TESTICULAR CYCLE AND TIMING OF REPRODUCTION IN THE COLLARED LIZARD (CROTAPHYTUS COLLARTS) IN ARKANSAS
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1 Herpetologica, 35 (2 ), 1979, O 1979 by The Herpetologists' League TESTICULAR CYCLE AND TIMING OF REPRODUCTION IN THE COLLARED LIZARD (CROTAPHYTUS COLLARTS) IN ARKANSAS ABSTRACT: The testicular cycle of Crotaphytus collaris was studied using samples of animals collected in northern Arkansas in 1971 and Males mature at 76 mm in snout-vent length and participate in breeding activities in their first year of life. Histological analyses of the testes showed that spermiation occurs from early May to late June. Abdominal fat bodies become depleted during this period. Testicular recrudescence begins in late July. Interstitial cells were abundant in testes of all adults. A concurrence between the duration of spermiation in males and the ovigerous condition of females in both years indicates a high degree of synchrony in the reproductive cycles of males and females in this species. Key words: Crotaphytus; Lacertilia; Spermatogenesis RECENT investigations of life history tactics in lizards have been based primarily upon phenomena relating to the female reproductive cycle. Ballinger (1977) reviewed much of the information on evolution and life history strategies, and other workers reviewed information on modeling ( Pianka, 1976; Steams, 1977) and on clutch size and reproductive effort (Avery, 1975; Ballinger and Schrank, 1972; Fitch, 1970; Goldberg, 1975; Martin, 1977; Newlin, 1976; Parker, 1973; Schall, 1978; Vitt, 1977; Vitt and Ohmart, 1977). However, charactelistics of the male reproductive cycle, such as the duration of sustained spermatogenesis or the duration of aggressive behavior, may be just as important as the female reproductive cycle in determining the total reproductive pattern of a species (Newlin, 1976; Schrank and Ballinger, 1973 ).
2 /h June HERPETOLOGICA 185,--. Evaluation of seasonal testicular cycles using histological analyses, as well as by determining cyclic variation in testicular length, weight, width, and volume (usually expressed as ratios of snout-vent length or body weight), usually has been the basis for indicating the exact time and duration of maximum testicular development and/or reproductive activity. Long-lived species (sensu Schrank and Ballinger, 1973; Tinkle, 1969) usually have small testes upon emergence from hibernation, with seminiferous tubules in some stage preceding spermiation. Furthermore, spermiogenesis and breeding activity are usually brief in these species. On the other hand, many short-lived species emerge with enlarged testes in which the seminiferous tubules are undergoing spermiogenesis and/or spermiation. In these, prolonged spermatogenesis and breeding activity typically occur. Precise information on the duration of spermiation may be useful as an index of male reproductive effort. Published information pertaining to reproduction in the collared lizard has emphasized the female cycle (Ferguson, 1976; Fitch, 1956, 1970; Hipp, 1977; Parker, 1973; Robison and Tanner, 1962; Trauth, 1974, 1978; Vitt, 1977). The present paper describes the testicular cycle of the eastern collared lizard ( Crotaphytus collaris) in Arkansas and discusses the concept of male reproductive effort. Eighty-five adult and juvenal collared lizards were collected by sampling weekly from April through August 1971, and from March through mid-september Most were taken by noose or by hand from xeric exposures in cedar glades or sandstone outcroppings in the northernmost counties of Arkansas ( elevation 112,455 m ). Occasional specimens were collected along shoreline habitats of Bull Shoals and Norfolk lakes in Baxter, Boone, and Marion counties, and also along the shoreline of Beaver Lake, Carroll County, Arkansas. Specimens were processed within 8-24 h TABLE 1.-Stages in the annual spermatogenic cycle of adult male Crotaphytus collaris from Arkansas as revealed by histological examination of testes. Parentheses identify features in the spermatogenic cycle of Crotaphytus that differ from those described by Mayhew and Wright ( 1970 ) for Uma. Stage Spermatogenic condition 1" Division of any germinal cells without the development of a lumen ( lumen present) 2 Primary spermatocytes at luminal margin 3 Secondary spermatocytes at luminal margin 4 Undifferentiated spermatids at luminal margin 5 Metamorphosing spermatids at lurninal margin 6 Mature sperm in lumen 7 Early regression, cellular debris in lumen (debris atypical in lumen; sperm still present within lumen ) 8 Complete regression, no cell division, no lumen ( lumen present ) a Seminiferous tubules in stages comparable to stages 2-5 may occur in Umu without the development of a lumen. after capture. Data recorded prior to preservation included snout-vent length ( SVL ), tail length, and body weight (to the nearest 0.1 g). The lizards were killed with an injection of sodium pentobarbitol and fixed in 10% formaldehyde for 2448 h. Reproductive tracts were removed and placed in vials of 70% ethanol. Preliminary measurements indicated that there are only minor differences in weight between right and left fat bodies; therefore, the total weight of fat bodies was estimated by weighing the right fat body and doubling its weight. Lengths and widths were recorded for both testes, and testicular volumes were determined using the formula for an ellipsoid (Mayhew, 1963). The left testis with attached epididymis of 70 adults and 7 juveniles was prepared for examination by light microscopy. Testes were embedded in paraffin, sectioned serially at 10 pm, and stained with Harris' hematoxylin and eosin. Diameters of true to nearly true cross sections of 10 seminiferous tubules were measured in each testis. The epithelial thickness of each seminiferous tubule was determined by measuring from spermatogenic cells touching the basement membrane to the
3 HERPETOLOGICA [Vol. 35, No. 2 i;, I I I...I,,,,,-,,I I,,,I.,,I I,,,I,,fi1 I.,,In,,I I,;,I~~~I MAR APRAPR MAY MAY JUN JUN JUL JUL AUGAUG FIG. 1.-Seasonal changes in testicular volumes for adult Crotaphytus collaris from Arkansas. Vertical lines = ranges; vertical bars = +2 SE; horizontal lines = means and sampling intervals. Numerals above vertical lines represent number of testes in sample. Iuminal margin. The cliameter of epididyma1 tubules varies regionally; therefore, measurements of cross sections were taken primarily from the most columnar region of the epididymis. Twenty interstitial cell nuclei (five from each of four clusters in various regions of the sectioned testis) were measured to the nearest 0.01 pm. When means are given, they are accompanied by plus or minus two standard errors unless otherwise indicated. Specimens and prepared slides are currently in the possession of the author. Testicular Cycle Histological analyses of the testes of C. collaris revealed several differences from the spermatogenic cycle (Table 1) proposed by Mayhew and Wright (1970). In general, testes begin maturing during the hatchling-juvenile growth period prior to hibernation in October. Testes of young as well as older adults (> 76 mm SVL) enlarge the following spring and early summer, and lizards in both age groups participate in breeding activities. As the breeding season ceases in late June, the testes enter a regressed, quiescent phase, and the cycle is completed. Recrudescence of testes in late I I I I I I I I I - l I I I I I MAR APR MAY JUN JUL AUG SEP FIG. 2.-Seasonal variation in the size of the seminiferous and epididymal tubules and their epithelia in adult male Crotaphytus collaris from Arkansas collected in Numbers represent testicular stages; symbols are located at the midpoint of the duration of each stage. = diameter of semi- niferous tubule; m = thickness of epithelium in seminiferous tubule; 0 = diameter of epididyrnal tubule; tubule. = thickness of epithelium in epiclidymal July and August initiates the next testicular cycle. The cyclic nature of the testicular changes is illustrated by seasonal fluctuations in testicular volumes ( Fig. 1 ). Following is a description of spermatogenesis derived from specimens collected in Emergence to mid-april.-primary spermatocytes were most numerous within the seminiferous tubules during late March and early April (stage 2) and often occluded the lumina. Epididymal tubules were much reduced. With the onset of stage 3 the lumina of seminiferous tubules enlarged greatly ( Fig. 2) and secondary spermatocytes ( Fig. 3A) began to appear near the margins of the lumina. Epithelial thickness of the seminiferous tubules decreased slightly as the diameter of the tubules increased. The epididymal tubules showed pseudostratification-of the epithelia and contained cellular debris. Mid-April to early May.-Spermatogenesis continued at an accelerated rate during this period and was typically represented by testicular stages 4 and 5. The seminifer-
4 r' June HERPETOLOGICA 187 FIG. 3.-Photomicrographs of senliniferous tubules and epiclidymis of Crotaphyttrs collaris. (A) Partial section of a sen~iniferous tubule ( stage 3 ) exhibiting secondary spermatocytes at the luminal margin ( x 479 ). Arrow points to a cluster of interstitial cells situated between three seminiferous tubules. ( B ) Par- tial section of a seminiferous tubule (stage 6) bearing mature sperm ( x 479). IC = interstitial cells. (C) Portion of a seminiferous tubule (stage 5) exhibiting metamorpl~osing spemn~aticls at the luminal mar- gin ( x 479). Arrow points to a group of four nuclei of Sertoli cells next to the basement membrane. ( D ) Epididymal tubule packed with sperm ( x 293). Note simple columnar epithelium of the tubule. ous tubules reached their maximum size of pm concurrently with maximum testicular volume (f = 359 mm"). Secondary spermatocytes were transforming into unclifferentiated spermatids ( stage 4), although only two specimens showed this trai-~sitory stage. The epithelium of seminiferous tubules appeared somewhat pyramidal where metamorphosing spermatids were grouped together (stage 5; Fig. 3C). Large Sertoli cells were evident adjacent to the basement membrane. The epididymal tubules were extended anteriorly, but were relatively constant in size throughout the most columnar region. Early May to late June.-Spermiogenesis (stages 5 and 6) occurred throughout May to late June with mature sperm filling the seminiferous tubules and lining the luminal margins (Fig. 3B). The mean testicular volume for stage 6 in 1971 and 1972 was rnm" (n = 18) and m1n3 (n = 26), respectively. Spermatocytogenesis continued throughout May and June, and sperm often were present in regressing testes (Fig. 4A). Expanded epididymal tubules ( pm) were ovoidal, possessed simple columnar epithelia, and contained centrally located masses of sperm (Fig. 3D). Following breeding activities in June, the seminiferous tubules regressed and were characterized by a re-
5 HERPETOLOGICA [Val. 35, No. 2,- FIG. 4.-Photomicrographs of seminiferous tubules of Crotaplaytus collaris. (A) Section through a regressing testis (stage 7) showing greatly reduced seminiferous tubules ( x 108). Mature sperm are still present within lumina. Note the prominence of interstitial cells in this stage. ( B ) Sen~iniferous tubules of a spent testis (stage 8); the lumina may contain some cellular debris, but are usually empty (X 293). TA = tunica albuginea. (C) Section through a testis illustrating recrudescence of the seminiferous epithelium (stage 1). Proliferation of germinal cells results in little increase in tubule diameter and the lumen remains ( X 200). ( D) Magnification of C ( x 479). Arrow points to dividing germinal cell at the luminal margin.,- duction in luminal size (stage 7; Fig. 4A). A few sperm remained in the lumina. Sloughing of epithelial cells, typical of other lizard species at this stage (Mayhew and Wright, 1970; Vitt, 1973), was encountered only occasionally. he epididymal tubules had decreased to a diameter of 132 * 15.2 pm, were devoid of sperm, and were mostly lined by a pseudostratified columnar epithelium. Some late-maturing males possessed sperm in the posterior segment of the epididymis as late as 17 August. Also associated with this period of regression were large numbers of interstitial cells within the incorporated within a Sertoli cell syncytium along the basement membrane of the seminiferous tubules (stage 8; Fig. 4B). The lumina remained and often contained cytoplasmic debris. Interstitial cells were most obvious in this stage as they encircled most of the regressed tubules. The epididyrnal tubules were much reduced and were similar in appearance to all testicular stages other than 3-6. The proliferation of resting spermatogonia marked the beginning of recrudescence in the testes in late July. There was little increase (19 pm) in the diameter of the seminiferous tubules of stage 1 (Fig. intertubular regions of the testes. 4C) from stage 8. Lumina persisted within July to hibermtion.-the spent testis con- the tubules, and mitotic figures charactertained one or two rows of germinal cells ized this restoration process (Fig. 4D).
6 r'. Tune HERPETOLOGICA n MAR APR MAY JUN JUL AUG FIG. 5.-Total weight of fat bodies expressed as a ratio of total body weight ( x 100) for male CTO- taphytus collaris from Arkansas. Vertical lines = ranges; vertical bars = 2 2 SE; horizontal lines = means; numerals above bars = sample size. Juvenal males exhibited testes in stage 1 just prior to hibernation. Several juveniles showed advanced stages (3-6) prematurely upon emergence in early March which may indicate brumal testicular activity. Epididymal tubules were greatly reduced during stage 1 as epithelial cells contained large nuclei and little cytoplasm. Interstitial cell cycle.-scattered between the seminiferous tubules of C. collaris and of most lizards (exceptions are found in the genus Sceloporus) are small clusters of interstitial (Leydig) cells (Figs. 3, 4). These cells play an important endocrine role in vertebrates and are also related to spermatogenic activity in lizards (Duda and Koul, 1976). Testes of collared lizards showed a high incidence of these cells at all times of the testicular cycle, although actual counts were not made. Cytoplasmic materials of interstitial cells remained eosinophilic in all testes of adults examined. Nuclear diameters of interstitial cells were relatively constant in size (range pm; i = 5.6 pm) throughout the activity season in contrast to those of Agama tuberculata ( Duda and Koul, 1976). Minimal interstitial cell size was observed in spermatogenic stages 7 and 8. A circumtesticular tunic of interstitial cells, characteristic of many species of the lizard genus Cnemidophorus (Lowe and Goldberg, 1966), was not observed. Fox (1977) provided the most recent work on various aspects of interstitial cell activity in reptiles. Fat Body Cycle Hahn and Tinkle's ( 1965) experimental evidence showing a depletion of stored fat
7 HERPETOLOGICA [Val. 35, No. 2.- accompanying follicular development in female Uta stansburiana has provided the foundation for numerous studies correlating changes in size of abdominal fat bodies with reproductive cycles. Brenner and Brenner ( 1973) found an inverse relationship between total body fat and testicular size in collared lizards. Figure 5 illustrates the seasonal and yearly variation in ratios of fat body weight/total body weight in male C. collaris from Arkansas. A similar condition (data not presented) exists between fat body weight and SVL ( > 76 mm) in males. Mean monthly fat body weight/body weight ratios ( X 100) were smallest for both years in the month following maximum testicular development (June 1971, ; May 1972, ). Maximum fat body weight ( 1.46 g) occurred in July 1972, and represented slightly over 3% of the total body weight (57.7 g) of the largest lizard collected. In 1971, the mean fat body weight/body weight ratio was increasing just prior to hibernation, while in 1972, the reverse was true. The decrease in August 1972 could be associated with a reduction of foraging activities related to an observed late summer aestivation. In Texas, Hipp (1977) found a significant decrease in fat body weight in C. collaris in August. He attributed this to a combination of decreased food availability along with increased energy expenditures related to selection and defense of a hibernaculum. The utilization of fat body lipids during winter dormancy occurs in many lizard species ( Derickson, 1976). In Arkansas, C. collaris emerging in March 1972 had a mean fat body weight/body weight ratio (0.91 * 0.38) similar to lizards just prior to hibernation in August 1972 (0.89 * 0.88). This suggests minimal use of fat body reserves during hibernation. Reproductive Effort and Timing Reproductive effort is loosely defined here as an organism's total investment or expenditure of energy in acts directly or indirectly associated with reproduction. Ratios of weights or energy content of reproductive tissues relative to total body weight have typically been used as empirical indicators of the intensity of reproductive effort (Pianka, 1976). The energy costs of reproductive activities ( ter~itorial defense and courtship) in male C. collaris may explain the declines in weight of fat bodies in May and June. These are comparable to those costs sustained by female C. co1lari.s in vitellogenesis ( Trauth, unpublished). A similar relationship was found in Cnemiclophorus tigris (Parker, 1973; Vitt and Ohmart, 1977) and Sceloporus graciosus ( Goldberg, 1975). As suggested by Schrank and Ballinger (1973), a strong selection for synchronization of male and female reproductive cycles should occur in lizards; such would be of prime importance in determining the timing of the testicular cycle. A synchronization of spermiation in males with ovulation in females would maximize reproductive efficiency while allowing in turn for optimal foraging and nonreproductive successes. This interpretation of male reproductive timing would be especially significant in oviparous species which do not rely on,-- oviducal sperm storage for delayed fertilization, since fertilization of eggs must occur before shell deposition begins in the oviducts. Although C. collaris is known to possess seminal receptacles in the oviducts ( Cuellar, 1966), almost complete concurrence was found between male and female reproductive cycles. In 1971, spermiation (stage 6) extended from 1 May to 20 June. Ovigerous females (n = 11) were collected from 15 May until 28 June (Trauth, 1978). As shown in Figure 1, this period also coincided with that of maximum testicular volume. Because of favorable weather conditions in 1972, males emerged from hibernation 3 wk earlier than in 1971, and maximum testicular volume was recorded in the last half of April during stage 5. However, spermiation occurred from 5 May to 25 June while testicular volume was markedly decreasing. Ovigerous females (n = 17) were collected from 11 May to 30 June. This indicates that the time of sperm release more closely coin-
8 n June cides with the ovigerous condition in females than with maximum testicular size; it appears that neither oviducal sperm storage nor delayed fertilization are functionally significant in this species in the eastern portion of its range. The precise mechanism triggering spermiation in C. collaris may be an interplay between hedonic stimulation and olfactory "social releasers" ( Fitch, 1956) during courtship behavior. Many studies on lizard reproduction have compared data on periods of maximum testicular size, of presence of sperm in the epididymis, and of sustained spermiogenesis in relation to the ovigerous condition of females, but few have shown a concurrence between the periods of spermiation and gravidity. A detailed review of these aspects of reproduction in lizards of the United States is currently under investigation by me. Acknowledgments.-This report was extracted from a thesis presented to the Department of Zoology, University of Arkansas, Fayetteville, in partial satisfaction of requirements for the Master /7 of Science degree. I thank Dr. Perry M. Johnston for the use of his microtechnique facilities. Dr. James M. Walker directed my efforts, for which I am sincerely appreciative. During the early course of this study, Dr. David Cundall (Lehigh University) and Mr. Doyne Martin offered numerous helpful suggestions. Drs. George W. Folkerts, Robert H. Mount, and Lawrence C. Wit of the Department of Zoology-Entomology, Auburn University, critically reviewed the manuscript. I thank my wife Joy for her patience during the preparation of this paper. AVERY, R. A Clutch size and reproductive effort in the lizard Lacerta vivipara Jacquin. Oecologica 19 : BALLINGER, R. E Reproductive strategies: food availability as a source of proximal variation in a lizard. Ecology 58: BALLINGER, R. E., AND G. D. SCHRANK Reproductive potential of female whiptail lizards, Cnemidophorus gularis gularis. Herpetologica 28 : BRENNER, F. J., AND P. E. BRENNER The relationship between body fat and reproductive cycle in two species of lizards (Reptilia: Iguanidae). Proc. Pennsylvania Acad. Sci. 47: CUELLAR, Oviducal anatomy and sperm storage structures in lizards. J. Morphol. 119: DERICKSON, W. K Lipid storage and utilization in reptiles. Am. Zool. 16: ~ D A P., L., AND 0. KOUL Interstitial cell cycle in Agama tuberculata Gray ( Reptilia, Lacertilia, Agamidae ). J. Herpetol. 10: FERGUSON, G. W Color change and re- ~roductive cycling in female collared lizards ( Crotaphytus collaris). Copeia 1976: FITCH, H. S An ecological study of the collared lizard ( Crotaphytus colla~is ). Univ. Kansas Publ. Mus. Nat. Hist. 8: Reproductive cycles in lizards and snakes. Univ. Kansas Mus. Nat. Hist. Misc. Publ. ( 52 ) : Fox, H The urogenital system of reptiles. Pp in Gans, C., and T. S. Parsons ( Eds. ), Biology of the Reptilia. Vol. 6. Academic Press, London. GOLDBERG, S. R Reproduction in the sagebrush lizard, Scelopmus graciosus. Am. Midl. Nat. 93: 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: HIPP, T. G Reproductive cycle and correlated hematological characteristics in CTOtaphytus collaris in west central Texas. M.S. Thesis, Angelo State Univ., San Angelo, TX. LOWE, C. H., AND S. R. GOLDBERG Variation in the circumtesticular Leydig cell tunic of teiid lizards ( Cnemidophorus and Ameiva). J. Mo~phol. 119 : MARTIN, R. F Variation in reproductive productivity of range margin tree lizards (UTOsaurus ornatus). Copeia 1977 : MAYHEW, W. W Reproduction in the granite spiny lizard, Scelopomts orcutti. Copeia 1963 : MAYHEW, W. W., AND S. J. WRIGHT Seasonal changes in testicular histology of three species of the lizard genus Uma. J. Morphol. 130: NEWLIN, M. E Reproduction in the bunch grass lizard, Scelopow scalaris. Herpetologica 32: PARKER, W. S Notes on reproduction of some lizards from Arizona, New Mexico, Texas, and Utah. Herpetologica 29 : PIANKA, E. R Natural selection of optimal reproductive tactics. Am. Zool. 16: ROBISON, S. G., JR., AND W. W. TANNER A comparative study of the species of the genus Crotaphytus Holbrook ( Iguanidae ). Brigham Young Univ. Sci. Bull. Biol. Ser. 2:l-31. SCHALL, J. J Reproductive strategies in sympatric whiptail lizards ( Cnemidophorus) :
9 192 - HERPETOLOGICA [Vol. 35, No. 2 - two parthenogenic and three bisexual species. Copeia 1978: SCHRANK, G. D., AND R. E. BALLINGER Male reproductive cycles in two species of lizards (Cophosaurus texanus and Cnemidophorus gularis). Herpetologica 29 : STEARNS, S. C The evolution of life history traits: a critique of the theory and a review of the data. Ann. Rev. Ecol. Syst. 8: TINKLE, D. W The concept of reproductive effort and its relation to the evolution of life histories in lizards. Am. Nat. 103: TRAUTH, S. E Demography and reproduction of the eastern collared lizard, Crotaphytzis collaris coh~ris (Say), from northern Arkansas. M.S. Thesis, Univ. Arkansas, Fayetteville Ovarian cycle of Crotaphytus collaris ( Reptilia, Lacertilia, Iguanidae ) from Arkansas with emphasis on corpora albicantia, follicular atresia, and reproductive potential. J. Herpetol. 12: VITT, L. J Reproductive biology of the anguid lizard, Ger~honotus coeruleus principis. Herpetologica 29 : Observations on clutch and egg size and evidence for multiple clutches in some lizards of southwestern United States. Herpetologica 33 : Vrrr, L. J., AND R. D. OHMART Ecology and reproduction of lower Colorado River lizards : 11. Cnemidophorus tigris ( Teiidae ), with comparisons. Herpetologica 33 : Accepted: 25 September 1978 Department of Zoology-Entomology, Auburn University, Auburn, AL 36830, USA v
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