AMER. ZOOL., 16:725-732 (1976).
Life History Patterns of Storage and Utilization of Lipids for Energy in
Amphibians
LLOYD C. FITZPATRICK
Department of Biological Sciences and Institute of Applied Sciences, North Texas State
University, Denton, Texas 76203
SYNOPSIS Amphibians utilize lipids, principally triglycerides, stored in abdominal fat bodies
and carcass depots for production of gametes and for metabolic maintenance during
dormancy. Stored lipids are maximal in early fall prior to winter dormancy and minimal after
breeding in the spring and early summer in most amphibians. Extirpation experiments
show that fat bodies are essential for gonadal maintenance. Patterns of lipid compartmentalization are discussed and quantified in a representative from the Salientia and Urodela.
Amphibians in temperate and arid zones
exhibit seasonal periods of activity and
dormancy. During brumation (= winter
dormancy in vertebrate poikioltherms;
Mayhew, 1965) or estivation, amphibians
experience an energy deficit (sometimes referred to as negative production) and must
rely on energy stored during periods favorable to energy acquisition. Thus, during
favorable periods amphibians must selectively budget or apportion their net
metabolizable energy (= consumption —
egestion and excretion) among maintenance metabolism (measured directly as
metabolic heat, or indirectly as (^consumption or CO2 production), growth, gamete
production and storage. The theory surrounding tactics by which animals apportion their energy, specifically among
growth, reproduction, storage and activity
(principally activity associated with foraging, i.e., foraging strategies), at different life
history stages has recently received considerable attention and is discussed by Pianka
elsewhere in this symposium.
Storage of energy during one season for
utilization in another complicates energy
budget analyses and interpretations of life
history tactics (e.g., reproductive effort) in
amphibians. Energy budget analyses necessary to quantitatively interpret life history
tactics of amphibians require energy and
mass balance equations which include rates
of assimilation, respiration, growth, gamete
production (specifically vitellogenesis) and
storage, and flows of energy and matter
among storage compartments, throughout
yearly cycles. Metabolic compensation
(Prosser, 1973) to seasonally encountered
temperatures which occurs in many amphibians (e.g., Triturus vulgaris, Pocrnjic, 1965;
Acris crepitans, Dunlap, 1969, 1971; Desmognathus ochrophaeus, Fitzpatrick et al., 1971,
Fitzpatrick and Brown, 1975; Desmognathus
fuscus, Fitzpatrick et al., 1972; Eurycea bislineata, Fitzpatrick, 1973b; Bufo woodhousei,
Fitzpatrick and Atebara, 1974), affects rates
of energy acquisition, utilization and storage, and should be considered in energy
budget analyses. Also, exact dates of beginning and ending of dormancy, and whether
any feeling occurs during that period are
important to know. Seymour's (1973) study
of spadefoot toads Scaphiopus couchii and 5.
hammondii and Fitzpatrick's (1973a) study of
the plethodontid salamander Desmognathus
ochrophaeus approximate complete assessments of energy compartmentalization and
utilization rates in amphibians.
Energy may be stored by amphibians as
carbohydrates, proteins or lipids. Although
all three may be important energy reserves
in Desmognathus ochrophaeus (Fitzpatrick,
I was partially supported by a North Texas State
University Faculty Research grant duringthe writingof
this paper. I thank Barney Venables, John Hughes, Joe
Fagan and Jerry Glidewell for their assistance.
1973a), carbohydrates and proteins are reported to be of only minor importance as
energy reserves in Bufofowleri (Bush, 1963),
Rana temporaria (Smith, 1950) and Rana pi-
725
726
LLOYD C. FITZPATRICK
piens (Mizell, 1965). Proteins are unlikely those urodeles that commonly sacrifice (auenergy reserves for dormant arid-zone am- totomize) their tails to escape predators.
phibians because of the water balance prob- Maiorana (1975) has studied such funclems associated with nitrogen excretion. tional conflicts in Batrachoseps attenuatus
However, Seymour (1973) suggested that whose tail is used for lipid storage, respiraproteins may be an energy source in tion, courtship and predator escape. In
Scaphiopus couchii and Scaphiopus hammondii.frogs and toads lipids are principally stored
McClanahan (1967) reported that respira- in finger-like fat bodies located at the
tory quotients for Scaphiopus couchii indicate anterior end of the gonads from which they
that primarily fats are metabolized during develop embryologically (Noble, 1931).
dormancy. Lipids, principally triglycerides, Lipids may also be stored in the pelvic
probably are the major energy reserves in region, carcass, body muscle, and liver
amphibians. They contain at least twice the (Athanasiu and Dragoiu, 1910; Ackerman,
weight-specific energy contained in car- 1949; Bush, 1963; Seymour, 1973).
bohydrates and proteins, and their
catabolism produces significantly more
metabolic water which should be important Abdominal fat bodies
to dormant arid-zone amphibians.
Abdominal fat bodies have received more
My objective in this paper is to briefly attention than other lipid stores, probably
outline general lipid storage and utilization because they are more conspicuous and lopatterns in selected amphibians from the cated near the gonads. Most beginning biolSalientia and Urodela. Although there are ogy students are familiar with fat bodies in
numerous papers that report qualitative the "laboratory" frog and that they often
and antecdotal data on fat reserves in am- differ considerably in size among specimens
phibians, I have selected only representative throughout the laboratory. This variation in
papers that present quantitative data.
fat body size probably results from the
specimens being collected and prepared at
different seasons. Seasonal variation in the
LIPID STORAGE SITES
size of fat bodies has been correlated with
Lipids are principally stored in the ab- periods of dormancy during unfavorable
dominal fat bodies (corpora adiposa), car- weather and reproduction (gamete and yolk
cass and tail of urodeles (Noble, 1931; Col- production, and breeding and brooding aclins etal. 1953; Rose, 1967; Rose and Lewis, tivities) in many amphibians: Rana pipiens
1968; Lewis and Rose, 1969; Fitzpatrick, (Mizell, 1965; Brenner and Brenner, 1969),
1973a; Maiorana, 1975). Fat bodies are usu- Rana temporaria (Smith, 1950), Rana clamially paired ribbons enveloped in folds of tans (Brenner, 1966; Bobes, 1973), Rana
peritoneum parallel to the kidneys and esculenta (Gaule, 1901; Ackerman, 1949),
gonads (Noble, 1931) and share a common Acris crepitans (Brenner, 1969), Scaphiopus
embryological origin in salamanders couchii (McClanahan, 1967; Seymour,
(Adams and Rae, 1929). Although quantita- 1973), Scaphiopus hammondii (Seymour,
tive differentiation between lipid reserves in 1973), Bufo arenarum (Mazzocco, 1938),
the carcass and tail of urodeles is not well- Bufo fowleri (Bush, 1963), Notophthalmus
known, most of the lipids are probably (Triturus) viridescens (Adams and Rae, 1929),
stored posterior to the pelvis and in the tail. Triturus carnifex (Collins et al., 1953), AmIn Desmognathus ochrophaeus there is a largephiuma means (Rose, 1967), Ambystoma tigdiscrete lipid deposition immediately pos- rinum (Rose and Lewis, 1968; Lewis and
terior to the pelvis, extending into the tail Rose, 1969), and Desmognathus ochrophaeus
(Fitzpatrick, 1973a). Approximately 66%of (Fitzpatrick, 1973a).
the lipids in the plethodontid salamander
Reproductive uses of fat body lipids.The close
Batrachoseps attenuatus are stored in the tail anatomical and general inverse size rela(Maiorana, 1975). Storage of energy in the tionships between abdominal fatbodies and
tail for important life history activities gonads suggest that the former are energy
should pose interesting compromises in stores for gonads. In general, abdominal fat
STORAGE AND UTILIZATION OF LIPIDS IN AMPHIBIANS
727
bodies are of minimal size immediately after conditions. Data from Bobes (1973) support
the breeding season, especially in females this. Studying environmental factors
after eggs are shed, and maximal in the fall (photoperiod, temperature and food quanbefore the overwintering period. Rose tity) affecting size and lipid composition of
(1967) reported an exception to this general gonads and fat bodies of Rana clamitatis,
pattern in female Amphiuma means from Bobes found that food consumption deterLouisiana. Their fat bodies did not decrease mined fat body size in both sexes before
in size as weights of ovaries increased, be- overwintering. Female green frogs chancause of the extended period of vitel- neled more of their food energy into
logenesis (7 months) during which females gonadal tissue than into fat body tissue. A
fed and replenished fat body lipids as they similar observation was made by Seymour
were used for yolk production. Rose specu- (1973) in female Scaphiopus couchii.
lated that Amphiuma means from more
Rose (1967) demonstrated that fat body
northern areas or from populations, unlike extirpation severely reduced yolk produchis, that inhabit ditches that become com- tion in Amphiuma means and concluded that
pletely dry in winter may deplete their fat fat body lipids were essential for follicle
body lipids to support vitellogenesis.
formation.
Metabolic maintenance functions of fat body
Although there is considerable indirect
evidence that abdominal fat bodies are es- lipids. As stated earlier, depletion of fat body
sential for maintenance and development of lipids or decreases in their sizesor both have
gonads, only a few studies have directly been demonstrated to occur during dortested their role in amphibians. Most nota- mancy in several amphibians. However,
ble are the fat body extirpation experiments when vitellogenesis continues during dorby Adams and Rae (1929) with the newt mancy quantitative separation of fat body
Notophthalmus viridescens and those by Rose lipids used for general metabolic mainte(1967) with Amphiuma means. In their classic nance from those used for gonadal dework Adams and Rae performed unilateral velopment requires integration of simul(left and right) and bilateral fat body abla- taneous measurements of all lipid stores,
tions on groups of fed and unfed newts. gonads and non-lipid tissue with measureRegeneration of fat bodies occurred in 43% ments of energy metabolism at appropriate
of fed newts, but not in unfed newts whose temperatures for both sexes. Adams and
fat bodies decreased in size. There was some Rae (1929) reported that changes in body
"compensatory" hypertrophy of the re- weight of unfed newts with abdominal fat
maining fat body in unilaterally ablated bodies did not differ from newts without fat
newts that were fed. Hypertrophy resulted bodies, suggesting that fat bodies were not
from enlargement of existing adipose cells used for general body nutrition. They reand not proliferation of new ones. Bilateral ported that the major effect of inanition was
ablation resulted in progressive, but com- the use of fat body lipids for gonadal
plete degeneration of testes and ovaries in maintenance. Seymour (1973) reported
both fed and unfed newts. Unilateral abla- that 55% of the metabolic maintenance
tion resulted in degeneration of the gonad energy for Scaphiopus couchii and 50% in
on that side. Gonadal degeneration pro- Scaphiopus hammondii came from fat body
ceeded in order from spermatozoa in the lipids during their 10-month dormancy.
testes and from largest to smallest ova in the Fitzpatrick (1973a) reported that Desmogovaries, each being resorbed. Adams and nathus ochrophaeus females apparently used
Rae concluded that the function of fat fat body lipids for maintenance during their
bodies is nutritive and essential for gonadal 6-week brooding period while they did not
feed. Since this usage was directly associated
development.
with reproduction, it is consistent with
Decrease in fat body size, absence of re- theory and evidence from other amphibians
generation and compensatory hypertrophy that fat bodies function principally for rein unfed newts demonstrated that lipid re- production in amphibians.
serves in the fat body were stored and maintained only under favorable nutritional
Biochemical, endocrinobgical and physiologi-
728
LLOYD C. FITZPATRICK
cal considerations. Rose (1967) suggested that exhibit the same seasonal pattern of variaamphibian fat bodies store fat-soluble vita- tion that fat bodies do.
mins, micronutrients and gonadal androReproductive and maintenance functions of
gens. Rose and Lewis (1968) and Lewis and carcass lipids. Decreases in carcass lipids in
Rose (1969) suggested that fat body fatty amphibians during periods of dormancy
acids and their co A esters function to and when ova are being yolked indicate that
change ovarian metabolism from structural lipids function in both reproduction and
synthesis in early stages to storage synthesis maintenance. Fitzpatrick (1973a) reported
in terminal stages of ova production mAm- that Desmognathus ochrophaeus females used
bystoma tigrinum. However, because liver carcass lipids for maintenance during brupreparations from Ambystoma tigrinum did mation and their 6-week brooding period.
not oxidize fat body fatty acids, Lewis and Maintenance during brooding while DesRose (1969) concluded that the liver did not mognathus ochrophaeus females were without
convert fat body fatty acids to compounds food must be considered as a reproductive
required for ovarian synthesis; instead these function of carcass lipids. Male Amphiuma
conversions were carried out directly in the means presumably used carcass as well as fat
ovaries. Using chloroform-methanol Rose body lipids for spermatogenesis and mating
and Lewis (1968) found that fat bodies in activities between June and September
Ambystoma tigrinum, regardless of size, were (Rose, 1967). However, females showed the
composed of 96.6-99.7% lipid (triglyc- same nominal seasonal variation in carcass
erides, free fatty acids, steroids and lipids as in their fat body lipids. Seymour
phospholipids). Although the total relative (1973) suggested that body lipids were used
percentage of lipids did not vary during for close to 50% of metabolic maintenance
vitellogenesis, concentrations of free fatty during dormancy in Scaphiopus couchii and
acids (lauric, myristic, palmitic, palmitoleic, Scaphiopushammondii. Bush (1963) reported
stearic, oleic, linoleic and arachidic) in- that carcass lipids in Bufo fowleri decreased
creased significantly as fat bodies were de- from 20% dry carcass weight in the fall to
10% in the spring, presumably for maintepleted.
Brown (1964) reported that fat body nance.
lipids in amphibians are largely triDirect evidence that carcass lipids are esglycerides. Tsukamoto and Ohtaki (1949) sential for reproduction is scarce. Maiorareported that the fat body lipids of Bufo na's (1975) study with Batrachoseps atmelanostictus were 98.3% triglycerides, of tenuatus, which stored 66% of its fat in the
which 41% was palmitic and stearic (satu- tail, provided direct evidence. Studying two
rated) and 59% was unsaturated. Bobes major competitive functions of the tail, lipid
(1973) reported that fat bodies of Rana storage as an energy reserve for reproducclamitans contained triglycerides, phos- tion and predator escape through aupholipids and cholesterol, with triglycerides totomy, Maiorana observed the following:
composing most of the fat body. Lupa di tail length was positively correlated with
Prisco et al. (1971, 1972) demonstrated in clutch size; removal of tails generally previtro that fat body tissue of male and female vented males and females from becoming
Triturus cristatus camifex synthesized andro- reproductive, whereas those with tails begens and estrogens.
came reproductive; and regeneration of an
autotomized tail appeared to have priority
over use of fat stores remaining in the intact
Carcass fat deposits
part of the tail for reproduction. Since all of
Lipid reserves in the carcass have been her experimental animals with autotomized
examined in several amphibians: Bufo fow- tails had large abdominal fat bodies, failure
leri (Bush, 1963), Scaphiopus couchii to become reproductive after tail removal
(Seymour, 1973), Amphiuma means (Rose, strongly indicates that tail lipid reserves
1967), Desmognathus ochrophaeus (Fitzpa- were essential for reproduction or that in
trick, 1973a) and Batrachoseps attenuatus Batrachoseps attenuatus tail regeneration is
(Maiorana, 1975). In general, carcass lipids more important than present production,
STORAGE AND UTILIZATION OF LIPIDS IN AMPHIBIANS
even though reproduction was possible, or
both. Conflicting evidence comes from experiments on fat body ablation which, it was
found, prevented ovarian development despite Iipid reserves in the carcass (e.g., Rose,
1967; and presumably Adams and Rae,
1929). Perhaps it is the absolute level of
lipids in the animal that determines whether
reproduction will occur rather than the level
in any one anatomical compartment.
Fitzpatrick (1973a) reported that large
amounts of caudal lipids were unused during brumation and brooding in Desmognathus ochrophaeus.Desmognathus ochrophaeus
females emerged from brooding in an
emaciated condition despite large caudal
Iipid reserves (23% dry carcass weight). Why
they should deplete lean carcass tissue (presumably glycogen and protein) during
brooding and not rely on caudal lipids is
unclear. A possible explanation is that
caudal lipids serve to rapidly replace depleted fat body lipids which are essential for
intensive vitellogenic activities that begin
immediately after emergence from brooding. Obviously, considerable work is necessary before the relative roles of both fat body
and carcass Iipid reserves in amphibians are
elucidated.
Liver
Although lipids have been shown to increase in the liver of amphibians prior to
reproduction {e.g., Ackerman, 1949; Bush,
1963; Mazzocco, 1938; Rose, 1967), the liver
probably functions more in Iipid metabolism {i.e., synthesis, degradation) than
storage.
Ovaries and ova
The presence of lipids in ovarian tissue
and ova of amphibians is well-known. Dehydrated ova of Desnwgnathns ochrophaeus
contained approximately 42% chloroform-methanol extractable Iipid (Fitzpatrick, 1973a). Seymour (1973) reported that dehydrated ova of Scaphiopus
couchii and Scaphiopus hammondii contained
23.9 and 22.9% Iipid respectively. Boyd
(1938) reported that ovaries in Rana pipiens
729
contained large quantities of neutral fats
and fatty acids as well as cholesterol and
phospholipids, and that during development of ova each Iipid class increased significantly. Ova-laden ovariesof springfrogs
contained 4800 to 14,950 mg (average of
7700 mg; 7.7% wet weight) of neutral fats
per 100 g wet weight of ovary. According to
Boyd this represented a 710% increase in
ovarian lipids during ova production. Bush
(1963) reported that one-half the total Iipid
in female Bufo fowleri was stored in the
ovaries in April, and that this Iipid was obtained from several body regions. As the ova
were shed by Bufo fowleri in May, total Iipid
decreased by a factor of three. Seymour
(1973) reported that much of the Iipid produced by Scaphiopus couchii was deposited in
ova by September at the expense of the fat
body. This concurs with the report by Bobes
(197 3) that female Rana clamitans channeled
more energy into ova than fat bodies, resulting in smaller fat bodies than males despite
similar food intake.
QUANTITATIVE LIPID
COMPARTMENTALIZATION AND UTILIZATION
Table 1 contains comparative quantitative data on Iipid distribution in representatives from the Salientia and Urodela before
and after dormancy. Data for Scaphiopus
couchii were calculated from Tables 1 and 2
in Seymour's (1973) paper, and values for
Desmognathus ochrophaeus were calculated
from Fitzpatrick (1970, 1973a). Seymour
reported that respiration measurements
indicated that a spadefoot toad used 800 mg
of Iipid during its 10-month dormancy. Calculated total Iipid depletion in male toads
(1358- 462 = 896 mg) accords with this. Fat
body lipids contributed 56% and carcass
lipids 44% to energy requirements of
metabolic maintenance in dormant male
toads. Female toads channeled 102 mg of
their fat body lipids or carcass lipids or both
into their ova and used the remainder (1725
- 938 = 787) for metabolic maintenance.
Fat body lipids contributed approximately
35% and carcass lipids 65% to metabolic
maintenance and lipids in the ova. However,
the relative contribution of these lipids to
each cannot be determined.
730
LLOYD C. FITZPATRICK
TABLE 1. Lipid energy reserve distribution in the spadefoot load, Scaphiopus couchiia and the salamander Desmognathus ochrophaeus" before (B) and after (A) dormancy.
Body wt.
Species
B
S. couchii
M
D. ochrophaeus
F
a
b
A
B
A
23
25
(g wet)
28
29
(g wet)
1358 462
215
195
(mgdry)
112 111
F
Fat body
Carcass
( m g)
(%)
( m g)
(%)
Total lipids
(mg)
1725 938
B
A
585 80
(43) (17)
2
321
(19) (•2)
7
(6)
4
(3)
B
A
773
(57)
1174
(68)
382
(83)
604
(64)
82 65
(73) (59)
Ova
(mg)
(%)
B
A
230 332
(13) (35)
23
(21)
42
(38)
Calculated from Seymour (1973).
From Fitzpatrick (1970, 1973a.)
Total body lipids in Desmognathus ochro-
phaeus changed only in relative distribution and not in quantity during dormancy
(Table 1; Fig. 1). The 20 mg depletionin fat
body ( 7 - 4 = 3 mg) and carcass (82 - 65 =
17 mg) lipids mass balanced the lipids accumulated in the ova (19 mg). However, as
with Scaphiopus couchii, lipid depletion did
not completely mass balance both vitel-
logenic and metabolic maintenance requirements during dormancy. The total increase in ova mass during dormancy in Desmognathus ochrophaeus was 46 mg which was
composed of 27 mg of non-lipid material.
The decrease in dry non-lipid body weight
(215 — 195 = 20 mg) approximately mass
balanced this. Respiration determinations
indicated thata maximum of 38 mg of lipids
were required to maintain a dormant Desmognathus ochrophaeus female during her
5-6 months of brumation. Thus, the energy
equivalent of38mg of lipid (ca. 342 cal) must
be accounted for.
Approximately 280 mg of non-lipid yolk
were depositied in ova of Scaphiopus couchii,
but cannot be accounted for by Seymour's
data. It is possible that both Desmognathus
70
60
s
I
t
50
ochrophaeus and Scaphiopus couchii fed in the
30
winter during favorable weather. Abundant
larvae and worms coexisted with Desmognathus ochrophaeus in their brumation sites.
Seymour suggested that dormant toads may
have used proteins for energy, but his reported changes in their body weight did not
support this. Obviously, more field data
concerning winter animals are necessary before energy and mass equations for Desmog-
20
nathus ochrophaeus and Scaphiopus couchii can
6-8
be completely balanced.
Although Figure 1 specifically illustrates
dynamics of lipid storage and utilization in
HID MAY
female Desmognathus ochrophaeus in refer-
FAT BODY LIPIDS
D
0
0-2
2-4
4-6
OVA SIZE CLASS (MY tTT./OVUR)
^S
iSTv
LATE
AM L
'
*
ence to stage of vitellogenesis and correFIG. 1. Annual lipid dynamics in Desmognathus ochro- sponding time of year, it can be used to
summarize the general seasonal pattern in
phaeus females.
CORRESHJMDlNG NDNTH
STORAGE AND UTILIZATION OF LIPIDS IN AMPHIBIANS
amphibians. A typical female emerged from
brumation in April with reduced lipid reserves and enlarged ova. Final yolking occurred before oviposition in mid-May.
Brooding, which is not characteristic of amphibians, lasted approximately 6 weeks,
during which metabolic maintenance requirements reduced lipid reserves to their
yearly minimum. After emergence from
brooding in late June, the emaciated
females rapidly replenished their lipid reserves and deposited large amounts of yolk
before brumating in late October.
Desmognathus ochrophaeus females, because of low maintenance requirements
(metabolic undercompensation; Prosser,
1973) during brumation, metabolic insensitivity to short-term temperature changes
in early spring after emergence and partial
metaboliccompensation(Prossner, 1973) to
temperature changes during the summer
(Fitzpatrick, 1971, 1973a; Fitzpatrick etal.,
1972), were capable of efficiently utilizing
lipids acquired during the summer to produce gametes during the winter; enabling
them to maximally exploit the relatively
short breeding season. Metabolic compensation may be a widespread mechanism
among temperate amphibians that minimizes metabolic maintenance demands
on lipid energy reserves, thus increasing the
stored energy available for reproductive
functions.
731
Brenner, F. J. 1969. The role of temperature and fat
deposition in hibernation and reproduction in two
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Brenner, F.J. and P. E. Brenner. 1969. The influence
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Brown, G. W.,Jr. 1964. The metabolism of Amphibia.
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