Spring emergence schedules and vernal behavior of Richardson's ground squirrels: why do males emerge from hibernation before females?

Transcription

1 Behav Ecol Sociobiol (1983) 14:29-38 Behavioral Ecology and Sociobiology 9 Springer-Verlag 1983 Spring emergence schedules and vernal behavior of Richardson's ground squirrels: why do males emerge from hibernation before females? Gail R. Michener Department of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, Canada T1K 3M4 Received March 8, 1983 / Accepted July 20, 1983 Summary. Schedules of emergence from hibernation were recorded for adult (> 1-year old) Richardson's ground squirrels each spring from 1979 to 1983 in southern Alberta, Canada. In all years and regardless of the calendar dates of emergence, males emerged from hibernation, on average, 8-16 days in advance of females. On the median date of emergence by males, % of females still remained in hibernation. On the day the last male appeared, the proportion of females still in hibernation ranged from 27% in 1979 to 89% in As females typically bred 1-4 days after resuming aboveground activity, late emerging males found that females that had been active several days had already been impregnated by earlier emerging males. Thus, late emergence by males resulted in reduced breeding opportunities. Male Richardson's ground squirrels differed from females in a constellation of behaviors related to male intrasexual competition for breeding opportunities. In the breeding season, males moved longer distances, occupied larger ranges, expended less time on burrow maintenance, engaged in more injury-producing fights, and lost more body weight than did females. Early emergence from hibernation by males relative to females is viewed as one of several behaviors exhibited by males to promote individual reproductive success by maximizing the number of potential mates available. The sex difference in time of vernal emergence by Richardson's ground squirrels is interpreted as an outcome ofintersexual selection and is an example of the phenological strategy of the mate-limited sex maximizing reproductive success by being on the breeding ground by the time the mate-limiting sex appears. Introduction Among those species of Marmotini (marmots, ground squirrels, prairie dogs) that are obligate hibernators, adult males typically resume aboveground activity prior to females (see Michener, in press a for review). Although this sex difference has long been recognized (Shaw 1925; Stockard 1929; Wade 1927), rarely has the difference been precisely quantified or its significance examined. The first male typically emerges before the first female, but the range of emergence dates within each sex usually results in overlapping schedules for the sexes (e.g., Beer 1962). Meaningful quantification of the sex difference in vernal emergence schedules requires measures such as mean and median emergence dates (Knopf and Balph 1977; Morton and Sherman 1978; Murie and Harris 1982) in addition to first emergence dates. Because age and climatic factors affect the time of emergence from hibernation (see Michener, in press a for review) assessment of the range and magnitude of sex differences in resumption of aboveground activity requires accurate data on emergence of known-aged individuals throughout the entire emergence period in '.several years. Currently the most complete information on emergence schedules is for Uinta, Belding's, and Columbian ground squirrels, all species in which yearling males typically are not sexually mature. On average, adult males (> 1-year old) preceded yearling and older females by about 5 days in Sperrnophilus armatus (Knopf and Balph 1977) and by about 10 days in S. beldingi (Morton and Sherman 1978). Among adult S. columbianus (> 1-year old for both sexes), males appeared 6 days (range 2-12 days over 6 years) before females (Murie and

2 30 Harris 1982). A difference of about 1-2 weeks in emergence schedules of males and females has been noted (though usually not accurately quantified) for S. franklinii (Iverson and Turner 1972), S. lateralis (Skryja and Clark 1970), S. parryii (McLean and Towns 1981), S. richardsonii (Dorrance 1974), S. tridecemlineatus (Clark 1971), and Cynomys leucurus (Stockard 1929). A somewhat greater sex difference of 3-4 weeks has been indicated for Marmota monax (Snyder et al. 1961) and S. tereticaudus (Dunford 1977). Females breed shortly after their emergence fi'om hibernation (Knopf and Balph 1977; McLean and Towns 1981; Michener 1980a; Morton and Sherman 1978; Murie and Harris 1982). Thus, to maximize his opportunities for successful insemination, a male should be active aboveground, reproductively competent, and in a location that assures access to estrous females by the time females emerge and are ready to mate. The purposes of this study were to document the vernal emergence schedule of Richardson's ground squirrels (Spermophilus richardsonii richardsonii) over a 5-year period and to monitor breeding condition, wound frequency, and behavior of males and females from emergence through the breeding season. Materials and methods The 5-year study, inclusive, was conducted 8 km E of Picture Butte, Alberta, Canada (49~ 112~ elev. 870 m) on untamed pasture stocked each spring with domestic cattle. The study area consisted of two adjoining pastures, an 11 ha East Pasture and a 7.5 ha West Pasture. Emergence of male Richardson's ground squirrels from hibernation was monitored on both pastures in all years. A complete record of emergence by females was obtained for only the East Pasture in 1979 and 1980, but for both pastures in The numbers of males emerging on the pastures were similar from 1979 to 1983 (22, 21, 21, 23 and 24 respectively). The numbers of females emerging on the East Pasture remained relatively constant from 1979 to 1981 (18, 23 and 23), but the population increased to 44 females in 1982 and 57 females in Similarly, the population of females on the West Pasture increased from 25 in 1981 to 53 and 52 in 1982 and 1983, respectively. Each year the area was visited in late February and early March to detect the first appearance of Richardson's ground squirrels. Once emergence commenced the area was frequently observed and live-trapped, usually daily through the period of peak emergence, until no additional animals appeared. Squirrels were captured selectively by placing traps (Tomahawk Live Trap Co., single-door, squirrel traps) at the opening of the burrow just entered by an animal and then temporarily blocking nearby burrows. This technique resulted in 96% trap success. On initial capture all adults were marked for permanent identification with a numbered metal tag in each ear (National Band and Tag Co., no. 1 monel self-piercing tag). Juveniles appearing on the area during the summer were ear-tagged to permit positive identification of yearlings in the subsequent spring. On first capture in spring, each squirrel was distinctively marked for observation with hair dye (Clairol Nice 'N Easy). At each capture squirrels were weighed, the appearances of the external genitalia and of the pelage were noted, and the animal's capture site was recorded. A vaginal lavage (Michener 1980 a) was obtained for each female at each capture from emergence until several days post-copulation. The size of the left testis of males was recorded at each capture in 1982 by holding the testis in the scrotal sac and measuring the maximum length to the nearest 1 mm with callipers. Because virtually any animal that was seen could be trapped, and because each squirrel was uniquely dye marked, I could detect and capture animals as they appeared on the study area. Flakes of dry skin in the fur or on the soles of the feet, fecal pellets that were small, wrinkled and dry, and a concave abdomen were used as indicators of recent emergence. For females two additional criteria were available to confirm recent emergence: vulva not yet fully perforate, and a pre-estrus or early estrus vaginal condition. Of 295 female emergences involving 203 different females over the 5 years, 260 were confirmed as recent emergences. The remaining females had been inseminated by the time of first capture and were excluded from the emergence data. No reliable reproductive criteria were available for males to equate their appearance in the population with emergence from hibernation. Based on known recent emergers (residents that hibernated on the area and had loose dry skin in the pelage on first capture in spring), many males had large descended testes on emergence (see Results). Males that bore fresh wounds, indicative of intraspecific fighting, on first capture were assumed not to be newly emerged. By this criterion five previously untagged males were eliminated, reducing the data set to 111 emergences (involving 85 different individuals) for the 5 years. Conception dates were determined for 258 pregnancies from 1979 to 1983 by detecting a copulatory plug in the vagina (n = 36), by detecting sperm in the vaginal lavage (n = 152), by inspecting the vaginal lavage sequence (n = 9), or by backdating 22.5 days (Michener 1980a) from the parturition date (n=61). Conception date was taken as the day that sperm were detected, but some females may have mated the previous afternoon after that day's vaginal smear was obtained. For squirrels on the East Pasture in 1982, I supplemented trapping records by noting the first daily sighting of each animal. Additional locations were recorded randomly throughout the day each time an individual was seen more than 25 m from its previous location. During the peak breeding season, I scanned the area again in the early afternoon to obtain an extra location for each active squirrel. Capture and sighting locations were estimated to the nearest 3 m using numbered fence posts, rocks, and other topographic features, and were plotted on maps of the area. A composite map was constructed for each resident squirrel showing all locations at which it had been seen during specific periods, such as the breeding season (for males) and the pre-iusemination period (for females). Distances between sites were measured from maps to the nearest 5 m. Ranges were calculated by drawing a minimum convex polygon enclosing all sightings of a squirrel. When two points greater than 25 m apart resulted in a line that nowhere along its length passed within 25 m of another sighting, the outlying point was not included in the polygon but was classed as an excursion location. Secondary polygons were constructed for individuals that had a cluster of 5 or more points located more than 25 m from the primary polygon.

3 31 Results Emergence schedules Although dates of emergence from hibernation varied among years, emergence schedules in all 5 years were characterized by males being the first animals to appear aboveground, by the majority of males resuming activity while the majority of females remained in hibernation, and by all males being aboveground before the last females emerged (Fig. 1, Table 1). The mean emergence date for males was significantly earlier than that for females in all years (t-tests, P< 0.001); the average annual sex difference in mean emergence dates was 12 days (range 8-16 days). In 1981, 1982 and 1983, years in which most males were of known minimum age, average (+_SD) emergence dates of yearling and older males did not differ significantly (26 February _ 3 days for 6 yearlings, 25 February 4-2 days for 11 older males in 1981, t= 1.12, P>0.20; 12 March _ 5 days for I0 yearlings, 8 March + 7 days for 6 older males in 1982, t= 1.35, P>0.10; 22 February 4-5 days for 16yearlings, 18 February _+3 days for 5 older males in 1983, t=1.90, P> 0.05). Similarly, in 1982 and 1983, years in which most females were of known age, there was no significant difference in average emergence dates of yearling and older females (25 March 4-8 days for 56 yearlings, 24 March + 5 days for 27 older females in 1982, t=0.63, P>0.50; 10March 4-6 days for 68 yearlings, 9 March _ 6 days for 34 older females in 1983, t=0.72, P>0.40). The proportions of females still underground on the median date of male emergence were 100%, 100%, 87%, 98% and 100% for , respectively. By the time the last male appeared, the proportions of females not yet emerged were 27%, 89%, 32%, 56% and 79%, respectively (Fig. 1). Latency to conception Female Richardson's ground squirrels produce one litter a year. All females, yearling and older, bred in all years of this study. Latency between emergence from hibernation and conception was determined for females for whom both the dates of emergence and insemination were known. Over the 5 years, most females (149/217=69%) bred 1-4 days after emergence. In , all females (n=51) were inseminated 1-7 days after emergence from hibernation. In , 130 of 166 females (78%) bred within 7 days of coming a UJ (.9 r,r" 50- LU UJ ~ o - Z W O100- n- LLI n U.I > 50- I-- < J 0- E3 ~ 100- o N=22o "q 9 15s N.-21o ~ 9 18s N=21O "~ 9 38s N=23o 'r 9 85s 9..v--v A A 9149 V / 9, / /9 / Mean Emergence / i Dates.v--/ --9 Mar 13 Mar 26 9 j J ,g./ / / / 9 7 / Mar 13 9 /9 /-/,v /, / f/ "2 A'.vv 9 v-- 9./v A--A" /v-v A/A / Feb 26 7,;;' ~v_v/v 9 / /,2.z / " 9 / / : AF Mar 25 Mar 6,,/' ~.'," Mar 12 Mar 24.v-v / 9 9 A/' v--v--v / A -~ 9 -A A-- 9 / A-A / / z N :24o~ v /v,04s / / /-!, / /- Feb 21 Mar 9 i i i i i lo 20 I.. lo I i~ 2~ FEB MARCH APRIL Fig. 1. Cumulative per cent of adult (> 1 year) male and female Richardson's ground squirrels emerged from hibernation. Data are based on squirrels with confirmed emergence dates (see Methods). Male emergence recorded on East and West Pastures in all years; female emergence recorded on East Pasture in 1979 and 1980, and on both pastures in 1981, 1982 and 1983 aboveground, and the remaining females bred 8-16 days after emergence. Although the breeding season (the period between the first and last days on which females were

4 32 Table 1. Difference, in days, between the times of emergence of the first, median, and last male and female Richardson's ground squirrel in 197%1983. Emergence dates (male-female) are indicated in parentheses. Sample sizes are as given on Fig. 1 Emergence First 11 d 18 d 1 d 18 d 8 d (7-18 Mar a) (1-19 Mar) (22-23 Feb) (22 Feb-12 Mar) (13-21 Feb) Median 9 d 9 d 9 d 12 d 18 d (12-21 Mar) (15-24 Mar) (24 Feb-5 Mar) (12-24 Mar) (20 Feb-10 Mar) Last 31 d 19 d 20 d 25 d 27 d (25 Mar-25 Apt) (21 Mar-9 Apr) (8-28 Mar) (22 Mar-16 Apt) (6 Mar-2 Apr) a The first female was captured on 15 March 1979, but as she was recently inseminated she was excluded from the emergence data (see Methods) Table 2. Dates of the breeding season (from first to last insemination) and the peak breeding season (shortest period during which 50% of females were inseminated). Duration of the breeding season, in days, is given in parentheses No. of females inseminated" Breeding season 15 Mar-10 Apr (27 d) 23 Mar-12 Apr (21 d) 26 Feb-30 Mar (33 d) 16 Mar-18 Apt (34 d) 3 Mar-6 Apr (34 d) Peak breeding season Mar Mar 3-11 Mar Mar Mar (3 d) (4 d) (9 d) (7 d) (3 d) Exact insemination dates were known for all females in 1979 and 1983, and for 17 females in 1980, 39 females in 1981 and 87 females in Insemination dates were estimated for the remaining nine females in 1980, 1981 and 1982 inseminated) spanned 3-5 weeks, half the females bred within a 3-9 day period each year (Table 2). Sex ratio Not all males appearing on the area remained resident for the breeding season. To be classed as a breeding-season resident, a male had to be present for 5 or more consecutive days during the period in which 95% of females bred; 15 males met this criterion in 1981 and in 1982 and 20 did so in The numbers of yearling, older, and unknown-aged males constituting resident populations were 5, 7 and 3 in 1981, 6, 4 and 5 in 1982, and 14, 4 and 2 in The sex ratio (breeding females: resident males) was significantly female biased in all years (45:15=3.0 females per male in 1981, 89:15=5.9 females per male in 1982, and 102:20 = 5.1 females per male in 1983). Of the resident males, 12, 13 and 18 were present throughout the peak breeding season (the shortest period within which 50% of females bred) and 6, 6 and 13 were present for the entire breeding season in 1981, 1982 and 1983, respectively. Male breeding condition Of 22 males that appeared on the area in March of 1982, 21 had descended testes on first capture. One male emerged early in 1982, on 22 February, and his testes assumed a scrotal position between 27 February and 5 March. Peak testis length of 22mm (SD=2, range mm) was achieved 11 days (SD = 4, range 3-17 days) after emergence by 15 males for whom a minimum of 5 testis measurements were available in For 14 males, peak testis length occurred between 20 and 30 March (average _+ SD date: 24 March 3 days), whereas the testes of the early emerging male attained maximum length on 11 March. Thus, testes were at maximum size prior to and during the peak breeding season (Fig. 2). However, gonadal regression commenced before the breeding season terminated. By 18 April, the day the last female bred, testis length of all males was less than 15 ram, and some males had inguinally or abdominally located gonads (Fig. 2). No information was obtained on the relationship between testis size and sperm production. Vernal behavior Incidental observations made while trapping in 1981 indicated that during the breeding season, males showed little fidelity to particular burrows and they rarely engaged in burrow related activities such as excavation or gathering of dry grass. Males were likely to take refuge in any burrow, and fre-

5 33 Breeding 25 - Peak E t, 20- / \ T (D uj 15- J... Season I.- 1or./) 9 LU I ll N s S 7 Nns I I 1 I I I MARCH APRIL Pig. 2. Average length of left testis of males resident during the breeding season in Range in testis lengths is indicated by vertical lines. Only those days on which at least 6 males were examined are shown. N s number of males with testes in scrotum; N,s number of males with testes not in scrotum. Nolid bar above curve indicates the durations of the breeding season (89 females bred) and the peak breeding season (47 females bred) quently entered burrows known to be used by females. Toward the end of the breeding season, males became more sedentary and resided in several burrows that they renovated and provisioned with dry grass. In 1982 I recorded instances of gathering of dry grass and of burrow excavation by squirrels resident on the East Pasture. Gathering of grass by females was first observed 20 March, whereas grass gathering by males was not seen until 16 April, by which time 56% (18/32) of surviving pregnant females had been seen gathering grass. Burrow excavations by females and males were first seen 29 March and 22 April, respectively. Relative to males, females were sedentary in the breeding season. On average, females resident on the East Pasture in 1982 traversed a distance of 52 m between emergence and insemination (SD=24, range m, n=39 females for whom an insemination day location and at least one prebreeding sighting 'were available, average of 7.4 sightings per female, distances measured between two furthest sightings). In the 5-day period March (when 24 of 42 females bred on the East Pasture), males moved 162 m (SD = 72, range m, n = 7, average of 17 sightings per male), and over the entire breeding season (22 March- 11 April on the East Pasture) males moved 197 m (SD=49, range m, n=8, average of 38 sightings per male). Within a day, males typically moved longer distances than females did during their entire prebreeding period. Of 72 intra-day movements noted for 8 males during the breeding season, 79% (n = 57) exceeded 50 m. No male established an exclusive range during the breeding season; the range of each male over- Pre-breeding Season Emergence-21 March t c-,/-",,,q Breeding Season 22 March-11 April 7 " z:, I" '- " X.-I "'.! 9.K "~ / ~ \ \r g~--'. ~ f.,'.~... " / ql., ~ \ / ~;,(:: 9.:",,.~ oca ion on Z_~...~...,..: ",, b insemination e i...,,' i V. / _\ I I ~ j 50 m Fig. 3. Ranges of adult male Richardson's ground squirrels resident on the East Pasture in 1982 during the pre-breeding season (left figure) and during the breeding season (right figure), and locations of 42 females on the day of insemination. On the East Pasture the first female bred on 22 March and the last on 11 April. Ranges are presented as polygons, and excursions as lines radiating from polygons (see Methods for details of constructing range boundaries). Average number of sightings per male and average proportion of male's sightings enclosed by his polygon are: 34 and 84% for pre-breeding ranges, and 38 and 91% for breeding ranges. Males a-d: yearlings; Males e-f: 2-year olds; Males g-h: unknown age. Male h appeared on the East Pasture (delineated by curved lines) only twice prior to 22 March, so a pre-breeding range could not be constructed. On 26 March Males a and e engaged in a fight; Male a expanded his range to the east and Male e disappeared the next day (see "Costs of early emergence" for further details). On 30 March Male f established a new range on tihe West Pasture and did not return to his former site on the East Pasture

6 34 lapped that of at least one neighbor, and virtually all males occasionally intruded into the ranges of several other males (Fig. 3). With the exception of the early emerging male (Male e), males did not establish well-defined areas which they attempted to defend until the beginning of the breeding season. Males adjusted the location of their range in the breeding season so as to increase their proximity to estrous females (Fig. 3). The behavior of males during the breeding season suggested that they were constantly monitoring females and assessing their estrous status. Males were alert to the movement of other squirrels and almost invariably approached any animal that moved. If the second squirrel was a male, the approach usually resulted in a fight/chase sequence. If the second animal was a female, the male attempted to sniff her genital region. Estrous females usually neither fled nor chased the male, but pregnant females responded aggressively to approaches by males. Proximity between resident males (n = 8) and estrous females (n = 42) on the East Pasture in 1982 was determined by noting whether the male's breeding-season range overlapped, either completely or partially, the area used by each female between emergence and insemination. On average, each male's range overlapped 10.5 estrous females (SD = 4.3). However, there was asymmetry among males in their propinquity to females; 5 males had ranges overlapping females whereas the ranges of the other 3 males overlapped only 5-7 females. Between emergence and insemination, females used areas overlapped by an average of 2.0 males (SD = 0.8). No male exhibited injuries prior to the emergence of females, but by the end of the peak breeding season all males still resident (12 in 1981, 13 in 1982) had sustained multiple injuries. On average, males sustained their first injury on 9 March (SD=5 days) 1981 and on 23 March (SD=3 days) Fresh wounds appeared over several days, but few males acquired additional injuries after 16 March 1981 and 30 March 1982, when the majority of females were already pregnant. Wounds were located primarily on the back and hips (24 of 27 males), on the face, especially around the eyes and ears (22/27), and on the forearms and shoulders (9/27). Females rarely bore wounds (4/45 in 1981, 6/89 in 1982) and, if they did, injuries were small both in number and size. Male-female interactions in spring rarely involved fights and were never seen to result in injury. Some copulations occurred in burrows, so the possibility that females inflicted injuries on males while underground cannot be eliminated. Most male-male interactions involved growling and squealing, consisted of brief fights interspersed with chases, and did not result in injury. However, three male-male fights resulting in extensive injury to participants were observed in In each case, the males were silent as they rolled and grappled with each other for about 1 min without interruption. On separation, participants appeared exhausted and did not engage in post-fight chases. After one fight I was able to approach within i m of one participant (presumed to be the victor as he subsequently resided in the area of his opponent, who disappeared the next day); while cleaning blood from his fur this male kept toppling to one side and his eyes drooped closed as if he was very weak. Costs of late emergence Late emerging males appeared to suffer no cost in terms of their ability to establish residency on the area. Of the last third of males to appear in 1981, 1982 and 1983, 71% (5/7), 75% (6/8) and 86% (6/7) became breeding season residents compared with 71% (10/14), 60% (9/15) and 82% (14/17) of the earlier emerging males. However, late emerging males did lose potential breeding opportunities. On 8 March 1981, the day the last male appeared, 21 of 29 (72%) emerged females were already pregnant. Thus, of 45 females bred in 1981, at least 47% were no longer available as mates to the last appearing male. As this male was not known to have been resident on the area in the previous year, he may have hibernated elsewhere and emigrated to the study area post-emergence. The latest emergence by a known local resident was 4 March 1981; 8 females were impregnated prior to 4 March, so 18 % of the female population was no longer available for breeding. In comparison with 1981, late emergence by males in 1982 and in 1983 incurred little cost, primarily because snowstorms delayed breeding by early emerging females. Although 31 females were active in 1982 and 22 were active in 1983 on the date the last known local resident male emerged, only one female bred prior to this date in each year. Thus, only 1 of 89 females that bred in 1982 and 1 of 102 females in 1983 was no longer a potential mate for the latest emerging males. Costs of early emergenee Males that emerge before the first females enter estrus have the maximum opportunity for locating unimpregnated females. However, can males

7 35 emerge too early? The only year in which a male emerged notably earlier than the remainder of his cohort was 1982 (Fig. 1); a 2-year old male was the sole squirrel active from 22 February to 5 March. This male (Male e) maintained and defended a large range throughout mid-march (Fig. 3). On 26 March, Male e and a neighboring yearling male (Male a) engaged in a fight that resulted in injuries to both (see "Vernal behavior" section). The older male was displaced and was not seen again after the following day; the yearling occupied his opponent's area for the remainder of the year. Although the 2-year old male weighed slightly more than the yearling prior to the fight (380 g vs 365 g on 24 March), in comparison with his opponent he had been active longer (33 vs 16 days), had defended a larger area for a longer time (Fig. 3), had lost mpre weight since emergence (17% vs 1%), and had smaller testes (18 vs 21 ram) that were already regressing. Because 55% of females were inseminated after his disappearance on 27 March, the early emerging male was not a potential mate for the majority of females on the study area. Discussion The 8-16 day difference in mean emergence dates of male and female Richardson's ground squirrels is of similar magnitude to that reported for Uinta, Belding's, and Columbian ground squirrels (Knopf and Balph 1977; Morton and Sherman 1978; Murie and Harris 1982), but in contrast to these species, yearling S. richardsonii do not emerge later than older squirrels of the corresponding sex. Emergence of male Richardson's ground squirrels in advance of females is not simply a reflection of the immergence sequence in the previous year. Adult males do enter hibernation earlier than adult females, but juvenile males immerge after females (Michener 1979 and in press a). Thus, the autumnal immergence sequence is adult males, adult females, juvenile females, juvenile males. Although juvenile males terminate aboveground activity as much as 2 months later than adult males (Michener 1974; Michener, in press a), the following spring they emerge as yearlings simultaneously with older males. Likewise, juvenile females commence hibernation later than adult females, but in the subsequent spring yearling and older females appear at similar times. Male Richardson's ground squirrels not only emerge from hibernation earlier than females, but they differ from females in a constellation of behaviors related to (1) intrasexual competition for breeding opportunities, (2) the biased adult sex ratio, and (3) the difference in effective length of the breeding season for males (3-5 weeks) and females ( < 1 day estrus occurring, typically, 1-4 days post-emergence). In comparison with females, males in this study moved longer distances, occupied larger home ranges, expended little or no time on burrow maintenance, and were involved in more injurious fights. Additionally, males lost weight for weeks during the breeding season, whereas females gained weight from emergence to parturition with a brief weight loss by heavy (> 250 g) females on the day of insemination (Michener, in press b). Males engaged in activities that were likely to enhance opportunities for inseminating females (monitoring all nearby squirrels, evicting potential male competitors, assessing the breeding condition of females) at the expense of personal body condition. Early emergence from hibernation, therefore, is just one of several behaviors used by male Pichardson's ground squirrels to enhance their breeding success. That early vernal emergence is a male reproductive strategy is suggested by the absence of this phenomenon in nonbreeding males. Yearling male Belding's, Columbian, and Uinta ground squirrels are usually sexually immature and emerge from hibernation after older males and breeding females have resumed aboveground activity (Knopf and Balph 1977; Morton and Gallup 1975; Murie and Harris 1982). However, as shown in this study, for species in which both sexes are reproductively mature as yearlings, e.g., Richardson's and Arctic ground squirrels, there is no age component to the emergence sequence (Dorrance 1974; McLean and Towns 1981). Occasional occurrences of late emergence by small, reproductively immature males in species in which yearlings are normally sexually mature (McLean and Towns 1981; Michener 1980b), and of early emergence by reproductively mature yearling males in species in which yearlings are normally not sexually active (Slade and Balph 1974) further suggest a relationship between time of emergence and reproductive competence. To be reproductively successful, males must both resume aboveground activity and be producing viable sperm by the time the first female is ready to breed. Typically, testes of male sciurids are at maximum size and descended into a darkly pigmented scrotum either when males emerge from hibernation or shortly thereafter (Fig. 2; Bakko and Brown 1967; McKeever 1966; Morton and Gallup 1975; Murie and Harris 1978; Stockard 1929). Furthermore, spermatogenesis is complete either when males emerge or several days post-

8 36 emergence (see Michener, in press a). Mitchell (1959) and Hock (1960) proposed that in Arctic ground squirrels, a species in which spermatogenesis is not complete at emergence, males emerge 7-10 days before females to ensure maturation of the reproductive system prior to female emergence and breeding. They did not discuss whether such maturation could occur underground while homeothermic. Liddle (1982) established that a period of homeothermy is essential for reproductive maturation in captive Belding's ground squirrels. As I have no information on the relationship between terminal arousal from torpor and resumption of aboveground activity for S. richardsonii, I do not know if males that emerged with descended testes had spent time underground in a 11omeothermic state before appearing aboveground. Olympic, hoary, and yellow-bellied marmots are species in which colony members typically hibernate communally, emerge synchronously, and reside in monogamous or one male-several female groups (Barash 1973; Holmes, in press; Johns and Armitage 1979). A sex difference in emergence has not been reported for these species (Michener, in press a); possibly a sex difference in terminal arousal occurs but is not manifest as a sex difference in resumption of activity because early arousers either wait for or stimulate arousal in hibernaculum members. There may be no advantage for a harem male to resttme aboveground activity before female group members if he is able to assess when his companion females are about to emerge, and when he has preferential, if not exclusive, access to estrous females in his group. Males that hibernate alone, as in most species of Sperrnophilus including S. richardsonii, must come aboveground to determine when females commence emergence. Additionally, they must compete for access to estrous females. The lack of either injuries or weight loss during the prebreeding period, when only males were aboveground, suggests that intrasexual competition among male Richardson's ground squirrels was insignificant prior to the emergence of females. When females began appearing aboveground, males shifted their ranges to encompass areas occupied by estrous females and they engaged in intense, often injurious, aggressive interactions with other males. Movements by males that bring them into contact with more estrous females have also been reported by Paul (1977) and Davis (1982). Evidence for intrasexual competition among males for mates has been noted for various sciurid species. Males have larger ranges, move longer distances, are more active, engage in more frequent and intense intrasexual aggression, and more frequently sustain injuries during the breeding season than do females or than do males in the non-breeding season (Clark 1977; Murie and Harris 1978; Paul 1977; Wistrand 1974). Males lose weight during the breeding season whereas females usually gain weight post-emergence (Bakko and Brown 1967; Knopf and Balph 1977; McLean and Towns 1981 ; Michener, in press b). Intrusions into ranges of other males increase when an estrous female is present, and males defend estrous females from such intruders (Barash 1981; Murie and Harris 1978; Paul 1977; Wistrand 1974). Thus, males monitor for the presence of potential mates and potential competitors for mates. An alternative perspective to the question of why male Richardson's ground squirrels emerge before females is raised by asking: why do females emerge after males? If males are able to resume aboveground activity and survive, why do females not advance their time of emergence by 1-2 weeks and likewise emerge early? Assuming that males achieve reproductive competence at or shortly after emergence, simultaneous appearance of females with males would still ensure that mates were available to females, thereby maintaining the brief latency between emergence and mating. I suggest that there has been selection for early emergence by females, and that the time of aboveground appearance of females is a compromise between (1) lengthening the time available for offpring to grow and fatten and (2) promoting survival of self and offspring by emerging at a time that assures abundant food during lactation and for weaned young. The date of emergence from hibernation by female Richardson's ground squirrels is flexible and correlates each year with rewarming of the subsurface soil (Michener 1979), suggesting that emergence is synchronized with vegetative regrowth. However, the selective pressures determining the time of female emergence are not the same as those determining when males emerge. Because there is variability among males in the date on which each individual terminates hibernation and because females mate shortly after they appear aboveground, each male must time his emergence to maximize access to estrous females. At the minimum, males should precede females by a period equal to the difference, if any, in lengths of the post-emergence period required by males to complete sperm potentiation and by females to enter estrus. Exceptionally early emergence by male Richardson's ground squirrels produces no reproductive return and it increases the risks of being active in inclement weather, of losing body condition

9 37 prior to the start of the breeding season, and, possibly, of being unable to sustain sperm production for the entire breeding season. Late emergence by males carries the cost of reduced reproductive success as females that have been active for at least 4 days are likely to have been impregnated by earlier emerging males. Selection will constrain the timing of male emergence from hibernation because those males that emerge slightly in advance of females are likely to sire more offspring than are males that appear either several weeks before or after females resume aboveground activity. Thus, the male-before-female emergence sequence characteristic of Richardson's ground squirrels can be viewed as an outcome of intersexual selection. Phenomena equivalent to the sex difference in vernal emergence noted for hibernating sciurids occur in a variety of species characterized by seasonal patterns of residency/activity on the breeding area. For migratory birds, males typically return to the breeding grounds in spring in advance of females (e.g., Lanyon 1957; Oakeson 1954). Correspondingly, in polyandrous avian species females precede males (Oring and Lank 1982). Males emerge from the hibernaculum in advance of females in some species of snakes (Gregory 1974), male bullfrogs precede females to mating ponds (Emlen 1976), and protandrous eelosion occurs in many insects (Robertson 1918; Wiklund and Solbreck 1982). Thus, the appearance of the mate-limited sex prior to the mate-limiting sex, apparently to maximize reproductive opportunities by being present and reproductively competent before potential mates are ready to breed, is a phenological strategy characteristic not only of Richardson's ground squirrels, but of many organisms in which breeding follows appearance of the mate-limiting sex on the breeding ground. Acknowledgements. Financial support was provided in by NSERC of Canada grant U-92. 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