© 2004 by The Society for Integrative and Comparative Biology
Interannual Variation in Timing of Parturition and Growth of Collared Pikas (Ochotona collaris) in the Southwest Yukon1
1 Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9 Canada
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SYNOPSIS |
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The length of the snow-free season has a significant influence on reproduction and growth in northern alpine environments, and these life history traits may provide sensitive indicators of the responses of organisms to climate change. We examined growth rates and timing of parturition of collared pikas (Ochotona collaris) from 1995–2002 in the Ruby Range, Yukon Territory, Canada. Growth rates were best described using a Gompertz model, in which the asymptotic mass, determined from the average male and female weights, was 157 g, the growth rate constant (K) was 0.0557, and the age at inflection (I) was 18.12 days, for a birth weight of 10 g. The maximum growth rate for North American pikas (O. collaris and O. princeps) increased with latitude, with maximum growth rates being approximately one-third greater in northern populations where the snow-free season is less than three months long. The mean parturition date varied significantly among years from 3 June to 3 July, and delayed parturition was correlated with indices of high snow accumulation and, to a lesser extent, late spring snowmelt. However, parturition date did not significantly affect the subsequent over-winter survival of juveniles in this population, suggesting that pikas are able to adjust to seasonal uncertainty associated with highly variable spring conditions.
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INTRODUCTION |
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The environment in which a species lives can affect a number of life-history parameters, including number and size of litters born, timing of parturition and the growth rate (Ricklefs, 1967
; Case, 1978; Roff, 1992; Charnov, 1993; Réale et al., 2003). Timing of parturition in northern alpine environments is particularly critical for mammalian herbivores because the snow-free season is very short, often less than 2 months. Young must be born late enough to avoid unsuitable conditions, such as snow or low-quality food resources, but they also must be born early enough in the summer to allow growth to a size at which they are able to acquire the resources necessary for over-winter survival. Depending on the species, this may involve accumulating fat stores for hibernation (e.g., marmots), migration (e.g., caribou), acquisition of territories and hoarding of food prior to the onset of winter (e.g., collared pikas), or a combination of these behaviors.
In highly seasonal environments, parturition tends to be synchronous (Rachlow and Bowyer, 1991), with the majority of all offspring being born in a short period of time when conditions are optimal for growth. Reproductive synchrony may result from individuals selecting similar times for reproduction in relation to climate, however, the temporal pattern of reproduction may also be a result of other ecological processes, such as predation, food availability, or density of mates (Ims, 1990; Eccard and Ylönen, 2001). There is also considerable evidence that mammals use changes in photoperiod or some secondary compounds in newly emerging vegetation as predictors of breeding season activity (e.g., Bronson, 1985; Goldman, 2001).
Generally it is assumed to be an advantage to be born earlier in a growing season (Roff, 1992), as shown in a number of species (e.g., yellow-bellied marmots, Armitage et al., 1976; snowshoe hares, Gillis, 1998). For territorial species, being born early may be critical when finding and securing a territory are necessary for survival. As well, individuals born earlier may have an advantage in terms of vegetation quality and availability. Because forage quality starts high and declines over the season, young that are born later have less time to adequately prepare for winter (e.g., Dall sheep, Rachlow and Bowyer, 1991; Uinta ground squirrels, Rieger, 1996). Also, because lactation is more energetically demanding than pregnancy, it is advantageous for an adult female to have lactation coinciding with early emerging vegetation, which has higher protein content (Millar, 1977; Rachlow and Bowyer, 1991; Rubin et al., 2000).
Seasonal environments not only affect the timing of parturition, but can also influence growth rates of animals. In general, at northern latitudes organisms grow faster to reach an optimal size during a shorter growing season. A number of studies have shown that growth rates are, in part, affected by latitude (Arctic ground squirrel, Case, 1978; sturgeon, Power and McKinely, 1997; bass, Brown et al., 1998; brown trout, Jensen et al., 2000; frogs, Merila et al., 2000; moose, Ferguson, 2002), with animals having faster growth rates in northern parts of their range. Increases in post-natal growth rates are usually found only in animals that are restricted to a short breeding season, although, some animals may use physiological and behavioral adaptations to counteract the short growing season without major increases in growth rates (Case, 1978).
One group of species that are affected by a short growing season are talus-dwelling pikas (Lagomorpha: Ochotonidae) (see Smith, 1988). This group of pikas are generalist herbivores that live in boulder fields (talus) in alpine environments that are often characterized by short summers. They are territorial and do not hibernate during the winter, but rather forage below the snow and on vegetation that was collected and stored in a haypile at the end of the summer. Pikas have low over-winter survival, especially in their first winter (Franken, 2002; Kreuzer and Huntly, 2003). They breed at one year of age, with average litter sizes of 3 (range 1–4) individuals, and an average of 2 individuals being weaned. Pikas generally produce one litter a year, but have a post-partum estrus allowing for a possible second litter. Breeding usually takes place while there is still snow on the ground and gestation is approximately 30 days. Litters are born in the talus (rock piles) and weaned at 3–4 weeks after birth.
The collared pika (Ochotona collaris L.) inhabits the mountains of Alaska, Yukon Territory, Northwest Territories, and northern British Columbia (MacDonald and Jones, 1987). Little is known about this species, and most of what we infer has come from work on its southern congener, the American pika (O. princeps). There is a gap in the distribution of these two species, with the American pika inhabiting mountain areas in western North America from 35°N to 54°N and the collared pika's distribution ranging from 59°N to 68°N. Both species have similar life history strategies, although, the length of summer growing season is generally longer for the American pika. A few studies have described the growth of the American pika in both wild (Alberta: Millar and Tapper, 1973; Colorado: Golian and Whitworth, 1985) and captive populations (Whitworth and Southwick, 1981). These studies have shown the importance of a rapid growth to ensure pikas reach an adult weight prior to the onset of winter.
We had two primary objectives in this paper. First, we developed a growth model for the collared pika and compared growth rates of pika populations in North America. Second, we used the growth equation to estimate dates of parturition of juvenile pikas at our study site and examined how parturition date affected survival and whether variation in spring conditions influenced the growth rate and timing of parturition of collared pikas.
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METHODS |
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The growth rate and timing of parturition of collared pikas was examined in the Ruby Range Mountains, Yukon Territory (61°12'N, 138°16'W; 1,800–2,000 m). The snow-free season generally extends from mid-June to early September. Numerous talus patches (boulderfields) inhabited by pikas are surrounded by extensive alpine meadows dominated by Dryas octopetala, Salix reticulata, and graminoid species (e.g., Carex consimilis). Cassiope tetrogona was common along the margin of the talus. McIntire (1999)
and Hik et al. (2001) provide more detailed descriptions. Our 4 km2 study site had 27 distinct talus patches ranging in size from 0.07 ha to 15.7 ha and separated by 15 m to 1,140 m of vegetation (Franken and Hik, 2004). Pikas were live-trapped mid-June to the end of August from 1995–2002, using Tomahawk live traps baited with fresh native vegetation and placed adjacent to haypiles used by pikas. Up to 6 traps at a single haypile where a pika was observed were opened for several hours each day and checked at 30 min intervals. Because pikas can be very difficult to trap, animals were targeted for trapping throughout the summer, so that by the end of the season all animals within the study area had been trapped at least once. Pikas are diurnal, have distinctive territorial calls, are highly visible and have distinguishable haypiles, permitting us to identify and capture all pikas resident within the study area. A permanent 50 m-interval grid system (±5 m accuracy) was used to determine locations of pikas within the study area.
Animals trapped for the first time were marked with numbered metal ear tags (Monel #1) and a unique color combination of thin wire. Age (adult or juvenile), sex, and weight (to the nearest 2 g using a 300 g Pesola balance) were recorded for all trapped individuals. Age (adult or juvenile) for each animal was determined based on weight, as well as fur color and molt patterns. Since pika nests are nearly impossible to access, juveniles were weighed at first-capture upon emergence when an intensive effort was made to capture these individuals. However, it was very difficult to capture all juveniles from a single litter, or even to be certain of litter size.
Sigmoidal growth curves have been used in numerous studies to describe the growth of organisms. We determined which of three sigmoidal growth models (Gompertz, von Bertalanffy, and the logistic equations) best described pika growth. Relative to the logistic curve, the Gompertz curve has a slower, more prolonged growth rate during the later stages of growth, and the von Bertalanffy shows this to even a greater extent (Ricklefs, 1967; Day and Taylor, 1997). Different studies have used various equations to examine growth, and while biological assumptions may be important, they are often overlooked (Day and Taylor, 1997). Nevertheless, once a growth curve has been established for an organism, the curve can be used to predict an organism's age at certain weights. It is also possible to predict the date of birth (parturition date) of individuals. This latter application is very useful for species where the birth date cannot be known exactly.
These sigmoidal growth equations required the asymptotic mass (A = mean adult weight) at a given age (t = days). We estimated the growth-rate constant K, and the inflection point I, using the equations in Table 1. Birth weight of pikas was set at 10 g, based on other studies of O. princeps in captivity (Millar, 1972; Millar and Tapper, 1973; Whitworth and Southwick, 1981; Golian and Whitworth, 1985). The asymptotic mass (A) was determined by calculating the average adult mass for all individuals at our study site, as there was no difference in the mass of adult males and females (Franken 2002).
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Since specific ages for juveniles were unknown, a growth curve was developed from weight gain over known intervals in a method similar to the one used by Millar and Tapper, (1973) and Golian and Whitworth, (1985). Initial weights (first capture weights) were grouped into 10-g intervals and the mean initial weight for each interval was taken. The second and subsequent captures provided weight changes over known time intervals. We only used captures that occurred within 10 days of each other, to avoid the likelihood that weight gain decreased over time. The mean growth rate between intervals was calculated and a growth curve was constructed using the mean rate of growth from one mean interval weight to the next. Although we were able to calculate the total elapsed time we still needed to determine how old individuals were at 70 g (our earliest-weight interval). We selected eight initial reference points (to scale the rest of our data) of 70 g from 20–27 days, and fit these to the three growth curves. Curves were fitted using non-linear regression in S-PLUS, with iterative least squares criterion (MathSoft, 1997), and the best model was chosen when the residual standard error of the equation was minimized.
To compare the growth rate of the collared pika to other pika populations in North America, the growth rate constant K (day–1) was converted to maximum growth rate (g/day) by multiplying K by A*e–1 (estimated mass at inflection point) (Zullinger et al., 1984). From this we were able to compare growth rates of pikas at different latitudes. We subsequently fit growth rates of Alberta and Colorado (wild) pikas to a Gompertz growth curve, so comparisons among populations could be standardized.
We estimated the parturition data and age of all juveniles at our study site using the best-fit curve (Zullinger et al., 1984), described by W = A*exp(–exp(–K(t – I))), where A is the asymptotic mass (g) at age t (days), K is a growth-rate constant (day–1), and I is age at the inflection point (days). To determine if the mean parturition data among years was different, a single factor ANOVA was used. Tukey's test (S-Plus, MathSoft 1997) was used to determine which years were significantly different from each other. For each year we compared the parturition date for juvenile pikas that survived their first winter, to those that did not, using logistic regression.
There is relatively little information about snow accumulation and spring snow melt in the mountains of the southwest Yukon, but we were able to utilize two measures of the timing of snowmelt and snow accumulation to examine if climate and weather affected the timing of parturition of pikas: (1) the snow accumulation on Mt. Logan (same latitude, 120 km W) measured as water equivalent meters (Moore et al., 2002; G. Holdsworth, personal communication—data for 2002 not available), and (2) the best estimate of snow-free dates on plots at our study site based on dataloggers and field records (1995–2002; D. Hik, unpublished data). These indices were correlated with the average parturition date for the corresponding year.
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RESULTS |
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Mass of adult male pikas was 157.3 ± 12.5 (SE) g (range, 130–185 g; n = 97); adult females were 157.4 ± 13.7 g (range, 130–200 g; n = 126). When all years were combined, weight was not significantly different between the sexes (t = 0.0853, df = 221, P = 0.9321), so male and female weights were combined from 1995 to 2001 to calculate a mean adult asymptotic mass of 157.4 g (n = 223).
Based on the three growth equations and parameter estimates (Table 1), the best-fit model was the Gompertz growth equation when pikas weighed 70 g at 22 days. The best-fit curve was described by W = 157*e–exp(–0.0557[–18.12]), where 157 is the asymptotic weight in grams of adult pikas, 0.0557 is the growth rate constant (K) and 18.12 is the age (days) at inflection (I) (Fig. 1). We were not able to capture pikas in the first 21 days after birth, and therefore extrapolated this part of the curve from the Gompertz equation. We compared growth rates of different populations of pikas using the maximum growth rate per day (g/day), and found it increased with an increase in latitude (Table 2).
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We used the Gompertz growth equation to determine the approximate date of birth for all juveniles that were captured and weighed at our site. Birth dates are not exact (±3 days) because we had to estimate a starting reference point based on the best-fit of the model. When all years were combined, most juveniles were born late June (Fig. 2). However, depending on year, the average parturition date of the majority of juveniles varied significantly over a three-month period (F = 9.652, df = 7, 152, P < 0.0001) (Fig. 3). Four years (1995, 1996, 2001, and 2002) were not significantly different from each other; the average parturition date for these years was early to mid-June. Two years (1999 and 2000) were also not significantly different from each other, but were significantly different from 1995, 1996, 2001, and 2002. The average parturition date for 1999 and 2000 was late June to early July. The average date of conception (late May) was determined by subtracting 30 days from the date of birth, since gestation is 30 days in the American pika (Severaid, 1950
; Millar, 1973).
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The snow-free dates at our study site were partially correlated with the net accumulation on Mt. Logan (r = 0.63, df = 6, P = 0.13), with later snow-free dates occurring in years with higher snow accumulation. The average parturition date for each year was positively correlated with the net accumulation on Mt. Logan (r = 0.74, df = 6, P = 0.051; Fig. 4), but not with the snow-free dates at our study site (r = 0.32, df = 7, P = 0.29).
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When all years were pooled, we found that juvenile survival did not vary with parturition date (logistic regression: coefficient = –0.6929, SE = 0.0086, P = 0.4898, df = 159). Similarly, parturition date did not affect survival when years were examined individually (logistic regression: all p-values >0.05: Table 3), and no general trend was observed in terms of earlier born individuals having greater survival.
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DISCUSSION |
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Northern latitudes have both short and unpredictable growing seasons. Two life-history strategies for coping with this uncertainty are (1) faster growth rates, and (2) variation in parturition dates among years to take advantage of the best conditions for growth. Collared pikas at our study site appeared to use both of these strategies in response to the highly seasonal environment.
Of the three sigmoidal curves, the Gompertz curve fit our data best. This equation has also been used to describe the growth rates of many mammalian species (Zullinger et al., 1984). Growth rates of pikas are among the fastest for lagomorphs (Golian and Whitworth, 1985), and growth rates of collared pikas at our study site were even higher than those of its southern congener, the American pika. Faster growth rates at higher latitudes are likely an adjustment to shorter growing seasons. It is possible that the growth rates may reflect an underlying difference between the two species, however, given the other similarities between them it is likely that latitude provides the best explanation. In this alpine environment, pikas must attain adult weights, establish territories, and begin collecting vegetation for their haypile before the onset of winter (Whitworth and Southwick, 1981; Golian and Whitworth, 1985).
American pikas can have two litters per year with the first litter conceived early summer, usually under snow-cover (Millar, 1972; Millar and Tapper, 1973; Smith, 1978a; Smith and Ivins, 1983) allowing parturition to coincide with snowmelt and the onset of vegetative growth (Millar, 1972; Smith, 1978). It is unknown if collared pikas at our site were able to conceive two litters per year. Some authors (Rausch, 1961; Youngman, 1975; Smith, 1978b) have indicated that collared pikas may have two litters per year based on females being pregnant and lactating at the same time, however, this does not provide evidence that two litters are successfully weaned. Only one litter of pikas born per female was detected at our site, and the mean conception date was estimated to occur in late May under snow cover. Similarly, Rausch, (1961) collected adult females and found them to be pregnant late May to early June.
We observed litters of 4 individuals upon emergence, however, this was not typical. The average number of successfully weaned juveniles was about one juvenile per female per year (based on number of juveniles and number of adult females at the site). Other studies have reported that the litter size of collared pikas ranges from 1–4 pikas, averaging 2.2–3 (Dixon, 1938; Rausch, 1961; Smith et al., 1990), and we assumed that litter sizes in our study were similar.
The timing of breeding in pikas at our site allows juveniles to be born at the start of vegetative growth when forage quality is high, even though peak biomass occurs later (late July) (Andruchow, 2000). Due to the high energy demands of females during nursing, higher quality vegetation may be more important than having higher biomass. The timing of initiation of first litters is a compromise between having young early enough, so they can be weaned early and have an advantage securing a territory, and having them late enough to ensure that the mother can meet the energetic demands of weaning a litter (Smith, 1978a).
Smith, (1978a) suggested that within a population there is a correlation between the amount of variation in initiation of the first litter and the amount of variation in timing of snowmelt. He found pikas breeding asynchronously within a year and suggested this occurred because snowmelt varies among years and pikas are not able to predict snowmelt. Therefore, he suggested that asynchronous breeding occurs to ensure some success. At our site, however, it appears that parturition was more synchronous within a year, with the majority of individuals being born in a short period of time, even though snowmelt varied among years. Perhaps because of the constrained summer environment at this northern latitude, breeding asynchronously within a year is unlikely. Instead, it appears that pikas may be able to use environmental cues to signal timing of snowmelt and adjust breeding accordingly.
Variation in the average parturition date among years, at our site, was partially correlated with net snow accumulation, with later parturition occurring after winters with large snow accumulation. Similar results have been observed with pikas in Colorado, where variation in initiation of first litters was positively correlated with snowmelt (Smith, 1978a; Smith and Ivins, 1983). Pikas may delay breeding following winters with high snow accumulation in order to coincide parturition with vegetative growth. However, it is also possible that in years of late snow-melt, pikas may lose litters or reabsorb litters and then breed again in post-partum estrus (Smith and Ivins, 1983). Other studies have also shown a delay in the timing of parturition in other northern mammals following winters with deep or persistent snow-cover (caribou, Adams and Dale, 1998), or when late spring storms create inhospitable conditions for young and limit forage availability (Dall sheep, Rachlow and Bowyer, 1991). Early onset of spring conditions has allowed earlier parturition dates in other species (e.g., snowshoe hare, O'Donoghue and Krebs, 1992; red squirrel, Réale et al., 2003).
Although parturition date varied among years, we could detect no apparent advantage to being born early or late for collared pikas. Their fast growth rate allows pikas to achieve near adult body size by fall and therefore timing of parturition does not seem to significantly influence the survival. However, since the growth data and subsequently the parturition dates are based on individuals that successfully emerged from the nest it is possible that timing may affect survival at earlier stages of life, prior to emergence, which is difficult to study in this species. For this reason we are unable to assess the potential effects other life history characteristics, such as birth weight, litter size, number of litters or maternal condition, on subsequent growth and survival, but based on the limited data available we do not think that including these factors would have substantially changed our conclusions.
Pikas in northern latitudes are constrained by the short-growing season, and timing of parturition appears to be influenced by environmental conditions such as snowmelt. In the Yukon, heavier snow accumulations are predicted in the future (Moore et al., 2002), which may result in a later snowmelt and even shorter growing season. It is also predicted that weather patterns may become even more variable and the chance of severe spring storms may increase in frequency (Houghton et al., 2001). Millar (1974) and Smith (1978a) reported that entire litters might be lost in response to severe weather storms during gestation in some pika populations. More subtlety, Kreuzer and Huntly (2003) have shown that birth rates of American pikas in Wyoming declined sharply with later snowmelt in snowbed habitats, but were unaffected by melt date in meadow habitats.
While collared pikas appear to be able to adjust to the conditions we observed in the Yukon over seven years, the predicted changes associated with climate warming may still adversely affect these populations (Franken, 2002). At southern latitudes, Beever et al. (2003) have already documented the local extinction of some populations of American pikas associated with climate warming and other disturbance in the Great Basin. Overall, the cumulative evidence available so far suggests that pikas are sensitive indicators of climate variability and change (Smith 1974; Beever et al., 2003; Li and Smith, unpublished data).
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ACKNOWLEDGMENTS |
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We are grateful to the many people who contributed to this study, especially J. Boulanger and A. Sykes. E. Beever, C. Gillies, J. Roland, F. Schmiegelow and A. T. Smith provided helpful comments on earlier versions of this paper. Financial support was provided by the Natural Sciences and Engineering Research Council of Canada, the Canada Research Chairs Program, the University of Alberta, the Canadian Circumpolar Institute, the Northern Scientific Training Program (DIAND), and Mountain Equipment Co-op.
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FOOTNOTES |
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1 From the Symposium Biology of the Canadian Arctic: A crucible for change in the 21st Century presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Canada.
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