ecology and physiological aspects of reproductive ...webapps.fhsu.edu/ksherp/bibfiles/5012.pdf ·...

Ecology (1976) 57: pp. 445-458

ECOLOGICAL AND PHYSIOLOGICAL ASPECTS OF

REPRODUCTIVE STRATEGIES IN TWO LIZARDS'

W. KENNETH DERICKSON2

Division of Biology, Kansas State University, Manhattan, Kansas 66506 USA

Abstract. Two lizard species, the northern prairie lizard (Sceloporus undulatus garmani) from Reno County, Kansas and the northern sagebrush lizard (Sceloporus graciosus graciosus) from Washington County, Utah, were used to test four hypotheses and one assumption related to the theory of r- and K-selection. The northern prairie lizard is short-lived, matures early, and has a high reproductive effort (r-strategist) while the northern sagebrush lizard is long- lived, has delayed maturity, and a low reproductive effort (K-strategist). One of the assumptions of the r- and K-selection theory is that competition for food is more intense for K- strategists than for r-strategists. Given this assumption, greater food availability for the prairie lizard was hypothesized to result in (1) a higher level of body lipids, (2) a higher rate of lipid utilization, (3) a lower percentage of ingested energy available for metabolism, and (4) an expenditure of less energy per offspring than in the sagebrush lizard.

Total lipid levels in the two species collected before and after hibernation indicated that prairie lizards had significantly higher lipid levels than sagebrush lizards during both collection periods. A comparison of the amount of body lipids lost and the amount of egg lipids gained during vitellogenesis of the first clutch suggested that more lipids are being utilized for egg production in prairie lizards than in sagebrush lizards.

Sagebrush lizards apparently are better adapted physiologically to lower food levels since they had lower rates of lipid utilization during starvation studies and they extracted more energy usable for metabolism from ingested food than prairie lizards.

Although both species expended about the same amount of energy on a given clutch of eggs, prairie lizards produced more offspring per clutch and therefore expended less energy per offspring. Prairie lizards produced as many as three clutches per season as compared to two clutches per season for sagebrush lizards, and changes in length-lean weight relationships for the two species over a given season suggested that the additional clutch of eggs produced by prairie lizards may be contributing to the higher mortality observed in this species.

Indirect evidence, based on precipitation levels and insect biomass at the two study sites and mouthgapes of the two species, supported the assumption that more food was available to the prairie lizards than the sagebrush lizard. Higher precipitation levels (indicating greater insect biomass) occurred at the prairie lizard collection site and this species had a smaller mouthgape index, indicating greater specialization in utilization of prey sites.

Key words: Energy, available for metabolism, expended per offspring; Kansas; lipids; prairie swift; sagebrusli lizard; strategy, reproductive; Utah.

INTRODUCTION

Although a number of studies have been done on

the importance of lipids in the life histories of

various animals, no one has attempted to correlate

differences in lipid storage and utilization with life

history differences. In most seasonal animal spe-

cies, lipids should be important since lipid storage

is a biochemically efficient way to package energy

for later usage. A gram of stored lipids represents

38 kJ (9 kcal) of energy, while a gram of carbo-

hydrate or protein, with the higher H,O content,

represents only 17-21 kJ (4-5 kcal) of energy.

Therefore, more energy can be stored in a smaller

package with lipids. In nonseasonal (acyclic) animal

'Manuscript received 10 June 1974; revised 19 De- cember 1975; accepted 19 January 1976.

2 Present address: Division of Environmental Impact Studies, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, Illinois 60439 USA.

species, lipid storage is probably not important since

food is always presumed to be limiting but never

critically short (e.g., reproduction still occurs at low levels).

Nikolskii (1969) has shown that a correlation

exists between lipid levels and fecundity in a number of commercial fishes. Odum (1960), Helms (1968) and King (1970) demonstrated marked increases in lipid storage prior to migration in several passerine bird species. Jameson and Mead (1964) and Davis (1967) indicated that lipids are used during hibernation in several small mammal species.

Sawicka-Kapusta (1968) found lipid depletion asso-

ciated with reproduction in field mice. A vast body

of literature on lizards indicates that some species use

lipids during hibernation (Dessauer 1955; Mueller

1969, Derickson 1974), while others use lipids during

reproduction (Hahn and Tinkle 1965, Licht and Gor-

man 1970, Telford 1970). Church (1962) could find

no evidence of lipid deposition and utilization in

446 W. KENNETH DERICKSON Ecology, Vol. 57, No. 3

three species of Jamaican House Geckos which live in a nonseasonal environment.

The literature on life history phenomenon is also bountiful. Several authors (Cole 1954; MacArthur and Wilson 1967; Gadgil and Bossert 1970; Hairston

et al. 1970; Pianka 1970, 1972) have put forth arguments to explain variations in life history phe-

nomenon. As a result of work done by these authors it is known that a gradient of life history strategies (strategy being used in a teleological sense) exists,

with the two extreme strategies being organisms with short lives, high reproductive efforts, and early ma-

turity and those with long lives, low reproductive effort, and delayed maturity. Tinkle (1969), Tinkle et al. (1970), and Gadgil and Solbrig (1972) have presented empirical evidence on lizards and dande- lions, respectively, that supports this dichotomy of life history strategies. This dichotomy has been more

popularly referred to as r- and K-selection (Mac- Arthur and Wilson 1967; Gadgil and Bossert 1970; Pianka 1970, 1972; Gadgil and Solbrig 1972), al-

though Hairston et al. (1970) choose to call it b and d selection. Basically, the theory of r- and K-selection states that fitness is determined by r (intrinsic rate of increase) in species living in an environment where mortality is unpredictable, while in species living in environments where mortality is more pre-

dictable, fitness is determined by K (environmental carrying capacity). In other words, fitness is determined primarily by density independent factors in r-

selected species and by density-dependent factors in K-selected species. For lack of better terminology, r- and K-selection will be used; however, the inde-

pendent variable identified as the causative agent is food availability per individual. This includes not only the potential productivity available but also an organism's access to that productivity. This avoids the issue of whether r-selected species are regu- lated by density-independent factors and K-selected species by density-dependent factors. Also, to avoid another problem with the theory it is assumed that the adult and juveniles of the species studied are both utilizing similar resources. Other assumptions are (1) that an optimum size for reproduction exists and that greater food availability will result in reach- ing this size at an earlier age; (2) that there is a positive correlation between food availability and reproductive effort; and (3) that an inverse relationship between reproductive effort per season and life span exists.

Since differences in life history strategies and in

patterns of lipid storage and utilization are known to

exist in lizards, it seems logical to conclude that

the two may be interrelated. In other words, given

the assumption that differences in food availability

per individual can result in a variety of life history

strategies, it is likely that this same factor may also

explain observed differences in lipid storage and

utilization.

Differences in food availability per individual

should also lead to differences in (1) rates at which

lipids are utilized during periods of food shortage,

(2) the percentage of ingested energy available for metabolism, and (3) the amount of energy expended

on each offspring. An individual of a species that

has historically been exposed to low food availabilities should maximize its usage of available food. This may

be done by maximizing net energy yield per unit of feeding time, as suggested by Emlen (1966), Mac- Arthur and Pianka (1966), MacArthur and Wilson

(1967) and Schoener (1971), through utilization of prey with high caloric values or by utilizing prey that can be captured with a minimum of pursuit and cap- ture time. Given no difference in quality or captur-

ability of prey, a species that has been exposed to lower food levels may maximize energy obtained from

ingested energy by (1) reducing losses of ingested

energy via respiration, secretions, and excretions, and (2) by conserving stored energy during periods of food shortage. On the other hand, individuals of a species that has historically been exposed to abundant food supplies need to be less stringent in their conservation of stored energy during periods of food shortage and in their utilization of ingested

energy.

Food availability to the offspring may dictate how a parent apportions the ingested and stored energy available for reproduction. If the offspring and adults of a given species have both been exposed to low levels of food, a parent may increase its fitness by expending more energy per offspring in the form of parental care or by producing larger offspring (Smith and Fretwell 1974). This assumes

that though fewer offspring are produced, their

survivorship is enhanced by an increased competitive

ability. If, on the other hand, food is abundant to

both adults and offspring, the parent may increase

its fitness by expending less energy per offspring.

This would result in the production of more offspring

and it is assumed that survivorship is enhanced by

sheer numbers. Harper et al. (1970) indicated that

plants under intense competition put more energy

into each offspring and produce fewer of them. Dr.

Eric R. Pianka (personal communication) compiled

a list of various lizard species and indicated that there

tends to be a negative relationship between the

amount of energy expended per offspring and the

number of eggs produced.

By using a r- and K-selected lizard species, an at-

tempt will be made to verify the following hy-

potheses:

Late Spring 1976 ASPECTS OF REPRODUCTIVE STRATEGIES IN LIZARDS 447

1) Given greater food availability for the r-se-

lected lizard species, this species should have

higher lipid levels before and after hibernation

than the K-selected lizard species.


lected lizard species, this species should have

a higher rate of lipid utilization during periods

of food shortage than the K-selected lizard

species.

3) Given greater food availability for the r-selected

lizard species, this species should obtain less

energy for metabolism per unit of ingested

food than the K-selected lizard species.


lected lizard species, this species should pro-

duce more offspring with less energy expended

per offspring, while the K-selected lizard spe-

cies should produce fewer offspring with more

energy expended per offspring.

SPECIES STUDIED

Females of the lizards Sceloporus undulatus gar- inani and Sceloporus graciosus graciosus were chosen

for this study. Some of the reasons for choosing

lizards and these particular species were (1) they

are easy to study either in the field or laboratory; (2) information related to the theory of the evolution of life history strategies in lizards is available from

work done by Tinkle (1969) and Tinkle et al. (1970); (3) a number of studies have looked at the

role of lipids in lizards; (4) reproductive effort can

be better approximated (since lizards exhibit no parental care, kilojoules per clutch and number of clutches per season should provide a reasonably accurate measure of reproductive effort); (5) these species are similarly sized; thus, effects of body size differences on metabolism are minimized; and (6) in terms of lifespan, age at maturity, and reproductive effort, these two subspecies are known (Ferguson and Bohlen 1973, on S. u. garmani and Tinkle 1973, on S. g. graciosus) to fit the r- and K-selection corre- lates of Pianka (1970).

Sceloporus undulatus garmani is a small iguanid

lizard found predominantly in eastern Colorado, Kansas, Nebraska, and Oklahoma. This subspecies, hereafter referred to as the northern prairie lizard, is found in a variety of habitats, including sandy areas, sandstone cliffs, sparse grass, woodpiles, and old trash piles (Smith 1946). At the collection site, located in Reno County, Kansas, they were found in grazed sand prairie around old fallen cottonwood (Populus sp.) trees and refuse piles.

Prairie lizards feed on arachnids, Coleoptera, Hy-

menoptera, Diptera, Orthoptera, and Hemiptera (Smith 1946). Their feeding strategy is to sit and

LaJ

m SCELOPORUS GRACIOSUS GRAC/OSUS

z2 I H S '1-I m C H s

SCEZOPORUS UNDULATUS GARMANI

co H S D

ti H S D

J A SON D J F M A MJJ A NDJFMAMJJASONDJ MONTH

FIG. 1. 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 northern prairie lizards, Sceloporus undulatus garmani and Utah northern sagebrush lizards, S. graciosus graciosus. 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 yr out of potentially 6 are shown graphically for S. g. graciosus. These graphs are partly based on data from studies done by Ferguson and Bohlen (1973) and Tinkle (1973).

wait until prey come within striking distance and

then give pursuit. The average lifespan is 1 yr, age

at maturity 8-9 mo, and reproductive effort is about

three clutches/season (Ferguson and Bohlen 1973). An early age at maturity and production of three

clutches results in considerable variation in egg-laying

times (Fig. 1). Offspring from the first clutch hatch

in mid-July, the second in mid-August, and the third

in early September. Lizards from the first clutch

will be ready to reproduce the following spring,

while those from succeeding clutches will not mature

until late spring or early summer. First clutch off-

spring have the potential for laying clutches in May,

June, and July of their first breeding season.

Probably, because of this high reproductive effort

at such a young age, the first clutch offspring rarely

reproduce a second season. Conversely, offspring

from the second and third clutches may produce 1-2

clutches in their first breeding season. These off-

spring from later clutches are more likely to survive

a second winter (but most do not) and produce addi-

tional clutches of eggs. Therefore, an early age at

maturity and the production of three clutches by

some lizards results in considerable variation of lay-

ing times and size of lizards laying eggs.

Sceloporus graciosus graciosus is found predomi-

nantly in Idaho, Nevada, Utah, and Wyoming at

altitudes > l,500 m. As the common name, northern

sagebrush lizard, suggests, this species is common


in sagebrush communities, but also may be found in open flat lands, bouldered regions, and forested slopes (Smith 1946). Tinkle (1973) studied this

subspecies in the Kolob region of Zion National Park in southwestern Utah. The Kolob includes

sandy sagebrush (Artemisia sp.) flats and sandy areas

between extensive areas of eroded sandstone. My collection site was a few kilometers east of Zion Na-

tional Park East Gate. The altitude is comparable to

that of Tinkle's study area, 2,000 m, and is char- acterized by sandy sagebrush flats.

Sagebrush lizards have the same general diet and foraging patterns as prairie lizards. They are known

to be long-lived, > 6 yr, and mature in 2 yr (Stebbins and Robinson 1946, Tinkle 1973). The number of

clutches produced probably varies with altitude and latitude, however, in southwest Utah this species lays

two clutches of about four eggs each season (Tinkle 1973). This reproductive schedule will allow an

average adult to produce about eight clutches in a lifetime. Unlike prairie lizards, sagebrush lizard hatchlings from first and second clutches reach reproductive maturity at the same time, the beginning of the third season. This results from an extra sum-

mer of growth prior to reproduction, which allows all hatchlings to reach reproductive size before their third season (Fig. 1) .

MATERIAL AND METHODS

Prairie lizards and sagebrush lizard females were collected over a 2-yr period (1972-1973) from Reno County, Kansas and Washington County, Utah, respectively. When possible 10 individuals of each species were collected after hibernation, during the vitellogenic and gravid periods of each clutch of eggs, and about 1 mo after reproduction had ceased. These collection periods were based on observed lipid cycling patterns in other lizard species, such as Anolis carolinensis (Dessauer 1955).

Field samples

Seventy-eight prairie lizards and 88 sagebrush lizards were collected in the field and kept cool until transferred to the laboratory, where they were quick- frozen immediately and analyzed at a later date for total lipids (simple and complex). The carcass (minus viscera) and eggs of each lizard were weighed and dried to a minimal and constant weight in a thermal vacuum oven at 40?C and 30 psi (Horwitz et al. 1970). Each part was then homogenized in 2: 1 vol/vol chloroform-methanol solution in a tissue homogenizer and the homogenates treated according to the Folch method (Folch et al. 1957). Weight of total lipids for each depot were recorded as a per-

centage of the lean (no lipids) dry body weight (LDBW) to correct for variations in body size. Pre-

liminary studies indicated that complex lipids, those

generally not available as storage lipids, represented < 10% of the total lipids. A similar figure for com-

plex lipids was found in Sceloporus jarrovi by Hadley and Christie (1974). Since complex lipids represent such a small percentage of the total lipids, no at-

tempt was made to exclude these lipids. Accordingly, all figures are slight overestimates of storage lipids

in both species.

Rates of lipid utilization were calculated for both

species from field samples by comparing lipid levels

in lizards that had come out of hibernation with those ready to lay their first clutch (gravid-initial

clutch). Individual lipid levels (mg/g LDBW) of the initial gravid sample was subtracted from the

mean lipid level of the posthibernation lizards and this figure was divided by the number of days be-

tween these two samples. The same method was used

to calculate rates of lipid deposition; only the mean

lipid level of the final gravid sample was subtracted from individual lipid levels in the postreproductive

sample.

Experimental studies

An additional 15 females of each species were collected in 1973 just after the lizards had finished laying their last clutch of eggs (mid-July for both species). Three lizards from each species were analyzed for total lipids to determine initial lipid levels. The remaining lizards of both species were placed in animal cages under similar moisture (watered every other day) and photoperiod regimes (14L: lOD) and were studied simultaneously to determine rates of lipid deposition when fed and utilization when starved. An infrared lamp was

placed in one corner of the cage to allow the lizards to thermoregulate. Each female was fed a surplus weight of crickets every other day. Feces, urates, and remaining crickets were removed and weighed before the next feeding. Feces and urates were frozen to prevent bacterial decomposition until they could be analyzed for energy content. When the lizards had gained 10% of their body weight, six were sacrificed and analyzed for total lipids as described above, to determine rates of lipid deposition for each species. Remaining lizards were starved until they had lost 10% of their body weight, then analyzed to determine rates of lipid utilization. By knowing the initial lipid levels (mg/g LDBW) and the number of days required to gain or lose 10%

of the body weight, rates of lipid deposition and

utilization could be calculated. The initial lipid

level for the fattening study was determined from the

initial sample of lizards mentioned above, while

the initial level for the starvation study was the

lipid level of the lizards that had gained 10% of their


body weight. In both cases initial values were computed as means and the difference between these mean values and each starved or fattened lizard was determined. This calculation yielded the number of milligrams of lipid per gram LDBW gained or lost, which was then divided by the appropriate number of days to yield rates of deposition and utilization for the two species.

Calorimetry

Both feces and urates collected during the fattening study and crickets and oviducal eggs from the different clutches, were placed in a drying oven at 60?C and dried to a minimal and constant weight. Some fecal and urate pellets, crickets, and oviducal eggs were then placed in a muffle furnace at 500?C for 4 h to measure ash content. Remaining dried feces, urates, crickets, and oviducal eggs were analyzed for caloric value using a Parr Semi-micro Oxygen Bomb Calorimeter (Model 1411) ' according to techniques described in Paine (1971). All caloric values were

corrected for ash. From these data it was possible to calculate calories per clutch of eggs, calories per egg, ingested and egested energy. Calories per clutch was considered the major proportion of energy ex-

pended on reproduction since lizards exhibit no parental care. The percentages of ingested energy available for metabolism (ME) and assimilation efficiency (AE) were calculated using the formulae,

ME IE- (FE + NE) /IE X 100 and

AE IE- FE/IE X 100,

where IE is ingested calories, FE is fecal calories, and NE is nitrogenous waste calories. It was also possible to calculate what percentage of the ME was being stored as lipids since the ME and fattening studies were run concurrently. This was done by

converting the lipid increases in the fattening study to caloric values (a gram of lipid is 38 kJ, or 9 kcal), dividing this figure by the amount of ingested energy available for metabolism, and multiplying by 100.

Statistical analyses

Least squares analysis of variance was used to compare lipid levels, calories per clutch, calories per egg, eggs per clutch, ME, AE, and the proportion of the energy available for metabolism that was converted to lipids. Rates of lipid deposition and utilization represented deviations from the mean value of the initial samples and these deviations were also compared using least squares analysis of variance. Regression analyses were used to assess relationships between any of the above parameters and LDBW. If relationships existed regression lines were compared

both within and between species to determine sta- tistically significant differences. Chow's (1960) tech- nique was used to compare residual sums of squares of the individual regressions with that of the data combined into a single regression line. If weight was correlated with a given parameter in both species, this parameter was expressed on a per gram basis from the regression equations. If no relationship existed between LDBW and a given parameter in either species, the raw data were compared. The rationale for seeking a relationship between LDBW and each of the above parameters was based on observed relationship of clutch size and body weight in a number of lizard species.

Evidence for the assumption that food level differences exist between

prairie lizards and sagebrush lizards

In order to provide some support for this assumption the following comparisons were made: (1) precipitation levels in the two study areas over the past 30 years using U.S. Weather Bureau data; and (2) mouthgape (head length X mouth width) vs. snout-vent length for the two species. Insect biomass is correlated with precipitation (Janzen and Schoener 1968) and mouthgape with prey sizes utilized (Schoener 1968). At low food levels a species should use a wider array of prey sizes.

RESULTS

Hypothesis 1

This hypothesis stated that r-selected lizard species (prairie lizards) should have higher lipid levels prior to and after hibernation than K-selected lizard species (sagebrush lizards). My results support this hypothesis (Fig 2A). Total body lipids per gram LDBW, pooled over the two collection years, were higher prior to and after hibernation in prairie lizards than in sagebrush lizards.

In prairie lizards, minimal lipid levels reached during production of the middle clutch were lower than in sagebrush lizards. In sagebrush lizards, lipid levels were minimal during production of the final clutch. Neither species apparently depleted their storage lipids since minimal levels (6%-7% of LDBW) were higher than polar lipid levels (2% of LDBW). However, prairie lizards utilized more of their stored lipids during reproduction than sagebrush lizards.

Lipid levels changed more in prairie lizards than in sagebrush lizards during egg production. The loss of lipids from posthibernation to the initial gravid sample was approximately 200 mg/g LDBW in

prairie lizards versus about 60 mg/g LDBW in sagebrush lizards. Simultaneously, there was an increase

of about 210 and 220 mg of lipids in the eggs of


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FIG. 2. Seasonal variation of mean lipid levels (per gram lean dry body weight, LDBW) in Kansas northern prairie lizards (open bars) and Utah northern sagebrush lizards (solid bars). Samples are posthibernation (PH), vitellogenesis (V), gravid-initial clutch (01), gravid- middle or initial clutch (02), gravid-final clutch (03). Horizontal bars represent the means; vertical lines the ranges; and vertical bars one standard error. Numbers above bars indicate sample sizes. (A) total body lipids; and (B) egg lipids.

prairie lizards and sagebrush lizards, respectively

(Fig. 2B). The relationship between body lipids

lost and egg lipids gained in both species is expanded

upon in Fig. 3. Body lipid loss was equivalent to egg

BODY LIPIDS LOST (mg/g LDBW) EGG LIPIDS GAINED(mg/g LDBW)

200 100 0 100 200

FIG. 3. Histogram comparing mean body lipid loss with mean egg lipid gain (mg/g lean dry body weight, LDBW) in field samples of Kansas prairie lizards (clear bar) and Utah sagebrush lizards (solid bar).

lipid gain in prairie lizards, while egg lipid gain far

surpassed body lipid loss in sagebrush lizards.

Presumably, sagebrush lizards had to rely more

on other sources of energy (i.e., ingested) to produce

egg lipids than did prairie lizards. In fact, some

prairie lizards had 30,125 J (7,200 cal) in stored

lipids which seems more than enough to produce an

initial clutch of eggs with a mean energy value of

22,175 J (5,300 cal). In sagebrush lizards maximum

lipid levels were equivalent to 15,062 J (3,600 cal),

less than a 21,338 J (5,100 cal) clutch of eggs.

Table 1 further emphasizes that sagebrush lizards

had to rely more heavily on external sources of

TABLE 1. Mean rates of body lipid loss (negative value) or gain and mean rate of egg lipid deposition in field and laboratory samples of Kansas prairie lizards (PL) and Utah sagebrush lizards (SL). LDBW - Lean Dry Body Weight; * = 0.05 level of significance; ** - 0.01 level of significance; NS - not significant

Body Eggs (mg/g LDBW day) (mg/g LDBW- day)

Period of lipid loss in field Posthibernation to gravid-

initial clutch

PL -4.5 4.0 ** **

SL -0.6 6.7

Period of lipid gain in the field Gravid-second clutch to

postreproduction PL 2.3 None

NS

SL 2.3 None

Laboratory samples

Starvation experiment PL -17.0 None

*

SL -6.5 None

Fattening experiment PL 3.2 None

NS

SL 3.6 None


TABLE 2. Mean assimilation efficiency (AE), percent of ingested energy available for metabolism (ME), and percent of ingested energy available for metabolism stored as lipids (SF) in Kansas prairie lizards and Utah sagebrush lizards during fattening experiments. * - 0.05 level of significance

Prairie lizards Sagebrush lizards

AE n 12 86.16% n = 12 89.55% * *

ME n 12 76.17% n = 12 81.70% * *

SF n 4 12.51% n= 4 23.46% * *

energy than prairie lizards for egg production. The

rate of body loss (in milligrams per gram LDBW)

exceeded the rate of egg lipid deposition in prairie

lizards. In sagebrush lizards the rate of body lipid

loss was < 10% of the rate of egg lipid deposition.

Hypothesis 2

Based on this hypothesis, r-selected lizard species

(prairie lizards) should have higher rates of lipid

utilization than K-selected lizard species (sagebrush

lizards) during starvation. Data from the starvation

study supported this hypothesis (Table 1). The rate

of lipid utilization was almost three times greater in

prairie lizards than in sagebrush lizards. This dif-

ference suggests that sagebrush lizards were better

adapted to conserve lipids at lower food levels than

prairie lizards.

There was no significant difference between the

two species in the rate of lipid deposition in either

field or experimental samples, although rates of depo-

sition were higher in the laboratory than in the

field. This suggests that food is not unlimited for

either species in the field. Since both species have roughly the same amount of time to store lipids

prior to hibernation there is no reason to suspect

differences in rates of lipid deposition between the

two species.

Hypothesis 3

According to the third hypothesis, prairie lizards

should have a lower percentage of ingested energy available for metabolism than sagebrush lizards. Both

assimilation efficiency and percentage of ingested energy available for metabolism were higher in sagebrush lizards (Table 2). Not only were sagebrush lizards absorbing more of the ingested energy across the intestine, but a higher percentage of this assimi- lated energy was retained and not lost as nitrogenous waste (urates) . This higher assimilation efficiency and percentage of ingested energy available for metabolism suggests that sagebrush lizards are better adapted for lower food levels than prairie lizards.

TABLE 3. Mean calories/dry g of egg, eggs/clutch, calories/clutch, and calories/egg in Kansas prairie lizards (PL) and Utah sagebrush lizards (SL). Values for eggs/clutch and calories/clutch are functions of weight and were computed from linear regression equations. Caloric values were corrected for ash to eliminate eggshell thickness differences. NC = no clutch produced at this time; NS - not significant at the 0.05 level; * = significant at the 0.05 level; ** = significant at the 0.01 level. To convert calories to joules, multiply by 4.184

Clutch

May June July

Calories/dry g of egg

PL 6,088 6,453 6,657

SL NC 6,453 6,688

Eggs/clutch

PL 6.0 * 7.0 * 6.0 ** **

SL NC 4.4 * 3.1

Calories/clutch

PL 4,450 * 5,000 * 4,450 NS NS

SL NC 4,450 NS 4,450

Calories/egg

PL 677 * 734 * 854 ** **

SL NC 1,059 * 1,394

Hatchling size (mm)

PL 22.8 ** 24.1

SL NC

Prairie lizards not only were less efficient at utiliz-

ing energy, but a higher percentage of the energy

available for metabolism was devoted to metabolic

activities other than lipid storage. In sagebrush liz-

ards, a higher percentage of energy available for

metabolism was converted into lipids.

Since house crickets were utilized as an energy

source in this study, it is not known how accurately

these efficiencies compare to actual efficiencies.

However, the difference between the two species

should still be valid.

Hypothesis 4

This hypothesis stated that sagebrush lizards should

expend more energy per offspring than prairie lizards.

Regression equations of calories per clutch versus

LDBW were significant for both species (Fig. 4).

However, regression lines did not differ significantly

(Table 3). Therefore, lizards of both species put

about the same number of calories into eggs per

clutch. The regression of number of eggs per clutch versus LDBW also was significant for both species

(Fig. 5). Regression lines did differ significantly between species. A prairie lizard produced significantly more eggs per clutch than an equivalent-sized

sagebrush lizard (Table 3). Since the number


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0.0 1.0 .o2.0 3.0

LEAN DRY BODY WEIGHT (g)

FIG. 4. Calories/clutch versus lean dry body weight in Kansas prairie lizards (second clutch, s *; first and third clutch, ?--?) and Utah sagebrush lizards (first and second clutch, (--O)r . All three regressions were significant at the 0.01 level. The regression line for sagebrush lizards did not differ significantly, at the 0.05 level, from those for prairie lizards.

of calories per clutch was the same for both species

and the number of eggs per clutch was different for

the two species, calories per egg should and did

differ (Table 3).

In both species the calories per egg increased with

successive clutches. Thus more energy was expended

on offspring in later clutches. Egg quality (calories

per gram of eggs) also increased seasonally in both

species, but did not differ between species.

The number of calories per clutch per gram LDBW

and egg calories per body calories provide estimates

of the cost per clutch of reproduction to the parent

(Table 3). While the cost per clutch was about the

same for both species, prairie lizards produced three

clutches versus two for sagebrush lizards. Thus,

prairie lizards put considerably more energy into

eggs than sagebrush lizards each season (Table 4).

This additional expenditure of energy on egg produc-

tion by prairie lizards resulted in nonlipid tissue

loss (Fig. 6A). Comparing the regressions of LDBW

versus snout-vent length for posthibernation and gravid-final clutch samples in both species revealed

the prairie lizards lost more nonlipid tissue during reproduction than sagebrush lizards (Fig. 6B). If there

is no net nonlipid catabolism, neither the slopes nor

=R.972

1 2

,j'R=.918

8~~~~~~~~~

m g<27 @ _@~~ ~ R =.839

I-. /~~~~~~~~A

0~~~~~~~~

0.0 1.0 2.0 3.0

LEAN DRY BODY WEIGHT (g)

FIG. 5. Eggs/clutch versus lean dry body weight in Kansas prairie lizards (second clutch, * ~*; first and third clutch, (D--(D) and Utah sagebrush lizards (first and second clutch, * - *). All regressions were significant at the 0.01 level. The regression line for sagebrush lizards differed significantly, 0.01 level, from those for prairie lizards.

the elevations of these lines should change throughout the season, since lean dry body weights were used. Therefore, any decrease in slope or elevation represents nonlipid tissue loss. The greater nonlipid tissue loss in prairie lizards may render this species more vulnerable to predation or harsh climatic con- ditions, which would in part explain the shorter

TABLE 4. Estimated eggs/season, egg calories/season, eggs/lifetime, egg calories/lifetime, body calories, and egg calories /season-body calories in Kansas prairie lizards (PL) and Utah sagebrush lizards (SL). Eggs/ season and egg calories/season were calculated by summing the average eggs/clutch and calories/clutch, respectively, for all clutches. Eggs/lifetime and egg calories/lifetime were computed by multiplying eggs/ season and egg calories/season by the average number of breeding seasons that members of each species ex- perience. The values of 5,390 cal/gram and 5,300 cal/gram ash free dry body weight were used to calculate body calories for PL and SL, respectively. Figures in parentheses are on a per gram lean dry body weight basis. To convert calories to joules, multiply by 4.184

Parameters PL SL

Eggs/season 20.9 ( 19.0) 10.4 (7.5) Egg calories/season 15,457 (13,900) 12,945 (8,900) Eggs/lifetime 20.9 ( 19.0) 41.6 (30.0) Egg calories/lifetime 15,457 (13,900) 51,780 (35,600) Body calories 6,127 8,902 Egg calories/season- body calories 2.53 1.45


/R=.992 3.0 /R.

_/ R=.995

I /

32.0 1"

C:1~~~~~~~~~~1

mU //

1.0-A ,

///

B

3.0

I-

2.0

> <= .9~~~~~~~86 m /

1.0- R _ =.985

40 5b 70 SNOUT-VENT LENGTH (mm)

FIG. 6. Lean dry body weight versus snout-vent length for posthibernation (0 0 ) and final clutch (*--*) in Kansas prairie lizards and Utah sagebrush lizards. (A) prairie lizards; (B) sagebrush lizards. All regressions were significant at the 0.01 level. Com- parisons between regression lines for both species were significant at the 0.01 level.

lifespan of females of this species. Since sagebrush

lizards are not expending as much energy on egg

production each season, this may reflect positively on

lifespan and enable sagebrush lizards to expend more

energy on egg production in a lifetime than prairie lizards (Table 4).

Assumption

The higher precipitation levels in Kansas than in Utah (Fig. 7) suggests that potentially more food

72

KANSAS

48

24

72

UTAH

48

24

0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0+

INCHES OF PRECIPITATION

FIG. 7. Precipitation levels from 1944-1973 for Reno

County, Kansas and Washington County, Utah. The graphs represent the number of months out of the 30-yr

period that had a given level of precipitation.

was available to the r-selected lizard species (prairie

lizard) than the K-selected lizard species (sagebrush

lizard). Sagebrush lizards also had a larger mouth-

gape than equivalent-sized prairie lizards suggesting

that they were able to utilize a wider array of prey

sizes than prairie lizards (Fig. 8).

DISCUSSION

The results of this study suggest general models to

explain observed differences in patterns of lipid

storage and utilization of various lizard species.

Specifically, the r-selected lizard (prairie lizards)

stored more lipids than the K-selected lizard (sage-

brush lizards). Greater lipid stores resulted in more

lipids being available after hibernation in the r-se-

lected species, and these were apparently used in the

production of the first clutch of eggs. Because of the

lack of total dependence on ingested food to produce

the first clutch of eggs, the r-selected species is able to start reproducing earlier in the season which re-

sulted in a higher reproductive effort. This higher reproductive effort appeared to have a negative feed-

back on lifespan. Lower lipid levels in the K-selected

lizard species resulted in this species being more de-

pendent on ingested energy for egg production. Egg laying occurred later in the season and fewer clutches

were laid. This lower reproductive effort had less

of a negative feedback on life span than in the r-se-

lected species. The r-selected species also had a

higher rate of lipid utilization when starved, a lower

percentage of ingested energy available for metabo-

lism, and expended less energy per offspring than the

K-selected lizard species. To test the generality of

these findings, lipid storage and usage, rates of lipid


140 2x2

2 K

R R930

120- / * /

2~~~~~~~~ x/ / R.980 100~ ~ ~ ~~~~~

/20 02

80- / R 98 60

40 50 60 SNOUT-VENT LENGTH (mm)

FIG. 8. Mouthgape (head length x mouth width) versus snout-vent length in Kansas prairie lizards ( 0 * ) and Utah sagebrush lizards ( X- -X ). Both regressions were significant at the 0.01 level. Com- parisons between regression lines were also significantly different at the 0.01 level.

utilization, percentage of ingested energy available for metabolism, and energy expended per offspring in other lizards will be examined.

Supporting evidence from studies

on other lizard species

It is difficult to compare lipid usage data avail-

able on other lizard species with data in the present study. Most of the data available on lipid usage is anecdotal, and does not look at all potentially available lipids, or at seasonal cycling of lipids. However, some data support my hypothesis that lizards with r-

strategist characteristics may have more lipids available for reproduction. Based on limited data, Parker and Pianka (1973) observed no correlation between

reproductive activity and fatbody length/snout-vent length in female Sceloporus magister. They indicated that this species requires at least 2 yr to reach matu-

rity, produces 1-2 clutches/season, and is probably long-lived (K-strategist). Hahn and Tinkle (1965) and Telford (1970) found a significant decrease in fatbody lipids during reproduction in female Uta

stansburiana and Takydromus tachydromoides, re-

spectively. According to Tinkle (1969) and Tinkle et

al. (1970), these two species are short-lived, mature early, and have a high reproductive effort (r-strategists). Based on seasonal cycling of carcass, fatbody,

and liver lipids in female Cnemidophorus tigris,

Gaffney and Fitzpatrick (1973) estimated that >

3,000 calories of lipid go into egg production, as

compared to 1,500 calories for hibernation. These

authors collected their C. tigris from western Texas,

where they mature in 1 yr and produce two clutches/ season (r-strategist; Tinkle 1969). Female Ameiva

festiva and A. quadrilineata (Smith 1968) and

Cnemidophorus sexlineatus (Hoddenbach 1966) also showed decreases in fatbody size during reproduction.

These three species can be classified as r-strategists (Tinkle 1969, Tinkle et al. 1970). Licht and Gor- man (1970), Ruibal et al. (1972), and Gorman and

Licht (1975) found an inverse relationship between

reproductive activity and fatbody size in a number

of tropical anoles. Those species that reproduced

throughout the year either had no fatbodies or very

small ones, while those that exhibited reproductive

cycles had large fatbodies during the nonreproductive

phase (dry season) and lacked fatbodies while reproducing (wet season). Licht (1974) also found that

fatbodies in Anolis cristatellus would increase during

reproduction via supplemental feeding in the field.

Apparently, egg production and deposition in many

of these anoles creates too much of an energy de-

mand to allow lipid storage from available food. All

of the anoles studied by these authors could be classi-

fied as r-strategists.

Anolis carolinensis (an r-strategist; Tinkle 1969,

Tinkle et al. 1970) may be an exception to the

hypothesis that r-strategists use lipids primarily for reproduction. According to Dessauer (1955), this

species is active most of the year in New Orleans, but only reproduces from April to August. During the

months of November and December they are inactive

and lipid levels decreased markedly during this

period of time. Mean air temperature (and presumably body temperature) in these 2 months is

relatively high (15?C) which may account for utili-

zation of large amounts of lipids. A higher hibernation temperature than that of the other lizards

mentioned above would result in greater metabolic

demands and hence greater utilization of lipid. Des- sauer (1955) also stated that A. carolinensis feeds

little if at all during November and December. Lack

of feeding activity plus high winter body temperature

may impose a heavy drain on lipid reserves so that

lipid levels are too low to use for reproduction in the

spring.

Little or no data from the literature support my

results on rates of lipid utilization, percentage of in-


gested energy available for metabolism (ME), and energy expended per offspring. This is the only study of rates of lipid utilization in lizards, so more empirical data on a number of species are needed to determine whether a low rate of lipid utilization is common to K-strategists. Some comparative data are available on assimilation efficiencies and ME, but it is difficult to draw conclusions from these. Mueller (1970) found a ME of 83% for the sagebrush lizard which is consistent with my results (82%). He also found a ME of 83% for Sceloporus occidentalis.

This lizard requires 2 yr to reach maturity; however, it is intermediate to sagebrush lizards and prairie lizards regarding lifespan and clutch number (Tinkle 1969, Tinkle et al. 1970, Goldberg 1973). It is difficult to predict whether S. occidentalis should have a high or low ME. Mueller (1970) felt a ME of 83% was an overestimate, because S. occidentalis was studied much of the time at body temperature below the optimum for this species. Sage- brush lizards, however, were studied at their optimum temperatures. If there is an inverse relationship between temperature and ME, S. occidentalis should have a lower ME than sagebrush lizards. However, it is still difficult to categorize S. occidentalis as a r- or K-strategist.

Avery (1971) found that the lizard Lacerta vivipara, a viviparous K-strategist with delayed maturity and low reproductive effort (Tinkle et al. 1970), had an assimilation efficiency (AE) of 89%. In the present study, the sagebrush lizard had an AE of 90%. Finally, Johnson (1966) assumed an AE of 67% for S. undulatus, S. magister, and C. tigris when he measured the number of calories of energy as- similated per gram per day. However, these efficiencies are probably not accurate since my study shows variation in ME between species, and both my data and Pough's (1973) indicate that an AE of 67% is low for insectivorous lizards. Most insectivorous lizards have high efficiency percentages (from the low 70s to > 80), which may be due to the relatively high energy value of insects, 5,400 calories/ g (Golley 1961).

Although data on calories per egg are generally lacking, egg weight data for S. undulatus support my findings on energy expenditure per offspring. Tinkle and Ballinger (1972) calculated egg weights for four populations of S. undulatus and found that, generally, longer-lived populations produced heavier eggs than shorter-lived populations. In Texas S. undulatus ma-

tured in < 1 yr, produced about 27 eggs/season, and each egg weighed 0.22 g. Conversely, Colorado S. undulatus matured in 2 yr, produced about 16 eggs/season, and each egg weighed 0.45 g. Ballinger

and Clark (1973) showed that relative clutch weight

is a good estimator of relative calories per clutch.

From Ballinger and Clark (1973) and Tinkle and

Ballinger (1972) one can conclude that Colorado S.

undulatus are putting more energy into each egg

than Texas lizards. In fact, if one uses the caloric

and percent water content values estimated by Bal-

linger and Clark for S. undulatus eggs (6,195 cal-

ories/g of egg and 54%), calories per egg can be estimated for each of the S. undulatus populations

studied by Tinkle and Ballinger. Such calculations

yield an estimate of 1,168 calories/egg for Colorado

lizards and 612 calories/egg for Texas lizards. These

figures are surprisingly close to those found for

sagebrush lizards and, prairie lizards respectively, in

the present study.

Data from Tinkle and Hadley (1975) support my

conclusion that the higher reproductive effort by

prairie lizards results in a shorter lifespan. These

authors examined a number of demographic variables

and measures of reproductive effort in 11 lizard spe-

cies and found that the only significant correlation

was an inverse relationship between clutch calories/

body calories and annual adult survivorship. (Inter-

estingly no correlation was noted for clutch weight/

body weight, frequently used as an index of

reproductive effort, and annual adult survivorship).

As seen in Table 4 the clutch calories/body calories

index was 2.53 and 1.45 for prairie lizards and sage-

brush lizards, respectively. Based on Tinkle and

Hadley (1975), prairie lizards would be expected to

have the lower annual adult survivorship that it does.

A comparison of this index with reproductive energy

total energy budget in these authors' study indicates

that clutch calories/body calories may not be a good index of reproductive effort. For example, while

U. stansburiana had a clutch calories/body calories

index of 2.54 the calculated reproductive energy/total energy budget was 19%. In S. graciosus, on the other hand, these values were 1.45 and 24%, respectively. This discrepancy is readily resolved when looking at differences in age-at-maturity. Uta stansburiana is

essentially an annual species and does everything

(matures, reproduces, and dies) in 1 yr, while S. graciosus requires 2 yr to reach maturity. Therefore,

for the comparisons to be meaningful, total energy

budgets of U. stansburiana and S. graciosus would have to be weighted to account for this difference.

This weighting should indicate that clutch calories/ body calories is a reasonable index of reproductive effort.

In summary, evidence in the literature parallels

the findings of this study. There are correlations of

reproductive strategies with lipid levels, percentage of

ingested energy available for metabolism, and energy

expended per offspring. Higher posthibernation lipid

levels are correlated with higher reproductive effort,

while percentage of ingested energy available for


metabolism and energy expended per offspring are

inversely related to reproductive effort.

More energy per egg and fitness

Based on demographic data on prairie lizards (Fer-

guson and Bohlen 1976) and sagebrush lizards

(Tinkle 1973) and my data on egg energy values, I

conclude that higher energy content per egg results

in large hatchlings with higher survivorship. Tinkle

and Ballinger (1972) indicated that survivorship of

offspring from larger eggs (greater energy) was

higher. Fourteen percent of Colorado S. undulatus

hatchlings survive to the next spring compared to

5% for Texas hatchlings. In sagebrush lizards first

clutch (4,431 J, or 1,059 cal/egg) hatchlings were

larger (x snout-vent length = 26 mm) than first

clutch (2,833 J, or 677 cal/egg) hatchling prairie

lizards (x snout-vent length - 23 mm). As men-

tioned earlier, this larger size in sagebrush lizards is

adaptive for using a wider array of food items at

lower food levels.

That selection is favoring larger size for lower

food levels is further supported by comparing suc-

cessive clutches of prairie lizards. The mean number

of joules (or calories)/egg was 2,833 (677), 3,071

(734), and 3,573 (854) for the first, second, and

third clutches, respectively. This suggests that the

hatchlings from these clutches should differ in size.

Indeed, hatchlings from the first clutch were signifi-

cantly smaller than those from the third clutch, 22.8

and 24.1 mm (Table 3). If food is critical at all for

prairie lizard hatchlings it should be when the last

clutch is hatching, late August to early September. During this period hatchling density is highest and insect productivity should be declining which should result in less food per individual.

Even within a given clutch larger-sized prairie lizard hatchlings can be shown to have a survival advantage to the next spring. Ferguson and Bohlen (1976) found that third clutch hatchlings with a snout-vent

length > 24 mm had a significantly higher survivor-

ship than those < 24 mm (43% and 21 %, respectively). He found no significant difference in survivorship for different-sized hatchlings of the first

clutch. These data suggest that larger hatchling size

is less important in the first clutch than in the third clutch. Besides the advantage to larger hatchlings of using a wider array of food, larger size confers a

dominance advantage during social contests which

could be related to food territories (Rand 1967).

Comparable data are not available on sagebrush lizards. However, since joules (calories) per egg are

significantly higher in the second clutch than in the

first, 5,832 (1,394) and 4,431 (1,059), respectively,

the above data would suggest that second clutch

hatchlings are larger than first clutch hatchlings. If

hatchlings from both clutches are competing for food

in sagebrush lizards, then survivorship should be

higher for the larger hatchlings in both clutches.

Evidence for food competition

A basic assumption underlying the hypotheses

tested in this study was that differences in the degree

of competition for food existed between the two

species. Additionally, it was assumed that the off-

spring of each species were exposed to the same de-

gree of competition for food as the adults. Although

no attempt was made to look at food levels in the

field, data on precipitation levels in the two study

areas and mouthgapes for both species suggest that

these may be valid assumptions.

Analysis of weather data over the past 30 yr for

the two study areas, indicates that precipitation levels

are predictably lower in Utah than in Kansas (Fig.

7). Janzen and Schoener (1968) showed that insect

productivity increases with precipitation levels.

Higher precipitation levels, typically, resulted in

greater insect diversity and abundance. Therefore,

a lower precipitation level suggests that there should

be lower food levels in Utah. Interestingly, there is

a greater density, 208/ha, of sagebrush lizards (Tinkle 1973) than prairie lizards, 42/ha (Ferguson

and Bohlen 1973). Less potential food and a greater

density of lizards strongly suggest that there was less

food per individual for sagebrush lizards than for

prairie lizards with their low density and more po-

tential food. Mid-July until late October should be a

critical time for both the parents and offspring of the two species, since during this time they grow and

store lipids for hibernation. Mean precipitation levels

at this time are 8.71 cm and 2.79 cm for Kansas and

Utah, respectively. Lower precipitation levels should result in less food being available for sagebrush lizard

adults and offspring. In sagebrush lizards, low adult

mortality during the breeding season results in large

numbers of adults surviving (65/ha) during, at

least, the early part of the mid-July to October

period to compete with offspring for food. High

adult mortality in prairie lizards during the breeding

season results in fewer adults (22/ha) to compete

with offspring. Data from Sexton et al. (1972) and

Parker and Pianka (1973) suggested that there is a

great deal of overlap in food resources of adult and

offspring lizards. Competition among the adults and

offspring may further reduce the amount of food

available to sagebrush lizard offspring, although this

may be mitigated by the juveniles utilizing smaller

prey due to their smaller mouths. Differences in pre-

cipitation levels and adult mortality during the

breeding season, therefore, may result in differences

in food availability for the two species after repro-

duction has ceased.


Additional data suggesting food competition was greater for sagebrush lizards were mouthgape and snout-vent length relationships for the two species (Fig. 8). Regression lines showed that given a prairie lizard and a sagebrush lizard of equal size, the latter had a larger mouth. Schoener (1968) found that average prey size and variance of prey size increased with head length in Bimini anoles. Presum- ably, longer heads resulted in larger mouths in anoles. Since sagebrush lizards had a larger mouthgape than prairie lizards they should be able to utilize not only larger prey but also a wider range of prey sizes. Species that are food limited should be generalists in their food habits (Emlen 1973). The capacity to handle a wider array of prey sizes suggests that sagebrush lizards may be less specialized in their food habits than prairie lizards.

Finally, Licht (1974) suggested that differences in lipid levels are indicative of different food availabilities. Licht was able to increase lipid levels in Puerto Rican anoles by supplemental feeding in the field. Lizards that were not given additional food in the field had much lower lipid levels, suggesting that a limited amount of food is available. My own laboratory experiments (Table 2) demonstrated that with ad libitum feeding, both species deposit lipids faster than field animals. Also, the discrepancy between lipid deposition rates in the field and laboratory were greater in sagebrush lizards (1.3 mg/g LDBW - day) than in prairie lizards (0.9 mg/g LDBW - day). Therefore, these data suggest that a positive correlation exists between lipid levels and food availability and that prairie lizards may have more food available than sagebrush lizards.

ACKNOWLEDGMENTS

I thank Donna, Kevin, and Todd for their support and understanding. Their sacrifices made this study possible. The patience, understanding, and considerable talents of my committee members, Drs. Stephen D. Fretwell, G. Richard Marzolf, Christopher C. Smith, and Roger Wein- berg, were instrumental in the development and fulfill- ment of the project. Words cannot express my gratitude to my major professor, Dr. Gary W. Ferguson, for the time and effort he devoted in helping me develop this research problem. Drs. Kenneth Kemp, George Milliken, and Don Yamashita were interested and kind enough to aid with the statistical analyses. Dr. William Klopfen- stein provided the biochemical expertise. Gerard Hod- denbach and his three sons, Billy, Jimmy, and Johnny, provided many of the lizards from Utah. Their interest and love of working with lizards was inspiring. Many graduate and undergraduate students helped collect lizards and acted as sounding boards for my ideas. They influenced my thinking and I am indebted to them. I am grateful to Dr. Donald Tinkle, Dr. Tom Poulson, and two anonymous reviewers for their helpful comments and suggestions. This research was supported in part by a NSF Doctoral Dissertation Improvement Grant (No. GB-35156) to me through Dr. Ferguson. The Division of Biology and its faculty supplied much of the materials and equipment needed for this research.

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