THE EFFECT OF SEX RATIO AND MALE AGE STRUCTURE ON REINDEER CALVING

THE EFFECT OF SEX RATIO AND MALE AGE STRUCTURE ON REINDEER CALVING ØYSTEIN HOLAND, Agricultural University of Norway, Department of Animal Sciences, Box 5025, N-1432 Ås, Norway KNUT H. RØED, Department of Morphology, Genetics and Aquatic Biology, Norwegian School of Veterinary Medicine, Box 8146, Dep. N-0033 Oslo, Norway ATLE MYSTERUD, Department of Biology, Division of Zoology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway JOUKO KUMPULA, Finnish Game and Fisheries Research Institute, Reindeer Research Station, Fin-99910 Kaamanen, Finland MAURI NIEMINEN, Finnish Game and Fisheries Research Institute, Reindeer Research Station, Fin-99910 Kaamanen, Finland MARTIN E. SMITH, Agricultural University of Norway, Department of Animal Sciences, Box 5025, N-1432 Ås, Norway Abstract: In polygynous ungulates, biologists commonly assume that the role of males in population dynamics is negligible since the male s physiological capacity to inseminate females normally will not be a limiting factor for calving rates. Recently, however, research indicates that the role of males may be more important than previously acknowledged because availability of males may affect conception dates and hence calving dates and synchrony. In many harvested or otherwise managed populations, a sex ratio highly skewed toward females and a young male age structure often exist. Both a skewed sex ratio and male age structure may affect conception times and may delay calving dates. We manipulated the sex ratio and male age structure in herds of reindeer (Rangifer tarandus) fenced in large-scale enclosures (14 15km 2 ). We compared calving rates, dates, and synchrony as well as (1) birth and autumn weights of calves among a skewed sex ratio and yearling males only, (2) a skewed sex ratio and an even male age structure, and (3) an even sex ratio and even male age structure. As predicted, calving dates were earlier in the treatment with an even sex ratio and even male age structure compared to the 2other treatments. Neither sex ratio nor male age structure impacted calving rates or birth synchrony. Timing of births is important for the survival of newborns, and this should be considered when harvesting or otherwise managing populations of polygynous ungulates. JOURNAL OF WILDLIFE MANAGEMENT 67(1):25 33 Key words: conception, demography, female reproductive performance, Finland, harvesting, Rangifer tarandus, reindeer, rut. Increased attention is focusing on how sex and age structure affect the dynamic of ungulate populations (Tuljapurkar and Caswell 1997, Coulson et al. 2001, Gaillard et al. 2001). Age structure is important since young and old individuals typically have lower survival rates than prime-aged individuals (Caughley 1966; Gaillard et al. 1998, 2000b), and for a given age, males frequently have lower survival rates than females (Coulson et al. 1997, Clutton-Brock et al. 1997). Also, variation in proportion of females breeding (Reimers 1983, Gaillard et al. 1992), twinning rates (Andersen and Linnell 1997, Keech et al. 2000), and calving dates (Bunnell 1982, Festa-Bianchet 1988) may have a considerable impact on population growth rates. Variation in female reproduction typically has been related to factors such as age (Langvatn et al. 1996, Gaillard et al. 2000a), reproductive history (Clutton-Brock et al. 1983, Sand 1998) and condition (Reimers 1983, Langvatn et al. 1996), predation (review in Linnell et al. 1995), population density (Fowler 1987, Gaillard et al. 1998), climate (Sæther 1997), and their interactions (Coulson et al. 2001). 1 E-mail: atle.mysterud@bio.uio.no 25 In most large herbivores, males typically do not help females raise young, and a polygynous mating system is the most common (Clutton-Brock 1989, Davies 1991). The male s physiological capacity to inseminate females normally will not be a limiting factor, although it may limit the number of offspring fathered by the dominant male in species with intense sperm competition (Soay sheep [Ovis aries]; Preston et al. 2001). For example, anecdotal information indicates that 1 mature reindeer bull can serve 50 females when confined to limited areas in production systems (Skjenneberg and Slagsvold 1968). Since females are the most important component of any herbivore population, the role of males in population dynamics has been largely ignored. Indeed, population dynamics of large polygynous ungulates often are modeled using only female numbers (Milner-Gulland et al. 2000). However, many, if not most, large herbivore populations in Europe and North America are harvested. Harvesting may have a considerable impact on population dynamics (Fryxell et al. 1991, Solberg et al. 1999) and largely affect the age and sex structure (Beddington 1974, Ginsberg and Milner-Gulland 1994, Langvatn and Loi-

26 POPULATION SEX- AND AGE-STRUCTURE AND REINDEER CALVING Holand et al. J. Wildl. Manage. 67(1):2002 son 1999). Intensive hunting of ungulate males, either for trophies as in Scotland (Clutton-Brock and Albon 1989) or increased meat production as in Fennoscandia (Langvatn and Loison 1999), often profoundly skews sex ratios toward females and skews age structure toward younger males. The effect of skewed sex ratio hypothesis (H 1 ). In polygamous species with a fixed, narrow birth interval, effects of skewed sex ratios may impose limitations concerning a male s ability to fertilize many females within a short breeding season (Ginsberg and Milner-Gulland 1994, White et al. 2001, but see also Laurian et al. 2000). Delayed conception may delay birth dates (Skjenneberg and Slagsvold 1968, Mitchell and Lincoln 1973, Noyes et al. 1996). If mating does not occur during the first ovulation cycle, reovulation occurs about 20 25 days later (Guinness et al. 1971). In northern regions, timing of birth is important to maximize access to plants with peak protein levels (Festa-Bianchet 1988) and/or as a predator swamping strategy (Bergerud 1975). A less synchronous calving period and a higher proportion of late-born calves may occur in populations when sex ratios are highly skewed toward females. Also, deer farmers assume that a threshold proportion of males is necessary to secure high fecundity (Haigh and Hudson 1993). A highly skewed sex ratio toward females may decrease calving rates (Skogland 1989, Haigh and Hudson 1993). The effect of skewed male age structure hypothesis (H 2 ). Recent studies on the rutting behavior of strongly polygynous species suggest that male age structure also may potentially affect calving times. Fallow deer (Dama dama) adjusted timing of estrus to the age of available males (Komers et al. 1999). In elk (Cervus elaphus), conception dates occurred earlier when more prime-aged bulls compared to yearling bulls were present and rutting became more synchronous (Noyes et al. 1996). During this study, however, the total number of bulls/100 cows increased from 20to 34and female condition was not controlled for (Noyes et al. 1996). Similar relationships also have been reported in many domestic ungulates (Sadleir 1969). So far, no controlled manipulation of sex ratios or male age structure comparable to harvested populations has been conducted to test whether these factors affect calving rates, dates, and synchrony. Reindeer is a strongly polygynous species (Skogland 1989) and is well suited to a study of the effects of skewed sex ratios and male age structure on population dynamics. We manipulated the sex ratio (H 1 ) and age structure of males (H 2 ) in herds of semidomestic reindeer to determine effects on calving rates, calving dates, and synchrony as well as birth weight and autumn weight of calves. STUDY AREA AND EXPERIMENTAL ANIMALS We conducted our study at the Kutharju Field Reindeer Research Station in Kaamanen, Finland (69 N, 27 E) in the northwest (Lauluvaara, 13.8 km 2 ) and southeast (Sinioivi, 15 km 2 ) sections. The area (43 km 2 ) is fenced and divided into smaller sections. Birch (Betula spp.) and pine (Pinus sylvéstris) forests with numerous lakes and bogs dominate the habitat in these areas. The experimental herd numbered about 120 animals and received supplementary feeding during winter only. METHODS Study Design Limitations set by the infrastructure and economy did not allow us to conduct a fully replicated experiment. Rather, prior to the breeding seasons in 1996and 1997, we separated the females into 2 isolated herds of about 40 females each such that weights, ages, and number of calves at foot were similar in both groups (Table 1). We manipulated the sex ratio and male age structure during rut between the 2years and the 2herds as follows: Treatment 1: Skewed sex ratio young males only (Lauluvaara site 1996 and 1997) Treatment 2: Skewed sex ratio even male age structure (Sinioivi site 1996) Treatment 3: Even sex ratio even male age structure (Sinioivi site 1997) We did not make a herd with even sex ratio and young males only because this cannot be obtained in either natural or harvested populations. All males had radiocollars attached. Females were individually marked with highly visible collars, each numbered and color-coded. We weighed animals in mid-september prior to their release into the large enclosures and again after the end of main rut in early November. The 2 herds were again joined and stayed together until the next breeding season, separated only during the rutting season. The animals were weighed and transferred to a calving enclosure in late April. Every day during calving, we surveyed the area captured, ear-tagged, sexed, and weighed newborn calves. We weighed the animals again at the end of the calving season.

J. Wildl. Manage. 67(1):2002 POPULATION SEX- AND AGE-STRUCTURE AND REINDEER CALVING Holand et al. 27 Table 1. An overview of manipulated reindeer herds used in our study in the Lauluvaara (northwest) and Sinioivi (southeast) sections of Kutharju Field Reindeer Research Station in Kaamanen, Finland, 1996 1997. Average Weight of Weight of age of 2-yr-old >2-yr-old 1.5-yr-old 2.5-yr-old 4.5 5.5-yr Females females females females males in males in old males Treatment Location Year in % (n) (yr) (kg) (kg) % (n) % (n) in % (n) 1. Skewed sex ratio (young males only) Lauluvaara 1996 88 (46) 6.0 63.2 79.1 13% (6) 1. Skewed sex ratio ( young males only) Lauluvaara 1997 92 (45) 5.5 60.0 76.9 9% (4) 2. Skewed sex ratio (even male age structure) Sinioivi 1996 88 (43) 6.2 60.7 82.9 6 (3) 6 (3) 3. Even sex ratio (even male age structure Sinioivi 1997 73 (48) 5.5 59.3 75.7 14 (9) 9 (6) 5 (3) Statistical Analysis and Possible Confounding Factors. Replication of all treatments was not possible (which is the unfortunate case in most population dynamics studies of large animals). Therefore, any difference between the 2 enclosures (Lauluvaara vs. Sinioivi) or the 2 years (1996 vs. 1997) during the rutting season may be confounding for any treatment effects. To control for the possibility of a spatial bias, we surveyed the habitat composition in the 2 enclosures. We found no significant difference in the composition of the 22habitat types in the 2 areas as estimated from satellite images (M. E. Smith et al., NEEDS EMPLOYER, unpublished data). Thus, any bias due to space was unlikely. To at least partly control for a possible temporal bias, we ran treatment 1in the same enclosure in both years. We assumed that any difference between years for treatment 1 would indicate whether a temporal bias may have affected the experiment. Note, however, that the herds were separated only during the brief rutting season. Calving dates and calf body weight. We used general linear models to test for treatment effects on calving dates and calf weight at birth (May/Jun) and in autumn (Sep). In the analysis, we controlled for possible confounding factors such as female age (and a second-order term for age [Bérubé et al. 1999, Ericsson et al. 2001]), female body weight, previous (last year) calving, and calf sex. We did this so that possible differences in the female segment of the population would not affect the results with regard to the treatment effect. We used a logarithmic transformation of calf body weight to obtain residuals with constant variance. We used parameter estimation (mean; 95% CI) to test for differences in calving dates and weights, which is equivalent to using type III tests (Venables and Ripley 1994). We used the Akaike s Information Criterion (AIC) to compare models (Venables and Ripley 1994). Calving rates. We used logistic regression to test for effects of treatment on calving rates (Hosmer and Lemeshow 1989, Venables and Ripley 1994). Calving synchrony. Birth synchrony was separated in frequency of very late-born calves (which indicates reovulation and defined as those born 9Jun or later; using χ 2 tests) and in synchrony among calves born in the main period (with F-test for equality of variances; Venables and Ripley 1994). RESULTS Date of calving was significantly earlier in treatment 3 than in treatment 1 (mean = 4.294; CI: 8.251to 0.336) and treatment 2(mean = 4.990; CI: 8.650 to 1.330). No difference occurred between treatment 1 and treatment 2 (mean = 0.754; CI: 2.754to 4.262). Mean calving date was 23 May (day 143) and 22 May (day 142) for treatment 1, in 1996 and 1997 respectively, 23 May (day 143) for treatment 2, and 18 May (day 138) for treatment 3 (Fig. 1). Calving date was not related to female age (mean = 1.534; CI: 3.928 to 0.860), age 2 (mean = 0.058; CI: 0.114to 0.231) or weight (mean = 0.007; CI: 0.143 to 0.157). Calving previous year had no effect on calving time (females 3 years or older; mean = 0.561; CI: 4.395 to 5.517). Year was not a significant factor when added to the model (mean = 1.088; CI: 2.847 to 5.023). The AIC value of the model with treatment and year was lower (AIC = 1,090.9) than for the model with only year (AIC = 1,097.3), indicating that treatment effect was included in the most parsimonious model. There was no effect of year (1996 vs. 1997) on calving dates for treatment 1, which was replicated (t-test, df = 78, t= 0.666, P= 0.508), indicating

28 POPULATION SEX- AND AGE-STRUCTURE AND REINDEER CALVING Holand et al. J. Wildl. Manage. 67(1):2002 8 6 A. Skewed sex ratio young males only (Laukuvaara 1996) 4 2 0 125 130 135 140 145 150 155 160 165 170 175 Calving day (Julian date) 8 6 B. Skewed sex ratio young males only (Laukuvaara 1997) 4 2 0 125 130 135 140 145 150 155 160 165 170 175 Calving day (Julian date) 8 6 C. Skewed sex ratio even male age structure (Sinioivi 1996) 4 2 0 125 130 135 140 145 150 155 160 165 170 175 Calving day (Julian date) 8 6 D. Even sex ratio even male age structure (Sinioivi 1997) 4 2 0 125 130 135 140 145 150 155 160 165 170 175 Calving day (Julian date) Fig 1. Histogram showing births/day for 4 different reindeer herds (A D) in the Lauluvaara (northwest) and Sinioivi (southeast) sections of Kutharju Field Reindeer Research Station in Kaamanen, Finland, 1996 1997. The arrow indicates mean birthdate (adjusted for female age and body weight).

J. Wildl. Manage. 67(1):2002 POPULATION SEX- AND AGE-STRUCTURE AND REINDEER CALVING Holand et al. 29 that there was no strong temporal effect that could confound the results. The most compressed 50% interval of births was 4 days in treatment 3, 7 days in treatment 2, and 6days in treatment 1(1996and 1997). A similar frequency of very late-born calves occurred in the different treatments (treatment 1 vs. treatment 2: df = 1, χ 2 = 0.535, P = 0.465; treatment 1 vs. treatment 3: df = 1, χ 2 = 0.092, P = 0.762; treatment 2 vs. treatment 3: df = 1, χ 2 = 0.188, P = 0.665). After removing these calves, no difference in birth synchrony among treatments was apparent (treatment 1 [1997; df = 38] vs. treatment 3[df = 37]: F= 1.245, P= 0.504; treatment 1 [1996; df = 37] vs. treatment 2[df = 34], F= 1.228, P= 0.548; treatment 2[df = 34] vs. treatment 3[df = 40]: F = 0.740, P = 0.373). No difference in calving rates among treatments was shown (treatment 3 vs. treatment 1: mean = 0.908[CI: 0.540to 2.356]; treatment 2vs. treatment 1: mean = 1.085 [CI: 0.196 to 2.367]; treatment 3 vs. treatment 2: mean = 0.958 [CI: 0.529 to 2.446]). Calving rates were related to female age (mean = 0.957; CI: 0.112to 1.802) and age 2 (mean = -0.064; CI: 0.123to 0.004), but not to female weight (mean = 0.026; CI: 0.027 to 0.079) or to previous year calving (females 3years or older; mean = -0.019; CI: 2.675 to 2.637). Birth weight of calves did not differ among treatments (treatment 3 vs. treatment 1: mean = 0.017 [CI: 0.060 to 0.095]; treatment 2 vs. treatment 1: mean = 0.014[CI: 0.054to 0.082]; treatment 3vs. treatment 2: mean = 0.046 [CI: 0.025 to 0.118]). Birth weight was highest when females were prime aged (mean = 0.082 [CI: 0.033 to 0.132]; age 2 : mean = 0.005[CI: 0.009to 0.002]). Male calves were heavier than female calves (mean = 0.070; CI: 0.016 to 0.124). Birth weight was not related to mother weight (mean = 0.002; CI: 0.001 to 0.004), date of birth (mean = 0.003; CI: 0.007to 0.001), or to previous year calving (females 3years or older, mean = 0.021; CI: 0.074 to 0.115). Autumn (Sep) body weight of calves was higher in treatment 3than in treatment 1(mean = 0.083; CI: 0.021 to 0.144) and treatment 2 (mean = 0.082; CI: 0.005, 0.158). No difference occurred between treatment 2 and treatment 1 (mean = 0.041; CI: 0.011to 0.093). However, when adding year to the model (mean = 0.071; CI: 0.014 to 0.123), no differences occurred between treatments (all P > 0.500). Weights were heavier in 1997 than in 1996 for treatment 1 (mean = 0.075; CI: 0.024 to 0.127). Therefore, the treatment effect was probably due to the confounding effect of year. Autumn weight of calves was not related to female age (mean = 0.040; CI: 0.002 to 0.083), or age 2 (mean = 0.003; CI: 0.006 to 0.001), but increased with female weight (mean = 0.002; CI: 0.000to 0.005). Male calves were heavier (mean = 0.062; CI: 0.020 to 0.103). Calves born earlier were heavier than late-born calves (mean = 0.006; CI: 0.010 to 0.003). Calving previous year had no effect on weights (including only females 3 years or older, mean = 0.042; CI: 0.035 to 0.118). DISCUSSION Our study showed that calving dates were later in the 2 herds with a highly skewed sex ratio, whereas birth synchrony was equal. Recruitment is highly variable in ungulate populations, suggesting that the factors affecting juvenile survival are especially important for population dynamics (Gaillard et al. 1998, 2000b). However, adult survival may be the k-factor at high density (Albon et al. 2000). Timing of births is regarded as crucially important for the survival of newborns (Rutberg 1987). The adaptive value of timing of birth in northern ungulates has been related to matching plant phenology and peak protein levels (Bunnell 1982, Thompson and Turner 1982, Reimers et al. 1983, Skogland 1989, Côté and Festa-Bianchet 2001). For example, late-born bighorn sheep (Ovis canadensis) lambs had lower survival, probably due to inadequate nutrition, as evidenced by low values of fecal crude protein of their mothers (Festa-Bianchet 1988). Delayed birthdate is most likely a result of delayed conception and may decrease summer survival of juveniles. Because females may adjust length of gestation (Berger 1992), we cannot rule out possible differences in gestation lengths between treatments. Although the difference in mean calving dates was less than a week, this may be biologically significant given the very short growth season at northern latitudes. Previous studies of reindeer at our study site in Kaamanen also showed that late calving was associated with increased calf mortality during summer (Eloranta and Nieminen 1986). In addition, because late-born calves were lighter during autumn, they probably also have lower overwinter survival (e.g., red deer [Cervus elaphus], Loison and Langvatn 1998). Another study showed earlier-born bison socially dominant to late-born peers (Green and Rothstein 1993). In addition to the negative effects of late calving on subsequent survival of the calf, delayed calving also may

30 POPULATION SEX- AND AGE-STRUCTURE AND REINDEER CALVING Holand et al. J. Wildl. Manage. 67(1):2002 reduce future fertility of females. Red deer females at Rum, Scotland, suffered a 1% reduction in fertility for every day past the date of median conception in previous year (Clutton- Brock et al. 1987) and late calving also decreased fertility in caribou (Cameron et al. 1993). Calving synchrony may be an important strategy to lower predation rates (Rutberg 1984, Ims 1990, Bowyer 1991, Sinclair et al. 2000, Gregg et al. 2001). A highly synchronous birth period may lead to a swamping effect (Estes 1976, Leuthold 1977). Birth synchrony is common in wild reindeer populations (Skogland 1989) and caribou (Bergerud 1975, Adams and Dale 1998), suggesting strong stabilizing selection pressure for a synchronized calving time in caribou and reindeer (Dauphiné and McClure 1974). Population sex ratio and male age structure did not affect calving synchrony in our study. No effect of treatment on calving rates was apparent in our study, suggesting that a male proportion of approximately 10% seems adequate to secure a pregnancy rate of approximately 85% during main rut. With this sex ratio, even 1.5 year-old males bred females successfully (see Noyes et al. 1996for a similar result in elk). Thus, no support was shown for the hypothesis that an uneven sex ratio or young male age structure affects calving rates in reindeer populations, as has been reported in the literature mainly from single-sire farmed deer production systems in small enclosures (male:female ratios: caribou: 1:12 [Bergerud 1974]; red deer: 1:10 if young males vs. 1:50 if prime-aged males [Haigh and Hudson 1993]; elk: 1:5 if young males vs. 1:25 if prime-aged males [Haigh and Hudson 1993]). Age at puberty of males may fluctuate with their physical condition (Skjenneberg and Slagsvold 1968). All 1.5-year-old males in this study were in good condition, weighing more than 60kg. However, we observed multiple copulations of several females over a 1 2 day period by young males (Lauluvaara, 1997; M. E. Smith et al., EMPLOY- ER?, unpublished data), suggesting that some of them were socially immature, although possibly physiologically mature. In contrast, during 1 day (Sinioivi, 1997), 4 successful copulations by the dominant male were observed within a time span of 6 hr. Assuming that copulation in reindeer is most intense at dusk and dawn, that activity is low during night (Espmark 1964), and if a mature bull is given free access to females, a potential exists for mating at least 10 females per day. The dominant bull in our study herd bred up to 20females (out of about 40bred) during the main rut (K. H. Røed et al., EMPLOYER?, unpublished data). Spatial distribution of females during rut may be an important factor influencing the reproductive success of individual males. Mating strategies in mammals mainly are determined by female dispersion (Ims 1988, Davies 1991). Grouping patterns among ungulates depend on habitat openness, which is positively correlated with group size and hence harem size (Geist and Bayer 1988, Gerard and Loisel 1995). Habitat likely is a key factor shaping the social organization and rutting behavior observed in reindeer (Lent 1965, Kojola 1986). However, recent evidence suggests that variation in female spatial organization during peak rut can occur depending on the availability of males. For instance, in red deer, the number of females using rutting areas increased during rut, possibly since females in larger harems were harassed less frequently (Carranza and Valencia 1999). If females close to ovulation leave a harem, they may be in transit while in heat. Hence, the chance for reovulation is increased resulting in reduced synchrony, though we failed to find solid evidence for this. Estrus is induced through stimuli from sight, sound, and odor provided by the males (McComb 1987, Miquelle 1991, Komers et al. 1999). The females in the herd with an even sex ratio and male age structure were simultaneously exposed to the antagonistic behavior and courtship display of many males, which may lead to earlier onset and synchronize mating (Henshaw 1970, Baskin 1990). We therefore suggest that timing of estrus is the dominating mechanism to determine the calving season in reindeer populations with an even sex ratio. MANAGEMENT IMPLICATIONS Until recently, management of harvested ungulate populations usually have neglected the potential role of males for population productivity. In Norway, populations of both semidomestic and wild reindeer populations have a femalebiased sex ratio and a young male-biased age structure. Managers should consider that such a population structure might delay calving. Regarding the reindeer herds in this study, late calving was associated with lower body weight in autumn. Therefore, although a skew in sex ratio toward females may increase the number of calves in the population, this must be balanced against the negative effects of reduced calf condition. Although we found no effect of a skewed

J. Wildl. Manage. 67(1):2002 POPULATION SEX- AND AGE-STRUCTURE AND REINDEER CALVING Holand et al. 31 sex ratio (even with young males) on calving rates, we urge conservative interpretation of results based on enclosure experiments when applying them to wild populations. The females in this study were in excellent nutritional condition, and effects may possibly vary if females are in poor condition. Further research also should explore how the effects of skewed sex ratio and male age structure on calving might vary with population density. ACKNOWLEDGMENTS We thank V. Tervonen and his crew at Kutuharju Experimental Reindeer Research Station for valuable assistance and logistic support. E. Reimers and E. Ropstad provided helpful comments and suggestions on earlier drafts. The Research Council of Norway and the Norwegian Reindeer Husbandry Research Council supported this research. LITERATURE CITED ADAMS, L. G., AND B. W. DALE. 1998. Timing and synchrony of parturition in Alaskan caribou. 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