Parturition and clutch characteristics of short-horned lizards (Phrynosoma douglassii brevirostre) from Alberta

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1 Parturition and clutch characteristics of short-horned lizards (Phrynosoma douglassii brevirostre) from Alberta G. LAWRENCE POWELL AND ANTHONY P. RUSSELL' Comparative Vertebrate Morphology Research Group, Department of Biological Sciences, The University of Calgary, 2500 University Drive NW, Calgary, Alta., Canada T2N IN4 Received January 29, POWELL, G. L., and RUSSELL, A. P Parturition and clutch characteristics of short-horned lizards (Phrynosoma douglassii brevirostre) from Alberta. Can. J. Zool. 69: Field capture records and observation of wild-caught females indicate that parturition in Alberta populations of Phrynosoma douglassii brevirostre, a viviparous lizard, is synchronized among females, taking place during a short period around the end of July, and generally around noon. Relative clutch mass appears to decrease with female age, and clutch size varies between 6 and 11 neonates, with an overall sex ratio of 1.O. Female behaviour during parturition consists of four distinct phases, involving straddling of the hind legs, abdominal contractions, and pelvic movements. After parturition, the female moves away from the neonate. Neonate behaviour is associated chiefly with escaping from the extraembryonic membranes. Male neonates have a greater snout-vent length than females, but neonate mass is similar. Gravidity appears to impose a great physiological cost upon reproducing females. POWELL, G. L., et RUSSELL, A. P Parturition and clutch characteristics of short-horned lizards (Phrynosoma douglassii brevirostre) from Alberta. Can. J. Zool. 69 : Des donnce relikes a la capture et l'observation de femelles capturces en nature indiquent que la parturition est synchronisce chez les femelles des populations albertaines de Phrynosoma douglassii brevirostre, un lczard vivipare, et qu'elle se produit au cours d'une courte pcriode, vers la fin de juillet, gcncralement vers midi. La masse relative des portces semble diminuer en fonction de l'ige des femelles; le nombre de nconates varie entre six et onze et le rapport miles:femelles global est Cgal 1,O. Le comportement de la femells durant la parturition se divise en quatre phases distinctes au cours desquelles on observe des Ccartements des pattes, des contractions abdominales et des mouvements pelviens. Aprks la parturition, la femelle s'cloigne du nouveau-nc. Aprks sa naissance, le nouveau-nc cherche surtout a se dcbarrasser des membranes extraembryonnaires. La longueur museau-cloaque est plus courte chez les miles que chez les femelles nconates, mais la masse est la meme chez les deux sexes. La reproduction semble comporter des coqts physiologiques trks ClevCs chez les femelles. [Traduit par la rcdaction] Introduction The distribution and ecology of the eastern short-homed lizard, Phrynosoma douglassii brevirostre, in Alberta have been studied by Powell and Russell (1984, 1985a, 1985b, 1991). The present contribution describes parturition and clutch characteristics of a small sample of eastern short-homed lizards from populations in southeastern Alberta and includes some observations of neonate behaviour and changes in female condition before and after parturition. Immediately postpartum neonate behaviour is not well known in lizards (Greenberg and Hake 1990), and this is especially true of viviparous species. Observing birth in viviparous lizards in the field is a rare event, and maintenance of gravid females in the laboratory to observe parturition has not often been attempted. In the course of field studies on species that have low population densities this becomes even more difficult. Members of the genus Phrynosoma are unusual among lizards in their reproductive characteristics. They produce large clutches of small offspring with low survivorship, but are relatively large and long-lived as adults (Pianka and Parker 1975). This can be explained as a consequence of their myrmecophagous (anteating) habits, part of a suite of features peculiar to the genus (Pianka and Parker 1975). Although most species of the genus Phrynosoma are oviparous, P. douglassii, P. orbiculare, P. braconnieri, and P. ditmarsi are viviparous (Blackburn 1982). Anecdotal accounts of reproduction in P. douglassii were reviewed by Milne and Milne (1950) and Pianka and Parker (1973, and the reproductive 'Author to whom all correspondence should be addressed. cycle was examined by Goldberg (197 1). Montanucci and Baur (1982) gave an account of mating behaviour in this species. The eastern short-homed lizard is currently listed as ' 'threatened" in Alberta (Alberta Energy and Natural Resources 1984), and its habitat is under continuous threat from commercial development and exploration. Population sizes of this species in Alberta appear to be low (a mean of 138 lizards per site were captured at three study sites in 1979 and 1980) and they are vulnerable to the removal of mature females. The procedures followed herein are not fatal to the animals involved, and represent a feasible means of garnering data on reproductive characteristics of these populations. Methods The lizards observed in this study were collected during a mark-recapture investigation of Phrynosoma douglassii brevirostre carried out in southeastern Alberta during the summers of 1979 and 1980 ( Powell and Russell 1985~). No data on parturition were collected in 1979; a sudden appearance of neonates and marked decrease in adult female mass between the last week of July and the resumption of fieldwork on August 9, 1979, indicated that the period of parturition in these populations is brief. In 1980 an effort was made to collect gravid females in the last week of July to obtain data on clutch size and parturition. The onset of warm weather and subsequent lizard emergence came early in 1980 (Laird and Leech 1980); this evidently advanced the start of gestation and, consequently, the date of parturition. Most females in this area had given birth before fieldwork resumed at the end of July. One female captured on July 16, 1980, at Bow Island (111 30'W, 49'55'N) gave birth in the laboratory on July 23,1980. This probably corresponded to the period during which most births were taking place in the field, since subsequent fieldwork yielded only one

2 2760 CAN. J. ZOOL. VOL gravid female at Bow Island and four at Comrey (1 10'4 1 'W, 49'05'N). Most sexually mature females encountered at these two sites over this period (July 25-27, 1980) displayed the marked loss of bulk typical of immediately postpartum female phrynosomes, and neonates were abundant at both sites (Powell and Russell 1985a, Figs. 2 and 5). The gravid females were transported to field quarters and maintained indoors in plastic rodent cages. Temperature was allowed to fluctuate according to daily insolation of the building, and the cages were illuminated by indirect sunlight. Water was available ad libitum, and food (locally collected insects) was offered daily. Neonates whose birth took place unobserved were measured, marked (Powell and Russell 1985a), and released with their mother at her point of capture. Maternal mass was taken at capture, and again as soon as possible after parturition. Three females were observed in the act of parturition on July 3 1,1980. The neonates produced in these bouts were otherwise treated like those whose births were not observed. Results Females and their clutches A total of 51 neonates in six clutches was produced by the females sequestered in this study. Not all the neonates within our sample were observed during parturition, and thus not all of the neonates yielded data to the same degree. Sophisticated statistical analyses of the relationship between female and clutch are precluded by the small number of females (six) for which data on parturition are available. These females ranged from 64 to 76 min (Fig. 1) in snout-vent length (SVL). The minimum SVL for a gravid female P. d. hernandesi in Arizona was found to be 65 mm (Goldberg 1971); this is comparable to the lower end of the range presented here. Previous recapture data and estimation of age from growth models (Powell and Russell 1985a) permitted division of our sample of females into two age-classes (second year, and third year and older). The second year females differed in the size of offspring produced; one (No. 077) produced a small number of very large neonates, whereas the other (No. 042) produced a larger number of smaller neonates, as did the third year and older females (Fig. 1, Table 1). However, the relative clutch mass (calculated as the total mass of neonates in clutchlmother's postparturition mass; Shine 1980) differs between the two ageclasses (Fig. 2). The two second-year females produced a much higher relative clutch mass ( ) than did the three thirdyear and older females ( ) for which this could be calculated. The sex ratio and number of neonates varied strongly among clutches (Table 1). Clutch size (live neonates) ranged from 6 to 11 (mean + 2 sd = ). Sex ratios (number of males1 number of females) ranged between 0.2: 1 and 2.5: 1. The overall sex ratio for all clutches, however, was not significantly different from 1.0. Three neonates in two clutches were stillborn. The mother of two of these (No. 006) died before completing parturition, and an additional clutch contained two undeveloped eggs. Parturition The summary of a typical parturition bout (Fig. 3) lists the common repeated features from observations of 10 parturitions of two females. A third female (No. 006) was observed during parturition but was not included in this representation, since her behaviours appeared atypical. It had been noted from previous longitudinal data that she was losing weight, and she died during parturition with one offspring still in her oviduct. A typical parturition event is shown in Fig. 3. There was no obvious difference in procedure between the first birth and the MATERNAL SVL (mm) FIG. 1. (A) Female Phrynosoma douglassii brevirostre (No. 193) and clutch. The female was captured at the Bow Island site. (B) Distribution of neonate masses within clutches over the snout-vent length range of six Alberta P. d. brevirostre females. Numbers are individual file numbers; No. 006 died during parturition (see text). births varied (Fig. 4), but was generally rather long (mean + 2 sd = min). After the clutch was complete, one female was observed to express some fluid from the everted cloaca. She then rubbed her cloaca against the substrate as she moved forward. In all cases where it was noted (four), the neonate emerged tail-first. No female exhibited any noticeable behaviour with regard to her offspring after parturition. Laird and Leech (1980) described both tail- and head-first births in the same clutch in a female from a South Saskatchewan River population. In this case the first four neonates were born at approximately 5-min intervals; the subsequent three were born over a 42-min period, at 12- to 15-min intervals (Laird and Leech 1980). Seasonal timing of parturition The strong seasonal synchronization of parturition in these populations has already been noted. The only other recorded last for a particular female. Time elapsed between individual parturition of a P. d. brevirostre in Alberta took place on July 27

3 POWELL AND RUSSELL TABLE 1. Clutch sex ratios and total clutch sizes of six Phrynosoma douglassii brevirostre females from two populations in southeastern Alberta No. 193 No. 077 No. 018 No. 005 No. 006 No. 042 Mother's postpartum mass (g) Offspring Male Female Sex ratio (malelfemale) 1.O Total clutch size NOTE: X2 statistic refers to the overall sex distribution of the 006, 018, and 193 are third-year and older females. MATERNAL SVL(mm1 FIG. 2. Relative clutch mass (RCM) plotted against snout-vent length for five Alberta Phrynosoma douglassii brevirostre. Numbers denote individual file numbers: 077 and 042 are second-year females; 0 18,005, and 193 are third-year and older females. RCM is calculated as the summed mass of all neonates / mother's postpartum mass. (Laird and Leech 1980). No data are available on gonadal cycles in P. d. brevirostre in Alberta. There is evidence to suggest that die1 synchronization of parturition exists in the Alberta populations. All the parturition series that were observed or could be placed closely in time (four in all) began shortly before or at noon and continued, for the most part, into early afternoon. Neonates and parturition During parturition the neonate directly involved is generally motionless; one was observed to move slightly while its head was still within its mother's cloaca. Once free of the cloaca, the neonate lies still within its extraembryonic membranes for a period ranging from 10 s to 9 min (mean 2.18 min, Fig. 5). Movement, once initiated, is generally violent; writhing with the forelimbs pinned to the sides may be accompanied by tongue movements, gulping, and head movements. The extraembryonic membranes are quickly tom by this activity, and breathing commences. Once the membranes are tom and the forelimbs are free, the neonate rapidly sheds the chorioallantois and begins X2 = 4.493, 5 df, p = offspring; Nos. 042 and 077 are second-year females; Nos. 005, running about with the yolk sac attached at the umbilicus. An effort to shed the yolk sac and any remaining parts of the chorioallantoic membrane is made through swimming movements, with the belly adpressed to the substrate. Head bobbing was noted within 1 h and feeding attempts within 2 h of parturition. Neonate morphology Differences in mass among neonates of different clutches are shown in Fig. 1B. The clutch with the lightest neonates was borne by the female that died during parturition, and this low mass can perhaps be attributed to her previous poor condition. The clutch with the heaviest neonates was borne by a primiparous female (see Fig. 1B). Phrynosoma douglassii brevirostre in Alberta displays pronounced sexual dimorphism. Females outweigh and attain a greater SVL than males (Powell and Russell 1985~). Differences in mensural characters are evident, even in most subadults (Powell and Russell 1985~). If the neonates obtained in this study are grouped by sex, there is no significant difference in mass (t = , 41.8 df, p = 0.624), whereas a highly significant difference in SVL (t = 3.335,48 df, p = ) was found. Male neonates (mean SVL mm) are slightly shorter than females (mean SVL mm). Costs of reproduction Longitudinal records of mass in females of the Alberta P. d. brevirostre populations (Fig. 6) show that females that can be assumed to have produced a clutch in any given reproductive season experience a loss of body mass, which is slowly regained before the onset of hibernation in the fall. Postpartum females in these populations are noticeably poor in condition, and the general gain in weight evident in these females (Fig. 6) probably represents recovery from the stress of gravidity as well as preparation for the onset of hibernation. Of the 10 females captured within a month of the start of hibernation and recaptured within a month of emergence, only 2 displayed minor decreases in mass. The other eight showed either no change or an increase in mass. Few of these females were recaptured near the putative date of emergence; nonetheless, adult females caught early in the active season did not display the poorness of condition typifying those captured shortly after parturition. Additional evidence for the physiological nature of the cost of reproduction in these populations is the death of one gravid female of the six examined here; as stated before, longitudinal data indicated a worsening of condition during the month preceding parturition and death. Although the proximate cause

4 2762 CAN. J. ZOOL. VOL. 69, PRELIMINARY PHASE Tail raised straight up.sometimes lashed; head may be raised; pelvis raised, may be lowered or waggled; hind legs straddled.may be raised;, cloaca may be everted. 2. CONTRACTION PHASE Tail raised straight up.may be lashed; hind legs straddled, may be alternately kicked; intermittent contract ions of the lower abdomen; pelvis raised and I lowered, may be waggled. I v 3. PARTURITION PHASE Tail raised straight up(l1,may be lashed (2); hind legs straddled(31, may be raised; head may be raised; pelvis ra ised(41, may be lowered (5) or waggled; lower abdominal contract ions strong and close together(61; cloaca everted(7); neonate appears at the cloaca(8) and is ejected. v I 4. POSTPARTUM PHASE Tail raised straight up; hind legs straddled, may be alternately kicked: moves forward one-half to one body I FIG. 3. (A) Summary of the behaviour of a female Phrynosoma douglassii brevirostre during an individual parturition bout. (B) Photographs illustrating features of the parturition phase (step 3 in A; the numbers correspond to those in the box). of death may have been unrelated to gravidity, the timing of death suggests that gravidity and (or) parturition were instrumental in this mortality. Discussion Recorded clutch sizes for Phrynosoma douglassii vary greatly over its geographic range (Smith 1947; Milne and Milne 1950; Goldberg 1971; Pianka and Parker 1975). There was a strong positive correlation between female SVL and the number of young in a clutch in an Arizona population (Goldberg 197 1). The clutch sizes recorded here are at the lower end of the recorded range. Phrynosoma douglassi brevirostre attains a relatively small adult SVL in this part of its range (A. P. Russell and G. L. Powell, unpublished data), and the small clutch sizes could be a function of the correlation between female SVL and clutch size observed by Goldberg (1971). The only other recorded clutch size for an Alberta P. d. brevirostre (of unstated size) is seven (Laird and Leech 1980), which is within the range recorded here. A female P. d. hernandesi, after giving birth to five neonates unobserved, bore eight more subsequently with a mean interval of 11.5 min between births (Milne and Milne 1950). The behaviour of this female differed in some regards from that reported here, but the differences were in timing and sequence of the actions performed. In this case, half of the neonates were deposited tail-first (Milne and Milne 1950). Smith (1941) reported that during parturition, a female raised her body, deposited the neonate, and moved on. We have no direct data on the gonadal cycles of P. douglassii of either sex in Alberta. Goldberg (197 1) noted testicular hypertrophy in male P. douglassii in Arizona on emergence from hibernation in March, with regression beginning in April and being completed by the end of that month. Mating takes place in late March to early April in these populations, and ovulation occurs in May (Goldberg 1971). Parturition is in August in Arizona; gestation takes approximately 3 months (Goldberg 197 1). Captive females rapidly (4-1 1 days) became unreceptive

5 POWELL AND RUSSELL INTERVAL BETWEEN BIRTHS (mid FIG. 4. Distribution of intervals between parturition events for three Alberta Phrynosoma douglassii brevirostre females TIME MOTIONLESS AFTER BIRTH (mid FIG. 5. Distribution of the interval between parturition and the first movement by neonates in three clutches of Alberta Phrynosoma douglassii brevirostre. to courtship overtures by males (Montanucci and Baur 1982). Sources reviewed by Milne and Milne (1950) gave dates of parturition ranging from early July to late August from a variety of locations over the geographic range of P. douglassii, but the evidence of Goldberg (1971) and Montanucci and Baur (1982) suggests that local dates of mating will vary with the local time of emergence from hibernation, and thus will depend upon local climate. Since the Alberta populations of P. d. brevirostre are strongly constrained in their annual activity by the brevity of the Alberta summer (Powell and Russell 1991), it is likely that mating takes place during a very short period following spring emergence in these populations, and thus parturition events are closely contemporaneous. TIME (DAYS SINCE JANUARY I) FIG. 6. Change in mass of sexually mature female Phrynosoma douglassii brevirostre over the period of late gravidity, parturition, and postparturition recovery. Females from Convey, Nerniskam Community Pastures, and Bow Island, Alberta; data pooled from 1979 and Each line represents longitudinal data for one female. Literature reports of daily timing of parturition vary: Milne and Milne (1950) recorded it as taking place in midmorning and at night, Smith (1941) recorded it in midmorning, and Pack (1918) recorded it as taking place at night. The synchrony of parturition among clutches recorded here for P. d. brevirostre from Alberta has not been reported for conspecifics originating from more southerly populations. Milne and Milne (1 950) and Smith (1 94 1) give accounts of neonate postparturition behaviour similar to that given here. Smith's (194 1) neonates remained motionless after parturition for between 5 and 55 min. As in our study, Laird and Leech (1980) noted feeding attempts by neonates an hour after birth. No other observers have reported an apparent difference in relative clutch mass between female P. douglassii of different ages, although Goldberg (1971) reported a strong positive correlation between number of young and female size. A female with a postpartum mass of 18.5 g gave birth to clutch of 15, ranging in mass from 0.8 to 1.1 g (Milne and Milne 1950), but her age cannot be assessed. As noted, lizards of the genus Phrynosoma produce a large number of small offspring, yet have high adult survivorship. This is an expression of the evident side effects of a large body cavity developed in response to a myrmecophagous diet (Pianka and Parker 1975). The costs of gravidity to a female lizard can be broadly divided into a loss of speed and agility, with concomitant greater vulnerability to predation, and a loss of energy available to invest in future clutches because of present investment. The first is generally the more important cost, since lizards of most species are too short-lived for a reduction in future potential investment to be very plausible as a strong selective force (Shine 1980). Although the size of the data set precludes any more definitive statements, there is evidence that for P. d. brevirostre the main yearly cost of reproduction is the excessive physiological cost of gravidity each time, which affects the possibility of survival to invest in another clutch in the next year. Speed and agility are of little importance to phrynosomes in predator avoidance (Pianka and Parker 1975). A similar depleted state, with subsequent increase in mass toward the onset of hibernation, was noted in postpartum female phrynosomes in Arizona by Goldberg (1971). A sit-and-wait predator with the sedentary strategy of P. d. brevirostre is unlikely to be greatly discommoded in its efforts to catch prey by the increased bulk caused by gravidity, so the overall loss of body mass may be due to the physiological effects of viviparity. The lack of change in condition over hibernation, another period of physiological stress, can be adduced as additional evidence for this hypothesis. We could obtain no data on fat body cycles in these lizards, but the pattern of whole-body mass change seen

6 2764 CAN. J. ZOOL. VOL. 69, 1991 here (Fig. 6) parallels that in fat body size in lizards inhabiting seasonally changing environments (reviewed in Derickson 1976). The seasonal synchrony of parturition documented here suggests that recruitment in the Alberta populations of P. d. brevirostre will be strongly affected by annual fluctuations in weather, particularly early in the active season, when mating appears to take place. Gravid females will also potentially be stressed by inclement weather, and both reproducing females and neonates must have a sufficient amount of time after parturition to gain mass in preparation for winter torpor. We have suggested elsewhere (Powell and Russell 1991) that the climate of Alberta is the major range-limiting factor affecting this species at the northern edge of its distribution. Phrynosoma douglassii brevirostre performs quite well as a thermoregulator within the thermally favourable active season (Powell and Russell 19856) and eschews by hibernation the colder portions of the year. The effects of climatic variation upon the tight reproductive schedule already imposed by climate upon females may be an important mode by which it acts as a range-limiting factor. Clutch sizes in the Alberta populations of P. d. brevirostre appear to be small in comparison with those reported for populations farther south in the range (Goldberg 1971 ; Milne and Milne 1950; Pianka and Parker 1975). Data on survivorship of neonates in the Alberta populations are scanty, and the demography of these populationg is poorly understood. In the course of a mark-recapture study (Powell and Russell 1985~1, the 1980 recapture rate after winter was 6.67% for neonates (n = 30) captured in the preceding summer (1979), comparable to the 9.09% recapture rate of individuals aged 1+ years (n = 99) marked in the summer of 1979 and recaptured in However, recaptures of individuals aged 1 + years are frequently serial; few individuals marked as neonates were recaptured more than once. This suggests that mortality is high for neonates in the Alberta populations. These populations are probably extremely sensitive to anthropic stresses, such as would accompany commercial exploration and development, upon their habitat. Any management plans must accommodate the requirements of populations whose recruitment is already strongly constrained by the climate. Acknowledgements We thank Leonard and Mary Jane Piotrowski and Lome and Joan Laidlaw for permission to work on their land, and Dr. E. Swierstra of the Dominion Agricultural Research Station in Lethbridge for the use of the Onefour schoolhouse as field headquarters. Bret Bennington kindly loaned us some computer time. Also, G.L.P. is deeply indebted to Ann and Larry Linton for the accommodations and the use of the computer while this paper was being written. Criticism of earlier drafts of the manuscript by three anonymous reviewers resulted in a greatly improved final product. Financial support for this project was provided partially by the Department of Biological Sciences, The University of Calgary, and partially by a Natural Sciences and Engineering Research Council of Canada grant (A-9745) to A. P. Russell. ALBERTA ENERGY AND NATURAL RESOURCES Status of the fish and wildlife resource in Alberta. Alberta Energy and Natural Resources, Fish and Wildlife Division, Edmonton, Alta. BLACKBURN, D. G Evolutionary origins of viviparity in the Reptilia. I. Sauna. Amphib. Reptilia, DERICKSON, W. K Lipid storage and utilization in reptiles. Am. ZOO^. 16: GOLDBERG, S. R Reproduction in the short-horned lizard Phrynosoma douglassi In Arizona. Herpetologica, 27: GREENBERG, N., and HAKE, L Hatching and neonatal behaviour of the lizard, Anolis carolinensis. J. Herpetol. 24: LAIRD, M., and LEECH, R Observations of the short-horned lizard in southeastern Alberta. Blue Jay, 38: MILNE, L. J., and MILNE, M. J Notes on the behavior of horned toads. Am. Midl. Nat. 44: MONTANUCCI, R. R., and BAUR, B. E Mating and courtshiprelated behaviors of the short-horned lizard, Phrynosoma douglassi. Copeia, 1982: PACK, H. J Some habits of the pigmy horned lizard. Copeia, 63: PIANKA, E. R., and PARKER, W. S Ecology of horned lizards: a review with special reference to Phrynosoma platyrhinos. Copeia, POWELL, G. L., and RUSSELL, A. P The diet of the eastern shorthorned lizard (Phrynosoma douglassi brevirostre) in Alberta and its relationship to sexual size dimorphism. Can. J. Zool. 62: a Growth and sexual size dimorphism in Alberta populations of the eastern short-horned lizard, Phrynosomu douglassi brevirostre. Can. J. Zool. 63: b. Field thermal ecology of the eastern short-horned lizard (Phrynosomu douglassi brevirostre) in southern Alberta. Can. J. Zool. 63: The distribution of the eastern short-horned lizard (Phrynosomu douglassi brevirostre) in Alberta. Northwest Nat. 72: SHINE, R "Costs" of reproduction in reptiles. Oecologia, 46: SMITH, C. F Birth of horned toads. Copeia, 1941 : 114. SMITH, H. M Handbook of lizards. Lizards of the United States and Canada. Comstock Press, Ithaca, NY. pp. i-xxi, 557.