ComlJ. Biochem. Physiol,, 1975, Vol. 50A, pp. 149 to 151. Pergamon Press. Printed in Great Britain
OXYGEN CONSUMPTION AND VENTILATION OF THE ANTARCTIC ISOPOD GLYPTONOTUS BRUCE W. BELMAN Department of Biology, University of California, Santa Barbara 93106, U.S,A. (Received 8 October 1973) Abstract--1. The rate of oxygen consumption of the isopod Glyptonotur antarcticus Eights at - 1.8~ was measured with an oxygen electrode. The mean rate for eight experiments was 216+_24/d O~/g per hr. 2. This species apparently does not regulate its oxygen consumption under hypoxic conditions. 3. Ventilation frequency was determined by counting pleopod beats during the oxygen consumption determinations. The data show that Glyptonotus maintains a constant ventilation with decreasing oxygen availability.
INTRODUCTION WHILE involved in the study of the oxygen consumption of the Antarctic echinoderms (Belman & Giese, 1974), the opportunity presented itself to measure oxygen consumption in Glyptonotus antarcticus, an exceptionally large idotheid isopod common to the relatively shallow benthic community in the Antarctic (Dearborn, 1965). Knowledge of the biology of Glyptonotus is limted. Aspects of the feeding behavior and reproduction (Dearborn, 1967; Menzies & George, 1968; White, 1970), molting patterns (George, 1972) and thermal sensitivity (George, 1971) have been published. Dearborn (1965) in his study of Antarctic invertebrates noted that "the ecological role of Glyptonotus as a large predator and scavenger on the bottom perhaps most closely resembles that of crabs and lobsters in the benthic community of more temperate zones". The metabolism of Glyptonotus is therefore of interest not only because the species is a unique, stenothermally adapted form, but from the point of view of its role in the total community energetics of the shallow benthos in the Antarctic.
Coolant (50~ ethanol) was circulated through the cooling jackets with a Forma.Temp. Jr. refrigerated water-bath. The experimental temperature was maintained at -1.8+0.1~ The respirometers were stirred with slowly revolving magnetic stirring bars, separated from the animal by Plexiglas grids. All experiments were carried out in fresh sea water passed through 1'4o. 1 Whatman filter paper. Oxygen consumption wa~ continuously monitored after the methods of Childres~ (1968). As a control on microbial respiration, the animal wa,, removed from the chamber at the end of each experiment: air saturated sea water was added to replace its volume and the rate of oxygen consumption in the chamber was again measured for at least 2 hr. Negligible rates of oxgyen consumption were recorded, The rate of oxygen consumption for each experiment was computed on a wet-weight basis at selected oxygen partial pressures from the strip-chart recording~ of oxygen partial pressures in the respirometer. Pleopod beats were counted visually for 5 rain each time the concentration of oxygen in the respirometer dropped 1 ml O~/1., as determined from the strip chart recordings being made of oxygen tension. As each experiment lasted approximately 4 hr, this occurred at roughly 30-min intervals.
MATERIALS AND METHODS
RESULTS
Specimens of Glyptonotus were collected by hand while SCUBA diving near Capte Armitage, McMurdo Sound, Antarctica (79 ~ S, 166 ~ E) during October and November 1972, All animals were obtained in less than 20 m of water. Following collection, the specimens were transported in insulated containers to the Eklund Biology Laboratory at McMurdo Station, where they were placed in refrigerated sea water aquaria held at -1.8~ The animals were not fed. Oxygen consumption rates were determined for individual animals in closed respirorneters with Clarktype oxygen electrodes. The respirometers consisted of glass containers surrounded by Plexiglas cooling jackets,
In Fig. 1, the oxygen consumption rate (QO,) of Glyptonotus at - 1"8~ is plotted against the partial pressure of oxygen (ppO,). It appears f r o m the slope of the QO~ curve that this species is probably not regulating its QO, as the ppO2 drops. The change in slope of the QO, curve at 5.0 ml/1. ppO2 suggests that partial regulation may be occurring near this ppO,, but below 4.0 ml/1. ppOa the decrease in the QO, is nearly proportional to the decrease in ppO~ and no regulation is apparent. Also plotted in Fig. I are pleopod beat frequencies (ventilation rate), each point being the m e a n of eight
149
150
BRUCE W . BELMAN
measurements with the range plotted about the mean. While highly variable, these data show that Glyptonotus maintains a more or less constant ventilation rate as the ppO~ drops. At about 2.0 mlfl. ppO, the rate drops off rapidly,
isopods and significantly lower than that of the tropical isopods. Therefore, there appears to b~ considerable metabolic adaptation in both Antarctic and Arctic isopods relative to tropical isopods. This conclusion is in keeping with the general hypothesis
480
IC>o
4PO
zs ~
560
-300
~ i h / m /d.
~40
O~
g .E ~o ~
//
ISO 120
o
60
I ,.I-
~.0
g.o
]
3.0
l
4,0
I
~.o
r
i
60
70
pO 2 - m I Oz/[
Fig. 1. Oxygen consumption in/~l O~/g per hr at - 1"8~ for the isopod G. antarctieu# ( ~ ) and pleopod-bcat frequency in beats/min (- . . . . ); both plotted against oxygen tension (ppO~, abscissa) In ml O2/1. Means are for eight experiments. Single standard deviation units are plotted about the mean QO2's. The range is plotted about the pleopod-beat frequency measurements. The mean percentage of saturation of dissolved oxygen of the sea water near McMurdo Station is 69 per cent with a range of only 6 per cent (Tressler, 1964). Since this is the oxygen level at which these animals occur, the mean QO~ has been calculated from the data in Fig. 1 at the corresponding ppOs (5.0 ml Odl.). For 25-30 g (wet weight) Glyptonotus at - 1.8~ the mean QO~ is 2 1 6 + 2 4 / 4 0 ~ / g per hr. DISCUSSION In Table 1, the mean QO ~of Glyptonotus at - 1.8~ is compared with the mean QO2 of both Arctic and tropical isopods. While the differences in size of these isopods is large and size alone affects the QOs (Wolvekamp & Waterman, 1960), this comparison does show that the mean QO, of Glyptonotus is of the same order of magnitude as that of the Arctic
Of climatic adaptation stated by Scholander et al. (1953). Marine isopods, as well as other crustaceans which tend to regulate their QO, under hypoxic conditions, usually increase the rate of ventilation as the available oxygen decreases, while non-regulating crustaceans, such as semi-terrestrial isopods and the homarid lobsters, do not (Walshe-Maetz, 1952; Thomas, 1954). The response o f the ventilation mechanism in Glyptonotus to hypoxia suggests nonregulation, as in semi-terrestrial isopods (WalsheMaetz, 1952). The QO, curve (Fig. 1) also shows a generally non-regulatory pattern. Since the oxygen tension of the waters in which this species occurs remain uniform at 69 per cent saturation (Tressler, 1964), there would appear to be n o adaptive significance to regulating oxygen consumption during hypoxic conditions.
Table 1. O~ consumption of isopods from polar and tropicalregions Species Glyptonotus (Antarctica) Mestdothea entomon (Alaska) Roeinela signata (West Indies)
Temperature (~ - 1.8 0 30
* Calculated from the author's data.
Wet wt (g) 25 1 0'05
QOs (~I O,/g per hr) 216_+24 260_.+120 840 + I10
Reference This paper Scholander et aL (1953)* Seholander et al. (1953)*
Oxygen consumption of Glyptonotua The fall of Glyptonottts' pleopod beat frequency below 2'0 nil O./1. (Fig. 1) is typical of the responses of crustacean ventilatory mechanisms to very low oxygen (Wolvekamp & Waterman, 1960). While the responsible mechanism is not understood, oxygen availability to the neural centers is indicated since the driving mechanisms of the oscillatory neurons in other crustacea are very highly oxygen sensitive (Mendleson, 1971).
Acknowledgements--This research was conducted under Antarctic NSF Grant No. GA4458 to A. C. Giese of Stanford University. Special thanks 0.re given to David Checkly and A. L. DeVries, who assisted in the diving program, to U.S. Navy Task Force 43 for logistical support and to Professor Giese for reviewing the manuscript. REFERENCES BELMANB, W. & GmsE A. C, (1974) Oxygen consumption of an asteroid and an echinoid fi'om the Antarctic. BioL Bull. 146, 157-164. CHILDRES$J. J. (1968) The respiratory physiology of the oxygen minimum layer mysid, Gnathophausia tngens. Doctoral dissertation, Stanford University. D~ARnORNJ. H. (1965) Ecological and faunistie investigations of the marine benthos at McMurdo Sound, Antarctica. Doctoral dissertation, Stanford University. DnARBOrtN J. H. (1967) Food and reproduction of Glyptonotus antarctlcus (Crustacea, Isopoda) at McMurdo Sound, Antarctica. Trans. R. See. N.Z. 18, 163-168. G~oRo~ R. Y. (1971) Thermal sensitivity of hyposychral species of Antarctic and high Arctic marine Crustacea. Abstracts of contributed papers, Proc. Joint Oceanogr. Assembly (Tokyo, 1970), D2-C-8, p. 474.
151
GEORO• g. Y. (1972) Biphasic moulting in isopod crustaeea and the finding of an unusual mode of moulting in the Antarctic genus alyptonotus. J. Nat. Hist. 6, 651-656. MEtCom.soN M. (1971) Oscillator neurons in crustacean ganglia. Science, Wash. 171, 1170-1173. M~Nzms R. J. & GEOROER. Y. (1968) Investigations of isopod crustaceans of Erebus Bay, McMurdo Sound. Antaret. J.U.W. 3, 129. SCHOLANDERP. F., FLAGOW., WALTERSV. dk IRVINGL. (1953) Climatic adaptation in Arctic and tropical poikilotherms. Physiol. Zo61. 26, 67-92. THOMASI--I.J. (1954) The oxygen uptake of the lobster (Homarus vulgarts Edw.). J, exp. BioL 31, 228-251. Ta~SSLER W. L, (1964) Marine bottom productivity at MeMurdo Sound. In Btologte Antaretique (Edited by CAP.RICKg., HOLDOATEM. & PREVOSTJ.). Hermann, Paris, WALSHI~-MAETZB. M. (1952) Environment and respiratory control in certain crustacea. Nature, Lend. 169, 750-751. WOLWKAMI'H. P. & WAT~aMANT. H. (1960) Respiration. Inl~hy.~'lologyof Crustaeea (Edited by WATERMAN T. H.), pp. 35-100. Academic Press, Now York. WHITE M. G. (1970) Aspects of the breeding biology of Glyptonotus antarctlcus (Eights) (Crustaeea, Isopoda) at Sigby Island, South Orkney Islands. In Antarctic Ecology (Edited by HOLOOAT~M.), Vol, I, pp. 279-285. Academic Press, New York.
Key Word Index--Oxygen consumption; Glyptonotus antaretieua; Antarctica; ventilation; crustacean respiration.
OXYGEN CONSUMPTION AND VENTILATION OF THE ANTARCTIC ISOPOD GLYPTONOTUS BRUCE W. BELMAN Department of Biology, University of California, Santa Barbara 93106, U.S,A. (Received 8 October 1973) Abstract--1. The rate of oxygen consumption of the isopod Glyptonotur antarcticus Eights at - 1.8~ was measured with an oxygen electrode. The mean rate for eight experiments was 216+_24/d O~/g per hr. 2. This species apparently does not regulate its oxygen consumption under hypoxic conditions. 3. Ventilation frequency was determined by counting pleopod beats during the oxygen consumption determinations. The data show that Glyptonotus maintains a constant ventilation with decreasing oxygen availability.
INTRODUCTION WHILE involved in the study of the oxygen consumption of the Antarctic echinoderms (Belman & Giese, 1974), the opportunity presented itself to measure oxygen consumption in Glyptonotus antarcticus, an exceptionally large idotheid isopod common to the relatively shallow benthic community in the Antarctic (Dearborn, 1965). Knowledge of the biology of Glyptonotus is limted. Aspects of the feeding behavior and reproduction (Dearborn, 1967; Menzies & George, 1968; White, 1970), molting patterns (George, 1972) and thermal sensitivity (George, 1971) have been published. Dearborn (1965) in his study of Antarctic invertebrates noted that "the ecological role of Glyptonotus as a large predator and scavenger on the bottom perhaps most closely resembles that of crabs and lobsters in the benthic community of more temperate zones". The metabolism of Glyptonotus is therefore of interest not only because the species is a unique, stenothermally adapted form, but from the point of view of its role in the total community energetics of the shallow benthos in the Antarctic.
Coolant (50~ ethanol) was circulated through the cooling jackets with a Forma.Temp. Jr. refrigerated water-bath. The experimental temperature was maintained at -1.8+0.1~ The respirometers were stirred with slowly revolving magnetic stirring bars, separated from the animal by Plexiglas grids. All experiments were carried out in fresh sea water passed through 1'4o. 1 Whatman filter paper. Oxygen consumption wa~ continuously monitored after the methods of Childres~ (1968). As a control on microbial respiration, the animal wa,, removed from the chamber at the end of each experiment: air saturated sea water was added to replace its volume and the rate of oxygen consumption in the chamber was again measured for at least 2 hr. Negligible rates of oxgyen consumption were recorded, The rate of oxygen consumption for each experiment was computed on a wet-weight basis at selected oxygen partial pressures from the strip-chart recording~ of oxygen partial pressures in the respirometer. Pleopod beats were counted visually for 5 rain each time the concentration of oxygen in the respirometer dropped 1 ml O~/1., as determined from the strip chart recordings being made of oxygen tension. As each experiment lasted approximately 4 hr, this occurred at roughly 30-min intervals.
MATERIALS AND METHODS
RESULTS
Specimens of Glyptonotus were collected by hand while SCUBA diving near Capte Armitage, McMurdo Sound, Antarctica (79 ~ S, 166 ~ E) during October and November 1972, All animals were obtained in less than 20 m of water. Following collection, the specimens were transported in insulated containers to the Eklund Biology Laboratory at McMurdo Station, where they were placed in refrigerated sea water aquaria held at -1.8~ The animals were not fed. Oxygen consumption rates were determined for individual animals in closed respirorneters with Clarktype oxygen electrodes. The respirometers consisted of glass containers surrounded by Plexiglas cooling jackets,
In Fig. 1, the oxygen consumption rate (QO,) of Glyptonotus at - 1"8~ is plotted against the partial pressure of oxygen (ppO,). It appears f r o m the slope of the QO~ curve that this species is probably not regulating its QO, as the ppO2 drops. The change in slope of the QO, curve at 5.0 ml/1. ppO2 suggests that partial regulation may be occurring near this ppO,, but below 4.0 ml/1. ppOa the decrease in the QO, is nearly proportional to the decrease in ppO~ and no regulation is apparent. Also plotted in Fig. I are pleopod beat frequencies (ventilation rate), each point being the m e a n of eight
149
150
BRUCE W . BELMAN
measurements with the range plotted about the mean. While highly variable, these data show that Glyptonotus maintains a more or less constant ventilation rate as the ppO~ drops. At about 2.0 mlfl. ppO, the rate drops off rapidly,
isopods and significantly lower than that of the tropical isopods. Therefore, there appears to b~ considerable metabolic adaptation in both Antarctic and Arctic isopods relative to tropical isopods. This conclusion is in keeping with the general hypothesis
480
IC>o
4PO
zs ~
560
-300
~ i h / m /d.
~40
O~
g .E ~o ~
//
ISO 120
o
60
I ,.I-
~.0
g.o
]
3.0
l
4,0
I
~.o
r
i
60
70
pO 2 - m I Oz/[
Fig. 1. Oxygen consumption in/~l O~/g per hr at - 1"8~ for the isopod G. antarctieu# ( ~ ) and pleopod-bcat frequency in beats/min (- . . . . ); both plotted against oxygen tension (ppO~, abscissa) In ml O2/1. Means are for eight experiments. Single standard deviation units are plotted about the mean QO2's. The range is plotted about the pleopod-beat frequency measurements. The mean percentage of saturation of dissolved oxygen of the sea water near McMurdo Station is 69 per cent with a range of only 6 per cent (Tressler, 1964). Since this is the oxygen level at which these animals occur, the mean QO~ has been calculated from the data in Fig. 1 at the corresponding ppOs (5.0 ml Odl.). For 25-30 g (wet weight) Glyptonotus at - 1.8~ the mean QO~ is 2 1 6 + 2 4 / 4 0 ~ / g per hr. DISCUSSION In Table 1, the mean QO ~of Glyptonotus at - 1.8~ is compared with the mean QO2 of both Arctic and tropical isopods. While the differences in size of these isopods is large and size alone affects the QOs (Wolvekamp & Waterman, 1960), this comparison does show that the mean QO, of Glyptonotus is of the same order of magnitude as that of the Arctic
Of climatic adaptation stated by Scholander et al. (1953). Marine isopods, as well as other crustaceans which tend to regulate their QO, under hypoxic conditions, usually increase the rate of ventilation as the available oxygen decreases, while non-regulating crustaceans, such as semi-terrestrial isopods and the homarid lobsters, do not (Walshe-Maetz, 1952; Thomas, 1954). The response o f the ventilation mechanism in Glyptonotus to hypoxia suggests nonregulation, as in semi-terrestrial isopods (WalsheMaetz, 1952). The QO, curve (Fig. 1) also shows a generally non-regulatory pattern. Since the oxygen tension of the waters in which this species occurs remain uniform at 69 per cent saturation (Tressler, 1964), there would appear to be n o adaptive significance to regulating oxygen consumption during hypoxic conditions.
Table 1. O~ consumption of isopods from polar and tropicalregions Species Glyptonotus (Antarctica) Mestdothea entomon (Alaska) Roeinela signata (West Indies)
Temperature (~ - 1.8 0 30
* Calculated from the author's data.
Wet wt (g) 25 1 0'05
QOs (~I O,/g per hr) 216_+24 260_.+120 840 + I10
Reference This paper Scholander et aL (1953)* Seholander et al. (1953)*
Oxygen consumption of Glyptonotua The fall of Glyptonottts' pleopod beat frequency below 2'0 nil O./1. (Fig. 1) is typical of the responses of crustacean ventilatory mechanisms to very low oxygen (Wolvekamp & Waterman, 1960). While the responsible mechanism is not understood, oxygen availability to the neural centers is indicated since the driving mechanisms of the oscillatory neurons in other crustacea are very highly oxygen sensitive (Mendleson, 1971).
Acknowledgements--This research was conducted under Antarctic NSF Grant No. GA4458 to A. C. Giese of Stanford University. Special thanks 0.re given to David Checkly and A. L. DeVries, who assisted in the diving program, to U.S. Navy Task Force 43 for logistical support and to Professor Giese for reviewing the manuscript. REFERENCES BELMANB, W. & GmsE A. C, (1974) Oxygen consumption of an asteroid and an echinoid fi'om the Antarctic. BioL Bull. 146, 157-164. CHILDRES$J. J. (1968) The respiratory physiology of the oxygen minimum layer mysid, Gnathophausia tngens. Doctoral dissertation, Stanford University. D~ARnORNJ. H. (1965) Ecological and faunistie investigations of the marine benthos at McMurdo Sound, Antarctica. Doctoral dissertation, Stanford University. DnARBOrtN J. H. (1967) Food and reproduction of Glyptonotus antarctlcus (Crustacea, Isopoda) at McMurdo Sound, Antarctica. Trans. R. See. N.Z. 18, 163-168. G~oRo~ R. Y. (1971) Thermal sensitivity of hyposychral species of Antarctic and high Arctic marine Crustacea. Abstracts of contributed papers, Proc. Joint Oceanogr. Assembly (Tokyo, 1970), D2-C-8, p. 474.
151
GEORO• g. Y. (1972) Biphasic moulting in isopod crustaeea and the finding of an unusual mode of moulting in the Antarctic genus alyptonotus. J. Nat. Hist. 6, 651-656. MEtCom.soN M. (1971) Oscillator neurons in crustacean ganglia. Science, Wash. 171, 1170-1173. M~Nzms R. J. & GEOROER. Y. (1968) Investigations of isopod crustaceans of Erebus Bay, McMurdo Sound. Antaret. J.U.W. 3, 129. SCHOLANDERP. F., FLAGOW., WALTERSV. dk IRVINGL. (1953) Climatic adaptation in Arctic and tropical poikilotherms. Physiol. Zo61. 26, 67-92. THOMASI--I.J. (1954) The oxygen uptake of the lobster (Homarus vulgarts Edw.). J, exp. BioL 31, 228-251. Ta~SSLER W. L, (1964) Marine bottom productivity at MeMurdo Sound. In Btologte Antaretique (Edited by CAP.RICKg., HOLDOATEM. & PREVOSTJ.). Hermann, Paris, WALSHI~-MAETZB. M. (1952) Environment and respiratory control in certain crustacea. Nature, Lend. 169, 750-751. WOLWKAMI'H. P. & WAT~aMANT. H. (1960) Respiration. Inl~hy.~'lologyof Crustaeea (Edited by WATERMAN T. H.), pp. 35-100. Academic Press, Now York. WHITE M. G. (1970) Aspects of the breeding biology of Glyptonotus antarctlcus (Eights) (Crustaeea, Isopoda) at Sigby Island, South Orkney Islands. In Antarctic Ecology (Edited by HOLOOAT~M.), Vol, I, pp. 279-285. Academic Press, New York.
Key Word Index--Oxygen consumption; Glyptonotus antaretieua; Antarctica; ventilation; crustacean respiration.
