AMER. ZOOL., 16:711-723 (1976).
Lipid Storage and Utilization in Reptiles
W. KENNETH DERICKSON
Division of Environmental Impact Studies, Argonne National Laboratory, Argonne,
Illinois 60439
SYNOPSIS. Lipids represent a biochemically efficient mechanism for storing energy to be
used at a later date for maintenance and/or reproduction. This storage and utilization at
different times results in seasonal patterns of lipid cycling. Reptiles exhibit a number of lipid
cycling patterns which can be explained by seasonal patterns of food availability. Seasonality
in food availability determines the quantity of lipids stored, when lipids are stored, and for
what purposes these lipids are utilized. Lipid cycling patterns are in turn correlated with life
histories.
INTRODUCTION
A study of lipid storage and utilization in
relation to certain environmental parameters (food availability, precipitation and
temperature) can provide valuable information for understanding reptilian life histories. Lipids represent an efficient
biochemical mechanism for concentrating
large amounts of stored energy in a small
space. As with most other animals, reptiles
utilize their lipids for a variety of needs
including growth, maintenance and reproduction. This paper will examine patterns
of lipid storage and utilization and attempt
to correlate these patterns with various
reptilian life histories.
In most reptiles, the bulk of the lipids are
stored subcutaneously or in visceral fatbodies (corpora adiposa). Most lipid studies
on reptiles have used some lipid index as a
measure of the quantity of stored lipids.
This index is typically wet fatbody weight
divided by wet body weight (Goldberg,
1972), or dry extracted lipids (either triglycerides or total) divided by lean dry body
weight (Dessauer, 1955; Mueller, 1969;
I would like to thank Dr. Paul Licht for his ideas
regarding the importance of reproduction and seasonality in lipid cycling and Dr. Edwin Pentecost for
the information on Eumeces. Thanks are extended to
Dr. Carl Bebnch, Kathie Hoekstra and Dr. Edwin
Pentecost for helping to improve the quality of this
paper. Thanks also goto Brenda Pruitte for typing this
manuscript and to ANL for its encouragement and
support.
Aleksiuk and Stewart, 1971; Sexton et al.,
1971; Gaffney and Fitzpatrick, 1973; Jameson, 1974; and Derickson, 1976). Other
studies have looked solely at fatbodies,
recording their weight (Licht and Gorman,
1970), length (Pianka, 1967; and Parker
and Pianka, 1973) or some subjective measure of fatbody size (Ruibal et al., 1972).
Studies done on lizards indicate that measures of fatbody lipids are good for tracking
lipid cycling patterns (Dessauer, 1955;
Gaffney and Fitzpatrick, 1973; and Derickson, 1974); however, fatbody lipids
rarely exceeded 50% of the total storage
lipids in these studies and therefore do not
indicate the absolute quantity of storage
lipids available. A study done by Derickson
(1974) also demonstrated that fatbody
lipids are the most labile; thus, storage or
utilization of lipids would be apparent in
this depot first.
In addition to studies on fatbody lipids,
Dessauer (1955), Gaffney and Fitzpatrick
(1973), Derickson (1974), and Jameson
(1974) measured triglyceride content in a
numberoflizardspecies. [Brians/al., 1972,
and Hadley and Christie, 1974, found that
triglycerides represent about 90% of the
stored lipids with oleic (18:1), palmitic
(16:0) and linoleic (18:2) acid being the
predominant forms]. These authors also
examined triglyceride cycling patterns for a
number of lipid depots, including the carcass, eggs, fatbodies, liver and tail. While
the bulk of the triglycerides are stored in
the carcass and fatbodies, some are tem-
711
712
W. KENNETH DERICKSON
porarily stored in the liver. According to
Hahn (1967) the liver is probably an intermediary organ for both the storage and
utilization of lipids.
Despite the use of different lipid indices
and differences in the depots analyzed,
trends in patterns of lipid storage and utilization are discernible, especially for lizards
and snakes. The remainder of this paper
will (1) identify these patterns for the various reptilian groups and examine differences in lipid cycling patterns within each
reptilian group; (2) identify factors that
appear to be responsible for differences in
lipid cycling patterns; and (3) relate differences in lipid storage and utilization in two
congeneric lizard species to differences in
life history strategies.
400-
WATER
200FAT
ASH-FREE
LEAN DRY
ASH
LIPID STORAGE AND UTILIZATION IN EACH REPTILIAN GROUP
Turtles
A review of the literature produced only
four studies (Belkin, 1965; Emerson, 1967;
Brisbin, 1972; and Morloch et al., 1972) on
turtles that pertain to lipid storage and
utilization. Belkin (1965) demonstrated
experimentally that the musk turtle (Sternothaerus minor) looses lipids during starvation. The net loss of body lipids after 120
days of starvation was about 62% of the
original lipid level. Emerson (1967), studying the false map turtle (Graptemys
pseudogeographica) found that liver lipid
levels were the highest during the reproductive period and lowest prior to hibernation. Based on observations by Hahn (1967)
on lizards, this would indicate that lipids
were being mobilized during reproduction
and stored prior to hibernation. Brisbin
(1972) could find no indication of lipid
storage and utilization in the eastern box
turtle {Terrapene Carolina Carolina), although
seasonal weight changes, not due to water,
did occur (Fig. 1). Brisbin suggested that
some other chemical compound, such as
glycogen, may be used as a stored energy
source. The turtles that Brisbin studied had
been kept captive, fed ad libitum and forced
into hibernation, a situation which may
have influenced lipid levels and provided a
MID-SUMMER
FALL
SPRING
FIG. 1. Seasonal variation in total live body weight
and major body components of captive South Carolina
box turtles maintained in an outdoor pen. (From
Brisbin, 1972)
different picture of the lipid cycling pattern
than may occur under more natural conditions. While it is possible that turtles do
store glycogen rather than lipids, there is
presently very little evidence to support this
theory. Morloch, et al. (1972) measured
weight loss and gain experimentally in the
eastern painted turtle (Chrysemys picta picta).
Body weight in this species fluctuated with
food supply as expected; however, it is not
known whether these changes in weight
were a function of fat, glycogen, protein or
water levels. Detection of any trends in lipid
storage and utilization in turtles based on
these meager data are difficult.
Snakes
The data available on lipid storage and
utilization in snakes indicate that some
snakes depend heavily on their lipids for
reproduction while others utilize their
lipids during hibernation. Vainio (1931)
found that lipid levels decreased during
pregnancy in the European viper (Vipera
berus), with the lowest lipid levels occurring
713
LIPID CYCLING AND REPTILIAN LIFE HISTORIES
after the cessation of reproductive activity.
Reproducing females were unable to store
large amounts of lipids prior to winter
dormancy and as a result did not reproduce
the next year. St. Girons (1957) indicated
that female asp vipers (Vipera aspis) with less
than 10% of their body weight in lipids
prior to winter dormancy would not reproduce the following spring. Tinkle (1962)
found that female western diamondback
rattlesnakes (Crotalus atrox) in reproductive
condition had fatbody lipid levels equivalent to 12% of their wet body weight, with
those not in reproductive condition having
only 8%. Tinkle suggested that the additional lipids were required for yolking of
the follicles. After parturition, reproductive females had lower lipid levels than
non-reproductive females, which had
stored fat during the reproductive season.
Tinkle also suggested that the nonreproductive females, having higher lipid
levels, would reproduce the next spring
while the reproductive females, due to insufficient lipids, would not. Wharton (1966)
and Gibbons (1972) found similar patterns
of lipid cycling and biennial reproduction
JAN
APR-MAY MAY-JUN JUN-AUG JUN-AUG SEP-OCT
MONTH
FIG. 2. Seasonal variation in fatbody weight in Utah
female Coluber constrictor mormon. The arrow on the
abscissa indicates the period of egg laying. (From Dr.
William S. Brown, personal communication)
tance of lipids for winter maintenance in
this species. Changes in body weight in a
number of other snake species also suggest
that lipids are important for winter
maintenance. Klauber (1956) observed
overwinter weight losses of 4 and 20% of
in the cottonmouth (Agkistrodon piscivorous) the body weight for adult and juvenile
and the canebrake rattlesnake (Crotalus hor- prairie rattlesnake (Crotalus viridis), respecridus atricaudatus), respectively. Dr. William tively. Hirth (1966) and Parker and Brown
S. Brown (personal communication) ob- (1974) found that adult great basin rattleserved an inverse relationship between fat- snakes (Crotalus virdis lutosus) lost 6.0-8.8%
body size and reproductive activity (Fig. 2) of their body weight during winter dorin female western yellow-bellied racers
(Coluber constrictor mormon). Unlike the pre-
vious studies, however, lipid levels prior to
winter dormancy were equivalent to those
found after winter dormancy, suggesting
that this species may reproduce annually
rather than biennially.
A number of other studies indicate that
some snakes may utilize lipids primarily for
maintenance during winter dormancy.
After converting Aleksiuk and Stewart's
(1971) data to total body lipids (mg dry
lipids/lean dry body weight x 100), prehibernation lipid levels were about 50%
higher than post hibernation levels (Fig. 3)
in the common garter snake (Thamnophis
sirtalis). During the following reproductive
months, lipid levels actually increased then
decreased just prior to winter dormancy.
This observation demonstrates the impor-
_ Thomnophis sirtalis poneialis ¥ ? + tfcf"
S o
FIG. 3. Seasonal variation in total body lipids in
Manitoba male and female Thamnophis sirtalis panelalis
(modified from Aleksiuk and Stewart, 1971). The
hibernation period extends from October to April and
reproduction occurs from June to August.
714
W. KENNETH DERICKSON
mancy. The desert striped whipsnake (Mas- cycles in a number of anoles and found that
Anolis trinitatus had no fatbodies throughloose about 9.4% of its body weight during out the year. Like the Javanese house gecwinter (Hirth, 1966). Finally, contrary to kos, this anole apparently reproduces all
Brown's observations on western yellow- year.
bellied racers, Hirth (1966) found that this
Three studies (Dessauer, 1955; Mueller,
species (from the same study area) lost con- 1969; and Avery, 1970) indicate that some
siderable weight during winter dormancy, lizard species may utilize their lipids
suggesting a variation in the amount of primarily for maintenance during winter
lipid used during winter dormancy be- dormancy. Dessauer (1955) in his comtween years.
prehensive and classic work on lipid storage
In summary, lipids appear to be impor- and utilization in the green anole (Anolis
tant for both reproduction and winter carolinensis) from New Orleans, Louisiana,
maintenance in snakes. In some snake found that lipid utilization occurred almost
species, lipids are sufficiently important for exclusively during winter dormancy
reproduction that an inability to restore (November-March). As seen in Figure 4,
lipids to a given level may result in biennial lipid deposition, on the other hand, took
reproduction. Other snake species are ap- place during the reproductive (Aprilparently able to restore their lipid levels to August) and post-reproductive (September
the required levels and can reproduce an- and October) seasons. This pattern of lipid
nually. Finally, species such as the common storage and utilization is in marked contrast
garter snake apparently do not use their to data on other anoles. A. carolinensis oclipids for reproduction but instead use curs at subtropical latitudes, while the other
anoles studied occurred at tropical latitudes
them during winter dormancy.
and this most likely is a contributing factor
for the observed differences. Mueller's
ticophis taeniatus taeniatus) was observed to
Lizards
Four patterns of lipid storage and utilizaIOO-|
Lipid Distribution
tion in lizards have evolved from the research of many investigators working with a
number of different species. These patterns include no lipid cycling, cycling associated only with winter dormancy, cycling
associated only with reproduction and cycling associated with both winter dormancy
Z 29
and reproduction.
The absence of lipid cycling has been
identified in five lizard species. Church
(1962) studying three species of Javanese
house geckos (Cosymbotus platyurus,
Hemidactylus frenatus and Peropus mutilatus) 73 - I I Liver
EZ3 Fot Bodies
found no fatbodies present throughout the
ES3 Carcass
year. These are tropical species and apparently undergo no seasonal cycle of reproductive activity. Hoddenbach and Lannom
(1966) examined a limited number of Mexican leaf-fingered geckos (Phyllodactylus
tuberculosus) and found no fatbodies present. They suggested that in frost-free
areas of Mexico this species may breed FIG. 4. Seasonal variation of triglyceride levels in
throughout the year and thus result in the various body components of Louisiana male and
Anolis Carolinensis (from Dessauer, 1955).
absence of fatbodies. Licht and Gorman female
Winter dormancy extends from November to March
(1970) examined reproductive and fatbody and reproduction occurs from April to August.
LIPID CYCLING AND REPTILIAN LIFE HISTORIES
(1969) data on the sagebrush lizard
(Sceloporus graciosus) indicates that this
species also utilizes most of its lipids during
winter dormancy. Total body lipids were
much higher prior to winter dormancy
than after this period. Finally, A very (1970)
found that the common lizard {Lacerta vivipara) utilizes the total lipids in its tail during hibernation.
A number of studies indicate that lizards
utilize most of their lipids during reproduction and that lipid storage only occurred
after reproductive activity ceased. Hahn
and Tinkle (1965), in another classic study
on lipid use in lizards, demonstrated experimentally the importance of fatbody
lipids to reproduction in the side-blotched
lizard (Utastansburiana). Female lizards that
had their fatbodies removed surgically
failed to produce their first clutch at the
same time as control lizards and lizards with
sham operations. This resulted in the
former female lizards producing one clutch
less than the latter female lizards, thus indicating the importance of fatbody lipids for
producing the initial clutch of eggs in this
species. Hahn (1967), studying this species,
induced lipid mobilization using 17-/3 estradiol and based on increases in lipids in
the liver suggested that the liver was an
intermediary organ in the synthesis of
plasma vitellin from body lipids. Hoddenbach (1966), Smith (1968), and Minnich
(1971) all found an inverse relationship
between fatbody size and reproductive
activity in the six-lined racerunner
715
females have two oviductal eggs early in the
reproductive season when fatbody levels
reach maximum size. As fatbody lipid levels
decrease, the frequency of females with two
oviductal eggs also decreases suggesting
that fatbody lipids are important for reproduction. In addition, Licht (1974)
found that fatbody levels could be increased during the reproductive season in
the tropical anole Anolis cristatellus by supplemental feeding in the field. Fatbody
lipid levels were much higher in those
lizards that were fed during the reproductive season, than those that were not fed.
This data provides further evidence that
fatbody lipids are being utilized for reproduction.
Several studies indicate that a number of
lizard species utilize their lipids for maintenance during dormancy and reproduction.
Telford (1970) found that both male and
female Takydromus tachydromoides used
about 50% of their fatbody lipids during
winter dormancy, with the remainder
being used for reproduction. Goldberg
(1972) and Marion and Sexton (1971) indicated that the ovoviviparous lizards,
Sceloporus jarrovi and S. malachiticus, respec-
tively, store lipids prior to vitellogenesis
and then use these lipids for vitellogenesis.
After ovulation occurred in these two
species, the lipids continued to decrease
through the dormancy period. Following
parturition lipid levels again increased.
This pattern was similar for both males and
females in these species, with lipids being
(Cnemidophorus sexlineatus), Ameiva /estiva used for spermiogenesis in males. Gaffney
and A. quadrilineata, and the desert iguana and Fitzpatrick (1973) estimated that the
(Dipsosanrus dorsalis), respectively. Licht whiptail lizard (Cnemidophorus tigris) utilizes
and Gorman (1970) and Gorman and Licht 3000 calories of lipid for reproduction and
(1974) studying a nu mber of tropical anoles 1500 calories of lipid for maintenance dur(Anolis cristatellus, A. evermanni, A. grahami, ing winter dormancy. Figure 5 actually
A. gundlachi, A. krugi, A. lineatopus, A. pulchel- shows a greater decrease in lipids during
lus, A. sagrei and A. stratulus) found that the dormancy period (August-May) than
fatbody levels were minimal during repro- the reproductive period (June-August);
duction (wet season) and maximal when however, this species actually starts depositreproductive activity was lowest (dry sea- ing yolk in follicles prior to emergence and
son). Sexton et al. (1971) and Ruibal et al. these calories were subtracted from the
total calories used during dormancy to de(1972) found similar patterns in the tropi- termine those used solely for maintenance.
cal anoles Anolis limifrons and/4, acutus, re- This figure also demonstrates a difference
spectively. Furthermore, data from Licht in the pattern of lipid storage and utilizaand Gorman (1970) and Sexton et al. (1971) tion between females and males, with lipid
indicate that a higher percentage of
716
W. KENNETH DERICKSON
1
1
1
i
a
o
MALES
-
\
12
TOTAL LIPIDS
-
FAT 800Y LIPIDS
-
CARCASS LIPIDS
-
\
V
\
V
V
s
V
western fence lizards (Sceloporus occidentalis)
-
Cnemidophorus tigris
\
winter dormancy, into tissue. Goldberg
(1974) and Jameson and Allison (1975)
found that two montane populations of
i
FEMALES
>
utilize their lipids for both winter dormancy and reproduction; however, a
higher percentage of lipids were utilized
for reproduction. Males exhibited a greater
decrease overwinter than females (again
probably due to spermiogenesis) and
lizards of higher altitudes had significantly
higher lipid levels throughout the year than
the same species at lower altitudes. Data
(Derickson, 1976) on female northern
prairie lizards (Sceloporus undulatusgarmani)
indicated that total body lipid cycles are
quite similar to those observed by Jameson
and Allison (1975). Both Jameson and Allison (1975) and Derickson (1976) found the
total body lipid losses were equivalent to the
o
tl
total amount of lipids in eggs for S. occiden1
talis and S. undulatus garmani. This was not
AUGUST
JULY
MAY
AUGUST
JUNE
1971
1970
the case for S. graciosus where total body
MONTH
lipid losses were equivalent to about 10% of
FIG. 5. Seasonal variation of triglycende levels in
the lipids in eggs.
various body components of Texas male and female
There is some evidence that lipids may be
Cnemidophorus ligris (from Gaffney and Fitzpatrick,
1973). Winter dormancy extends from August to May used by female skinks of the genus Eumeces
and reproduction occurs from June to August.
for maintenance during incubation when
the eggs are brooded. Brooding behavior
deposition occurring much sooner in the has been observed in the broad-headed
males. Moreover, these data, like Des- skink, Eumeces laticeps (Noble and Mason,
sauer's (1955) data, show that fatbody lipid 1933), five-lined skink, E. fasciatus (Fitch,
levels are a good measure for determining 1954), great plains skink, E. obsoletus
lipid cycling patterns, but are poor indi- (Evans, 1959) and red-tailed skink, E. egcators of the absolute quantity of stored regius (Mount, 1963). Pentecost (1972) oblipids. Jameson (1974) and Derickson served that female E. laticepts were
(1976) showed that total body lipids de- emaciated along the neural spines of caudal
creased during winter dormancy and re- and trunk vertebrae after brooding. He
production in the sagebrush lizard suggested that this was possibly due to de(Sceloporus graciosus). Derickson (1976) pletion of lipid reserves in this area in order
found the greatest decrease during dor- to fulfill maintenance needs during broodmancy when no vitellogenesis was occur- ing.
ring, while Jameson (1974) found the
In summary, lipids appear to be used
greatest decrease after vitellogenesis was predominantly for reproduction in most
complete. Jameson, however, included egg lizard species. Dessauer's (1955) study is the
lipids in his total body lipids which probably only one that clearly indicates the use of
accounted for the difference in observa- lipids exclusively for maintenance during
tions. Jameson (1974) looked at lipid stor- dormancy. The studies that indicated the
age and utilization in males and observed absence of lipid cycle were based on those
the greatest decrease during winter dor- species that reproduce throughout the
mancy when he felt spermiogenesis was oc- year. Some species, such as the tropical
curring. Jameson, also, indicated that anoles which undergo no winter dormancy
juveniles convert lipids, remaining after appear to utilize their lipids exclusively for
\
-
LIPID CYCLING AND REPTILIAN LIFE HISTORIES
reproduction. In most temperate species,
reproductive demands on stored lipids are
apparently much greater than maintenance needs during winter dormancy.
FACTORS AFFECTING PATTERNS OF LI PID STORAGE
AND UTILIZATION
Food availability (including an organism's access to its food supply) is the
ultimate factor that determines (1) whether
or not an organism stores lipids, (2) when
an organism stores lipids, (3) the quantity of
lipids that is stored and (4) for what purpose the stored lipids are used. Whether or
not an organism stores lipids appears to be
a function of the food supply. If a constant
level of food is available throughout the
year, it is unlikely that an organism will
store lipids. If food levels fluctuate seasonally however, it is likely that lipids will be
stored and utilized at different times of the
year, thus, exhibiting a seasonal cycle.
When lipids are stored, the quantity of
lipids stored, and the purpose for which the
stored lipids are utilized depends on which
of three factors is influencing food availability, length of the different seasons, precipitation, or temperature. The discussion
that follows on food availability and its influence on lipid cycling will deal with
lizards, since the data for this reptilian
group are more complete.
717
quirements will be constant throughout the
year. Continual reproduction and constant
maintenance requirements would account
for the absence of lipid cycling in these four
species, since there is no real need to store
lipids.
Seasonal fluctuations in food availability
Seasonal fluctuations in food availability
can be brought about by seasonal fluctuations in precipitation and temperatures.
Seasonal changes in precipitation result in
the wet and dry seasons common to tropical
latitudes, while seasonal changes in temperature result in the warm and cold seasons
typical of temperate latitudes. Food is
generally more available during the wet
and warm seasons, with the length of a
given season influencing availability also.
Usually a longer wet or warm season will
result in greater food availability than a
shorter wet or warm season irrespective of
food abundance on a per day basis. As will
be demonstrated below, this greater food
availability apparently results in greater
lipid storage with a higher proportion of
these stored lipids being utilized for reproduction.
The seasonal cycling of lipids (Fig. 6)
observed in some tropical anoles (Licht and
Gorman, 1970; Sexton etal., 1971; Ruibale*
al., 1972) can be explained by examining
fluctuations in precipitation and its affect
on food availability. As indicated in Licht
Constant food supply
and Gorman (1970), the environments in
When environmental conditions such as which these tropical anoles occurred exhibprecipitation and temperature remain con- ited wet and dry seasons. Studies by Janzen
stant, an organism's food supply should and Schoener (1968) and Sexton et al.,
also remain constant. This appears to be the (1972) indicate that insect productivity is
case for the three Javanese house geckos reduced during the dry season and that the
(Church, 1962) and Anolis trinitatus (Licht mean insect size is much larger. According
and Gorman, 1970). These four species live to Sexton et al. (1972), sufficient food is
in tropical areas that only undergo minor apparently available for the adults; howfluctuations in precipitation. As will be ever, other conditions such as soil moisture
shown later, insect productivity is closely or food availability for the offspring precorrelated with precipitation and this fairly vent reproduction during the dry season.
constant level of precipitation should result Sexton et al. (1971) suggest that the lower
in a fairly constant food supply for these soil moisture during the dry season would
four-insectivorous lizards. This constancy result in lower hatching success, since the
of food supply results in continual repro- eggs apparently need a great deal of moisduction by these species. Since temperature ture. While this is certainly a plausible
is also fairly constant, maintenance re- argument, it is also possible that an in-
718
W. KENNETH DERICKSON
%
50
Anolis grahami
J F M A M J J A S O N D
.'•,
J F M A M J J A S O N D J F M A M
l96
1968
Month
9
FIG. 6. Reproductive and fatbody cycles for Bermuda male and female Anolis grahami (from Licht and
Gorman, 1970). The upper graph depicts the percentage of females in reproductive condition (•
•) and
weight of fatbodies(»
•). The lower graph represents the same, only for males, and also contains the
number of lizards examined on the abscissa. These
cycles are representative for a number of tropical
anoles.
sufficient biomass of small insects is available to the hatchlings and juvenile anoles
during the dry season. The smaller mouth
size of these offspring would limit their
access to the available food, making offspring production during this time wasteful. Since sufficient food appears to be available to the adults during the dry season,
the energy that would have been put into
reproduction during this time is conserved
in the form of lipids. As a result, lipid levels
increase during the dry season, reaching
maximal levels prior to the onset of the wet
season and then begin to decrease as reproductive activity resumes. This stored
energy apparently allows these anoles to
produce a greater number of offspring
during the wet season, since a greater
frequency of females with two oviductal
eggs was observed early in the wet season
when lipid levels are high (Licht and Gorman, 1970; and Sextons a/., 1971). Anoles
typically produce a single egg every two
weeks, and the presence of two oviducal
eggs at the same time would indicate a
shorter time between laying of successive
eggs. As the lipid levels decrease, the abundance of females with two oviductal eggs
also decreases. At the end of the reproductive season lipid levels are minimal and
begin to increase with the onset of the dry
season.
The seasonal cycling of lipids (Fig. 5) in
many temperate lizards and some tropical
anoles (Gaffney and Fitzpatrick, 1973;
Goldberg, 1974; Gorman and Licht, 1974;
Jameson, 1974; Jameson and Allison, 1975;
and Derickson, 1976) can be explained by
examining seasonal fluctuations in temperature and its affect on food abundance and
access to available food. Insect productivity
should be less during the cold season, since
like lizards, insects are ectotherms. These
cold seasons would therefore result in
lower food availability and because of
metabolic limitations, as a result of ectothermy, restrict the lizards' access to what
food is available. Lizards have adapted to
this period of low food availability by becoming dormant, thereby reducing
metabolic needs. Even during dormancy,
however, lizards do need some energy to
maintain a minimal metabolic level. Mueller (1969) estimated that a five gram
Sceloporus graciosus would require 2100
calories for maintenance during dormancy
at 15°C. In order to meet this metabolic
demand lizards store lipids prior to dormancy and utilize them during dormancy.
Gaffney and Fitzpatrick (1973) estimated
that an average-sized adult Cnemidophorus
tigris uses about one-third of its stored lipids
during dormancy. The quantity of lipids
necessary for maintenance during dormancy depends on the length of the dormancy period. Apparently, any lipids remaining after dormancy is over are used
for reproduction. The greater the differential between the quantity of lipids stored
prior to dormancy and the quantity used
during dormancy, the more that are available for reproduction. In C. tigris about
two-thirds of the stored lipids are available after dormancy and these are used
for reproduction (Gaffney and Fitzpatrick,
1973). For Sceloporus graciosus over 50%
of the stored lipids are apparently used
during dormancy (Derickson, 1976). Of
LIPID CYCLING AND REPTILIAN LIFE HISTORIES
the lipids remaining after dormancy in
this species a large proportion are apparently utilized for maintenance purposes
since Tinkle (1973) indicates that this
species is out for several days before vitellogenesis occurs and Derickson (1976)
found that lipid levels decreased during
this period of time (both authors studied
lizards from the same general area). This
results in very little lipid usage for reproductive purposes in this species. Goldberg
(1974) and Jameson and Allison (1975)
719
months). Moreover, anoles that Gorman
and Licht (1974) collected from high altitudes were exposed to longer cold periods
and exhibited higher lipid levels, than
anoles at lower altitudes.
From the above data, it is clear that in
general there is an inverse relationship between stored lipid levels and reproductive
activity. When reproductive activity ceases
or is reduced, lipids begin to accumulate
and may be used at a later date exclusively
for reproduction (tropical anoles) or for
both found that Sceloporus occidentalis at both maintenance during dormancy and
higher altitudes used more of their lipids reproduction (most temperate lizards).
for dormancy than those at lower altitudes. The factor that ultimately determines these
The period of dormancy was longer at the patterns is food availability, and this factor
higher altitudes, resulting in greater lipid is strongly influenced by both precipitation
requirements. Populations at both altitudes and temperature. In general, the longer
utilized their lipids for reproduction, but the dry or cold season the more lipids that
the population of S. occidentalis at lower can be stored (tropical anoles) or the more
altitudes utilized a higher percentage of lipids that are used during dormancy
their stored lipids for reproduction. In- (temperate lizards). Among temperate lizterestingly, female S. occidentalis at higher ards, the amount of energy available for
altitudes produced fewer clutches and as a reproduction will be determined by the
result had a higher stored lipid level at the amount of lipids that can be stored prior to
end of the reproductive season than those dormancy and the amount of lipids reat lower altitudes. Apparently, the shorter quired during dormancy.
reproductive season at higher altitudes
prevents the use of all available stored lipids
LIPID CYCLING AND LIFE HISTORIES
for reproduction, or minimal lipid levels
are maintained to insure survival over the
A study of two congeneric lizards, the
long dormant period. On the other hand, S.
northern
prairie lizard {Sceloporus undulatus
occidentalis at lower altitudes and other
and
the northern sagebrush lizard
garmani)
species such as 5. undulatus garmani (De(S. graciosus graciosus), indicates how food
rickson, 1976) that have long reproductive
seasons utilize most of their available lipids availability can influence lipid cycling and
for reproduction. The consequences of this life histories (Derickson, 1976). The northextra expenditure of energy for reproduc- ern prairie lizard and northern sagebrush
tion are discussed below. Gorman and Licht lizard are both insectivorous and are active
(1974) found that tropical anoles in Puerto about seven months out of the year.
Rico exhibited similar patterns of lipid Though the two species have the same accycling to the anoles they studied in the tive season length, the two study areas
Caribbean, only the cycling was apparently where they were collected (Reno County,
due to seasonal fluctuations in tempera- Kansas for the northern prairie lizard and
ture. These authors suggested that temp- Washington County, Utah for the northern
erature, during the cold months are too low sagebrush lizard) had markedly different
for eggs to hatch successfully. If this is true levels of preciptation. Average annual rainthe energy that would be used for repro- fall over the past 30 years was 31 inches for
duction should be stored during these cold the Kansas study site and 10 inches for the
months. Their data do indeed indicate that Utah study site. The difference in precipilipid levels are lowest during the reproduc- tation should result in differences in food
tive season (warm months) and highest availability for these two species. Data from
during the non-productive season (cold French (1971) demonstrates that a significant positive correlation exists between
720
W. KENNETH DERICKSON
insect biomass and precipitation (Fig. 7) in
temperate latitudes. Janzen and Schoener
(1968) found a similar relationship between
insect productivity and precipitation in
tropical latitudes.
This difference in food availability can be
used to explain observed differences in
lipid cycling patterns and life histories for
the northern prairie lizard and northern
sagebrush lizard. Assuming that the northern prairie lizard does indeed have more
food available to it, this abundance results
in this species reaching reproductive size in
less than one year (Fig. 8) and having
higher lipid levels than the northern sagebrush lizard before and after the five
month dormancy period (Fig. 9). The
northern sagebrush lizard with its low food
availability requires about two years (Fig. 8)
to reach reproductive size and has lower
lipid levels before and after its five month
dormancy period (Fig. 9). The greater lipid
levels after dormancy apparently enable
female northern prairie lizards to start
producing the initial clutch of eggs from
stored energy, while the northern sagebrush lizard is apparently more dependent
on ingested energy to produce its initial
clutch of eggs. This results in the northern
prairie lizard laying its first clutch in May
and the northern sagebrush lizard depositing its first clutch in June when the Kansas
species is laying its second clutch. Both
species deposit their final clutch in July
(Fig. 8). Therefore, the ability to store
greater quantities of lipids, due to greater
food availability, effectively extends the reproductive season for the northern prairie
lizard, enabling it to get off 3 clutches of
FIG. 7. Insect biomass as a function of annual precipitation, constructed from data in French (1971).
**—0.01 level of significance.
-JLiLS
SflA.ILl 1
1
>
1
,1 J
J
A
S
J
i
D
J
FIG. 8. Time required to reach sexual maturity and
the number of clutches produced seasonally by adults
originating from the initial and final clutches of a
season of Kansas Sceloporus undulatus garmani and
Utah S. graciosus graaosus. Clear areas represent
periods of either maintenance, growth, or vitellogenesis. Stippled and cross-hatched areas represent
periods of hibernation and reproduction, respectively.
Hatching, sexual maturity and death are indicated by
the letters H.S.and D, respectively. Only 2 years out of
potentially 6 are shown for S. graaosus graciosus (from
Derickson, 1976).
eggs compared to only 2 clutches for the
northern sagebrush lizard.
As seen in Table 1, production of an additional clutch of eggs results in an additional expenditure of 5000 calories for the
northern prairie lizard. A comparison of
the total calories in eggs in a given season
and total body calories indicates clearly that
the northern prairie lizard has a higher reproductive effort in a given season than the
northern sagebrush lizard. This higher reproductive effort in the Kansas species apparently results in a greater mortality since
very few lizards live to a second reproductive season (Fig. 8). The northern sagebrush lizard, on the other hand, has a lower
reproductive effort and reproduces for
about four years (Fig. 8). Interestingly, this
longer life span enables the Utah species to
put more energy into reproduction in its
life-time than the northern prairie lizard
(Table 1). Tinkle and Hadley (1975) have
found this same correlation between life
span and reproductive effort for a number of lizard species. The greater emaciation of the northern prairie lizard at the
end of the reproductive season (Fig. 10)
may make this species more vulnerable to
721
LIPID CYCLING AND REPTILIAN LIFE HISTORIES
predation and thus accounts for its higher
mortality.
In summary, greater food availability
would enable species to reach reproductive
size at an earlier age and to store greater
quantities of lipids. Greater quantities of
stored lipids in turn can result in higher
reproductive efforts which can result in
shorter life spans. Conversely, lower food
availability would result in a longer time to
reach reproductive size and lower quantities of stored lipids. Smaller quantities of
stored lipids can result in lower reproductive efforts which can result in longer life
spans. It is apparent, therefore, that in
some cases a correlation exists between patterns of lipid cycling and life histories, with
food availability being the ultimate determining factor.
CONCLUSIONS
13
I
A number of lipid cycling patterns have
been observed among reptiles: (1) no lipid
cycling, (2) storing and utilizing lipids exclusively for maintenance during dormancy, (3) storing and utilizing lipids exclusively for reproduction, and (4) storing and utilizing lipids for both maintenance during
dormancy and reproduction. Because of its
effects on food availability, seasonality of
precipitation and/or temperature appears
to determine when lipids are stored, the
quantity of lipids stored, and the purposes
for which they are utilized. In tropical
latitudes, lipids may be stored during the
dry season and utilized for reproduction
during the wet season. In temperate
latitudes lipids may be stored prior to
winter dormancy and utilized during dormancy, with the remaining lipids being
used for reproduction. In both cases, howTABLE 1. Estimated egg calories/season, egg calories/
lifetime, body calories, and egg calories/season/body calorie
PH
V
01
02
03
PR
for Kansas Sceloporus undulatus garmani (PS) and
Utah S. graciosus graciosus (SL).
S»NPLE
PS
SL
FIG. 9. Seasonal variation of mean lipid levels in
Kansas S. undulatus garmani (open bars) and Utah S. Egg calories/season
13,900 8,900
graciosus graciosus (solid bars). Samples are posthiber- Egg calories/lifetime
13,900 35,600
nation (PH), vitellogenesis (V), gravid-initial clutch
8,902
6,127
Body calories
(01), gravid-middle or initial clutch (02), gravid-final Egg calories/season/body calorie
2.53
1.45
clutch (03) and postreproduction (PR). Horizontal
bars represent means; vertical lines the ranges; and Egg calories/season and egg calories/lifetime are on
vertical bars one standard error. Numbers above bars a per gram lean dry body weight basis to correct for
indicate sample sizes. (A) total body lipids; (B) egg size differences between the two species. These data
lipids. (From Denckson, 1976)
are from Derickson (1976).
722
3.0-
2.0-
W. KENNETH DERICKSON
As summarized above, lipid cycling can
be correlated with life history features, with
food availability being the ultimate determining factor. Studies that look at demographic and physiological features as well
as prey availability are needed to support
these correlations. By doing such studies on
reptiles and other animals it should be possible to determine the role of lipids in their
life histories.
REFERENCES
3.0-
2.0.
1.0-
Aleksiuk, M. and K. W. Stewart. 1971. Seasonal
changes in the body composition of the garter snake
(Thamnophis sirtalis parietalis) at northern latitudes.
Ecology 52:485-490.
A very, R. A. 1970. Utilization of caudal fat by hibernating common lizards, Lacerta vivipara. Comp.
Biochem. Physiol. 37:1 19-121.
Belkin, D. A. 1965. Reduction of metabolic rate in
response to starvation in the turtle. Slenothaerus
minor. Copeia 1965:367-368.
Brian, B. L., F. G. Gaffney, L. C. Fitzpatrick, and V. E.
Scholes. 1972. Fatty acid distribution of lipids from
carcass, liver and fat bodies of the lizard,
Cnemidophorus ligris, prior to hibernation. Comp.
Biochem. Physiol. 41B:66 1-664.
Bnsbin, I. L., Jr. 1972. Seasonal variations in the live
weights and major body components of captive box
turtles. Herpetologica 28:70-75.
Church, G. 1962. The reproductive cycles of the
Javanese House Geckos, Cosymbotus platyurus, Hemidactylus frenatus, and Peropus mullilatus. Copeia
1962:262-269.
Derickson, W. K. 1974. Lipid deposition and utilization in the Sagebrush Lizard, Sceloporusgraciosus: Its
significance for reproduction and maintenance.
Comp. Biochem. Physiol. 49A:267-272.
0.0Derickson, W. K. 1976. Ecological and physiological
50
60
70
aspects of reproductive strategies in two lizards.
SNOUT-VENT
LENGTH(nn)
Ecology 57:445-458.
Dessauer, H. C. 1955. Seasonal changes in the gross
FIG. 10. Lean dry body weight versus snout-vent
organ composition of the lizard Anolis carolinensa. J.
length for post hibernation (•
•) and final clutch
Expt. Zool. 128:1-12.
(*
•) in Kansas S. undulalus garmani and Utah S
graciosus graciosus. (A) Kansas lizards; (B) Utah lizards. Emerson, D. N. 1967. Preliminary study on seasonal
liver lipids and glycogen and blood sugar levels in
All regressions are significant at the 0.01 level. Comthe turtle Graptemys pseudogeographica from South
parisons between regression lines for both species
Dakota. Herpetologica 23:68-70.
were also significant at the 0.01 level (from Derickson,
Evans, T. L. 1959. A motion picture study of maternal
1976).
behavior of the lizard, Eumeces obsoletus Baird and
Girard. Copeia 1959:103-110.
ever, it is only after reproduction ceases Ferguson,
G. W. and C. H. Bohlen. 1973. The regulathat lipids are stored. Apparently, the more
tion of Prairie Swift (Lizard) populations. A progfood that is available the more lipids that
ress report. Proceedings of the Third iMidwestern
Prairie Conference 3:69-72.
will be utilized for reproduction. This in
turn will result in a higher reproductive Fitch, H. S. 1954. Life history and ecology of the fivelined skink. Univ. Kans. Publ. Mus. Nat. Hist. 8:1effort in a given season. Greater reproduc156.
tive effort in a given season may result in a French, N. 1971. The grassland biome: Analysis and
shorter life span.
synthesis of first year data. Range Science Depart-
LIPID CYCLING AND REPTILIAN LIFE HISTORIES
723
meni Science Series No. 10. Colorado State Univer- Morlock, H., S. Herrington, and M. Oldham. 1972.
Weight loss during food deprivation in the eastern
sity, Fort Collins, Colorado.
painted turtle, Chrysemys picta picla. Copeia
Gaffney, F. C. and L. C. Fitzpatrick. 1973. Energetics
and lipid cycles in the lizard, Cnemidophorus tigris. 1972:392.
Copeia 1973446-452.
Mount, R. H. 1963. The natural history of the redGibbons,J. W. 1972. Reproduction, growth and sexual
tailed skink, Eumeces egregius Baird Amer. Midi.
dimorphism in the canebrake rattlesnake (Crotalus
Natur. 70:356-385.
horridus atricaudatus). Copeia 1972:222-226.
Mueller, C. F. 1969. Temperature and energy characteristics of the sagebrush lizard (Sceloporus graaosus)
Goldberg, S. R. 1972. Seasonal weight and cytological
in Yellowstone National Park. Copeia 1969:153changes in the fat bodies and liver of the iguanid
160.
lizard Sceloponisjarrow Cope. Copeia 1972:227-232.
Goldberg, S. R. 1974. Reproduction in mountain and Noble, G. K. and E. R. Mason. 1933. Experiments on
lowland populations of the lizard Sceloporus occiden- the brooding habits of the lizards Eumeces and
talis. Copeia 1974:176-182.
Ophisaurus. Am. Mus. Nov. 619:1-29.
Gorman, G. C. and P. Licht. 1974. Seasonality in ovar- Parker, W. S. and W. S. Brown. 1974. Mortality and
ian cycles among tropical Anolis lizards.
weight changes of great basin rattlesnakes (Crotalus
Ecology 55:360-369.
xnndis) at a hibernaculum in northern Utah. Herpetologica 30:234-239.
Hadley, N. F. and W. W. Christie. 1974. The lipid
composition and tnglyceride structure of eggs and Parker, W. S. and E. R. Pianka. 1973. Notes on the
ecology of the iguanid lizard Sceloporus magister.
fat bodies of the lizard Sceloporus jarrovi. Comp
Biochem. Physiol. 48B:275-284.
Herpetologica 29:143-151.
Hahn, W. E. 1967. Estradiol-induced vitellinogenesis Pentecost, E. D. 1972. Bioenergetics and population
and concomitant fat mobilization in the lizard Uta
dynamics of the broad-headed skink, Eumeces
stansburiana. Comp. Biochem. Physiol. 23:83-93.
laticeps. Ph.D. Diss. Univ. of Illinois, Urbana.
Hahn, W. E. and D. W. Tinkle 1965. Fatbody cycling Pianka, E. R. 1970. Comparative autecology of the
lizard Cnemidophorus tigris in different parts of its
and experimental evidence for its adaptive significance to ovarian follicle development in the
geographic range. Ecology 51:703-720.
lizard Uta stansburiana. J. Expt. Zool. 158:79-86. Ruibal, R., R. Philibosian, and J. L. Adkins. 1972. Reproductive cycle and growth in the lizard Anolis
Hirth, H. F. 1966. Weight changes and mortality of
aculus. Copeia 1972:509-518.
,
three species of snakes during hibernation. Herpetologica 22:8-12.
Sexton, O. ] . , E. P. Ortleb, L. M. Hathaway, R. E.
Hoddenbach, G. A. 1966. Reproduction in western
Ballinger,and P. Licht. 1971. Reproductive cyclesof
Texas Cnemidophorus sexlineatus (Sauria: Teiidae). three species of anoline lizards from the isthmus of
Panama. Ecology 52:201-215.
Copeia 1966:110-113.
Hoddenbach, G. A. andj. R. Lannom.Jr. 1967. Notes Sexton, O. J., J. Bauman, and E. Ortleb. 1972.
Seasonal food habits of Anolis limifrons. Ecol.
on the natural history of the Mexican gecko, Phyl53:182-186.
lodactylus tuberculosus. Herpetologica 23:293-296.
Jameson, E. W.,Jr. 1974. Fat and breeding cycles in a Smith, R. E. 1968. Studies on reproduction in Costa
montane population of Sceloporus gracwsus. J. of Rican Ameiva /estiva and Ameiva quadrilineata
(Sauria: Teiidae). Copeia 1968:236-239.
Herpetol. 8:311-322.
Jameson, E. W., Jr. and A. Allison. 1976. Fat and St. Girons, H. 1957. Le cycle sexual chez Vipera aspis
breeding cycles in two montane populations of
(L.) dou l'ouest de la France. Bull. Biol. de la France
etde la Belgique 91:284-350.
Sceloporus ocadentalis. J. of Herpetol. (In press)
Janzen, D. H. and T. W. Schoener, 1968. Differences Telford, S. R., Jr. 1970. Seasonal fluctuations in liver
and kidney weights of the Japanese lacertid Takyin insect abundance and diversity between wetter
dromus tachydromoides. Copeia 1970:681-689.
and drier sites during a tropical dry season. Ecology
49:96-110.
Tinkle, D. W. 1962. Reproductive potential and cycles
Klauber, L. M. 1956. Rattlesnakes: their habits, life his- in female Crotalus alrox from northwestern Texas.
tories and influence on mankind. Vol. 1. Univ. of Calif. Copeia 1962:306-313.
Tinkle, D. W. 1973. A population analysis of the
Press, Berkeley, Calif.
Sagebrush Lizard, Sceloporus graciosus in southern
Licht, P. 1974. Response of Anolis lizards to food
supplementation in nature. Copeia 1974:215-221.
Utah. Copeia 1973:284-296.
Licht, P. and G. C. Gorman. 1970. Reproductive and Tinkle, D. W. and N. F. Hadley. 1975. Lizard reprofat cycles in Caribbean Anolis lizards. Univ. Calif.
ductive effort: Caloric estimates and comments on
its evolution. Ecology 56:427-434.
Publ. Zool. 95:1-52.
Marion, K. R. and O. J. Sexton. 1971. The reproduc- Vainio, I. 1931. Zur verbreitung und biologie der
tive cycle of the lizard Sceloporus malachilicus in Costa Kreuzotter, in Finland. Ann. Soc. Zool. - Bot. Fenn.
Rica. Copeia 1971:517-526.
12:1-19.
Minnich, J. E. 1971. Seasonal variation in weight Wharton, C. H. 1966. Reproduction and growth in the
length relationships and fat body size in the desert
cottonmouth, Agkistrodon piscivorous Lacepede, of
iguana, Dipsosaurus dorsalis. Copeia 1971:359-362. Cedar Keys, Florida. Copeia 1966:149-161.