ANNUAL LIPID CYCLES IN THE LIZARD CNEMIDOPHORUS TIGRIS APPROVED: Major ^/ofessor. XUIITlX. Director of the Department of Biology.
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1 ANNUAL LIPID CYCLES IN THE LIZARD CNEMIDOPHORUS TIGRIS APPROVED: Major ^/ofessor XUIITlX Director of the Department of Biology or Graduate School
2 Gaffney, Fred G, Annual lipid cycles in the lizard Cnemidophorus tigris«master of Arts (Biology), August, 1972, 42 pp., 5 tables, 11 figures, bibliography, 43 titles. Annual lipid cycles were determined for adult male and female Cnemidophorus tigris collected near El Paso, Texas during In whiptails, most lipids are stored In the carcass, tail, and post-coelomic fat bodies. Females had greater total lipid reserves than males in most collections. Fat body and carcass lipids appear to be used by males for maintenance during brumation ( winter dormancy from September to May) and by females for maintenance and vitellogensis during brumation. Although reduction of lipid reserves in the carcass during brumation was not significantlydifferent between sexes: females, as a result of vitellogenesis, used significantly more fat body lipids than males during brumation. Males replaced all lipid reserves depleted during brumation by July while females showed no significant change. Females significantly depleted fat body and carcass lipid reserves from July to early August, probably for the production of the second annual clutch of eggs. Immediately after the deposition of the second clutch in August, there was a trend for females to rapidly increase lipid reserves in preparation for brumation in late August. Liver lipid levels were significantly greater in females than males collected in late August. Results from field collections of adult C. tigris indicate that major seasonal activity is from mid May
3 to late August; testes size is cyclic and maximal size of testes coincides with observed mating; females laid two clutches of eggs; and the overall ratio of males to females in collections was 3 J 2. Different microhabitat preferences and size of home range contributed to biased ratios in the collections.
4 ANNUAL LIPID CYCLES IN THE LIZARD CNEMIDOPHORUS TIGRIS THESIS Presented to the Graduate Council of the North Texas State University in Partial Fulfillment of the Requirements For the Degree of MASTER OF ARTS By Fred G. Gaffney, B. S, Denton, Texas August, 1972
5 TABLE OF CONTENTS ABSTRACT LIST OF TABLES. LIST OF ILLUSTRATIONS Chapter, iii vi... vii Page I. INTRODUCTION 1 II. METHODS AND MATERIALS 3 Description of Study Area Field Collections Reproductive Cycles Lipid Extraction Procedure Statistical Treatment III. RESULTS 7 Field Collections Reproductive Cycles Lipid Cycles IV. DISCUSSION 13 Field Collections Reproductive Cycles Lipid Cycles Acknowledgements APPENDIX 22 LITERATURE CITED... 39
6 LIST OF TABLES Table Page 1. Average monthly air temperatures in El Paso, Texas during Number of male and female Cnemidophorus tigris collected in El Paso during Monthly variations in collection sites of male and female Cnemidophorus tigris Mean - standard deviation of snout-vent length; lean carcass tissue: dry weight of lipids,total tissue, and percent lipids for fat bodies, liver, ova, carcass and total tissue for monthly samples of male and female Cnemidophorus tigris Mean i standard deviation of snout-vent length; lean carcass tissue; dry weight of lipids, to-, tal tissue, and percent lipids for fat bodies, liver, ova, carcass and total tissue for monthly samples of female Cnemidophorus tigris placed in three ova size classes vx
7 LIST OF ILLUSTRATIONS Figure Page 1. Monthly variations in size of testes for Cnemidophorus tigris Monthly variations in size of follicles for Cnemidophorus tigris Monthly variations in weight of lean carcass tissue in male and female Cnemidophorus tigris Monthly variations in weights of lean carcass tissue in female Cnemidophorus tigris placed in three ova size classes Monthly variations in percentage of fat body lipids for male and female Cnemidophorus tigris Monthly variations in percentage of fat body lipids for female Cnemidophorus tigris placed in three ova size classes Monthly variations in percentage of liver lipids for male and female Cnemidophorus tigris Monthly variations in percentage of carcass lipids for male and female Cnemidophorus tigris Monthly variations in percentage of carcass lipids for female Cnemidophorus tigris placed in three ova size classes Monthly variations in percentage of total lipids for male and female Cnemidophorus tigris Monthly variations in percentage of total lipids for female Cnemidophorus tigris placed in three ova size classes Vll
8 CHAPTER I INTRODUCTION The whiptail lizard, Cnemidophorus tigris, is conspicuous and abundant in desert and semi-arid communities from southern Idaho to northern Mexico (Pianka, 1970). Whiptails, characteristically, are active only in the late spring and summer months,and hibernate during the remainder of the year. The length of this activity period is greater in the southern than northern parts of its geographic range (Pianka, 1970). In West Texas, adults are active 3-4 months per year (Hoddenbach, 1965)«Hoddenbach (1965) suggested that brumation (=winter dormancy in ectothermic vertebrates, Mayhew, I965) for 8-9 months per year may be a physiological adaptation which reduces the effects of predation, starvation and inclement weather. Maintenance during brumation without food for 8-9 months should require utilization of a considerable amount of fat reserves. However, Hoddenbach (I965) reported that sizes of fat bodies did not change significantly during brumation in C. tigris. I find it difficult to believe that C. tigris can fast for 8-9 months without using some energy reserves. Perhaps lipids stored in the carcass or elsewhere are used by C. tigris for maintenance during brumation. In many lizards, fat also is stored in the carcass and tail (Avery, 1970; Clark,
9 1970) and has been reported to be used during brumation (Avery, 1970: Dessauer, 1955) Although numerous ecological studies have been made on C. tigris (Echternacht, 1967? Hoddenbach, 1965; Medica, 1967; Milstead, 1957a, 1957b, 1965; Pianka, 1970) inadequate quantitative data are available concerning the use of its lipid reserves. Therefore, my objectives were to examine lipid levels quantitatively in several possible storage sites (i.e., livers,post-coelomic fat bodies, and carcasses) in adult lizards collected throughout the year; determine if there are any differences in lipid levels between males and females; determine the amounts of lipids used during brumation by males and females; and determine the amount of lipids used by females for reproduction.
10 CHAPTER II METHODS AND MATERIALS Description of Study Area, The study area was in a tract of Chihuahuan Desert located near the northeast city limits of El Paso, Texas (latitude 31 55'N; longitude 'W; elevation 3918 ft.). The area around El Paso is characterized by mild winters and hot summers. Table 1 shows the monthly mean air temperatures recorded in El Paso during Summer temperatures usually exceed 90 F during the day whereas daily winter temperatures are usually below 60 F. Most of the annual 7.5 inches of rain falls between July and September. High wind velocities (>45 MPH) are common during each month. The dominant plant, mesquite (Prosopis.juliflora). was found in association with small aeolian mounds which are separated by large open areas of loose igneous derived sand and limestone (Shreve, 1942). Other conspicuous plants include ratany (Krameria parvifolia). sagebrush (Artemesia filifolia). and catclaw (Mimosa biuncifera). Field Collections Whiptails were collected from 15 August 1970 to 20 August 1971 during the first of their two peaks of their daily activity ( and hr MST). Several methods
11 were used to capture lizards: pit falls traps, grape blowguns, and 22 caliber dust shot. The last method was most efficient, but head wounds were necessary so as not to damage fat bodies and reproductive organs. Wounds to the hind legs or abdomen were usually not fatal and the lizard would escape into the nearest pack-rat (Neotona sp.) hole. Captured lizards were tagged, placed in plastic bags,and kept on ice in a styrofoam container to prevent tissue deterioration until they could be frozen and stored without chemical preservation in the laboratory. Reproductive Cycles The reproductive cycle was studied by examining changes in the gonads of males and females during the year. Males and females were considered mature if they were a72 mm snoutvent length (SVL) (Hoddenbach, I965). The sex of each lizard was determined by internal examination of the gonads. The left testis was measured (length + width in mm) in all adult males. These measurements were grouped by month of collection for comparison with similar data reported by Hoddenbach (1965), Follicles with yolk (diameter in mm) and oviducal eggs (length and width in mm) were measured in all adult females. Females were also examined for expanded oviduct which indicated they were recently spent. Results of the presence or absence of follicles with yolk and oviducal eggs in conjunction with expanded oviducts were used to elucidate the reproductive cycle of females.
12 Lipid Extraction Procedure Lipid levels of liver, fat bodies, and carcass were determined monthly for samples of adult male and female C. tigris. A modified Folch et al. (1957) technique was used to extract lipids from fat bodies, ova, livers, and carcasses of 73 females and 57 males. Carcasses (minus fat bodies, livers, gonads, and digestive tracts)were homogenized with a minimal amount of distilled water in a two-speed Waring Micro-blendor for one minute. Other tissues were homogenized in a Potter-Elenhjnor tissue grinder for approximately two minutes. Homogenized tissues were transferred to Erlenmeyer flasks using a minimal amount of distilled water and 20 ml of chloroform.-«methanol (2:1, V/V) were added to the flasks per gram of tissue (wet weight). After the contents of the flasks were agitated on a two-speed Eberbach shaker at low speed for one hour, they were transfered to a separatory funnel and enough distilled water was added to establish the 8:4:3 (chloroform:methanol:water) ratio necessary to insure proper separation (Folch et al., 1957) The contents of the separatory funnel formed a bi-phasic system when allowed to separate for 12 hours at room temperature. The lower layer of the bi-phasic system was pure dissolved lipids and chloroform. This layer was separated into a tared aluminum container, vacuum desiccated to remove the chloroform, and weighed to the nearest 0.1 mg. This value represented dry weight of lipids, The tissue-methanol-water layer was poured into a tared beaker,
13 vacuum desiccated to remove the methanol and water, and weighed to the nearest 0.1 mg. This value represented the dry weight of lean tissue. Statistical Treatment All C. tigris collected during a month,were pooled by sex for statistical treatment. Females were placed into three ova size classes (OSC) to examine the relationship between reproductive condition and lipid levels in various tissues (Fitzpatrick, 1970). Adult females without follicular development (henceforth non-reproductive) were placed in OSC 1; females with yolking follicles in OSC 2; and females with oviducal eggs in OSC 3 The percentage of lipid in each tissue was calculated as dry weight of lipids/total dry weight of tissue X 100. Dry weights of lipids/dry weightsof lean carcass tissue X 100 was used to compare individual lipid levels for the separate tissues of each lizard. All percentage data were angular-transformed prior to statistical analysis (Sokal and Rohlf, 1969). Single-factor analysis of variance (AN0VA) was used to test the effect of time (month) on tissue lipid levels of males and females. Differences among the means were tested with a Duncan's 5% New Multiple Range Test (NMRT) (Steele and Torrie, i960).
14 CHAPTER III RESULTS Field Collections Age and sex of C. tigris collected from 15 August 1970 to 20 August 1971 are given in Table 2. Most of these lizards were adults. Dr. Walter Whitford (per. com.) reported that adult whiptails entered brumation in El Paso before the first week of September The presence of only first year juveniles in my collections on 11 and 12 October 1970 indicates that adults began brumation before juveniles. According to Whitford, all juveniles entered brumation before the last week of October 1970 and did not emerge from brumation until the first week of April I made an intensive but unsuccessful search for brumating lizards between 18 December 1970 and 14 January Early spring collections (April) contained only juveniles. The first adults were captured on 15 May The unbalanced ratio of adult males to females (3 : 2) found in the collections was not observed in juveniles (Table 2). In order to test the hypothesis that the unbalanced sex ratios derive from a collection bias which results from adult males and females occupying different microhabitats, the exact site where each lizard was first sighted was recorded during C. tigris were either encountered on mesquite
15 8 mounds or in the open areas between mounds. If the lizards were first sighted in open areas, whether foraging or running to avoid capture, they were classified as being in the open; and if found only on one mesquite mound and would not leave the mound to escape capture, they were classified as being on a mound. Approximately equal numbers of males (adults and juveniles) were observed in open areas as were observed on mounds (Table 3). However, almost twice as many females (adults and juveniles)were first sighted on mounds as were sighted in open areas (Table 3)«Reproductive Cycles Monthly variations in the size of testes for C. tigris from El Paso and Kermit, Texas are shown in Figure 1. Copulation and courting behavior observed in the field on 19 and 23 May 1971 correlates with maximal size of testes. Two peaks of adult females with large follicles occured in May and July 1971 (Fig. 2). Females with oviducal eggs were collected in May and July. All adult females collected in July and August 1971 had expanded oviducts,which indicated they were recently spent. None of the pre-brumation females collected in late August 1970 had developing follicles or oviducal eggs. However, in the post-brumation sample (mid- May 1971? N* 3 9), 11 % of the adult females had oviducal eggs, had follicles with yolk (x= 4*5-0.6 mm), and 33% were non-reproductive. In the June 1971 collection (N= 11), of the adults had follicles with yolk (x= mm) whereas 36% were non-reproductive. In the July 1971 collection
16 (N= 24), 67% of adult females contained follicles with yolk (x= 5.8-0,2 mm) and 33% contained oviducal eggs (x= 9-8 x 17.0 mm). Follicles from females collected in May and July were significantly larger than follicles from females collected in June (t= 3.75; df= 12; P< 0.01 and t= 2.87; df» 23; P< 0.05, respectively). Lipid Cycles Results of the examination of lipid levels in fat bodies, livers, ova,and carcasses throughout the year are seen in Fig. 3 through 11, and in Tables 4 and 5. Lean Carcass Tissue Single-factor ANOVA revealed that time (month) had a significant effect on variation in LCT weights in males (F= 2.96; df= 6, 57) and females (F== 6.47; df= 6, 73). The mean LCT weight for males ( mg) was significantly (t= 23.6: df= 130; P< 0.01) larger than the mean LCT weight for females ( mg) (Fig. 3). Means of LCT weights for monthly collections of males were similar except in July, when they were significantly higher than other months (Fig. 2). Mean LCT weights of females OSC 1 and 0SC 2 collected in June were significantly lower than in all other months (Fig. 4). SVL measurements showed a high correlation to LCT weights in males (r^ 0.90) and females (r= 0.73). Fat Body Lipids Analysis revealed that time (month) significantly
17 10 contributed to variation in levels of fat body lipids (FL) of males (F= 2,98; df= 6, 57) and females (F= 7.56; df= 6, 73). Significant reduction of FL occured during brumation in both sexes (Fig. 5). Females lost significantly more FL (x=* mg) than males (x= 70.1 mg) from August 1970 to May 1971 (Table 4). FL increased significantly in males from May to July (83.3 mg) but remained unchanged in females. Females lost a mean of 35.8 mg of FL from July to early August Analysis revealed that the effect of time (month) significantly contributed to variation in FL levels for females in OSC 1 (F 6,,34; df= 6, 36) but not for females in OSC 2 (F= 0.47s df= 3, 28). There was a significant depletion of FL in females in OSC 1 during brumation (Fig. 6), but there was no significant change in FL levels from May to July for females in OSC 1 (Table 5). There was a significant difference between FL levels of females in OSC 2 and OSC 3 in July (t= 4.97; df= 21; P< 0.05). Liver Lipids Monthly variation in levels of liver lipids (LL) was not significant in males (F= 1.59; df= 6, 57) or females (F= 1.28: 6, 73). The only significant difference in LL between males and females occured in late August 1970 collections (t= 2.44; df= 28; P< 0.05) (Fig. 7).
18 11 Carcass Lipids Monthly variation in carcass lipid (CL) levels was significant for males (F= df= 6, 57) and females (F= 5.06; df= 6, 73). CL levels decreased significantly between late August 1970 and May 1971 in males and females (Fig. 8). There was no significant difference in the CL lost by males (x=«90.4 mg) and females (x= mg) during brumation (Table 4). Males deposited CL in a pattern similar to their FL deposition with a significant increase (x= mg) occuring between May and July. CL levels did not change significantly from May to July in females. Time (month) had a significant effect on variation in CL levels of females in OSC 1 (F= 7.01; df= 6, 36) but no effect on CL levels of females in OSC 2 (F= 0.02; df 3, 28). Significant differences in CL levels were apparent for females in OSC 1 during brumation (Fig. 9). There was a significant difference (t= 2.22; df= 23; P< 0.05) in CL levels between females in OSC 1 of August 1970 and females in OSC 2 in May No significant change in CL levels of females in OSC 1 from May to July was observed. Total Lipids Females had significantly more total lipids (TL= FL + LL + CL) than males in most collections (Fig. 10). Monthly variation in TL levels was significant for males (F= 4.10; df= 6, 57) and females (F= 6.02; df= 6, 73). TL levels decreased significantly during brumation in both sexes (Fig, 10). The
19 12 difference between the mean TL depletion in males (x= mg) and females (x= mg) was significant (t= 3.26; df= 19; P<0.05). Males, but not females, deposited a significant quantity of TL (x= mg) in fat bodies and carcasses from May to July (Table 4). Females lost a mean of mg of TL from July to early August 1971 whereas TL levels in males remained unchanged for the same period. Analysis revealed that time (month) had a significant effect on TL level variance for females in OSC 1 (F= 6.80; df= 6, 36) but no effect on females in OSC 2 (F= 0.04; df= 3, 28). TL depletion was significant for females in OSC 1 during brumation, but remained unchanged from May to July (Fig. 11). There was a significant depletion of TL for females in OSC 2 of July and females in OSC 1 of August 1971 (t= 4.37; df=» 21; P< 0.05). TL levels were significantly different for females in OSC 2 of July and females in OSC 1 of August 1971 (t= 2.37; df= 12; P< 0.05).
20 CHAPTER IV DISCUSSION Field Observations The biased sex ratios in ray monthly collections may partially result from females restricting their activities to mesquite mounds,whereas males range more widely. Since it was impossible to distinguish sexes in the field before capture, sex ratios of the collections represent frequency of encounters and not necessarily true sex ratios. Adult males out-numbered adult females in every collection. The overall ratio of 3 s 2 (males to females) is in accord with previous reports for whiptails (Hoddenbach, 1965; McCoy, 1965: Tanner and Jorgenson, I963). The ratio of juvenile males to females, though biased in some months, was equal in the total sample. Equal ratio of juvenile males to females has been previously reported (Hoddenbach, 1965) and suggests that differential mortality during the egg stage does not account for the unequal sex ratios in adult collections. The lower number of adult females than males in my mid-may and early August collections may be explained by the cryptic behavior of gravid females. Most adult females oviposit during early June and early August in El Paso. Blair (I960) and Anderson (1962) suggested that heavy egg burdens which impair locomotion and feeding activities may account for the 13
21 14 cryptic behavior of gravid females. Cryptic behavior may have adaptive value in reducing chances of predation on gravid females whose agility is impaired by heavy egg burdens. Hoddenbach (1965) suggested that biased sex ratios in collections were an artifact produced by differential activities of the two sexes. McCoy (1965) suggested that there is an actual bias which results from differential mortality. Different microhabitat preferences, size of home ranges, differential mortality, and cryptic behavior of gravid females, all probably contribute to unbalanced sex ratios of adults in my collections,, The difference in the length of seasonal activity of adults and juveniles that I observed probably was a result of the additional feeding time required by juveniles prior to brumation. Longer seasonal activity by juvenile C. tigris has previously been reported (Echternacht, 1964; Hoddenbach, I965? McCoy, 1965)- Woodbury and Woodbury (1945) suggested that juvenile Sceloporus graciosus begin brumation later than adults because they require more feeding time. Since both adult and juvenile whiptails consume similar food items (e.g., termites, bettles) (Milstead, 1958; Pianka, 1970) earlier brumation by adults may fortuitously remove them from competition with juveniles. Reproductive Cycles The changes in size of gonads and copulation that I observed in the field in adult C. tigris suggest that mating
22 15 occurs during late May; when the testes of males are of maximal size: and that adult females probably produce two clutches annually, one in early June and a second in early August. McCoy (1965) and Hoddenbach (1965) report that C. tigris mates only in late spring,whereas, Milstead (1957b) reported that mating lasts from 28 May to 31 July. Adult females which emerge from brumation with yolk in their follicles, produce oviducal eggs and deposit them by early June and another clutch by early August. All adult females collected in August 1970 and 1971 were non-reproductive, indicating that females enter brumation without yolking follicles or oviducal eggs. Echternacht (1964) and Hoddenbach (1965) also report that adult females enter brumation without oviducal eggs or follicles with yolk. Females I collected in early spring, immediately after brumation, had follicles with yolk. Apparently some females begin depositing yolk in follicles during brumation. Hoddenbach (1965) reported that because of the small size of his early spring collection he could not confirm whether or not some yolking of follicles occurs during brumation. However, he reported that most females collected in early May had follicles with yolk, indicating rapid yolking occurs after emergence. All females I collected in July had either follicles with yolk or oviducal eggs. Most of these females had expanded oviducts, which indicates they were recently spent. Therefore, it is apparent they were producing their second seasonal clutch. Hoddenbach
23 16 (1965) also reported that C. tigris from West Texas layed two clutches. However, recently matured females may lay one or two clutches depending upon whether maturation occurs early or late during their first season as a reproductive (Hoddenbach, 1965)«Late maturation in the first season as an adult, could account for the presence of several non-reproductive females in my mid-may collection,while all females collected in July were reproductive. The number of follicles with yolk and oviducal eggs (i.e., potential clutch size) as well as number of clutches laid per season vary geographically in C. tigris (McCoy and Hoddenbach, 1966: Pianka, 1970). Females from northern parts of the range lay one clutch with an average of 3.4 eggs while females from southern parts of the range lay two clutches each with an average of 2.3 eggs (McCoy and Hoddenbach, 1966). However, throughout its range the size of the largest follicles produced and mean size of oviducal eggs are relatively constant. The largest size of'follicles with yolk and mean size of oviducal eggs I measured was in accord with that reported by Echternacht (I964), Hoddenbach (1965), McCoy (I965), Pianka (1970), and Shaw (1952). Apparently, maximal size of follicles with yolk and oviducal eggs is less variable than the number of follicles produced or number of clutches laid. Variable environmental factors (e.g., length of growing season, rainfall, food supply) have been reported to influence size and number of cluches in C. tigris (McCoy and Hoddenbach, 1966;
24 17 Pianka, 1970) and probably accounts for conflicting reports on numbers of yolked follicles produced (Carpenter, I960; Fautin, 1946; Gehlbach, 1965; Goldberg and Lowe, 1966; Stebbins, 1954) Lipid Cycles Lean Carcass Tissue Since my collection in July contained more large males than in other collections, the mean weight of LCT was correspondingly higher than in other monthly collections. Large males were probably more active (foraging) than small males because of their preparation for earlier entrance to brumation (late July). McCoy (1965) and Hoddenbach (1965) reported that large males were most abundant in July and began brumation before females and small males in late July, My June collections of females were smaller than in other collections and therefore, had smaller LCT weights than other months. Apparently, large females were brooding their first clutch Gf the season and their cryptic behavior reduced the chances of their being collected. None of these small females collected in June had expanded oviducts, indicating that they were probably producing their first clutch. Fat Body. Liver. and Carcass Lipids Females had significantly larger lipid reserves in their carcasses and tat bodies than males immediately before and after brumation. Although there was no significant difference
25 18 in the amounts of carcass lipids depleted by each sex, females used significantly more fat body lipids than males during brumation. Since both sexes probably experience similar physical conditions during brumation (i.e., temperature, fasting), their energy requirements for maintenance should be nearly equivalent. Therefore, the additional lipids depleted from fat bodies by females were probably used in the production of the yolk. The presence of follicles with yolk in recently emerged females supports this hypothesis. The use of carcass lipids for maintenance during brumation has been reported for other lizards (Avery, 1970; Darevsky, 1957; Dessauer, 1953, 1955; Moberly, 1963) and salamanders (Fitzpatrick, 1970). Fat body lipids appear to be used by females that are producing yolk during May and July. Fat bodies have been reported to be involved in gonadal maintenance (Adams and Rae, 1929; Altland, 1941) and show an inverse size relationship with follicle development in many ectothermic vertebrates (Barwick, 1959; Bostic, 1964; Fitzpatrick, 1970; Hahn and Tinkle, 1965; Hoddenbach, 1965} Lewis and Rose, 1969j Marion and Sexton, 1971; Mayhew, 1971; Miller, 1948; Pianka, 1970; Rose and Lewis, 1968; Smith, 1968; Telford, 1970). Hahn and Tinkle (1965) reported that although fat body lipids appear to be used for the production of the first clitch in the lizard, Uta stansburiana. fat body lipids are not used for production of subsequent clutches. Rather, they suggest that
26 19 feeding is sufficient to supply all the energy needs for the second and third clutches. Surely limited feeding has an impact on the energy requirements of gravid female C. tigris while brooding. Although gravid female C. tigris are cryptic and difficult to capture on my study site, gravid U. stansburiana are active and easily collected. Though feeding may be significantly decreased, thereby requiring greater energy depletion for maintenance during vitellogenesis, the adaptive value would be an increased surviorship among gravid females. Hoddenbach (1965) reported the life expenctancy of U. stansburiana to be one year,while C. tigris has a life expectancy of at least four years. The higher lipid levels in livers of females than males during late August suggest that females were storing lipids at a greater rate than males. After production of the second clutch in early August, femaleswere severely depleted of lipids, whereas males havereplenished lipid reserves which they depleted during brumation. Females which produced a second clutch had only one month to replace approximately twice the amount of lipids that males replaced in two months. Therefore, these females should be processing large quantities of lipids through the liver for deposition in the carcass and fat bodies. Telford (1971) reported that wet weight of livers is maximal in the lizard, Takydromus tachydromides. prior to brumation. The energy expended by males for maintenance and females
27 20 for maintenance and production of ova during brumation can be approximated by converting the weight of lipids depleted (Tables 4 and 5) into calories. Since the mean caloric equivalent of lipids is 9000 cal g~^- (White et ajl., 1964), the minimal energy used by males and females during brumation was 1468 and calories, respectively. If both sexes expended nearly equivalent amounts of energy for maintenance during brumation, the additional 484 calories used by females represent reproductive costs. The average caloric equivalent of lipids in the follicles with yolk in females which had recently emerged from brumation was 407 calories. The additional 77 calories probably represent energy expended for synthesis of yolk, lipid mobilization, etc. The amount of lipid depleted while females were producing their second clutch (July to early August), averaged 2531 calories. The average caloric equivalent of lipids in oviducal eggs was 1196 calories. This difference in energy (1335 calories) probably represents energy depleted for maintenance during brooding and synthesis of yolk. Acknowledgements I would like to thank Dr. Ben G. Harris (North Texas State University) for helpful suggestions on lipid extraction procedures. I wish to express my gratitude to Drs. John R. Bristol, Albert G. Cannaris, Curtis E. Eklund, and Richard D. Worthington of the University of Texas at El Paso for providing laboratory space and assistance. For helpful discussion
28 21 of the study I thank Dr. Charles 0. McKinney (University of Dayton), Dr. Walter G. Whitford (New Mexico State University), and Dr. Eric Pianka (University of Texas at Austin). For assistance in field collections my thanks to Mr. Arves E. Jones, Jr., and Mr. Vincent Gentz of El Paso, Texas.
29 APPENDIX 22
30 23 w <D U 3 -P ftj u (U & CD 4J M rj ro g 3 E a H e c m G m Q) B m e >1 o rh r- rd <r> P H tjv c rh C 0 e CD tn 3 ro CD 03 > (0 C X I <D I Eh rh 0) o H CQ IXJ m 04 & ph H a H U w p I Eh U O a* w CO O & < & 04 c as m m fe 65 s VD in m vd in i> 00 av oo in cr> vo CO r- vx> \D m <3* CM in 00 \D r* r- CM CM r- oo VD 00 m oo in ro ro & 00 o in o vo in VD o r* r- KO oo in oo oo oo ro 00 CM
31 24 CO O Eh OS VO in CM r^ CO <T\ LO r- 00 V0 00 m U tn H P W 3 ^1 o x: a o *0 -H g <D G u fxi f B O EH!* 3 fa oo in oo <3* (30 GO o ih in i> CM o VD CM r- vd r- oo in CM ro oo CM CD H ra g a) MH rh *0 r- a <T> ro rh f 's, o <s a r* * CTi H CD»H fcn ro G g H fa 00 oo 00 o H in r-4 o CM <Tv H 00 Cft CM in oo r U 0 Q) 0) PQ g fa 0 H 1 W CM a H CD rh A CD fo 4J Eh a CD rh rh 0 o 8 I > CO CN l> Ai fa o m VD 00 Eh B << o r- m w PQ s H «H PS fa as *C H 00 vo h r* < CTI S»H CM 00 I o 1> Cft 00 CM CM Eh B 01 <C o rl o CM CO»-5 g O, EH
32 25 Table 3 Monthly variations in collections of male and female Cnemidophorus tigris on specific sites (mounds and open) by month for See text for discussion of specific sites. MAY JUNE JULY AUGUST TOTAL ADULT MOUND MALES OPEN JUVENILE MALES MOUND OPEN ADULTS FEMALES MOUND OPEN MOUND JUVENILE FEMALES OPEN
33 Table 4 Mean ± standard deviation of snout-vent length of lipids (LIP in mg), total tissue (TOT in mg) and percent for monthly samples of males (M) and females (F). MONTH SEX SVL LCT FAT 1 BODIES LIVER (N) LIP TOT % LIP TOT % M B3.3 ' "~ LATE (16) ±1.0 ±178.7 ±31.5 ±33.5 ±3.2 ±1.8 ±5.3 ±2.4 AUGUST 1970 F o (18) ±3 7 ±121.2 ±35.2 ±36.6 ±1.5 ±1.4 ±3,5 ±1.6 M (10) ±0.7 ±170.4 ±6.5 ±6.9' ±7.5 ±1.4 ±3.8 ±2.5 MAY 1971 F (9) ±1.4 ±182.5 ±21.9 ±22.4 ±1.5 ±1.9 ±9.3 ±1.8 M (11) ±1.2 ±272.0 ±2.5 ±2.6 ±5.1 ±1.4 ±6.5 ±2.6 JUNE 1971 F (11) ±1.7 ±173.6 ±6.7 ±10.8 ±3.7 ±1.9 ±2.8 ±3.9 M (10) ±1.0 ±218.5 ±36.4 ±37.4 ±1.9 ±2.1 ±7.7 ±1.8 JULY 1971 F (24) ±1.2 ±133.8 ±1.7 ±17.5 ±1.9 ±1.6 ±5.4 ±1.7 M EARLY (5) ±1.7 ±282.6 ±15.8 ±17.6 ±4.2 ±3.2 ±5.2 ±3.3 AUGUST 1971 F (6) ±1.9 ±319.6 ±9.8 ±10.4 ±9.1 ±2.7 ±7.6 *2.9 MID AUGUST F (5) ±3.2 ±393.3 ±48.2 ±51.5 ±1.4 ±1.1 ±9.0 ±3.6
34 26 (SVL in mm) and lean carcass tissue (LCT in mg); and dry weight lipids (%) for fat bodies, liver, ova, carcass and total tissue OVA CARCASS TOTAL LIP TOT % LIP TOT *36.7 ±111.7 % 5.0 ±0.6 LIP TOT % " ±66.1 ±259.5 ± ±21.9 ±119.0 ± ±50.6 ±121.2 ± ±18.8 ±182.7 ± ±42.5 ±35.4 ±9.1 ±19.1 ±182.8 ± ±29.4 ±184.6 ± ±47.7 ±234.1 ± ±17.6 ±270.9 ± ±18.4 ±276.1 ± ±1.9 ±2.4 ± ±17.3 ±170.6 ± ±28.9 ±170.3 ± ±39.6 ±246.9 ± ±12.8 ±61.6 ±3.3 ±17.6 ±123.8 ± ±71.1 ±271.0 ± ±30.8 ±131.5 ± ±46.1 ±325.6 ± ±25.5 ±338.2 ± ±63.7 ±344.1 ± ±35.7 ±353.8 ± ±28.4 ±410.5 ± ±71.9 ±423.2 ±1.3
35 Table 5 Mean ± standard deviation of snout-vent length of lipids (LIP in mg), total tissue (TOT in mg) and percent for monthly samples of females placed in ova size classes (OSC) MONTH OSC SVL LCT FAT BODIES LIVER (N) LIP TOT % LIP TOT % AUGUST (18) ±3.7 ±121.2 ±35.2 ±36.6 ±1.5 ±1.4 ±3.5 ± (3) ±7.1 ±499.6 ±15.0 ±15.3 ±2.6 ±0.3 ±7.2 ±2.6 MAY (5) ±4.3 ±167.3 ±37.8 ±38.6 ±2.4 ±1.9 ±3.4 ± T (4) ±2.2 ±135.5 ±18.9 ±20.1 ±5.8 ±1.8 ±4.0 ±4.0 JUNE (7) ±5.9 ±227.8 ±13.8 ±13.7 ±5.4 ±2.7 ±2.6 ± * (16) ±6.2 ±171.2 ±24.6 ±24.6 ±1.6 ±2.1±7.0±2.0 JULY (8) ±4.8 ±199.2 ±8.1 ±6.7 ±4.4 ±3.4±8.7±2.9 AUGUST (6) ±1.9 ±319.6 ±9.8 ±10.4 ±9.1 ±2.7±7.6±2.9
36 27 (SVL in mm) and lean carcass tissue (LCT in mg); and dry weight lipids (%) for fat bodies, liver, ova carcass and total tissue OVA CARCASS TOTAL LIP TOT % EXP TOT % LIP TOT % ±21.9 ±119.0 ±0.6 ±50.6 ±121.2 ±2.9 Mi ±32.7 ±479.1 ±1.8 ±47.8 ±467.7 ± ±4.5 ±6.8 ±1. 0 ±20.9 ±160.7 ±0.4 ±55.2 ±191.0 ±1.1 M ±39.3 ±146.8 ±1.8 ±56.1 ±154.2 ± ±1.9 ±2.3 ±1. 1 ±18.1 ±218.0 ±1.1 ±35.2 ±212.8 i ±3.5 ±9.4 ±3. 7 ±15.8 ±171.0 ±0.5 ±41.3 ±197.2 ± ±17.2 ±68.9 ±3. 9 ±35.0 ±144.8 ±1.3 ±58.3 ±135.9 ± ± 25.5 *338.2 ± 0.6 ± 35.7 * *0.7
37 Figure 1 Monthly, variation in mean testes size (length + width in mm) for Cnemidophorus tigris from El Paso (triangles) and Kermit, Texas (circles). Data from Kermit from Hoddenbach (1965). 28
38 N CD < =3 D C 3 mmmmmmrn «MMJLM» o R O) D < o 00 CD (M+~l)3 ZIS S 3 1 S 3 1 NV31A1
39 Figure 2 Monthly variations in size of follicles (diameter in mm) for Cnemidophorus tigris females. Means are the horizontal lines; standard deviation the rectangles; and 95% confidence limits the vertical lines. 29
40 CD D < X O R CD ^ c\j O (LULU Ul) S3~iomoddodaiaiAivia
41 Figure 3 Monthly variations in lean carcass tissue means (horizontal lines), standard deviation (rectangles) and 95% confidence limits (vertical lines) for male (open rectangles) and female (closed rectangles) Cnemidophorus tigris. 30
42 O) < F: D) =3 ~> 13 IE z O jwmmm R I I i ± o 1 in o o CO o (6uj)3nSSIl SSVOdVDNV3~1
43 Figure 4 Monthly variations in weights of lean carcass tissue for females in three ova size classes (OSC). Means are the horizontal lines? standard deviation the rectangles; and 95% confidence limits the vertical lines. OSC 1 females are the open rectangles; OSC 2 females the closed rectangles; and OSC 3 females the black and white rectangle. 31
44 (AJ i O) 3 N 3 I I N 3 z: C o -c V/- 13 R CD 3 < o O o 0 o ID C\J (6w)3nssil SSVOdVD NV31 o ID
45 Figure 5 Monthly variations in percentage of lipids (dry weight) in fat bodies compared to lean carcass tissue weights for male and female Cnemidophorus tigris. Symbols same as in Figure 2. 32
46 CVJ mm mm 'S, O ) E 3 IE I o R O ) 00 CD CM O Qldll!N30d3d
47 Figure 6 Monthly variation in percentage of lipids (dry weight) in fat bodies compared to lean carcass tissue weights for female Cnemidophorus tigris in three ova size classes. Symbols same as in Figure 3. '33
48 CM < I W S 3 h* C D x z: O nttwum 5 R CD CD CM o a i d n i N 3 o ^ 3 d
49 Figure 7 Monthly variations in percentage of lipids (dry weight) in livers compared to lean carcass tissue weights for male and female Cnemidophorus tigris. Symbols same as in Figure 2. 34
50 %. CM v C7) D < h- ay 3 mm, =J D X I- z: O jfrmiiim N R CD O aidn ^T o CM o ln30d3d o
51 Figure 8 Monthly variations in percentage of lipids (dry weight) in carcasses compared to lean carcasses tissue weights of male and female Cnemidophorus tigris. Symbols same as in Figure 2. 35
52 W<M c\] R D D) < S 5 I I Z o R < 5 D) 00 (O CM aid 11 in3dm3d
53 Figure 9 Monthly variations in precentage of lipids (dry weight) in carcasses compared to total carcass tissue weights for females Cnemidophorus tigris in three ova size classes. Symbols same as in Figure 3. 36
54 C\J CJ) * I I <-z o X A M H - f t - R 3> < J ^ O I i i ««i m o Qldll INBOdBd
55 Figure 10 Monthly variations in percentage total lipids (dry weight) compared to total tissue weights for male and female Cnemidophorus tigris. Symbols same as in Figure 2. 37
56 ' CM 9 < D) N 3 % N & 2 z hmm«w» O 2 R O) 3 < \o ' 1 *,r - I > «...1 «i in O aidn in30d3d -» L /A i Cvj
57 Figure 11 Monthly variations in percentage total lipids (dry weight) compared to total tissue weight for female Cnemidophorus tigris in three ova size classes. Symbols same as in Figure 3. 38
58 eg =J O) < U ) H: b u c =? r^ X I o R 3 O) < CD eg -/A o OJ 1 1 1» I o a L o a Id II ln30&3d
59 LITERATURE CITED Adams, A. E. and E, E. Rae An experimental study of the fat bodies in Diemectylus viridescens. Anat. Rec. 41: Altland, P. D Annual reproductive cycle of the male fence lizard. Elisha Mitchell Scientific Soc. Jour. 57: Avery, R. A Utilization of caudal fat by hibernating common lizards, Lacerata vivipara. Comp. Biochem. Physiol. 37: Barwick, R. E The life history of the common New Zealand skink, Leiolopisma zealandia (Gray, 1843). Trans. Roy. Soc. New Zealand 86: Blair, W. F. i960. The rusty lizard, a populational study. University of Texas Press, Austin, Texas. I80p. Bostic, D. L. I964. The ecology and behavior of Cnemidophorus hypervthrus beldingj Cope (Sauria: Teiidae). Unpub. M. S. Thesis, San Diego State College. 112p. Carpenter, C. C. i960. Reproduction in Oklahoma Scelooorus and Cnemidophorus. Herpetologica 16: Clark, D. R The strategy of tail-autotomy in the ground skink, Lygosoma laterale. J. Exp. Zool. 176: Darevsky, I. S Seasonal change of fat bodies and gonads in some lizards of the Arax River Valley in Armenia. Zoologichesini Zhurnal 39: Dessauer, H. C Hibernation of the lizard, Anolis carolinensis. Proc. Soc. Exp. Biol. Med. 82: Dessauer, H. C. 1955«Seasonal changes in the gross organ composition of the lizard, Anolis carolinesis. J. EXD. Zool. 128: Echternacht, A. C Ecological relationships of two species of the lizard genus Cnemidophorus in the Santa Rita mountains of Arizona. Am. Midi. Nat. 78:
60 40 Fautin, R. W Biotic communities of the northern desert shrub biome in western Utah. Ecol. Mono. 16: Fitzpatrick, L. C The energy allocation to reproduction by the female Allegheny Mountain salamander Desmognathous ochrophaeus. Ph. D. dissertation, Kent State University, Kent, Ohio. 115p. Folch, J., M. Lees and G. Sloane-Stanley A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: * Gehlbach, F. R Herpetology of the Zuni Mountain region, northwestern New Mexico. U. S. Natl. Museum, Proc. 116: Goldberg, S. R, and C. H. Lowe The reproductive cycle of the Western Whiptail lizard (Cnemidophorus tigris) in southern Arizona. J. Morphol. 188: Hahn, W. E. and D. W. Tinkle Fat body cycling and experimental evidence for its adaptive significance to ovarian follicle development in the lizard Uta stansburiana. J. Exp. Zool. 158: Hoddenbach, G. A A comparison of reproduction in two lizards: Cnemidophorus tigris marmoratus and Uta stansburiana ste.ineri. Master's thesis, Texas Tech. College, Lubbock, Texas. Lewis, H. L. and F. L. Rose Effects of fat body fatty acids on ovarian and liver metabolism of Ambystoma tigrinum. Comp. Biochem. Physiol. 30: Marion, K. R. and 0. J. Sexton The reproductive cycle of the lizard Sceloporus malchiticus in Costa Rica. Copeia 1971: Mayhew, W. W Hibernation in the horned lizard Phvnosoma m'calli. Comp. Biochem. Physiol. 16: Reproduction in the desert lizard Dipsosaurus dorsalis. Herpetologica 27: McCoy, C. J Life history and ecology of Cnemidophorus tigris septrionalis. Ph. D. dissertation, University of Colorado, Bolder, Cblorado. 167p. _and G. A. Hoddenbach. I966. Geographic variation in ovarian cycles and clutch size Cnemidophorus tigris. Science 154:
61 Medica, P. A. 1967* Food habits, habitat preferences, reproduction and diurnal activity in four sympatric species of whiptail lizards (Cnemidophorus) in South Central New Mexico, Bull. So. Calif. Acad. Sci. 66: Miller, W. M The seasonal histological changes occurring in the ovary, corpus luteum, and testis of the viviparous lizard, Xantusia vigilis. Univ. Calif. (Berkely) Publ. Zool. 47: Milstead,. W. 1957a. Observations of the natural history of four species of whiptail lizard, Cnemidophorus (Sauria, Teiidae) in Trans-Pecos Texas. Southwestern Nat. 2: b. Some aspects of competition in natural populations of whiptail lizards (genus Cnemidophorus). Texas J. Sci. 9: A list of the arthropods found in the stomachs of whiptail lizards from four stations in Southwestern Texas. Texas J. Sci. 10: Moberly, W. R Hibernation in the desert iguana, Dipsosausorus dorsalis. Physiol. Zool. 36: Pianka, E. R, Comparative autecology of the lizard Cnemidophorus tigris in different parts of its geographic range. Ecology 51: Rose, F. L. and H. L. Lewis Changes in weight and free fatty acid concentration of fat bodies of paedogenic Ambystoma tigrinum during vitellogenesis. Comp. Biochem. Physiol. 26: , Shaw, C. E Notes on the eggs and young of some United States and Mexican lizards. Herpetologica 8: Shreve, F The desert vegetation of North America. Botan. Rev. 8: Smith, R. E Experimental evidence for a gonadal-fat body relationship in two lizards (Amevia festiva. A. quadrilineata). Biol. Bull. 134; Sokal, R. R. and F. J. Rohlf Biometry. W. H. Freeman and Co., San Francisco. 776p. Stebbins, R. C Amphibians and reptiles of western North America. McGraw-Hill Book Co., Inc. New York.
62 42 Steele, R. G. and J. H. Torrie. I960. Principles and procedure of statistics. McGraw-Hill Book Co., Inc. New York. Tanner, W. W. and C. D. Jorgensen Reptiles of the Nevada Test Site. Brigham Young Univ. Sci. Bull., Biol. Ser. 3s Telford, S. R Seasonal fluctuations in liver and fat body weights of the Japanese lizard Takydromus tachydromides Schlegel. Copeia 1970: White, A., P. Handler,and F. L. Smith. 1964* Principles of biochemistry. McGraw-Hill. New York. 1106p. Woodbury, M. and A. M. Woodbury Life-history studies of the sagebrush lizard Scelooorus g. graciosus with special reference to cycles in reproduction. Herpetologica 2;
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