Annual variation in reproductive traits in the lizard ...

Annual variation in reproductive traits in the lizard Acanthodactylus erythrurus AURORA M. CASTILLA Department of Biology, University of Ant~lerp(U.I. A.), Universiteitsplein 1 , B-2610 Wilrijk, Belgium

L. JAVIER BARBADILI,~ Unidad de Paleontologia, Departamento de Biologia, Universiciad Autonotna de Madrid, E-28049 Madrid, Spain AND

DIRKBAUWENS

Can. J. Zool. Downloaded from www.nrcresearchpress.com by China University of Petroleum on 06/05/13 For personal use only.

Institute of Nature Consenution , Kiewitdreef 3 , B-3500 Hasselt, Belgium Received June 6, 1991 Accepted September 25, 1991

CASTILLA, A. M., BARBADILLO, L. J., and BAUWENS, D. 1992. Annual variation in reproductive traits in the lizard Acanthodactylus erythrurus. Can. J. Zool . 70: 395 -402. During a 2-year period we studied the reproductive and fat body cycles and reproductive characteristics (clutch size, egg size) of the oviparous lizard Acanthodactylus erythrurus in central Spain. Testes exhibited their maximal volume during April - June and decreased in size throughout the summer. Fat bodies of males were smallest during the spring mating period. Vitellogenesis started in May or June, with oviposition occurring during June- July. Female fat bodies declined in size during the period of yolk deposition. A delay in the timing of reproductive events in 1 year was associated with adverse weather conditions during early spring. During the "good" year, reproduction was initiated early enough to allow some females to produce a second clutch. Both clutch size and egg size increased with female body length, but did not vary between years. Environmental factors that induced temporal variation in the timing of reproduction and clutch frequency did not affect clutch characteristics.

CASTILLA, A. M., BARBADILLO, L. J., et BAUWENS, D. 1992. Annual variation in reproductive traits in the lizard Acanthodactylus erythrurus. Can. J. Zool. 70 : 395 -402. Durant 2 ans, nous avons suivi les cycles de la reproduction et des graisses corporelles et etudie les caracteristiques reliees a la reproduction (nombre d'oeufs par couvee, taille des oeufs) chez le Iezard ovipare Acatzthodactylus erythrurus dans le centre de 1'Espagne. Les testicules ont atteint leur volume maximal entre avril et juin et ont diminue par la suite tout au cours de I'ete. C'est au cours de la periode d'accouplement, au printemps, que les corps gras des miles se sont averes le plus petits. La vitellogenttse commenqait en mai ou en juin et la ponte avait lieu en juin-juillet. Les corps gras des femelles diminuaient de taille durant la periode de formation du vitellus. Les phases de la reproduction ont ete retardees une annee a cause de mauvaises conditions climatiques au debut du printemps. Pendant la N bonne annee, la reproduction a commence assez t6t pour que quelques femelles produisent une seconde couvee. Le nombre d'oeufs dans la couvee et la taille des oeufs augmentaient en fonction de la longueur de la femelle, mais ne variaient pas d'une annee a l'autre. Les facteurs ecologiques responsables de la variation temporelle du dkclenchement de la reproduction et de la frequence des couvees n'ont pas affecte les caracteristiques reliees aux couvees. [Traduit par la redaction]

Introduction Initial studies of lizard reproductive strategies attempted to explain interspecific variation as adaptive responses to the environment and demographic profiles (e.g., Tinkle 1969; Tinkle et al. 1970). Subsequently, several investigators have stressed the importance of considering morphological (Vitt and Congdon 1978; Vitt 1981; Vitt and Price 1982) and phylogenetic (Dunham and Miles 1985; Dunham et al. 1988) constraints on interspecific variation in reproductive traits. In addition, it became evident that life-history traits vary among populations of a single species (Tinkle and Ballinger 1972; Dunham 1982; Ballinger 1983; Tinkle and Dunham 1983) and within populations over time (Ballinger 1977; Dunham 1978, 1981 ; Ferguson et al. 1980; Jones et al. 1987). Two important recommendations can be made on the basis of these findings. First, in studies of single species, temporal variation in lifehistory attributes should be considered and an attempt should be made to identify the proximal factors that induce this variation. Second, studies of interspecific differences ought to be restricted to comparisons among members of a single family, the lowest taxonomic level wherein variation in life histories seems not to be accounted for by taxonomic affinity (Dunham and Miles 1985; Dunham et al. 1988). The latter type of study P r ~ n t e dIn Canada I Irnpr~mCau Canada

is at present hampered by our very incomplete knowledge of the life histories of most lizard groups except the New World family Iguanidae (Dunham et al. 1988). Hence the call of earlier workers (Tinkle 1969; Tinkle et al. 1970) for more detailed information on a wider variety of lizard taxa is still relevant. Lizards of the family Lacertidae are abundant and widespread in the Old World. Nevertheless, few accounts of their life histories have been published and virtually all deal with European species. We provide information herein on the reproductive characteristics of Acanthodactylus erythrurus, a member of an advanced lacertid genus that has radiated extensively in desert habitats of North Africa, the Middle East, and Northwest India (Arnold 1989). This lizard has rather recently reached the European continent, where it is found in open sandy areas with sparse shrubs in south and central Iberia (Barbadillo 1987). Acanthodactylus erythrurus is a diurnal, heliothermic, swift, ground-dwelling lizard that differs from other European lacertids in having a relatively high selected ; Bauwens, unpublished data) body temperature ( ~ 3 7 ° C D. and a diet that is largely based on ants (Pollo and PerezMellado 1988). It shares these characteristics with several North African congeners (Perez-Mellado 1992).

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TABLE1. Summary of meteorological data during the 2 years of study, and the mean for the period 196 1- 1986

1984

r

Rainfall (mm)

Mean temperature ("C) 1984 1985 1961-1986

1984

1985 1961-1986

6.6 14.4 10.8 19.6 25.8 23.2 20.1 14.4 10.6 22.9 17.3

48.9 35.5 86.1 33.2 0.1 9.2 5.5 25.4 170.5 42.5 30.9

9.6 31.0 32.5 25.3 1.3 0.0 0.1 0.1 73.1 26.6 0.2

-.-

0.40 4-

0.10 -

.-Ca

;

.-u,

-0.20-

,, I

--0--

i

1985

2'1


4-

Mar. Apr . May June July Aug . Sept. Oct. Mar.-May June-Aug. Sept.-Oct.

8.4 12.9 14.3 21.6 26.3 24.8 24.2 17.3 11.9 24.2 20.8

9.0 11.5 15.5 20.5 24.5 23.8 20.2 14.6 12.0 22.9 17.4

37.2 53.3 41.5 25.4 12.0 11.4 27.7 41.4 132.0 48.7 69.1

NOTE: Values shown are the average daily mean temperature and the total amount of rainfall.

W e report the results of a 2-year study of the reproductive biology of A. erythrurus in central Spain. Our aim is to (i) describe the male and female reproductive and fat body cycles; (ii) analyse relationships between female size, egg numbers, and egg size; (iii) examine between-years differences in the timing and intensity of reproduction and identify environmental factors that are associated with this variation.

Materials and methods The study was conducted during 1984 and 1985 in an area situated between the townships of Torreledones and Hoyo de Manzanares (40°37'N, 3 "54'W; province of Madrid, Spain). The site is an open, sandy, degraded oak forest; the vegetation consists mostly of Quercus ilex rorundifolia, Juniperus communis, Lavendula sroechas, Cisrus sp., and Tymus sp. bushes. Weather data were obtained from the nearest meteorological station, "Cuatro Vientos," 28 km SSE of the study area. We captured 91 males and 75 females either directly by hand or after they had been stunned with rubber bands. Collections were made at biweekly intervals when weather conditions permitted. Lizards were immediately frozen and remained at -20°C for a week. They were defrosted for measurement and dissection. Preserved animals were deposited in the vertebrate collections of the Unidad de Zoologia Aplicada (Madrid). The following measurements were taken for each specimen: (i) snout-vent length (SVL); (ii) length and width of the pileus; (iii) testis weight; (iv) maximum diameter of the epitheliumepididymis; (v) kidney weight; (vi) abdominal fat body weight (only available for 1985); (vii) number and diameter of the ovarian follicles; (viii) number, length, and width of oviducal eggs. In addition, we recorded secondary sexual coloration, turgidity and developmental stage of the gonads, presence or absence of copora lutea, and the appearance of the oviduct as indicators of the degree of sexual activity. Sexual maturity was assessed by the presence of enlarged ovarian follicles ( > 3 mm diameter) or oviducal eggs or corpora lutea, and the appearance of the oviduct and testes. Body measurements were made with a caliper to the nearest 0.05 mm; organs were measured with an ocular micrometer to the nearest 0.01 mm. Organs were weighed with an electronic balance to the nearest 0.001 g. Right and left abdominal fat bodies and kidneys were weighed together. For all other organs, measurements for the left and right side of the body were highly correlated (P < 0.001 in all cases). We used the size of the left organ in subsequent analyses. An estimate of egg volume was obtained using the formula for the volume of an ellipsoid ( V = 413 n a 2 b , where a is half the shortest diameter and b is half the longest diameter).

u,

4Q,

.-> -a

-0.50-

4-

Q,

'1-------- &/ 1

-0.80-

[r

1

-

0

A . --- * A* aI l gA = L= zA z ; L -k k I " I " 5 a a , : : : = = a ; ? a

Y

E

a

n

~n

al

al

V)

V)

!

FIG. 1. Seasonal changes in the SVL-adjusted mean testis weight of Acanrhodacrylus eryrhrurus during 1984 and 1985. Vertical bars show standard error. All analyses of organ sizes were performed on logarithmically transformed data. Testicular weight, maximum diameter of the epididymis, and kidney weight each increased significantly with SVL. An index of SVL-adjusted dimensions for each organ was calculated using residuals from the least-squares regression line between organ size and SVL (both variables log transformed). We examined variation in organ size (SVL-adjusted where appropriate) by two-way analyses of variance (ANOVA) with year and biweekly sampling interval as factors. The year x biweekly sampling period interaction effect assesses the significance of a between-years difference in the timing of reproductive cycles. As a complement to this study, 10 females were maintained in outdoor terraria for the purpose of obtaining data on clutch and egg sizes. Eggs were dug up, buried in soil-filled terraria, and maintained under ambient environmental conditions. The timing of oviposition and eclosions were noted through daily inspections. Juveniles were measured (SVL) immediately after eclosion.

Results Sexual dimorphism a n d maturity In both years, males were slightly larger in SVL, on average, than females (males: x f 1 S D = 72.87 f 5.40; range = 61.3-85.5, N = 91; females: x f 1 S D = 71.02 _+ 4.85; range = 61 .O-83.8, N = 75; Mann-Whitney U-test: z = 2.06, P < 0.05). Males had larger and wider heads than females, even after accounting for the effect of body size (ANOVAwith S V L as a covariate; pileus length: FL1,1241 = = 43.68, P < 20.98, P < 0.001; pileus width: F[1,1241 0.001). The smallest reproductive male and female in 1984 measured 6 5 . 0 and 63.4 m m SVL, respectively. Corresponding values for 1985 were 61.3 and 6 1 . 0 mm. Lizards surpass this size in their third season of activity (age 21 months) o r later. Field observations Weather conditions differed markedly between 1984 and 1985, especially during spring (Table 1). March 1984 was cold; May 1984 was exceptionally cold and wet, including a 20-day period of continuous cloudy and rainy weather. March 1985 was very dry. Comparison of our study years with the long-term data (1 961 - 1986) indicates that, for the total spring period (March -May), 1984 was cold and wet, whereas 1985 was extremely dry but with typical temperatures. During


CASTILLA ET AL.

397

Fic. 3. Seasonal changes in the mean diameter of the largest follicle in preovulatory (circles) and postparturient (squares) female Acanthodactylus erythrurus during 1984 (solid symbols) and 1985 (open symbols). Vertical bars show standard error.

Fic. 2. Seasonal variation in the percentage of sexually mature female Acanthodactylus erythrurus in distinct reproductive states during 1984 (a) and 1985 (6). Fol 1, nonvitellogenic follicles ( 6 mm); ovr, oviducal eggs; POST, postparturient.

summer (June -August) and fall (September -October), 1985 continued to be hotter and drier than 1984 (Table I). In 1984, emergence from hibernation was late relative to 1985. We did not detect lizard activity in our study area until the second half of May in 1984, whereas in 1985 animals were present from the beginning of April onwards. In both years, males became active before females. Mating behaviour and copulations began shortly after the onset of female activity. The reddish colouring of the hind legs and tail in adult females and the bright yellow spots on both sides of the male's body are considered signs of mating activity (Seva 1982; Barbadillo 1987). In 1984 they were not visible until the first half of June. During 1985 these features were present from early May onwards. Copulations were observed from mid-May to July and took place in open areas near bushes. Four copulations observed in the field lasted from 20 s to 8 min. In captivity, one couple copulated twice a day during 2 consecutive days. The minimum time interval between copulations was 3 h. Copulation behaviour was similar to that described for A. boskianus (Carpenter and Ferguson 1977).

Reproductive cycles A significant biweekly variation in SVL-adjusted testicular = 33.70, P < 0.001). The weight was evident (Fig. 1; 48,74j

interaction year x 2 weeks was highly significant (F,5,74j= 3.83, P < 0.001). In 1984 the highest testicular weight was recorded during the second half of June, whereas in 1985 this happened during the second half of May. In both years, testicular weight declined over the summer, reaching a minimum during August -September. ~ a x i m u mdiameter of the epididymis, adjusted for SVL, also exhibited seasonal changes (Fi8,,] = 30.23, P < 0.001). A significant interaction effect of year x 2 weeks was evident (F,,,,, = 5.83, P < 0.001). Diameters were largest in 1984 during June -July. In 1985, diameters were at their maximal size from the second half of May until the first half of July. Ovarian follicles that were > 2.5 mm in diameter presented signs of vitellogenesis. Females containing follicles of this size exhibited the reddish reproductive colouring on their hind legs. Females with vitellogenic follicles (2.6 -6.0 mm diameter), yolking follicles ( > 6 mm) or oviducal eggs, and postparturient females appeared ca. 1 month earlier in 1985 than in 1984 (Fig. 2). During August all females from both years were reproductively inactive. In 1984 none of the females exhibited the simultaneous presence of vitellogenic follicles and oviducal eggs or corpora lutea, nor did we find any other indication that more than one clutch per female was produced in that year. Five out of 24 ovigerous or postparturient females captured during June July 1985 presented, at the same time, vitellogenic or yolking follicles and oviducal eggs or corpora lutea corresponding to the previous ovulation. These findings indicate that some females laid two clutches in 1985. Maximum follicular diameter showed significant biweekly variation during both years (Fig. 3; F,9,59j= 2.17, P < 0.05). When all females are considered, no significant year x 2 weeks interaction effect was detected ( P < 0.10). Nevertheless, the between-years difference in follicular growth was most apparent in the preovulatory females, whereas the ovigerous and postparturient females had small and similarsized follicles in both years (Fig. 3). An analysis considering only the preovulatory females revealed a significant year x fortnight interaction effect (42.241= 3.40, P < 0.05), indicating a between-years difference in the timing of follicular growth.

CAN. J . ZOOL. VOL. 70, 1992

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1

-m-

Males

T

Snout-vent

FIG. 4. Seasonal changes (mean f 1 SE) in mean abdominal fat body weight (log-transformed) in male and female Acanthodactylus erythrurus during 1985.

length (mm)

FIG.5. Relationship of clutch size to female size (SVL) in Acanthodactylus erythrurus during 1984 and 1985. The regression equation is CS = -3.23 0.094 SVL; r = 0.376.

+

Kidney cycles Kidney weight was related to SVL in both sexes (males: 41,741 = 190.84, P < 0.001; females: F11,40! = 31.52, P < 0.001). There was clear seasonal variation in SVL-adjusted kidney weight in both males (F19,741 = 22.57, P < 0.001) and females (F[9,401= 4.04, P = 0.001). Male kidneys were heaviest from May until the first half of July. In females, kidney weights were highest during May -July. We also detected a significant year x fortnight interaction in males (F[5,741= 3.16, P = 0.01) and females (F[5,401= 2.53, P < 0.05). In both sexes maximal weights were recorded ca. 1 month later in 1984 than in 1985. Fat body cycles In neither sex was the weight of abdominal fat bodies related to SVL (P > 0.20). They showed a clear seasonal cycle (Fig. 4; males: F19,401 = 19.91, P < 0.001; females: 49,251 = 6.46, P < 0.001). The fat stores of the males decreased rapidly in weight during April and were at their lowest levels during May and the first half of June. The fat bodies of females were lightest in June and became greatly enlarged during July -August. Fat body weight seemed to decrease only slightly during hibernation (Fig. 4). Clutch characteristics We found no differences between the numbers of enlarged vitellogenic follicles ( > 3 mm in diameter; N = 25 females) and oviducal eggs (5 females) or eggs deposited in the vivaria with SVL as a covariate: F,1,371 = (10 females) (ANOVA 0.003, P > 0.90). Also, we found only two atretic follicles in the ovaries of one female. These data indicate that the rate of follicular artesia was very low in our population. Therefore, the number of enlarged vitellogenic follicles and the number of oviducal eggs both provide a reliable estimate of clutch size (see also Worthington 1982; Abts 1988; Castilla and Bauwens 1989; but see MCndez de la Cruz et al. 1988). Clutch size increased significantly with female SVL (Fig. 5; F[1,37] = 6.47, P = 0.01) and did not differ between the 2 vears (ANOVA with SVL as a covariate, FI1 ,371 = 2.203, P > 0.10). Mean clutch size, when only first clutches were considered, was 3.6 (SD = 1.2, range = 2-6, N = 40; mean female SVL = 7 1.7 mm, SD = 4.7). The average number of eggs for second clutches was 2.8 (SD = 0.8, range = 2 -4, N = 6; SVL: x 1 SD = 71.3 3.2).

+

+

Snout -vent

length (mm)

FIG. 6. Correlation between mean egg volume in a clutch and female size (SVL) in Acanthodactylus erythrurus.

Estimated egg volume did not differ between years (FI,,451= 1.23, P > 0.02) or with developmental stage (oviducal or oviposited; F, ,451 = 1.16). The average length of 5 1 eggs from 14 clutches was 15.31 mm (SD = 1.99), mean width was 9.40 mm (SD = 0.85), and mean estimated volume was 72 1 mm3 (SD = 187). Egg volume differed significantly among clutches (F[,3,37] = 2.756, P < 0.01); mean egg volume for a female's clutch increased significantly with her SVL (Fig. 6; r = 0.901, P < 0.00 1). The partial correlation between egg volume and clutch size, with SVL held constant, was not significant (r = 0.064, P > 0.80). Hence, mean egg volume for a clutch increases with female SVL, irrespective of the number of eggs in the clutch. Mean egg width for a litter increased with female SVL (r = 0.578, P < 0.05), but the residual variation was not affected by egg number (partial correlation, with SVL held constant: r = 0.409, P > 0.10). Average egg length for a clutch increased with female SVL (r = 0.830, P < 0.001). The residual variation in egg length was negatively correlated with clutch size (partial correlation, with SVL held constant: r = -0.577, P < 0.05). Oviposition in the terraria was recorded between July 19 and August 5 during 1984. In 1985, four females oviposited between June 27 and July 8 and an additional female laid eggs on July 26. We suspect that the latter laying was the second clutch of that female.

CASTILLA ET AL.

Incubation in outdoor terraria lasted from 73 to 78 days. SVL of hatchlings ranged from 3 1.3 to 32.8 mm (a 1 SD = 31.8 0.6; N = 7).


+

+

Discussion In this study, the reproductive cycles and characteristics of A. erythrurus were examined over a 2-year period. We will first comment on general aspects of the reproductive biology in this species, and subsequently examine the observed temporal variation in reproductive processes and its possible proximal causes. Reproductive and fat body cycles The reproductive cycle of female A. erythrurus from central Spain is similar to that of other European lacertids (e.g., Xavier 1982; Braiia 1983; Hraoui-Blocquet 1987, Castilla and Bauwens 1990) and of temperate-zone lizards in general (Fitch 1970). Vitellogenesis starts in May or June, ovulation occurs in June-July, and the first clutch is laid during June-July. These findings parallel those of Pollo and Pkrez-Mellado (1990) for another central Spanish population of A. erythrurus. However, the observed timing of reproductive events was delayed compared with that in southern Spain (Seva 1982) and Morocco (Bons 1972), where follicle growth starts during April -May and many females produce two clutches per year. The spermatogenetic cycle is of the "prenuptial" or "vernal" type, in the terminology of Saint Girons (1982). Testicular recrudescence starts upon emergence from hibernation, and testes attain their maximal volumes during April -June. This interval coincides with the period during which courtship and mating are observed in the field. Testicular volume decreases throughout the summer. The vernal spermatogenetic cycles are characteristic of lizards and snakes from arid or Mediterranean climate zones (Bons and Saint Girons 1982; Saint Girons 1982). All European lacertids studied to date, including lizards that are sympatric with A. erythrurus over large parts of the Iberian peninsula (Podarcis hispanica (PkrezMellado 1982), Psammodromus algirus (Bons and Saint Girons 1982), Psammodromus hispanicus (Pascual and PkrezMellado 1989), Lucerta lepida (Castilla and Bauwens 1990)), exhibit a mixed-type reproductive cycle, in which spermatogenesis is completed in two successive seasons of activity. We suggest that the vernal reproductive cycle of male A. erythrurus reflects the evolutionary history of the genus Acanthodactylus, which radiated extensively in deserts of North Africa and the Middle East, whereas the primitive Paleartic lacertids (genera Lucerta and Podarcis) probably originated in mesic habitats of Eurasia (Arnold 1989). In the absence of data on other Acanthodactylus, this conclusion remains tentative. The observed seasonal variation in kidney weight tracked the cyclicity of the reproductive organs of both sexes. During the breeding season, the sexual segment of the kidney in many reptiles accumulates high concentrations of acid phosphatase and unsaturated lipids (see review in Fox 1977). These secretions, which are under androgen control, help to separate the semen from the urine and may ensure retention of semen in the female's cloaca and oviduct (Volsoe 1944). Misra et al. (1965) suggested that these secretions serve as an energy source for the sperm; Cuellar et al. (1972) demonstrated that the secretions may activate the sperm. The fat body cycles were closely coupled with the timing of reproductive events in both sexes. In females, the precipitous drop in fat body weight during June coincides with follicular growth and ovulation. Parallel findings have been reported for

399

a variety of other lizard species, mainly from temperate climatic zones (e.g ., Derickson 1976; Guillette and Sullivan 1985; Loumbourdis and Kattoulas 1985; Ortega 1986; Castilla and Bauwens 1990). These observations suggest that lipid stores are mobilised for follicular maturation and yolk production; experimental evidence for this process has been provided by Hahn and Tinkle 1965). The fat body stores of males begin to decline soon after their emergence from hibernation and remain at a low level throughout the mating period. The depletion of fat stores probably reflects high energy requirements associated with the acquisition and defence of a territory, searching for and guarding a mate, and courtship (e.g., Vitt et al. 1978; Ortega and Barbault 1986; Mkndez de la Cruz et al. 1988). In both sexes, fat bodies increased rapidly in size during the summer. There was no obvious decline in fat body weight during hibernation, indicating that energy demands for winter maintenance represent only a small fraction of the total amount of fat stored during autumn. Clutch and egg sizes Clutch size increased with female SVL, as in other lacertids (e.g., Pilorge et al. 1983; Bauwens and Verheyen 1987; Hraoui-Blocquet 1987; Barbault and Mou 1988; Henle 1988; Castilla and Bauwens 1989) and lizards in general (references in Fitch 1970; Dunham et al. 1988). However, both the regression coefficient (b = 0.094) and the predictive power (R2 = 0.14) of the equation relating clutch size to SVL are low compared with those for other lacertid lizards (b = 0.15 0.45; R2 = 0.23 - 0.60; values reported by or calculated from data in Avery 1975; Pilorge et al. 1983; Bauwens and Verheyen 1987; Pilorge 1987; Hraoui-Blocquet 1987; Barbault and Mou 1988; Henle 1988; Castilla and Bauwens 1989; Braiia et al. 1991). Egg size, which determines hatchling size (Sinervo 1990), was very variable in our population (extreme values for a clutch differed by a factor of more than 2) and increased with female SVL. The coefficient of variation (CV) for estimated egg volume equalled 26%, which is considerably higher than that reported for other lacertids (CV = 6- 16%; calculated from data in Castilla and Bauwens 1989 and Braiia et al. 1991). Stewart (1979), elaborating on the ideas of Smith and Fretwell ( 1974) and Brockelman (1975), presented a graphical model depicting relations among body size, clutch size, and egg size in lizards. The model predicts distinct patterns of covariation among these traits: (i) populations with a steep slope for the clutch size - female size regression should have constant egg or offspring size; (ii) in populations where egg size is positively related to female size, the regression coefficient for the clutch size - female SVL relation should be low. Acanthodactylus erythrurus fits the latter pattern, whereas other European lacertids seem to exhibit the former suite of covarying traits (see earlier comments on relations among clutch size, egg size, and SVL). Stewart (1979) envisaged directional selection for large hatchling size as the main mechanism inducing a positive correlation between egg size and female size. Performance functions and fitness components correlate with hatchling size in several lizards: larger hatchlings sprint faster (Sinervo and Adolph 1989; Sinervo 1990; Sinervo and Huey 1990; Van Damme et al. 1992), have prior access to limited resources (Ferguson et al. 1982), and have higher survival rates in some populations (Fox 1978; Ferguson and Fox 1984; but see Sinervo 1990). These observations support the idea of a selec-


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C A N . J . ZOOL. VOL. 70, 1992

tive advantage of larger young, favouring females producing bigger eggs. However, it does not adequately explain why the smaller females do not channel their reproductive investment into fewer, larger eggs. One benefit of producing small eggs is that they incubate faster and hence hatch earlier than bigger eggs (Sinervo 1990). A delay in reproduction in the smaller females (Bons 1972; Van Loben Sels and Vitt 1984; Bauwens and Verheyen 1985; Castilla and Bauwens 1990) hence may be compensated for, at least partially, by reduced incubation times. Alternatively, female size may constrain egg size, as evidenced in several freshwater turtles (Congdon and Gibbons 1987). In these turtles, egg width is directly proportional to the diameter of the pelvic opening and hence body size. Eggs of A. erythrurus are bigger than those of lacertids of similar size and shape (Pollo and Pkrez-Mellado 1990), supporting the idea that eggs may approach the size limit imposed by morphological constraints. In our population, both egg width and egg length increased with female length. When the effect of SVL was statistically removed, an increase in clutch size resulted in decreasing egg length, but egg width and volume were unaffected. Hence, female SVL influenced egg size, whereas clutch size affected the shape but not the size of the eggs. For eggs that are arranged linearly in the oviduct, egg length should be limited by the length of the oviduct (Ford and Seigel 1989), whereas egg width is probably constrained by the width of the pelvic girdle. In females of a given length a large number of eggs can only be accommodated at the expense of reducing egg length. This inverse relation between egg length and clutch size should only be evident when total clutch volume approaches limits set by female size. Our results demonstrate a negative correlation between egg length and clutch size, and provide further indirect support to the hypothesis that body volume constrains clutch volume and egg size. Annual variation in reproductive traits The most striking between-years difference in reproductive characteristics was the delay in the timing of reproductive events in 1984. During 1985, spring reproduction was initiated early enough to allow some females to produce a second clutch during the summer months. The shortening of the 1984 breeding season was associated with low ambient temperatures and prolonged rainfall during spring. Two causal pathways, not mutually exclusive, may link weather conditions to the timing of reproduction. First, the initiation of the yearly activity period is triggered by spring temperatures, and daily weather conditions (particularly direct sunshine) determine the duration of daily activity during the nonhibernation period (Avery 1976; House et al. 1980; Van Damme et al. 1987). Postponement of activity and (or) reduction of the time potentially available for activity probably result in a delay in the storage of energy necessary for synthesising the clutch, and hence in the timing of reproductive events (Bauwens and Verheyen 1985). Second, ambient temperature may have a direct effect on reproduction. In a variety of lizards, high temperatures are known to stimulate spermatogenesis and follicular growth, to such an extent that temperature is considered the primary external timer of reptile reproduction (Duvall et al. 1982). Despite the differences in length of the reproductive season and in clutch frequency, we detected no between-years variation in SVL-adjusted clutch and egg sizes. Hence, environmental factors that induced temporal variation in the timing of reproductive events seemingly did not affect fecundity.

Numerous studies of other lizards have revealed significant among-years variation in egg and (or) clutch sizes (e.g., Ballinger 1977; Dunham 1981 ; Worthington 1982; Jones et al. 1987; DeMarco 1989; Ferguson et al. 1990). This has most often been attributed to differential food abundance, which was either inferred from precipitation levels or, less often, empirically demonstrated (Ballinger 1977; Dunham 1981). In contrast, invariant reproductive performance, despite fluctuations in weather conditions and (or) food availability, was reported by Van Loben Sels and Vitt (1984) and Bauwens and Verheyen (1987). Jones et al. (1987) found no relations between precipitation and food consumption rates, or between the mass of food ingested and fecundity. These authors therefore questioned the generality of the causal link between rainfall, food availability, and fecundity of lizards. Although we lack data on food abundance and consumption rates, the absence of a response of reproductive intensity to yearly differences in rainfall and temperature complements this conclusion.

Acknowledgements We thank Paco Borreguero for assistance with the fieldwork. The manuscript benefited from the helpful comments of Martin Gil and Raoul Van Damme. Preparation of the manuscript was aided by a postdoctoral grant of the Consejo Superior de Investigaciones Cientificas (C.S.1.C .) (A.M.C.), by DGICYT project No. PB88-0009 (A.M.C. and D.B.), and by the logistic support of Iberia, the national Spanish airline. Abts, M. L. 1988. Reproduction in the saxicolous desert lizard, Sauromalus obesus : the female reproductive cycle. Copeia, 1988: 382-393. Arnold, E. N. 1989. Towards a phylogeny and biogeography of the Lacertidae: relationships within an Old-World family of lizards derived from morphology. Bull. Br. Mus. (Nat. Hist.) Zool. 55: 209 -257. Avery , R. A. 1975. Clutch size and reproductive effort in the lizard Lacerta vivipara. Oecologia (Berl.), 19: 165 - 170. Avery, R. A. 1976. Thermoregulation, metabolism and social behaviour in Lacertidae. In Morphology and biology of reptiles. Edited by A. d'A Bellairs and C. B. Cox. Linn. Soc. Symp. Ser. No. 3. pp. 245-259. Ballinger, R. E. 1977. Reproductive strategies: food availability as a source of proximal variation in a lizard. Ecology, 58: 628 -635. Ballinger, R. E. 1983. Life-history variations. In Lizard ecology. Studies on a model organism. Edited by R. B. Huey, E. R. Pianka, and T. W. Schoener. Harvard University Press, Cambridge. pp. 241-260. Barbadillo, L. J . 1987. La guia de Incafo de 10s anfibios y reptiles de la Peninsula IbCrica, Islas Baleares y Canarias. Incafo, Madrid. Barbault, R., and Mou, Y. P. 1988. Population dynamics of the common wall lizard, Podarcis muralis, in southwestern France. Herpetologica, 44: 38 -47. Bauwens, D., and Verheyen, R. F. 1985. The timing of reproduction in the lizard Lucerta vivipara: differences between individual females. J. Herpetol. 19: 353-364. Bauwens, D., and Verheyen, R. F. 1987. Variation of reproductive traits in a population of the lizard Lctcerta vivipara. Holarct. Ecol. 10: 120-127. Bons, N. 1972. Variations histophysiologiques du tractus genital femelle du lezard Acanthodactylus erythrurus lineomaculatus Dum. et Bibr. au cours de cycle annuel. Bull. Soc. Sci. Nat. Phys. Maroc, 52: 59- 120. Bons, J., and Saint Girons, H. 1982. Le cycle sexuel des reptiles males au Maroc et ses rapports avec la rkpartition geographique et le climat. Bull. Soc. Zool. Fr. 107: 71 -86.


CASTILLA ET AL.

Braiia, F. 1983. La reproduccion de 10s saurios de Asturias (Reptilia, Squamata): ciclos gonadales, fecundidad y modalidades reproductoras. Rev. Biol. Univ. Oviedo, 1: 29-50. Brafia, F., Bea, A., and Arrayago, M. J. 1991. Egg retention in lacertid lizards: relationships with reproductive ecology and the evolution of viviparity. Herpetologica, 47: 2 18 -226. Brockelman, W. Y. 1975. Competition, the fitness of offspring, and optimal clutch size. Am. Nat. 109: 677-699. Carpenter, C. C., and Ferguson, G. W. 1977. Stereotyped behavior in reptiles. In Biology of the Reptilia. Vol. 7. Edited by C. Gans and D. W. Tinkle. Academic Press, London. pp. 335-554. Castilla, A. M., and Bauwens, D. 1989. Reproductive characteristics of the lacertid lizard Lacerta lepida. Amphib.-Reptilia, 10: 445 -452. Castilla, A. M., and Bauwens, D. 1990. Reproductive and fat body cycles in the lizard, Lacerta lepida, in central Spain. J. Herpetol. 24: 261 -266. Congdon, J. D., and Gibbons, J. W. 1987. Morphological constraint on egg size: a challenge to optimal egg size theory? Proc. Natl. Acad. Sci. U.S.A. 84: 4145-4147. Cuellar, H. S., Roth, J. J., Fawecett, J. D., and Jones, R. E. 1972. Evidence for sperm sustenance by secretions of the renal sexual segment of male lizard Anolis carolinensis. Herpetologica, 28: 53-57. DeMarco, V. G. 1989. Annual variation in the seasonal shift in egg size and clutch size in Sceloporus woodi. Oecologia (Berl.), 80: 525 - 532. Derickson, W. K. 1976. Ecological and physiological aspects of reproductive strategies in two lizards. Ecology, 57: 445 -458. Dunham, A. E. 1978. Food availability as a proximate factor influencing individual growth rates in the iguanid lizard Sceloporus merriami. Ecology, 59: 770 - 778. Dunham, A. E. 1981. Populations in a fluctuating environment: the comparative population ecology of the iguanid lizards Sceloporus merriami and Urosaurus ornatus. Misc. Publ. Mus. Zool. Univ. Mich. No. 158. pp. 1-62. Dunham, A. E. 1982. Demographic and life-history variation among populations of the iguanid lizard Urosaurus ornatus: implications for the study of life-history phenomena in lizards. Herpetologica, 38: 208-221. Dunham, A. E., and Miles, D. B. 1985. Patterns of covariation in life history traits of squamate reptiles: the effects of size and phylogeny reconsidered. Am. Nat. 126: 23 1-257. Dunham, A. E., Miles, D. B., and Reznick, D. N. 1988. Life history patterns in squamate reptiles. In Biology of the Reptilia. Vol. 15. Edited by C. Gans and R. B. Huey. John Wiley & Sons, Inc., New York. pp. 443-51 1. Duvall, D., Guillette, L. J., Jr., and Jones, R. E. 1982. Environmental control of reptilian reproductive cycles. In Biology of the Reptilia. Vol. 3. Edited by C. Gans and F. H. Pough. Academic Press, London. pp. 20 1 -23 1. Ferguson, G. W., and Fox, S. F. 1984. Annual variation of survival advantage of large juvenile side-blotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution (Lawrence, Kans. ), 38: 342 - 349. Ferguson, G. W., Bohlen, C. H., and Woolley, H. P. 1980. Sceloporus undulatus: comparative life history and regulation of a Kansas population. Ecology, 61: 3 13 - 322. Ferguson, G. W., Brown, K. L., and DeMarco, V. G. 1982. Selective basis for the evolution of variable egg and hatchling size in some iguanid lizards. Herpetologica, 38: 178 - 188. Ferguson, G. W., Snell, H. L., and Landwer, A. J. 1990. Proximate control of variation in clutch, egg, and body size in a west-Texas population of Uta stansburiana stejnegeri (Sauria: Iguanidae). Herpetologica, 46: 227 -238. Fitch, H. S. 1970. Reproductive cycles in lizards and snakes. Univ. Kans. Mus. Nat. Hist. Misc. Publ. No. 52. pp. 1-247. Ford, N. B., and Siegel, R. A. 1989. Relationships among body size, clutch size, and egg size in three species of oviparous snakes. Herpetologica, 45: 75 - 83.

40 1

Fox, H. 1977. The urogenital system of reptiles. In Biology of the Reptilia. Vol. 6. Edited by C. Gans, and T. S. Parson. Academic Press, London. pp. 1 - 157. Fox, S. F. 1978. Natural selection on behavioral phenotypes of the lizard Uta stansburiana. Ecology, 59: 834 - 847. Guillette, L. J., Jr., and Sullivan, W. P. 1985. The reproductive and fat body cycles of the lizard, Sceloporus jormosus. J. Herpetol. 19: 474 -480. Hahn, W. E., and Tinkle, D. W. 1965. Fat body cycling and experimental evidence for its adaptive significance to ovarian follicle development in the lizard Uta stansburiana. J. Exp. Zool. 158: 79 - 86. Henle, K. 1988. Dynamics and ecology of three Yugoslavian populations of the Italian wall lizard (Podarcis sicula campestris De Betta) (Reptilia: Lacertidae). Zool. Anz. 220: 33 -48. House, S. M., Taylor, P. J., and Spellerberg, I. F. 1980. Patterns of daily behaviour in two lizard species Lacerta agilis L. and Lacerta vivipara Jacquin. Oecologia (Berl.), 44: 396 -402. Hroaui-Blocquet, S. 1987. Le cycle sexuel des femelles chez Lacerta laevis Gray 1838 dans la montagne du Liban. Amphib.-Reptilia, 8: 143- 152. Jones, S. M., Ballinger, R. E., and Porter, W. P. 1987. Physiological and environmental sources of variation in reproduction: prairie lizards in a food rich environment. Oikos, 48: 325 -335. Loumbourdis, N. S., and Kattoulas, M. E. 1985. Seasonal changes in liver and fat body masses in the lizard Agama stellio stellio (Sauria, Agamidae). Amphib.-Reptilia, 6: 155 - 162. MCndez de la Cruz, F. R., Guillette, L. J., Jr., Villagran Santa Cruz, M., and Casas-Andreu, G. 1988. Reproductive and fat body cycles of the viviparous lizard, Sceloporus mucronatus (Sauria: Iguanidae). J. Herpetol. 22: 1 - 12. Misra, U. K., Sanyal, M. K., and Prasad, M. R. 1965. Phospholipids of the sexual segment of the kidney of the Indian house lizard, Hemidactylus flaviviridis Ruppel. Life Sci. 4: 159 - 166. Ortega, A. 1986. Fat body cycles in a montane population of Sceloporus grammicus. J. Herpetol. 20: 104 - 108. Ortega, A., and Barbault, R. 1986. Reproduction in the high elevation Mexican lizard Sceloporus scalaris. J. Herpetol. 20: 1 1 1 - 114. Pascual, J. A., and PCrez-Mellado, V. 1989. Datos sobre la reproduccion y el crecimiento de Psammodromus hispanicus Fitzinger, 1826 en un medio adehesado de la Espaiia Central. Dofiana Acta Vertebr. 16: 45 -55. PCrez-Mellado, V. 1982. Algunos datos sobre la reproduccion de dos especies de Lacertidae (Sauria, Reptilia) en el Sistema Central. Bol. R. Soc. Esp. Hist. Nat. Biol. 80: 165- 173. PCrez-Mellado, V. 1992. Ecology of lacertid lizards in a desert area of eastern Morocco. J. Zool. (Lond.). In press. Pilorge, T. 1987. Density, size structure, and reproductive characteristics of three populations of Lacerta vivipara (Sauria : Lacertidae). Herpetologica, 43: 345 -356. Pilorge, T., Xavier, F., and Barbault, R. 1983. Variations in litter size and reproductive effort within and between some populations of Lacerta vivipara. Holarct. Ecol. 6: 38 1- 386. Pollo, C. J., and PCrez-Mellado, V. 1988. Trophic ecology of a taxocenosis of mediterranean Lacertidae. Ecol. Mediterr. 14: 13 1 - 147. Pollo, C. J., and PCrez-Mellado, V. 1990. Biologia reproductora de tres especies mediterraneas de Lacertidae. Mediterranea Ser. Biol. 12: 149- 160. Saint Girons, H. 1982. Reproductive cycles of male snakes and their relationships with climate and female reproductive cycles. Herpetologica, 38: 5 - 16. Seva, E. 1982. Taxocenosis de Lacertidos en un arena1 costero alicantino. Publicaciones de la Universidad de Alicante, Alicante. Sinervo, B. 1990. The evolution of maternal investment in lizards: an experimental and comparative analysis of egg size and its effects on offspring performance. Evolution (Lawrence, Kans.), 44: 279 - 294. Sinervo, B., and Adolph, S. C. 1989. Thermal sensitivity of growth


402

CAN. J. ZOOL. VOL. 70, 1992

rate in hatchling Sceloporus lizards: environmental, behavioral and genetic aspects. Oecologia (Berl.), 78: 4 11-4 19. Sinervo, B., and Huey, R. B. 1990. Allometric engineering: an experimental test of the causes of interpopulational differences in performance. Science (Washington, D.C.), 248: 1106- 1109. Smith, C. C., and Fretwell, S. D. 1974. The optimal balance between size and number of offspring. Am. Nat. 108: 499-506. Stewart, J. R. 1979. The balance between number and size of young in the live bearing lizard Gerrhonotus coeruleus. Herpetologica, 35: 342-350. Tinkle, D. W. 1969. The concept of reproductive effort and its relation to the evolution of life histories of lizards. Am. Nat. 103: 501 -516. Tinkle, D. W., and Ballinger, R. E. 1972. Sceloporus undulatus: a study of the intraspecific comparative demography of a lizard. Ecology, 53: 570 - 584. Tinkle, D. W., and Dunham, A. E. 1983. Demography of the tree lizard, Urosaurus ornatus, in central Arizona. Copeia, 1983: 585-598. Tinkle, D. W., Wilbur, H. M., and Tilley, S. G. 1970. Evolutionary strategies in lizard reproduction. Evolution, 24: 55-74. Van Damme, R., Bauwens, D., and Verheyen, R. F. 1987. Thermoregulatory responses to environmental seasonality by the lizard Lucerta vivipara. Herpetologica, 43 : 405 -4 15. Van Damme, R., Bauwens, D., Brafia, F., and Verheyen, R. F. 1992. Incubation temperature differentially affects hatching time,

egg survival and hatchling performance in the lizard Podarcis muralis. Herpetologica, 48. In press. Van Loben Sels, R. C., and Vitt, L. J. 1984. Desert lizard reproduction: seasonal and annual variation in Urosaurus ornatus (Iguanidae). Can. J. Zool. 62: 1779- 1787. Vitt, L. J. 1981. Lizard reproduction: habitat specificity and constraints on relative clutch mass. Am. Nat. 117: 506-514. Vitt, L. J., and Congdon, J. D. 1978. Body shape, reproductive effort, and relative clutch mass in lizards: resolution of a paradox. Am. Nat. 112: 595-608. Vitt, L. J., and Price, H. J. 1982. Ecological and evolutionary determinants of relative clutch mass in lizards. Herpetologica, 38: 237 - 255. Vitt, L. J., Van Loben Sels, R. C., and Ohmart, R. D. 1978. Lizard reproduction: annual variation and environmental correlates in the iguanid lizard Urosaurus graciosus. Herpetologica, 34: 24 1-253. Volsoe, H. 1944. Structure and seasonal variation of the male reproductive organs of Vipera berus (L.). Spolia Zool. Mus. Haun. 5: 7- 157. Worthington, R. D. 1982. Dry and wet year comparisons of clutch and adult body sizes of Uta stansburiana stejnegeri. J. Herpetol. 16: 332-334. Xavier, F. 1982. Progesterone in the viviparous lizard Lucerta vivipara: ovarian biosynthesis, plasma levels, and binding to transcortin-type protein during the sexual cycle. Herpetologica, 38: 62-70.