Table Of ContentZOOLOGICAL SCIENCE 8: 625-638 (1991) i L991 Zoological Societ) ofJaps
REVIEW
Endocrine Regulation of the Oxidative Metabolism in
Poikilothermic vertebrates
B. B. P. Gupta and J. P. Thapliyal1
Environmental Endocrinology Lab., Dept. of Zoology, North-Eastern
Hill University, Shillong-793 014, India
other to different extents under different
INTRODUCTION
physiological/environmental conditions to meet
Vertebrateshaveevolveda numberofmetabolic the energy demand in the most suitable way [5-9].
pathways to meet various requirements for suc- A minimum metabolic rate operates even in the
cessful survival. The oxidative metabolism is re- absence ofphysical performance, and is termed as
sponsible for cellular oxidation of metabolic subs- obligatory, basal, maintenance or standard meta-
trates and generation of energy which is stored in bolic rate (SMR) [9]. SMR is essential to meet the
the form of ATP. The entire process of the minimum energy demand for vital processes like
biological oxidation (oxidative metabolism) in- ventilation, circulation and the maintenance of
\olves a number of enzymes, co-enzymes and ionic gradients across the cellular and sub-cellular
metabolic substrates, and consumes oxygen at the membranes. Recent findings suggest that the
mitochondrial level. Further, the amount ofener- metabolic reactions are nearly similar in all verte-
gy produced is directly proportional to the amount brates with respect to the metabolic substrates.
of oxygen consumed. Therefore, the rate of ox- enzymes, co-factors, activators and inhibitors with
ygen consumption actsasan indexofthe metabolic few exceptions [10]. However, SMR is generally
rate oxidative metabolism, and also reflects over- higher in homeotherms (birds and mammals) as
all physiological status of an organism. compared to the poikilothermic vertebrates
The metabolic rate (MR)ofvertebratesdepends (fishes, amphibians and reptiles). A high
on a number of external (environmental) and homeothermic SMR is essential for maintaining
internal (physiological) factors, i.e., temperature, relatively a constant body temperature. Poiki-
photoperiod. food, activity, body size and weight, lotherms are unable to maintain then bode
age, sex. time of the day and month of the year. temperature that changes with ambient tempera-
blood circulation and phylogeny etc. [1-3). The tures. The neuroendocrine s\stem is involoved in
neuroendocrine system plays an important role in metabolic regualtion in both homeotherms and
the regulation of the metabolic rate. Hormones poikilotherms [11-13]. In the present article, we
and neurohormones act at cellular and sub-cellular have tried to give a brief account of the involve-
levels and alterthe oxidative metabolism primaril) ment ol various hormones m the regulation <it the
b\ influencing the activities of enzymes of the oxidative metabolism of the poikilothermic verte
oxidative pathways [4]. Central nervous system brates.
(CNS) and endocrine system interact with each
Thyroid hormones and the oxidative metabol
Received: April 13. 1991
1 Present address: B 1 2 Shccsh Mahal Colnm Notwithstanding variations m morph< >l . oca-
Kamachha.Varanasi-221 010 India. tion and organization of the tin id m
626 B. B. P. Gupta and J. P. Thapliyal
different classes ofvertebrates, the follicularstruc- for the first time, importance of acclimation
ture and function in relation to iodide metabolism temperature came to light [82]. The information
and hormone synthesis as well as storage have that thyroid hormones are calorigenically effective
been largely conserved. However, the same hor- only at comparatively high (at or above 25°C) and
—
monal molecules triiodothyronine (T3) and thyr- ineffective at low (20°C or below) temperatures in
—
oxine (T4) produce a wide range of diverse the lizard, Anolis carolinensis reopened the issue
biological actions. Thyroid hormonesplayamajor ofthe possible involvement ofthe thyroid glandin
role in the regulation of SMR of birds and mam- the energy metabolism of the ectotherms, and
mals [5, 11, 12, 14-17]. These hormones are also providedastrongbaseforfurtherstudiesincluding
essential for the calorigenic action of the catecho- review of the previously reported negative results
lamines in mammalian species [5, 7, 11, 18]. [8, 13, 20, 23, 24, 83].
However, unlike in the homeotherms, the calor-
igenic function of the thyroid hormones in the
poikilothermic vertebrates is not unequivocally Temperature-dependent calorigenic effect
ofthyroid hormones
accepted [8, 19-24].
In the last six decades, numerous attempts have Most of the earlier investigations were carried
been made to establish the calorigenic action of outundercontrolled laboratory conditions, butno
thyroid hormones in the ectothermic vertebrates. importance was given to the acclimation tempera-
In the first few decades, a large number ofinvesti- tures. As mentioned earlier, the decisive role
gators studied the effects of experimentally- played by the ambient temperature became evi-
induced hypo- and hyper-thyroidism on the meta- dent when the effects of thyroxine and thyroidec-
bolic rate of a large number offishes, amphibians tomywerestudiedontherespiratoryrateofAnolis
and reptilian species, and reported both positive carolinensis at high and low temperatures [82].
and negative results. Several investigators have Both administration of thyroxine and thyroidec-
reported stimulation following administration of tomy were found to be effective in lizards main-
thyroid hormones and decrease in the respiratory tained at high (ecritic) temperature and ineffective
rate following thyroidectomy (chemical/surgical/ at low temperature. Subsequently, temperature-
radiological) in a number of piscine species [25- dependent effects of thyroid hormones and thyr-
45]. In contrast to these reports, an equally large oidectomy on the oxidative metabolism was con-
number of scientists could not find any effect of firmed in Lacerta muralis [84], Eumeces obsoletus
thyroid hormones and thyroidectomy on the SMR [85], Eumecesfaciatus [86], Sceloporuscyanogenys
ofmany species offishes [46-62]. Similarly, many [87], and Natrix rhombifera [88]. Similarly, Tha-
workers could not find any change in the SMR of pliyal and co-workers have reported temperature-
amphibian species following the administration of dependent stimulatory effect of thyroxine and in-
the thyroid hormones and thyroidectomy [63-70]. hibitory effect ofthyroidectomy on the respiratory
Further, both endogenous and exogenous thyroid rateofthewhole body, liverandskeletalmuscleof
hormonesreportedlyhavenoeffectonthe SMRof four tropical reptiles, i.e., Calotes versicolor,
metamorphosing amphibian larvae [69, 71-74]. Hemidactylus flaviviridis, Natrix piscator, and
Notwithstanding these negative results, the re- Ptyas mucosus [83, 89, 91-100].
spiratory rate has been found to be stimulated by When acclimation temperature was considered,
thyroid hormones in many amphibians [75-80]. even in amphibians the temperature-dependent
As in fishes and amphibians, even in reptiles a few effect of thyroid hormones and thyroidectomy on
early attempts made to stimulate the rate of ox- the metabolic rate became evident. Thyroxine
ygen consumption by thyroid hormones were not administration and thyroidectomy were found to
successful [26, 47, 81]. Nosatisfactoryexplanation be effective at higt temperatures and ineffective at
was provided for the contradictory reports regard- low ambient temperatures in influencing the SMR
ing the calorigenic effect of thyroid hormones in of a number of amphibian species [101-106]. Re-
the poikilothermicvertebrates till latefiftieswhen, cently, both in vivo andin vitro treatmentswithT3
Hormones and ectothermic Metabolic Rate 627
and T4 did not stimulate the oxygen consumption cellular levels [8. 83]. This suggestion is further
rate of liver and muscle tissues of the Indian supported by a numberofrecent reports indicating
streaked frog, Rana timnocharis exposed to a that both T3 and T4 stimulate a wide range of
natural temperature of 15°C (during the hiberna- mitochondrial enzymes in a number of tissues
tion phase) and 21°C (during the post-hibernation (skeletal muscle, cardiac muscle, liver, gills, brain,
phase) [107]. However, both T3 andT4 stimulated kidney etc.) of fishes [40, 43, 111-113], amphi-
tissues respiration of the toad. Bufo melanostictus bians [114-118], and reptiles [119-130]. Thyroid
during the post-hibernation phase (25°C) but not hormonesare alsoinvolved in the regulationofthe
during the hibernation phase (15"C) [108]. These intermediary metabolism of the cold-blooded
findings suggest that the calorigenic effect of the vertebrates [20, 23, 24, 89, 90, 105, 131-146].
thyroid hormones may vary with the species and Involvement ofthese hormones in both intermedi-
temperatures. ary and oxidative metabolisms seems to suggest
A strong correlation has been reported between that even the metabolic function of the thyroid
the thyroid activity and the oxygen consumption gland has been conserved to a greater extent
rate in an airbreathingsiluroid fish, Heteropneustis during the complex course of evolution.
fossilis [45]. In the same study, thyroxine adminis- After monitoring the circulating level ofthyrox-
tration increased and treatment with thiouracil ine following administration of 200 ng T4/g body
decreasedthe rateofwhole bodyoxygen consump- weight in a lizard (Dipsosaurus dorsalis), John-
tion under both surfacing-allowed and surfacing- Alder [119] concluded that in most of the earlier
not allowed conditions. In a recent study, in vivo studies, pharmacological doses of thyroid hor-
and in vitro administrations of T3 and T4 did not mones were used, therefore, the physiological
stimulate the respiratory rate of liver and skeletal significance of those studies remained doubtful.
muscle tissues of an air breathing fish. Clarias Further, these studieswere conducted undersimu-
batrachus maintained at 16°C [109]. This report lated high and/or low temperatures, and no
again confirms the ineffectiveness of thyroid hor- attempt was made to study the metaboliceffectsof
mones at low temperature. thyroid hormones under natural climatic condi-
It is. thus, apparent from the studies conducted tions with reference to the annual activity cycle.
at different temperatures that thyroid hormones Therefore, we tried to understand the physiologic-
are involved in the regulation of the oxidative al importance ofthyroid hormones in the oxidative
metabolism of the ectotherms exposed to high metabolism ofthe Indian garden lizard. Effects of
(favourable) temperatures. Moreover, the calor- thyroidectomy and administration of T4 were stu-
igenic ineffectiveness is conspicuous in all most all died on the respiratory rate ofthe whole body and
studies conducted at low ambient temperatures or tissues (liver, skeletal muscle, kidney and brain) of
during the hibernation phase (cold winter theeuthyroidicand thyroidectomized lizardsmain-
months). So far there is no information about the tained under natural temperatures and photo-
mechanism by which temperature influences the periods during every month (January to Decem-
sensitivity of the oxidative pathways for thyroid ber) ofthe year [83]. We also used a comparative-
hormones in the ectothermic vertebrates. Since ly low dose ofT4 (66 ng/g body weight) which has
temperature regulates a numberofseasonal events been found recently to be well within the physiolo-
(including activity, molt and reproduction) in gical range [124-126. 130]. Findings of the study
poikilotherms. therefore, the calorigenic action of clearly suggest that the calorigeniceffect ofthyroid
thyroid hormones in these vertebrates might be hormones is associated with the annual activit)
related to energy dependnet annual events [83. cycle, and seems to be independent of the annual
110]. rhythm of temperature. Further, different tissues
In vitro stimulation of oxygen uptake of various exhibit different annual sensitivity rhythms lor
tissues of fishes, amphibians and reptiles strongly thyroxine [83].
suggests that thyroid hormones stimulate oxidative At present it is difficult to explain the tact
processe by acting directly at cellular and or sub- mechanism responsible for the chang< itiv-
628 B. B. P. Gupta and J. P. Thapliyal
itv of tissues for T4 with the changing seasons. lothermic vertebrates. Now attempts should be
However, changes in the nuclear and/or made todefine the mechanism that regulatessensi-
mitochondrial receptors, alterations in the binding tivity of the metabolic pathways for thyroid hor-
siteson the receptorproteins, degree ofsaturation mones in cold-blooded vertebrates.
of receptors with the endogenous thyroid hor-
mones, metabolic state of tissues, availability of
Mechanisms ofcalorigenic action of
substrates and energy demand, separately or in
thyroid hormones
combination(s), might be responsible for the
annual changes in tissue sensitivity for thyroxine. Thyroid hormones have multiple sites of action
So far there is no information about the annual within the body, even within a cell, and multiple
rhythms of tissues sensitivity for T3. Significant mechanisms of action [17]. Three basic mechan-
stimulation by a physiological dose of thyroxine isms are reportedly involved in the calorigenic
and marked decrease following thyroidectomy in action of thyroid hormones in mammals [7, 17].
the respiratory rate of the whole body and tissues These are (i) rapid stimulation of mitochondrial
(liver and skeletal muscle) during the entire active respiration under coupled state [148-159], (ii) an
phase (post-hibernation to pre-hibernation), when increase in the total mitochondrial content of
energy demand for various purposes (foraging, tissues [160-163], and (iii) an increase in the
offence/deffence, courtship etc.) is high [147], activity of membrane-bound enzyme Na+-K+-
strongly favour a physiological role of thyroid ATPase [164-171]. These mechanisms are not
hormones in regulation of the oxidative metabol- delineated, therefore, may operate simultaneous-
ism of the lizard as suggested in earlier studies. ly. Further, it is also difficult to assess the relative
Thyroidectomy is found to increase the tissue contribution of each mechanism in mammalian
sensitivity forT4 [83]. This is furthersupported by calorigenesis. Thyroidhormonesrapidlystimulate
the fact that thyroxine increases the SMR of the respiratory rate by acitng at mitochondria [17,
thyroidectomizedbut notoftheeuthyroidiclizards 157]. This suggestion is further supported by
[124]. dissociation between nuclear receptor concentra-
Implantation ofT4 to release physiological dose tion and stimulation ofoxygen consumption in the
in the field active lizards has been reported to neonatal rat brain, and also by the absence of
stimulate SMR, Vo2max, runningendurance anda mitochondrial thyr—oid hormone recptors in brain,
numberofoxidative enzymes [122, 123, 125, 130]. testis and spleen the tissues in which oxygen
However, the same dose of implanted thyroxine consumption is not stimulated by thyroid hor-
could not increase the SMR of the captive lizards mones [156]. Nuclear receptors of thyroid hor-
significantly. This might be probably due to the mones are supposed to be involved in anabolic
difference between the natural thermal range effects (growth, differentiation, maturation and
(23.6°C to 40.8°C) and the thermal range (19.3°C cell maintenance) andprolongedcalorigenesis [17,
to 34.6°C) provided under captivity. Alternative- 157]. So far only a few attempts have been made
ly, stress-induced starvation and/or decreased to investigate the calorigenic mechasnisms ofthyr-
muscularactivity undercaptive condition mightbe oid hormones in the ectothermic vertebrates. In
responsible for the insignificant increase in the the Indian garden lizard a single dose ofthyroxine
SMR. Starvation has been reported to decrease produces early (within 1 hr) and delayed (after 24
the thyroid hormone receptors in mammals [17]. hr) stimulatory effects on the respiratory rate of
Further, starvation also blocks the stimulatory the liver and skeletal muscle tissues [89]. While
effects ofT3 and T4 on the respiratory rate ofliver the early stimulatory effect of T4 is blocked by
and skeletal muscle in a frog, Rana limnocharis ouabain (an inhibitor of Na+-K+-ATPase), man-
maintained at 28°C (Gupta, unpublished). Thus, itol (an inhibitor ofNa+ transport), and chloram-
in addition to other factors, low temperatures and phenicol (an inhibitor of mitochondrial protein
stress-induced starvation/anorexia also can negate synthesis), the delayed stimulatory effect of thyr-
thecalorigeniceffectofthyroid hormonesin poiki- oxine on the tissues respiration is inhibited by
Hormones and ectothermic Metabolic Rate 629
actinomycin D (an inhibitor of nuclear transcrip- ine was calorigenically ineffective. The annual
tion) [172, Sharan. Gupta and Thapliyal, unpub- sensitivity rhythms oi the tissues for testosterone
lished]. These findings suggest that even in the were found to be different. Castration decreased
lower vertebrates, thyroid hormones stimulate the the respiratory rate of the whole body, liver and
oxidative metabolism mainly by acitng at cell brain significantly during the post-hibeination
membrane, mitochondrial and nuclear levels. phase, and of the skeletal muscle and kidney
Now attempts should be made to find out the during all the months except December and Janu-
relative importance of these mechanisms in the ary (hibernation phase). Testosterone administra-
cold-blooded animals with special reference to the tion invariably reversed the ill-effect of castration
ambient temperature and the phases of the annual on the oxygen consumption rate ofthe whole body
activity cycle. and the tissues. Testosterone also reversed de-
crease in the respiratory rate following thyroidec-
tomy. Stimulation ofrespiratory ratesofthe whole
Calorigenic action of gonadal hormones
body and tissuesofthe thyroidectomi/ed lizards by
Gondal steroids play a major role in the de- testosterone strongly suggests a direct role of
velopment, growth, maturation and maintenance gonadal hormones in the energy metabolism ofthe
of the primary and secondary sex organs and sex lizards during the cold and non-breeding phase.
characters in all vertebrates. In addition, sex Testosterone has been found to be calorigenic
hormones have also been reported to influence even at the simulated low temperature (15°C)
metabolism ofsome othertissuesofhomeotherms. where thyroxine failed in stimulating the oxygen
In poikilotherms, gonadal hormones seem to be uptake rate [95]. Calorigenic effect of gonadal
involved in the regulation ofthe metabolic rate [8, hormones seems to be determined by the energy
B3, 107]. Administration of testosterone in males demand of various tissues. Recently testosterone
and estradiol in females is followed by stimulation has been reported to stimulate a number of
of respiratory rate in a number of fishes [50, 60, mitochondrial enzymes in the liver of the Indian
109, 173-175]. In some ofthe fishes, hypophysec- garden lizard [129].
tomy resulted in decreased metabolic rate, pre- In vivo and in vitro administration of testoster-
sumably due to decreased levels of gonadal hor- one and estradiol in low doses also stimulate the
mones [33. 176-178]. respiratory rate ofliver and skeletal muscle tissues
In a series of in vivo and in vitro experiments, ofboth the sexesofthe Indian streaked frog. Rana
Thapliyal and co-workers have reported significant limnocharis [107]. Testosterone is found to be
increase in respiratory rates of vital tissues follow- more potent in males and estradiol in females.
ing administration of gonadal hormones, and re- Gonadal hormones stimulate tissues oxygen con-
duction in the respiratory rates following sumption during both hibernation and active
castration/ovarietomy in a number of reptilian phases at low temperatures where both I\ and T<
species [92. 93. 95. 96. 98. 99. 129. 179. 180]. We do not stimulate respiration ofthe tissues followins:
have studied the role oftesticular hormones in the both in vivo and in vitro administration 107).
[
regulation of oxidative metabolism of the Indian Similarly, estradiol has been found to be calorige-
garden lizard in detail. In this extensive study, nic in the liver and muscle tissues of the female
effects of testosterone and thyroxine administra- toad. Bufo melanostictus following both in vivo
tion in intact, castrated and thyroidectomi/ed and in vitro treatments irrespective of season
lizards were recorded on the respiratory rates <>t activity phase [108]. Gonadal hormones have also
the whole body and tissues (liver, muscle, kidney been reported to exert Significant effect on tin
and brain) during all the twelve months ofthe year intermediary metabolism and erythropn
under natural climatic conditions [83]. In general, pokilotheimic vertebrates [181 189] •
testosterone was found to be calorigenically more steroids are also involved in the caioi ni(
effective at low temperatures (during hibernation mechanismofbirds[14-16, 190] [Tie m nism
and early post-hibernation phases) where thyrox- of calorigenic action of gonadal hormon
630 B. B. P. Gupta and J. P. Thapliyal
to be workedout. Involvement ofgonadalsteroids noradrenaline in the euthyroidic lizards, however,
in the oxidative metabolism of lower vertebrates, both the hormones were equipotent in the thyr-
especially at low ambient temperatures, might be oidectomized animals [227]. Furthre, the presence
ofgreat significance for the survival and successful of thyroid is a pre-requisite for the calorigenic
breeding of these cold-blooded animals under di- action ofadrenaline in thegarden lizardduringthe
verse climatic conditions [8, 83]. breeding phase [203].
Recently, administration of EP and NE have
been reported to inhibit the resting metabolic rate
Calorigenic action ofcatecholamines (RMR) of Alligator mississipiens for about two
RMR
Catecholamines (norepinephrine and epineph- hours and thereafter to stimulate the which
rine) are synthesized and stored in the sympatho- remains increased for many hours [220]. A large
adrenomedullary (SAM) system, and released amount of ATP formed immediately after the
under diverse physiological conditions, i.e., stress intra-muscular injections of the catecholamines as
(emotional, physical and physiological), emergen- aresultofglycolysishasbeenfoundtoberesponsi-
cy, danger etc. In addition to their effect on the ble for the transient inhibition of the RMR. A
cardio-vascular system, catecholamines invariably similar mechanism might be responsible for the
accelerate tissue respiration (non-shivering ther- reported inhibition of fish oxygen consumption
mogenesis) in mammals. Both norepinephrine [221-223]. It is noteworthy that the calorigenic
(NE) and epinephrine (EP) play a major role in action ofthe catecholamines in fishes, amphibians
the regulation of the oxidative metabolism of and reptiles is independent of ambient tempera-
mammals exposed to low temperatures (191-201). ture and needs a very short lag period [107-109,
The release of NE and EP is regulated as per 203, 220]. Due to these reasons, catecholamines
erquirement by the central nervous system aresupposedtoactasemergencyhormonesforthe
(hypothalamus) [5, 11, 202]. regulation of the energy metabolism in the poiki-
In poikilothermic vertebrates, calorigenic func- lothermic vertebrates [8, 13, 107-109, 203, 227].
tionofthecatecholaminesisnotwellstudied [203]. The mechanisms of calorigenic action of
Both EP and NE are reported to play a significant catecholamines is well studied in mammals [200].
role in the regulation ofthe intermediarymetabol- The catecholamines act throught a- and /?-
ism offishes [204-211], amphibians [212-217] and adrenergic receptors [228]. The binding of
reptiles [139, 218-220]. In a limited number of catecholamines to the adrenergic receptors stimu-
earlierstudies, catecholaminesinhibited the whole lates production of cAMP which activates a pro-
body oxygen consumption of fishes [221-223]. tein kinase. The cAMP-stimulated protein kinase
However, notwithstanding these reports, in vivo phosphorylates and stimulates lipase which
and in vitro treatments with comparatively low accelerates mobilization offree fatty acids (FFA).
doses of EP and NE stimulated significantly the Then FFA are converted to acyl carnitine and acyl
respiratory rate ofliver and skeletal muscle tissues Co A. The increased levels of FFA stimulate
of the fish, Clarias batrachus [109]. Similarly, proton conductance in the inner mitochondrial
adrenaline administration in the fish Anabas testi- membrane. Finally, theincreasedprotonconduct-
duneus produces time- and dose-dependent sti- ance accelerates oxidation of acyl carnitine and
mulatory effect on activities ofa number ofoxiad- results in increased rate of mitochondrial oxygen
tive enzymes in the liver tissue [224]. Catechola- consumption. Thus, the catecholamines stimulate
mones are also reported to stimulate the oxidative oxidative metabolism of mammals by accelerating
metabolism ofamphibians [106-108, 225, 226] and mobilization as well as oxidation of FFA and
reptiles [95, 203, 227]. In amphibians the relative involve cAMP as a second messenger. As in
potencies of EP and NE seem to vary with the mammals, EP and NE also mobilize FFA in the
species, tissues and seasons. In the Indian garden ectothermic vertebrates [139, 204, 229-232]. In-
lizard, intra-muscular injection of adrenaline was directevidencessuggestthateveninpoikilotherms
found to be calorigenically more potent than the catecholamine hormones stimulate oxygen
Hormones and ectothermic Metabolic Rate 631
consumption by stimulating oxidation of FFA energy consuming anabolic processes, mobiliza-
[203]. In addiition. EP and NE may also influence tion and oxidation of FFA, and osmoregulation.
energy metabolism by their action on glycogenoly- The question, whether corticosteroids influence
sis and electron transport chain [203. 211. 21S. the oxidative metabolism of ectothermic verte-
224). bratesdirectlyorindirectly by playing a permissive
role to support the calorigenic actions of other
hormones (as reported in mammals), remains to
Calorigenic effects ofcorticosteroids
be answered. Further attempts should be made to
The adrenal gland has evolved both structurally study effects ofcorticosteroid hormones on activi-
and functionally duringthe courseofevolution. In ties ofenzymes associated with the oxidative path-
homeotherms. corticosteroids are functionally di- ways and energy-dependent osmoregulatory pro-
—
vided into two groups glucocorticoids and cess.
mineralocorticoids. However, a functional clas-
sificationofthe cortical hormonesisnotpossiblein
Melatonin in calorigenesis
the lower vertebrates where various corticoids
share overlappingfunctions [233]. Glucocorticoids It has been suggested that photoperiod, acting
are reported to stimulate the oxidative metabolism via pineal gland, is capable of influencing energy
in mammals by their action on oxidative enzymes metabolism andthermoregulation in mammalsand
and the electron transport directly. They also birds [9]. Short photoperiods and melatonin admi-
support the calorigenic action of other metabolic nistration increase the behavioral thermoregula-
hormones [5, 11. 234. 235]. An intact and normal- tion as well as non-shivering thermogenesis. and
lv functioning adrenal cortex is essential for nor- also improve the thermogenic capacity of
mal thermoregulation at low temperatures [5, homeotherms [245-253]. However, it is not clear
23b]. Unlike in mammals, there is scarcity of whether melatonin affects the oxidative metabol-
information regarding the calorigenic function of ism directlyorpotentiatesthe calorigeniceffectsof
corticoid hormones in lower vertebrates [233]. In catecholamines [247, 254, 255]. There are a few
the Indian garden lizard, corticosterone adminis- indications that melatonin can influence metabolic
tration had no effect on the whole body oxygen rate of mammals also by affecting thyroid activity
consumption in any season. However, depending [256]. There is scarcity of information on the role
on the season (activity phase) and thyroidal status, of pineal and melatonin in the energy metabolism
it may stimulate, inhibit or produce no effect on ofthe ectothermicvertebrates. There is practically
respiratory rate of liver, muscle, kidney and brain no information on the metabolic effect of melato-
[203]. Corticosterone seems to be calorigenic in nin in any fish. The role of the pineal complex in
aquatic (fish) and semiaquatic (amphibians) verte- thermoregulation ofamphibians and reptiles is not
brates where corticosteroids are involved in the clear [255, 256]. Effect of parietalectomy in the
energy-dependent osmoregulatory mechanisms. frog, Rana temporaria reported at different
Corticosterone stimulates respiratory rate of liver temperatures is inconsistent [257, 258]. Some of
and muscle tissues ofa fish [109], a frog [107] and a the findings suggesl that interactions between
toad [108]. Hydrocortisone stimulates cytochrome temperature and photoperiod. depending on the
oxidase activity in the liver of Calotes versicolor in circannual phase, produce varied effects on the
a dose-dependent manner [237]. The calorigenic amphibian metabolic rate [257. 25(^. 260]. Howev-
effect of corticoid hormones has been found to be er, there is complete lack ol information regarding
rapid and temperature independent. There are effects of melatonin and pincalcctonn on the
many reports which suggest that adrenocortical oxidative metabolism and oi thermo-regulai
hormones play an important role in the regulation amphibians.
ofintermediary metabolism in cold-blooded verte- The pineal complex, however, seems i i in-
brates [238-244]. Corticosterone-induced increase volved in the thermoregulation ol lizai [261
in the respiratory rate might be associated with 263]. In general, parietalcctnim is reported to
632 B. B. P. Gupta and J. P. Thapliyal
increase [264] and pinealectomy to decrease the pinealcomplex, whicharecontrolledmainlybythe
bodv temperature of lizards [265-267]. These circadian and circannual variations in day-lenghth
reports suggest that the pineal complex mediates (photoperiod), seems to synchronize and couple
both behavioral and physiological thermoregula- the annual cyclesofenergymetabolism andbreed-
tion through the CNS (hypothalamus) involving ing phase to ensure successful and timely repro-
neuroendocrine mechanisms [268]. The precise duction. Stimulation of the respiratory rate by
role of the pineal complex in the regulation ofthe gonadal steroids at low temperatures probably
reptilian energy metabolism remains to be investi- ensures timely emergence from hibernation, and
gated. In aseriesofreports, photoperiodhasbeen also helps in calorigenesis during the active phase
found to influence the body temperature of the in the event of sudden drop in environmental
European green lizard, Lacerta viridis [269-272]. temperature.
In this lizard, short photoperiods and administra- Adrenal hormones in general and catechola-
tion ofmelatonin reduce body temperature. Since mines in particular act as emergencyhormonesfor
the environmental light-dark cycle not only acts as the regulation of calorigenesis in ectotherms.
a "Zeitgeber" (time keeper) but also provides the Catecholamines (NE & EP) accelerate respiratory
main source for behavioral thermoregulation, rate of all tissues instantly irrespective of seasons
therefore, the thermoregulatory effect of photo- andenvironmentaltemperatures. Thereisscarcity
period via pineal complex is supposed to be of of information on the calorigenic action of corti-
adaptive significance. The precise mode of mela- costeroid hormones in lower vertebrates.
tonin action in the poikilothermic metabolism re- On the basis ofthe available information, it can
mains practically unknown. be concluded that the oxidative metabolism of
pokilothermic vertebrates is regulated by a neuro-
endocrine mechanism having three major compo-
Summary and Conclusions —
nents (i) thyroid hormones (regulated primarily
The oxidative metabolism of poikilothermic by temperature), (ii) Hormones of gonads and
vertebrates is regulated by a complex neuro- pineal (controlled mainly by environmental light),
endocrine mechanism. Hormones of thyroid, and (iii) sympatho-adrenomedullary system (reg-
gonads, adrenal andpineal are activelyinvolvedin ulated by the central nervous system). While the
the regulatory process. Recent reports, based on first two components govern strategies for long
carefully designed experiments, unequivocally and term energyproduction associatedwiththe annual
strongly suggest that thyroid hormones play a events, the third component seemstoensure rapid
leading role in the metabolic regulation of lower but transient energy production under emrgency/
vertebrates during the active phase. The calorige- life-threatening situations. It is, thus, apparent
nic action of thyroid hormones seems to depend that the cold-blooded vertebrates possess an en-
largely on the energy demand associated with dogenous mechanism which regulates energy
physical and/or physiological activities of the metabolismefficientlyaccordingtoenergydemand
animals. In addition to temperature, hormones and ensures successful survival even at the ever-
associated with feeding and fasting seem to in- changing body temperature.
fluence the calorigenic action of these hormones.
The precise mechanism, which regulatesmetabolic
ACKNOWLEDGMENTS
action of T3 and T4 at cellular level, remains
unknown Indirect evidences suggest that the FinancialassistanceprovidedbytheUniveristyGrants
calorigenic action of these hormones might be Commission and the Council ofScientific and Industrial
regulatedbyreceptorsofthyroidhormonesand/or Research, New Delhi is gratefully acknowledged.
inducibility of the oxidative enzymes which are
influenced by a number of external and internal
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