (1963) Resistance of the purple sea urchin to osmotic stress. Biol. Bull. 124, 182-192. GIESE A. C., FARMANFARMAIANA., HILDEN S. & DEOZEMAP. (1966) Respiration during the reproductive cycle in the sea urchin Strongylocentrotus purpuratus. Biol. Bull. 130, 192-201. LEwis J. B. (1958) T h e biology of the tropical sea urchin Tripneustes esculentus Leske in Barbados, British West Indies. Can. J. Zool. 36, 607-621. MONTUORI A. (1913) Les processus oxydatifs chez les animaux marins en rapport avec la loi de superficie. Arch. ital. Biol. 59, 213-234. MooRE H. B. (1966) Ecology of echinoids. In Physiology of Echinodermata (Edited by BOOLOOTXANR. A.), pp. 73-85. Interscience, New York and London. ~/[OORE H. B., JUTARET., JONES J. A., McPHERSON B. F. & ROPER C. F. E. (1963) A contribution to the biology of Tripneustes esculentus. Bull. mar. Sci. GulfCarib. 13 (2), 267-381. MooRE H. B. & McPHERSON B. F. (1965) A contribution to the study of the productivity of the urchins Tripneustes esculentus and Lytechinus variegatus. Bull. mar. Sci. I5, 855-871. PROSSER C. L. (1955) Physiological variation in animals. Biol. Rev. 30, 229-262. SCHOLANDER P. F., FLAGG W., WALTERS V. ~ IRVING L. (1953) Climatic adaptation in Arctic and tropical poikilotherms. Physiol. Zool. 26, 67-92. SPARCK T. (1936) On the relation between metabolism and temperature in some marine lamellibranchs, and its zoogeographical significance. K. danske Vidensh. Selsk., biol. Medd. 13, 1-27. THORSON G. (1936) T h e larval development, growth and metabolism of Arctic marine bottom invertebrates compared with those of other seas. Medd. Gronland 100, 1-155. VERNBERG F. J. (1959) Studies on the physiological variation between tropical and temperate zone fiddler crabs of the genus Uca--I I. Oxygen consumption of whole organisms. Biol. Bull. 117, 163-184. ZEUTrmN E. (1953) Oxygen uptake as related to body size in organisms. Quart. Rev. Biol. 28, 1-12.