Ole-Gunnar Støen Ole-Gunnar Natal dispersal and social organization in in organization and social dispersal Natal brown bears

Norwegian University of Life Sciences • Universitetet for miljø- og biovitenskap Department of Ecology and Natural Resource Management Philosophiae Doctor (PhD) Thesis 2006:6 Natal dispersal and social organization in brown bears

Ole-Gunnar Støen

PhD thesis

Department of Ecology and Natural Resource Management Norwegian University of Life Sciences

Ås, 2006 Contents

Abstract ...... 1 Sammendrag...... 2 List of papers...... 3 Introduction ...... 4 Objectives of the study...... 6 Methods...... 6 The study areas and populations ...... 6 Field and genetic methods...... 7 Main results...... 8 Natal dispersal...... 8 Inversely density-dependent natal dispersal (Paper I)...... 8 Causes of natal dispersal (Paper II)...... 8 Spatial structure...... 9 Home range size in subadults (Paper III)...... 9 Kin-related spatial structure (Paper IV) ...... 9 Sociality and reproduction ...... 10 Delayed primiparity; a consequence of sociality? (Paper V)...... 10 Primiparity in Scandinavian brown bears (Paper VI) ...... 11 Habitat selection...... 11 Preference for undisturbed rugged terrain (Paper VII) ...... 11 Discussion ...... 12 Management implications ...... 17 Acknowledgements ...... 19 References ...... 20 Compilation of papers ...... 25

i Abstract

Dispersal has important implications for population ecology, genetics and conservation of animal populations through the redistribution of individuals, whereas social organization has important implications for individual resource acquisition and reproduction. This study, which used radio-collared and shot brown bears in two areas in Scandinavia, revealed that the spatial distribution of bears was determined by the presence of other bears (i.e. population density), relatedness among adjacent individuals, and habitat quality. Natal dispersal and home range size were inversely density dependent, indicating some sort of territorial behavior in Scandinavian brown bears. The amount of home range overlap among adult females was determined by relatedness, and most related females formed matrilinear assemblages from which unrelated females were excluded. Almost all males and 40% of the females dispersed from their natal area. Inbreeding avoidance seemed to determine natal dispersal in males, whereas competition for philopatry was probably the reason for natal dispersal in females, even if staying close to relatives might entail reproductive suppression. The age of primiparity was higher in philopatric than in dispersing females, possibly due to behavioral reproductive suppression, but the youngest primiparious females (4-year-olds) lost most cubs. Matrilinear assemblages might lead to spatial variation in population dynamics, which implies that monitoring programs of population trends must have a large enough scale to even out this spatial heterogeneity. Harvest that changes the local density of bears may influence dispersal patterns and expansion of brown bear populations. Both males and females showed a strong preference for undisturbed rugged terrain, and because bears are sensitive to human disturbance, a coordination of ongoing recreational developments is needed to avoid further degradation of the brown bear habitat quality in Scandinavia.

1 Sammendrag

Spredning av unge dyr fra fødestedet har en viktig innvirkning på arters populasjonsøkologi, genetikk og forvaltning, fordi dette fører til en romlig omfordelig av individene, mens sosial organisering påvirker individuell ressurservervelse og reproduksjon. Dette studiet, som benyttet radiomerkete og skutte brunbjørner i to studieområder i Skandinavia, fant at fordelingen av bjørn i terrenget avhenger av forekomsten av andre bjørner (dvs. bestandstetthet), slektskap mellom naboer, samt habitatkvaliteten. Spredningen og størrelsen på hjemmeområdet var omvendt tetthetsavhengig, noe som tyder på en form for territoriell adferd hos Skandinavisk brunbjørn. Beslektete voksne hunners leveområder overlappet mer enn ubeslektete, og de fleste beslektete hunner dannet ansamlinger hvorfra ubeslektede hunner ble utestengt. Nesten alle de unge hannene og 40% av hunnene vandret ut fra fødestedet. Den bakenforliggende årsaken til at hanner utvandret var for å unngå innavl, mens konkurranse om å få bli på fødestedet mellom kullsøstre antas å være årsaken til utvandring hos hunner, selvom det å bli på fødestedet kunne føre til reproduktiv undertrykkelse. Alder for førstefødsel var høyere hos gjenværende enn hos utvandrete hunner, muligens på grunn av reproduktiv undertrykkelse, men hunner som fødte første gang i ung alder (4 år gamle) mistet flest unger. Ansamlinger av beslektede hunner kan føre til en romlig variasjon i populasjonsdynamikken. Dette gjør at skalaen i overvåkning av populasjonstrender må være stor nok til å kunne utjevne denne hetrogeniteten. Jakt som endrer den lokale tettheten av bjørn kan påvirke spredningsmønstret og ekspansjonen av brunbjørnbestander. Både hanner og hunner foretrakk uforstyrret kupert terreng, og viser at bjørner er følsomme overfor menneskelig forstyrrelse. Derfor er det nødvendig med en koordinering av den pågående hytteutbyggingen for å unngå en ytterligere forringelse av kvaliteten på bjørnens habitat i Skandinavia.

2 List of papers

Paper I Støen OG, Zedrosser A, Sæbø S, Swenson JE (2006) Inversely density-dependent dispersal in brown bears Ursus arctos. Oecologia (in press)

Paper II Zedrosser A, Støen OG, Sæbø S, Swenson JE. Should I stay, or should I go? Natal dispersal in the brown bear. Submitted

Paper III Dahle B, Støen OG, Swenson JE. Factors influencing home range size in subadult brown bears. J Mammal (2nd revision submitted)

Paper IV Støen OG, Bellemain E, Sæbø S, Swenson JE (2005) Kin-related spatial structure in brown bears Ursus arctos. Behav Ecol Sociobiol 59: 191-197

Paper V Støen OG, Zedrosser A, Wegge P, Swenson JE. Socially induced delayed primiparity in brown bears Ursus arctos. Behav Ecol Sociobiol (2nd revision submitted)

Paper VI Zedrosser A, Dahle B, Støen OG, Swenson JE. Primiparity, litter size and cub survival in a species with sexually selected infanticide, the brown bear. Submitted

Paper VII Nellemann C, Støen OG, Kindberg J, Swenson JE, Vistnes I, Ericsson G, Katajisto J, Kalternborn B, Martin J. Terrain use by brown bears in relation to resorts and human settlements. Manuscript

3 Introduction Dispersal has important implications for population ecology, genetics and conservation through the redistribution of animals. Studies of dispersal are fundamental to many problems in theoretical and applied ecology, such as responses to habitat loss and fragmentation and re- establishment in species recovery programs etc. (Bullock et al. 2002). Natal dispersal is the most common mechanism of natural population redistribution, because the distance moved and proportion of both birds and mammals moving are commonly larger in subadults than in adults (Greenwood 1980, Dobson 1982, Gese and Mech 1991, Paradis et al. 1998, Nelson and Mech 1999). Intra-sexual competition and inbreeding avoidance has been proposed to explain the ultimate causes of natal dispersal and sex-biased dispersal in mammals (Greenwood 1980, Dobson 1982, Waser and Jones 1983, Moore and Ali 1984, Pusey 1987, Wolff 1993, 1994). According to the inbreeding avoidance hypothesis, individuals disperse to avoid mating with related animals, whereas according to the intra-sexual competition hypothesis individuals disperse to avoid competition for mates or environmental resources. Numerous other hypotheses have also been proposed to explain natal dispersal. One example is the resident fitness hypothesis, where females gain fitness through philopatry and the retention of daughters (Wiggett and Boag 1992). Despite many theoretical and empirical studies of dispersal, there is still controversy in the literature about both ultimate and proximate causes of dispersal. Another controversy is about the presence of density dependence in dispersal. Several studies have shown that emigration is more likely to occur at high population densities (Fonseca and Hart 1996, Herzig 1995). However, other studies have found evidence for inverse density dependence in emigration, and almost all studies have found a negative relation between density and immigration (Wolff et al. 1988, Woodroffe et al. 1995, Blackburn et al. 1998, Lambin 1994a, Andreassen and Ims 2001). Natal dispersal patterns are different among social systems in mammals and theoretical models supported by empirical data predict that dispersal should be density independent in non territorial mammals and inversely density dependent in territorial species (Wolff 1997). In contrast to birds, where natal dispersal is usually female biased, natal dispersal in mammals is mostly male biased (Greenwood 1980, Pusey 1987). The brown bear (Ursus arctos L.) is a large carnivore with a promiscuous mating system (Pasitschniak-Arts 1993, Schwartz et al. 2003, Bellemain et al. 2006) and, as expected in promiscuous mammals

4 (Greenwood 1980), dispersal has been reported to be sex biased in brown bears. Philopatric females establish their breeding home ranges inside or adjacent to their natal areas, whereas males generally disperse relatively long distances from their mothers’ home ranges (Glenn and Miller 1980, Blanchard and Knight 1991, McLellan and Hovey 2001, Kojola et al. 2003, Proctor et al. 2004). The Scandinavian brown bear population was nearly extirpated around 1930 (Swenson et al. 1995). Since then it has increased in numbers and expanded in range (Swenson et al. 1994, 1995). Using data from hunter-killed bears, Swenson et al. (1998) concluded that presaturation dispersal exists in the Scandinavian brown bear, and although there was male- biased dispersal, females that dispersed did not differ from males in distance from core areas of reproduction. This is in contrast to what has been reported in North-American brown bear studies, and may be due to the expansion of the Scandinavian population into suitable habitat available. Social organization has important implications for resource acquisition and reproduction within animal populations. In group living species, cooperative hunting may be important to obtain food (Moehlman 1989), and frequently only the dominant individuals reproduce due to reproductive suppression of subdominants (Wasser and Barash 1983). All mammalian species are more or less social and regularly interact with conspecifics, so being solitary does not mean that the animals do not show social behavior (Sandell 1989). The social organization in mammals varies along a continuum from group-living and gregarious to solitary and strict territoriality (Barnard 2004). Brown bears are generally not considered to be territorial (Pasitschniak-Arts 1993, Schwartz et al. 2003), but dominance hierarchies develop when they aggregate at garbage dumps and at salmon (Oncorhyncus spp.) spawning streams (see IGBC 1987 for a review, Craighead et al. 1995, Gende and Quinn 2004). Home range size is inversely density dependent in Scandinavian brown bears (Dahle and Swenson 2003a), which suggests some form of territorial behavior. Also McLoughlin et al. (2000) found in North American brown bear populations that home range overlap varied with habitat quality, and that home ranges in interior populations were nearly exclusive. Many vertebrate species show intraspecific variation in their social system (Lott 1991). Although wolverines (Gulo gulo) are strictly solitary and territorial carnivores, when females are kept in a highly aggregated social environment in captivity, reproductive failure was related to low social rank (Dalerum et al. in press). This suggests behavioral reproductive suppression and that the social flexibility of solitary carnivores might be greater than commonly observed (Dalerum et al, in press).

5 Objectives of the study

The objective of this study was to examine the process of natal dispersal in the expanding Scandinavian brown bear population and how it affects the spatial structure in a population where suitable unoccupied habitat is available. I further investigated this spatial structure in relation to kinship and how the social organization affected female reproduction.

Methods

The study areas and populations

The study was conducted in two areas in Scandinavia, separated by 600 km (Fig. 1). The southern study area, hereafter named the south, was in Dalarna and Gävleborg counties in south-central Sweden and Hedmark County in southeastern Norway (61º N, 18º E) and contains a hunted bear population. The northern study area, hereafter named the north, was in Norrbotten County in northern Sweden (67º N, 18º E). The north contains three national parks, where hunting is not allowed; however hunting is allowed in the surrounding forestlands. The rolling landscape in the south is covered with coniferous forest, dominated by Scots pine (Pinus sylvestris) or Norway spruce (Picea abies), whereas in the north, the landscape is mountainous, with altitudes up to 2000 m and subalpine forest dominated by birch (Betula pubescens) and willows (Salix spp.) below the tree line and coniferous forest of Scots pine and Norway spruce below the subalpine forest. For a detailed description of the study areas see Zedrosser et al. (in press). The density of bears is lower and the home ranges are generally larger in the north (Dahle and Swenson 2003a). In the south almost all cubs are weaned as yearlings, whereas in the north 40% of the litters are weaned as 2 year olds (Swenson et al. 1994, Dahle and Swenson 2003b). The populations also differ in mortality regimes and in the age structure of males (Swenson et al. 2001). Even though hunting within the three national parks in the north is not allowed, there is evidence of intensive poaching in the area (Swenson and Sandegren 1999). The poaching is male-biased, because most of the poaching occurs on snow in early spring when primarily males have emerged from the den. Due to this poaching, there are few adult males and very little male immigration into the northern study area. There is a more evenly distributed male age structure in the south, in spite of a fall hunting season (Swenson et al. 2001a, Bellemain et al. 2006).

6 Field and genetic methods

Brown bears were darted from helicopters with immobilizing drugs (Arnemo et al. in press). All captured bears were weighed and measured, and blood, hair and tissue samples were taken for later analysis. A premolar tooth (P1) was removed from bears not followed from birth for age determination by counting the annuli on a cross-section of the premolar root (Matson et al. 1993). The bears were radio-marked and located approximately weekly during their active period using standard triangulation methods from the ground or the air (Dahle and Swenson 2003a). Dispersing bears were monitored until death or radio-transmitter failure; some were tracked far beyond the areas where bears were captured. The methods used to capture, mark and radio track bears are described by Dahle and Swenson (2003ac). We isolated DNA from the tissue samples taken from marked and hunter-killed bears (Waits et al. 2000; Bellemain 2004). The DNA extractions and amplifications were performed following the protocol described in Waits et al. (2000). Individuals were genotyped using 18 microsatellite loci. We calculated basic genetic data (allelic frequencies, observed and expected heterozygosities and probabilities of identities) using the software Gimlet (Valière 2002). Pedigrees were deduced from field data and genetic analysis using the software PARENTE (Cercueil et al. 2002, Bellemain 2004).

North

Sweden

South

N

100 0 100 200 Kilometers

Figure 1. Map of Sweden with the study areas defined by 100% minimum convex polygons based on 702 and 3717 locations of 24 and 31 radio-collared adult female brown bears in the northern and the southern study areas, respectively.

7 Main results

Natal dispersal

Inversely density-dependent natal dispersal (Paper I)

In this paper we investigated how population densities experienced by 129 individual brown bears (69 females and 60 males), monitored from birth in two study areas, influenced the probability of natal dispersal and natal dispersal distances. Cumulatively 32% and 46% of the females and 81% and 92% of the males dispersed before reaching 5 years of age in the north and south, respectively. The average population density around the study bears was 11/1000 km2 in the north and 29/1000 km2 in the south. Density had a negative effect on both the probability of dispersal and dispersal distances, when controlling for study area, sex and age. Age had a positive effect on dispersal probability, but most males dispersed as 2 year olds, whereas most females dispersed as 3 year olds. Dispersed males had longer dispersal distances than dispersed females for all ages above 1 year, and they had moved more than 3 times the distance for females as 4 years olds. Bears in the south were more prone to disperse and dispersed farther than bears in the north, even if the density was lower in the north. This was probably due to larger home ranges, poaching (bears were shot before they had completed their dispersal), and a lower carrying capacity in the north. The longest recorded dispersal distances were 90 km for a female and 467 km for a male, which were both the longest recorded natal dispersals in male and female brown bears. On average, females moved more than twice the distance, and males moved more than 4 times farther from their natal area in Scandinavia than brown bears in British Columbia, Canada.

Causes of natal dispersal (Paper II)

In this paper we studied the causes of natal dispersal in the two study areas. We analyzed the dispersal probability of 48 individuals (16 males and 32 females) monitored from birth until 4 years of age, which gave a lower sample size than in paper I. We found that males had a higher dispersal probability than females; 94% of the males and 41% of the females dispersed from their natal area. In spite of differences in population density and sex ratio, there was no difference in male dispersal probability between the two study areas, because almost all males dispersed. There was also no difference in mean male age of dispersal between the two areas. Additionally, the number of males around a subadult male did not significantly influence its dispersal probability. These results support the inbreeding avoidance hypothesis as the cause

8 for male natal dispersal. Female natal dispersal probability decreased with increasing maternal age and decreased with increasing body size. However, an interaction between maternal age and body size suggested that the importance of body size for dispersal probability decreased with increasing maternal age. Non-dispersing females stayed closer to their mother than their dispersing sibling sisters in the period between weaning and dispersal, suggesting that a dominance hierarchy among female litter mates based on body size may cause the subdominant sister to disperse. We suggest that dispersal in juvenile female brown bears can be explained by the resident fitness hypothesis.

Spatial structure

Home range size in subadults (Paper III)

In this paper we report sizes of 90 annual home ranges of 66 weaned non-dispersed, sexually immature (1.5- and 2.5-year-old) brown bears in the two study areas and how home range size is influenced by sex, age, body size, food availability and population density. Home range size was larger in males than females and home range size increased with increasing body size, independent of age. Home range size decreased with increasing population density, but less so in females than males. This is consistent with the existence of matrilinear assemblages in female brown bears, where female kin have greater home range overlap than nonkin (Paper VI). This might restrict movement at high densities less for the females relative to males, which disperse away from kin. Although home ranges were larger in the less productive northern study area than in the southern one, home range size was not related to a general index of food availability within a study area.

Kin-related spatial structure (Paper IV)

In this paper we used molecular methods and field data from the two study areas to test whether kin-related spatial structure exists in the brown bear. This was done by determining whether home ranges of adult female kin overlap more than those of non kin, and whether multigenerational matrilinear assemblages, i.e. aggregation of related females, are formed. A total of 288 adult bears (5 years and older) were included in the analysis. Pair wise geographic distance was calculated based on arithmetic centers of localizations of 75 radio-marked females and 67 radio-marked males, and from shot locations of 75 unmarked females and 71 unmarked males, giving a total of 9,566 dyads <100 km apart. Pair wise genetic relatedness between female dyads declined significantly with increasing geographic distance, but no

9 relationship between relatedness and distance was found for male dyads or dyads of opposite sex. Among female dyads, this pattern was consistent in both study areas and among shot and radio-marked animals. The amount of overlap of multiannual home ranges was positively associated with genetic relatedness among adult females across all dyads and in both study areas. Later tests, not included in paper IV, revealed that there was no significant relationship between home range overlap and population density (general linear model, ȕ = -0.001, P = 0.55, df = 54 ), showing that the results were not an artifact of higher density in areas with more related animals. Using pedigrees of adult females, we identified four matrilines consisting of more than three generations or more than five individuals in the south and three such matrilines in the north. Plotting the multiannual home range centers of adult females revealed two types of matrilines: 1) matrilinear assemblages that used an area exclusively and excluded non kin females, and 2) dispersed matrilines spread over larger geographic areas. The variation in matrilinear structure might be due to differences in competitive abilities among females and habitat limitations.

Sociality and reproduction

Delayed primiparity; a consequence of sociality? (Paper V)

In this study we tested whether natal dispersal status influenced age of primiparity in the south. The sample consisted of 18 females successfully monitored until primiparity. Ten daughters remained within their natal area or within their mother’s multiannual home range until they had their first litters, and were defined as philopatric. Eight daughters left their natal area and were never observed again within the natal area, including the year of primiparity, and were defined as dispersers. The average age of leaving the natal area was 2 years. The average age of primiparity was 4.3 years among females that dispersed outside their mother’s home range (n=8) and 5.2 years among philopatric females (n=10). Only overlap with their mother’s home range, and not body size, body mass, growth, local population density or overlap with their father’s home range had a significant influence on the age of primiparity. Due to the low risk of inbreeding and frequent exposure of young females to unrelated males, we conclude that it is resource competition within female hierarchies that causes reproductive suppression in young females.

10 Primiparity in Scandinavian brown bears (Paper VI)

In this study we investigated the effects of primiparity on litter size and cub loss in brown bears in both study areas. The litter size of both the cubs-of-the-year and yearling litters were significantly smaller when the mother was primiparous than when she was multiparous. A primiparous female also lost significantly more cubs than when she was multiparous; however a primiparous mother did not seem to invest less in her offspring than a multiparous mother, because the yearling offspring of primiparous females were not smaller than the yearlings of multiparous females. We found that the probability of cub loss was higher in the area where sexually selected infanticide (SSI) was suggested (south), than in the area without SSI (north). The probability of cub loss for primiparous mothers increased with male turnover (a variable identifying SSI), but was not related to environmental conditions, their body size or population density. Primiparous mothers lost more offspring than multiparous mothers, which suggests that they are less able to or less experienced in defending their offspring. In general, females in the south were primiparous earlier than females in the north, however females raised their first successful litter at the same age in both areas. In the south we found suggestive evidence that females that were primiparous at age 4 had the highest probability of cub loss.

Habitat selection

Preference for undisturbed rugged terrain (Paper VII)

In this study we analyzed habitat use of 106 radio-collared male (51) and female (55) brown bears in relation to terrain ruggedness, habitat type, and distance to towns and resorts in 1985- 2003. In addition, distributions of 145 individual bears were derived from DNA analyses of bear scats collected independently by hunters during 2001. Habitat use derived from radio collar data and scat data revealed similar results. More than 74% of all female bear locations were in the 29% of the area classified as rugged and forested located >10 km from any town or resort, rugged forested habitat near towns or resorts was avoided. Males preferred undisturbed rugged forested terrain types, but also used bogs and flatter terrain > 10 km from towns and resorts more often than females did.

11 Discussion

This study has revealed that the presence of other bears (i.e. relatedness among adjacent bears and population density) and habitat are important factors determining the spatial distribution of brown bears in Scandinavia. Natal dispersal and home range size were inversely density dependent and both males and females showed a strong preference for undisturbed rugged terrain. The amount of home range overlap among female brown bears was determined by relatedness, and related females formed matrilinear assemblages from which unrelated females were excluded. Inbreeding avoidance seemed to determine natal dispersal in males, whereas competition for philopatry was probably the ultimate reason for natal dispersal in females, even if staying close to relatives might entail reproductive suppression. The high proportion of females dispersing in Scandinavia (Paper I) is in clear contrast to the strong female philopatry that has been reported in North American populations (Glenn and Miller 1980, Blanchard and Knight 1991, McLellan and Hovey 2001). This difference might be due to lower densities in relation to carrying capacity and the recent population expansion into unoccupied areas available at the edges of the population (Swenson et al. 1998). The North American studies of dispersal referred to above were in stable or declining populations, with a higher density of bears. The ultimate reason for male natal dispersal can be explained by the inbreeding avoidance hypothesis. This is because similar male natal dispersal behavior was found in two study areas (Paper II), in spite of differences in density and sex ratio (Swenson et al. 2001, Bellemain et al. 2006), and that the density of older males around young males did not significantly influence their age of dispersal (Paper II). North American studies have shown that almost all males leave their natal area (Glenn and Miller 1980, Blanchard and Knight 1991, McLellan and Hovey 2001, Schwartz et al. 2003), despite differences in these factors. However, even if the dispersal behavior in males seems to be similar among different brown bear populations, their natal dispersal distances decreased with increasing population density (Paper I). Cockburn (1985) hypothesized that males, if they disperse to avoid inbreeding, should move shorter distances from their natal site at high than at low densities in expanding populations. This is because there are shorter distances among unrelated animals and increased heterozygosity due to successful migration and fusion of demes in high-density populations. Cockburn’s (1985) hypothesis might explain the shorter dispersal distances in North American males compared to those in Scandinavia. Thus, the longer dispersal distances

12 by Scandinavian males may be due to an increased searching for potential future mates in peripheral areas, which have lower densities of females (Swenson et al. 1998). It is unlikely that the negative effect of increasing density on dispersal distances was due to inbreeding avoidance for females, because 60% of the females are philopatric and the dispersers did not move far enough to be outside the reproductive reach of their fathers (Bellemain et al. 2006, Paper I). The inverse density dependence found for both dispersal probability and dispersal distance in female brown bears (Paper I) might be due to a “social fence”. The social fence hypothesis was first presented by Hestbeck (1982) as an alternative population regulation mechanism in cyclic small mammals. One important assumption of the social fence hypothesis is that aggressive interactions among unfamiliar individuals are more severe than aggressive interactions among familiar individuals. This has been seen in a long- term study on aggregated brown bears in Yellowstone National Park, where the peak in aggression was observed soon after the bears emerged at the feeding sites, followed by a gradual decrease in aggression after the animals had established a dominance hierarchy (Craighead et al.1995). This shows that the highest aggression levels are exerted by bears that are unknown to each other (Craighead et al.1995). The social fence hypothesis describes a process by which both dominants and subdominants maximize their fitness (Hestbeck 1982). The strategy which maximizes their fitness, however, changes with the density. At low densities (relative to carrying capacity), a dominant individual would maximize its fitness by expelling subdominants, and subdominants would maximize their fitness by dispersing into lower density, neighboring habitats. This is presaturated dispersal, i.e. dispersal occurring before the carrying capacity of the habitat has been reached, and has been documented in the Scandinavian brown bear population (Swenson et al. 1998). The inverse density dependent dispersal also demonstrates that natal dispersal is most frequent at low densities (Paper I). At high densities (relative to carrying capacity), where neighboring areas are fully occupied, the social fence hypothesis predicts a different scenario (Hestbeck 1982). Because aggressive interactions among unfamiliar individuals probably are more intense than among familiar individuals, a subdominant minimizes aggressive interactions and potential severe injury by remaining with familiar individuals. The subdominant maximizes its fitness by remaining in the area and continuing to be submissive to the dominant animal(s). If subdominants are relatives of the dominant(s), the dominant(s) maximize(s) its/their inclusive fitness by allowing the subdominants to remain within the common home range. In paper II we show that small female bears are more prone to disperse, which suggests sibling

13 competition for philopatry. However dispersal probability and the importance of size decreased with increasing maternal age. This may be related to the formation of matrilinear assemblages, independent of population density, where older mothers probably are surrounded by more related individuals than younger mothers, thus promoting philopatry among females born to older mothers. Most brown bear studies report extensive intra- and inter-sexual home range overlap (see review in IGBC 1987) and no territoriality (Mace and Waller 1997). However, McLoughlin et al. (2000) found that home range overlap in North American brown bear populations varies geographically, and that home ranges in interior populations were nearly exclusive. The inversely density dependent dispersal (paper I) and inversely density dependent home range size, independent of habitat quality, found in both subadults (paper III) and adults (Dahle and Swenson 2003a) indicate some sort of territoriality among Scandinavian brown bears. Wolff (1997) proposed that vulnerability of altricial young to infanticide is an important determining factor for female territoriality in mammals. In brown bears adult females have been observed to kill cubs of other females (Hessing and Aumiller 1994, McLellan 1994). Thus, protection of young might be one reason for territorial behavior in this species. The reason why territorial behavior has been observed in Scandinavian (paper I and III) and interior populations in North America (McLoughlin et al. 2000) might be due to their similar ecological conditions, which are different from coastal and barren ground populations (McLoughlin et al. 2000). Intraspecific variation in the social system under different ecological conditions is common in many species (Lott 1991). In paper IV we demonstrated that proximity and home range overlap among female brown bears is based on relatedness and not only philopatry. We also found that some matrilines form multigenerational assemblages of related females occupying exclusive areas. This shows that antagonistic behavior and thus territoriality may vary with relatedness among adjacent animals. When resources are not divided among individuals by territoriality, they are often divided by dominance (Lott 1991). Although we were not able to investigate it, a dominance hierarchy may develop within matrilinear assemblages, where younger females stay within the home ranges of related, older females. Dominance hierarchies have been observed in several brown bear populations, especially when aggregated at dumps and at salmon spawning streams (Pulliainen et al. 1983, see IGBC 1987 for a review, Craighead et al. 1995, Gende and Quinn 2004). By becoming a subdominant at high population density, an individual lowers its reproductive potential relative to an individual that disperses at low densities. However the subdominant’s reproductive potential at high density is probably

14 higher when remaining with the group of known animals than by entering a new group (Hestbeck 1982). Reproductive suppression can occur in subdominant females as a result of behavioral dominance by older females (see review by Wasser and Barash 1983) or when young females remain in contact with male relatives and are not exposed to unrelated males (Wolff 1992, Lambin 1994). Such intrinsic reproductive suppression has been documented in several mammalian species, especially among rodents and group-living carnivores (see Wolff 1997). Reproductive suppression by a young female can be adaptive if the individual is responding to its social environment and if withholding reproductive effort would result in greater reproductive success later than if she attempted to breed under current conditions (Wasser and Barash 1983, Wolff 1997). According to Wolff (1997), the threat of infanticide and corresponding suppression is most likely to occur at high densities or when young females have not gained an alpha status. In brown bears this situation may occur when the population density increases and a social fence obstruct dispersal. In this case, females become philopatric and overlap with their mother and other related adult females within matrilinear assemblages. In paper V we found that female philopatry was associated with an increased age of primiparity, suggesting a social suppression of reproduction in philopatric daughters residing within their mother’s home range. Natural selection should favor mothers that allow their daughters to remain in the natal area (which leads to higher fitness) and daughters that suppress their own reproduction when philopatric, thus reducing competition with their mothers. Male brown bear can overlap with their daughters; however there was no significant difference in the age of primiparity between females that dispersed outside their father’s home range and those that overlapped with their fathers until primiparity. Because of the low risk of inbreeding shown by theoretical modeling (McLellan & Hovey 2001) and empirical data showing only 2% incestuous matings, i.e. reproduction between the daughter and her father (Bellemain et al. 2006), we believe that fathers probably have little influence on female primiparity in brown bears. In addition, extensive home range overlap among adult males and a promiscuous mating system, as shown by frequent occurrence of multi-paternal litters (Bellemain et al. 2005), indicate a high exposure of females to unrelated males. Frequent exposure of young females to unrelated males may counteract potential reproductive suppression from related males (McGuire and Getz 1991, Sillero-Zubiri et al. 1996). One reason why female brown bears are mostly philopatric, even if this entails delayed primiparity, might be the fitness advantages of philopatry, i.e. improved survival of the female

15 and her cubs, familiarity with the local area and neighbors, a proven resources base, and the benefits of kin selection (see Wiggett and Boag 1990), that exceed the disadvantage of delayed primiparity. The results in paper VI suggest that females primiparous at age 4, which is the age when most dispersers were primiparous (Paper V), had the highest probability of cub loss. Only females in the south reached primiparity at this age, but the age of first successful litter in both study areas were very similar (Swenson et al., 2001). It is unclear why females primiparous at age 4 have a higher probability of cub loss. It was not related to a larger body size of females that were primiparous at later ages, because body size at primiparity did not influence the probability of cub loss (Paper VI). In addition, observations in more southern parts of Europe show that females can successfully raise cubs already at age 3 (Frkoviü et al. 2001; Zedrosser et al. 2004). It may be that an additional year of experience with other potentially infanticidal bears within the area the female had immigrated to increases a young female’s chance of successfully raising a litter. However it is unknown whether lifetime reproduction is increased by philopatric behavior in brown bears. We were able to test the effect philopatry had on age of primiparity in the Scandinavian population, because of the frequent dispersal of females in the population. In stable continuous populations in North America, where dispersal in females is rare, we probably would not be able to see this effect. Higher densities over larger areas and reproductive suppression of subdominant young females may be one factor explaining the higher age of primiparity observed in North America (Kingsley 1988, McLellan 1994, Schwartz et al. 2005) compared with Scandinavian (Swenson et al. 2001) and other European populations (Zedrosser et al. 2004). Intraspecific variation in the social system that organizes a particular population at a particular time is common in many species (Lott 1991). Dalerum et al. (in press) found that reproductive failure in captive female wolverines was related to low social rank when kept in a highly aggregated social environment. Dalerum et al. (in press) suggested that the social tendencies and physiological mechanisms mediating this reproductive suppression may be viewed as reaction norms to the social environment in wolverines. The social tendencies observed in brown bears in this study might also be viewed as reaction norms to the social environment as seen in wolverines, indicating that sociality in solitary carnivores probably is more flexible than previously assumed.

16 Management implications

Conservation and protection efforts in Sweden during the last 30 years have resulted in population growth and range expansion, but re-colonization has occurred only in a portion of the areas formerly used by bears (Swenson et al., 1994; 1998). Data both from radio-telemetry and scats revealed that undisturbed (>10 km from towns or resorts) forested rugged terrain was the most preferred habitat for both males and females (Paper VII). This preference for undisturbed rugged terrain and the inversely density-dependent dispersal (Paper I) contribute to a spatially heterogeneous abundance of bears over relatively short distances in the landscape. Because brown bears are spatially structured into matrilinear assemblages (Paper IV), this might lead to spatial variation in population dynamics within the whole population and among matrilines, as seen in other species and theoretical studies (Johst and Brandl 1997, Lecomte et al. 2004, Ims and Andreassen 2005). This is a challenge for the management of brown bears in Scandinavia. One important management implication is that the spatial scale of monitoring programs of bear population trends must be large enough to even out this small-scale heterogeneity in population density. Another important management issue is the implication that the inversely density dependent natal dispersal has for harvesting to change the local density of brown bears and influencing dispersal (both frequency and distances) and thus expansion of a population. If the management goal is to keep the population size at a certain level by harvesting the population, but still stimulate geographical expansion of the population, harvest should be directed to the centre of the population, where the density is high. The reduced density due to harvest will stimulate natal dispersal out of these areas and thus expansion of the population. If the management goal is to maintain the population size at a certain level by harvesting and at the same time restrict expansion, the harvest should be directed to the periphery of the population, where the density is low. The increasing density at the centre of the population, due to reduced harvest there, will function as a social fence and reduce dispersal from these areas. In the high density areas reproductive suppression would lead to delayed primiparity and thus reduced reproductive output (Paper V) in addition to other density effects i.e. smaller home ranges, increased territoriality, and increased resource competition. In the high density areas, territoriality and reproductive suppression could contribute to self-regulation of the population (see Wolff 1997), however this has not been documented in brown bears. Another important management implication is the documentation of the sensitivity of brown bears to human disturbance and development, and that females seem to be more

17 sensitive than males (Paper VII). If degradation of brown bear habitat quality in Scandinavia is to be avoided, municipalities must coordinate their planning regarding establishment of resorts and recreational cabins in order to provide large undisturbed patches of rugged forested terrain and potential bear migration routes between such patches. This will be necessary to fulfill the Swedish goal of establishing female bears throughout the present range of brown bears in Sweden (Riksdagen 2000). Unfortunately, there are presently few national policies in place to secure continuous undisturbed wildlife habitat against piecemeal development (UNEP, 2004).

18 Acknowledgements

This thesis is the product of a four-year PhD scholarship that I received from the Norwegian University of Life Sciences from 2002-2006 and data that has been collected within the Scandinavian Brown Bear Research Project (SBBRP). I would like to thank my supervisor, Professor Jon Swenson, for accepting me in the SBBRP and for his enduring encouragements, excellent supervision and always quick and thorough responses to my work throughout this period. I would also like to thank my second supervisor Professor Per Wegge for his excellent comments always provided the next day, and for prioritizing to assist Jon in supervising me during this last year. I feel fortunate to have been one of ten PhD students that have been part of the SBBPR during these four years. SBBPR arranged PhD meetings for us twice a year, sometimes in exotic places like Sarek National Park in northern Sweden, Deosai National Park in Pakistan and in the French Alps, where we all presented our work and discussed it with the other PhD students. In addition, we met at bear conferences all over the world; Steinkjer, Norway; San Diego, USA and Riva del Garda, Italy. Thank you all for making those meetings so socially nice and scientifically stimulating, and a special thanks to Jon for making this possible. Andreas, Bjørn, Eva, Ali and Andrés all spent some time in Ås. Thank you for good collaboration, constructive feedback and all the great discussions on our (almost) weekly bear meetings. We all stayed in “Brakka” (Futurum) together with several other PhD students that all have contributed to a great working environment and making the lunch the peak of the day. Thanks to all of you. I also want to thank Sven for letting me take part in the exciting fieldwork in the spring when we captured bears from helicopters. I have done much fieldwork around the world, but never been with a more professional team. Thanks to Jonas for housing me when I have been in Sweden and for sharing with me the common challenge we have of being married to “exotic” wives. I also want to thank Christian for taking interest in bears and being a great friend, bringing me along horse riding in Argentina when the PhD work was at its most hectic. Finally, I would like to thank my parents Torill and Asbjørn for the love and support they have given me throughout my life, and for always encouraging me to do what I want with my life. Last but not least I would like to thank my children Ximena and Ignazio, and my dear wife Mariel, for their love, care and companionship, and for sharing with me the happy and sometimes frustrating days that a PhD study entails. It has been four nice years.

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24 Paper I

Oecologia (2006) DOI 10.1007/s00442-006-0384-5

BEHAVIOURAL ECOLOGY

Ole-Gunnar Støen Æ Andreas Zedrosser Solve Sæbø Æ Jon E. Swenson Inversely density-dependent natal dispersal in brown bears Ursus arctos

Received: 1 July 2005 / Accepted: 26 January 2006 Springer-Verlag 2006

Abstract There is considerable controversy in the liter- might be due to lower densities in Scandinavia and re- ature about the presence of density dependence in dis- cent population expansion, with unoccupied areas persal. In this study, we exploit a data series from a long- available at the edges of the population. The longer term study (>18 years) on radio-marked brown bears dispersal distances in female Scandinavian brown bears (Ursus arctos L.) in two study areas in Scandinavia to suggest less social constraints on movements than for investigate how individual-based densities influence the North American females. The longer dispersal distances probability of natal dispersal and natal dispersal dis- by Scandinavian males may be due to increased tances. Cumulatively, 32% and 46% of the females and searching for potential mates in peripheral areas with 81% and 92% of the males dispersed before reaching lower densities of females. These results, in addition to 5 years of age in the northern and southern study area, results of other brown bear studies, suggest that brown respectively. Density had a negative effect on both the bears might be more territorial than previously thought, probability of dispersal and dispersal distances for the and that density is regulated by social interactions. dispersing animals, when controlling for study area, sex and age, making this the first study to show that natal Keywords Dispersal behaviour Æ Dispersal distance Æ dispersal probability and distances are inversely density Population density Æ Population expansion Æ dependent in a large carnivore. We suggest that female– Scandinavia female competition for space caused females in higher density areas to settle closer to their natal area. For males, however, merging of demes, resulting in de- Introduction creased relatedness and increased heterozygosity in an expanding population, might be the reason for shorter Dispersal has important implications for population dispersal distances in males living at higher densities. ecology and conservation through redistribution of This has been hypothesised for small mammals. The animals. The most common mechanism of population high proportion of dispersing female brown bears in redistribution in space is the movement of young ani- Scandinavian compared with North American studies mals, because the distance moved and proportion of animals moving are commonly larger in subadults than Communicated by Diethart Matthies adults in both birds and mammals (Greenwood 1980; Dobson 1982; Gese and Mech 1991; Paradis et al. 1998; O.-G. Støen (&) Æ A. Zedrosser Æ J. E. Swenson Nelson and Mech 1999). Department of Ecology and Natural Resource Management, There is abundant evidence that the dispersal rate Norwegian University of Life Sciences, P.O.Box 5003, 1432, A˚ s, Norway increases with increasing competition for limiting re- E-mail: [email protected] sources. However, there has been considerable contro- Tel.: +47-64-965800 versy in the literature about the presence of density Fax: +47-64-965801 dependence in dispersal (Lambin et al. 2001). Both po- A. Zedrosser sitive and inverse density dependence has been demon- Institute for Wildlife Biology and Game Management, strated, perhaps reflecting that emigration and Department for Integrative Biology, University of Natural immigration show contrasting responses to density Resources and Applied Life Sciences, Wien, Austria (Lambin et al. 2001). Several studies have shown that emigration is more likely to occur at high population S. Sæbø Department of Chemistry, Biotechnology and Food Science, densities (Fonseca and Hart 1996; Hertzig 1995). How- Norwegian University of Life Sciences, A˚ s, Norway ever, other studies have found evidence for inverse density dependence in emigration, and also an even the probability of natal dispersal and natal dispersal clearer negative relation between density and immigra- distances. In this paper, we define natal dispersal as the tion (Wolff et al. 1988; Woodroffe et al. 1995; Blackburn permanent movement out of the natal area. We at- et al. 1998; Lambin 1994a; Andreassen and Ims 2001). tempted to determine whether the probability of dis- The social fence hypothesis predicts an inverse density persal in brown bears was related to density and, if so, in dependence of dispersal, due to increased aggression which way. Because brown bears are generally not within and among groups, and thus inhibition of considered to be territorial (Pasitschniak-Arts 1993; immigration and emigration at high densities relative to Schwartz et al. 2003), we predicted that dispersal dis- carrying capacity (Hestbeck 1982). tance is density independent. Density-dependent dispersal is probably a widespread process and models have shown that density-dependent dispersal strategies almost always evolve (Travis et al. Materials and methods 1999) and might affect population dynamics of spatially structured populations and the probability of local Study area extinction in source-sink populations (Jost and Brandl 1997; Amarasekare 2004; Lecomte et al. 2004). How- This study was conducted in two study areas in Scan- ever, density-dependent dispersal has been the subject of dinavia, separated by 600 km. The southern study area, relatively few empirical studies, possibly because wide hereafter named the south, was in Dalarna and Ga¨ vle- ranges of population densities are rarely encountered borg counties in south-central Sweden and Hedmark over the relatively short duration of many intensive field County in southeastern Norway (61N, 18E). The studies (Sutherland et al. 2002). Thus, many of the northern study area, hereafter named the north, was in studies and models on density-dependent dispersal are Norrbotten County in northern Sweden (67N, 18E). based on small mammals and insects in patchy envi- The rolling landscape in the south is covered with ronments and metapopulations (Midtgaard 1999; Alb- coniferous forest, dominated by Scots pine (Pinus syl- rectsen and Nachman 2001; Lambin et al. 2001; vestris) or Norway spruce (Picea abies), whereas in the Amarasekare 2004). north the landscape is mountainous, with altitudes up to The brown bear (Ursus arctos L.) is a solitary carnivore 2,000 m and subalpine forest dominated by birch with a promiscuous mating system (Pasitschniak-Arts (Betula pubescens) and willows (Salix spp.) below the 1993; Schwartz et al. 2003; Bellemain et al. 2005a). Males tree line and coniferous forest of Scots pine and Norway have larger home ranges than females, but both males and spruce below the subalpine forest. Both study areas are females have intra- and inter-sexually overlapping home described in Dahle and Swenson (2003a). ranges (Pasitschniak-Arts 1993; Dahle and Swenson 2003a). Dispersal in brown bear populations has been reported to be sex-biased, with highly philopatric females Natal areas, dispersal and distance calculations establishing their breeding home ranges in or adjacent to their natal areas and males dispersing long distances from During 1984–2001, 326 different bears were captured their mothers’ home range (Glenn and Miller 1980; with helicopters (203 in the south and 123 in the north), Blanchard and Knight 1991; McLellan and Hovey 2001; of which 284 were radio-marked (172 in the south and Kojola et al. 2003). The Scandinavian brown bear popu- 112 in the north). Offspring of radio-marked females lation has increased in numbers and expanded in range were first captured as yearlings. Age of bears not fol- from four small remnant areas after their near extirpation lowed from birth was estimated by counting the annuli around 1930 to encompass more than half of Sweden and on a cross-section of a premolar root (Matson et al. parts of Norway, today (Swenson et al. 1994; 1995). A 1993). The bears were radiomarked and located weekly previous study using data from hunter-killed bears con- during their active period using standard triangulation cluded that pre-saturation dispersal exists in the Scandi- methods from the ground or the air (Dahle and Swenson navian brown bear (Swenson et al. 1998), suggesting that 2003a). Dispersing bears were followed until death or dispersal in brown bears is either density independent or radio-transmitter failure; some were followed far beyond inversely density dependent. the areas where bears were captured. The methods used Wolff (1997) predicted that dispersal distances should to capture, mark and radiotrack bears are described by be longest at low densities in territorial species, because Dahle and Swenson (2003b). emigrants should experience the least resistance and To determine whether dispersal occurred, natal areas lowest cost. Boonstra (1989) and Lambin (1994a, b) were estimated as 95% minimum convex polygons found that dispersers moved shorter distances at higher (MCP) with the Ranges 6 computer package (Anatrack, densities in Townsend voles (Microtus townsendii), but to 52 Furzebrook Rd., Wareham, Dorset, UK). A 95% our knowledge no published studies have described how MCP was used to avoid the influence of unusual forays density influences dispersal distances in large mammals. and because MCP is the most frequently reported home In this study, we exploit the data series from a long- range estimate reported in brown bear literature (Sch- term study (>18 years) on brown bears in Scandinavia wartz et al. 2003). Most brown bear family groups to investigate how individual-based densities influence (mother and offspring) break up during the mating season in June-July when the cubs are 1.5 years old, but calculated the arithmetic mean of the radio locations of some may stay with their mother for a longer period every radio-marked bear in the year 2002 (the year with (Dahle and Swenson 2003b). Because female brown most radio-marked individuals). We then counted the bears are reported to be highly philopatric, we used number of centres of these adult males, adult females conservative criteria to define dispersers. A bear was and subadult females in the year 2002 that were within a defined as a disperser if it left its natal area and did not distance of 17.84 km from the annual arithmetic mean return before reproducing or reaching reproductive age, centres of all radio-marked bears throughout the entire or did not return within a minimum of 2 years, for those study period. We chose a radius of 17.84 km because it where monitoring ceased before reproduction or reach- approximates an area of 1,000 km2 commonly used as ing reproductive age. Five years was used as the repro- the basis of density measure for bears (McLellan 1994); ductive age for both females and males, because mean the median adult male home range was 833 km2 in this age of first successful litter is 5 years both in the south area (Dahle and Swenson 2003a). The number of cubs and in the north (Swenson et al. 2001; Bellemain 2004). present per adult female was estimated by dividing the We had data from only 1 year after leaving the natal mean litter size in our northern study area (2.4; Swenson area for some bears, which could not be classified et al. 2001) by the mean litter interval (2.6 years; according to these criteria. These bears were categorised Swenson et al. 2001), which resulted in estimated 0.92 as dispersers only if the dispersal distance exceeded the cubs present per adult female per year. Because no mean dispersal distance of dispersers of the same sex and radio-marked subadult males were represented in the age with all locations outside the natal area for two or initial count of bears surrounding a given individual, we more active seasons. multiplied the number of subadult females by 2, An underestimation of the size of a natal area could assuming an even sex ratio (Bellemain 2005b). The 2 possibly overestimate the number of dispersers using individual density index Id per 1,000 km was calculated these criteria. We therefore estimated the natal areas as Id=nad.m+ 1.92nad.f+2nsubad.f, where nad.m is the based on all locations of the mother in the 2 first years of number of radio-marked adult males, nad.f is the number life for the offspring and not only from positions when of radio-marked adult females and nsubad.f is the number accompanied by the offspring. This was done because of of radio-marked subadult females. We subtracted the two reasons: (1) relatively few locations were obtained area within the 17.84-km radius around a bear that ex- annually for each litter due to the long time between tended beyond the borders of our study area using the successive locations, the prolonged period (5–7 months) software ArcView GIS 3.2a (Environmental Systems spent in winter dens, and because using few locations Research Institute, 1992–2000), and extrapolated the underestimates home range sizes when using the MCP number of bears to an area of 1,000 km2. method (Macdonald et al. 1980); and (2) a 95% MCP The Scandinavian brown bear population has re- underestimates the real home ranges of brown bears. By cently expanded in size and distribution (Swenson et al. including all positions of the mother in the second year, 1995). Sæther et al. (1998) reported a population growth we achieved a more reasonable estimate of the real home rate of 14% annually in the northern study area in 1985– range the mother used when accompanied with the cubs. 1995. The numbers of marked animals remained similar To further limit underestimation of range size, only throughout this period, despite a high and comparable natal areas with >15 locations were used (Fig. 1). To capture effort in all years, suggesting stable densities. reduce the effect of autocorrelation in the data, only locations separated by at least 100 h were used. Because animals that are dispersing do not have a defined home range, according to the home range definition by Burt 25 (1943), the dispersal distance was measured from the arithmetic mean centre of the natal area to the median 20 distance of all the annual positions. Thus, only locations outside the natal area were used in this analysis. When calculating the proportions of dispersed bears in differ- 15 ent age classes, animals that were lost (e.g. radio-trans- mitter failure or died) before denning were removed from the analysis for the year when monitoring ceased. 10 Number of natal areas 5 Individual population density index

North 0 16-20 21-30 31-40 41-50 51-60 61-70 71-87 From 1995 to 2002, virtually every adult male and fe- Number of locations male and all subadult female bears were radio-marked in Fig. 1 Histogram of the number of locations used in the estimation our northern study area (Swenson et al. 2001). We of 85 brown bear (Ursus arctos L.) natal areas in Scandinavia The temporally corrected individual density index tId for Team 2005). The logit function was used as link function an individual bear in year y (for y<1995) was then between the probability of dispersal and the linear (1995–y) tId=Id/1.14 , where Id is the individual density expression of the regression variables. The fixed effects index for 1995–2002. The estimates of individual popu- variables of interest were density, study area, sex, year lation density indices in both study areas rely on the and age. In addition, the random effect of the mother assumption that the spatial distribution obtained in 2002 was included to account for possible dependence in (northern study area) and 2001–2002 (southern study dispersal probability for siblings. The random effect in- area, see below) reflect the spatial distribution in both duces a common positive correlation among all siblings. study areas over the entire study period. For several individuals, there are repeated observations of dispersal/non-dispersal, and ideally an additional random term for individual should be included in the South model to account for this dependence. However, when the fixed effect of age is included in the model, a situa- A population size estimate, based on a DNA analysis of tion known as ‘‘complete separation’’ arises, under non-invasive sampling of scats, was carried out in the which the maximum-likelihood estimates for the fixed southern study area in 2001 and 2002 (Bellemain 2005b). effects do not exist. In our case, this means that a perfect We have used these results as a basis to calculate an fit of the model can be accomplished by letting the individual density index around each individual in our variance of the individual random term be sufficiently analysis. For each radio-marked bear, we counted the large and the estimate of the age effect approach infinity. number of genetically identified individuals within a This is because no animal can be both dispersed and 17.84-km radius, based on the centres of the locations of non-dispersed at a given age. Hence, a random term for all scat samples for each individual. The median adult 2 individual cannot be included in the model, and the male home range was 1,055 km in this area (Dahle and estimated effects of the fixed covariates will therefore be Swenson 2003a). Bellemain et al. (2005b) found that at the population level rather than at the individual level. 71% of all radio-marked bears in the southern study Neuhaus et al. (1991) showed that omitting a random area were represented in the genetic sample. To account intercept term in a logistic model reduces the magnitude for the individuals not detected in the non-invasive of the estimated regression coefficients. This means that population sampling, we divided the individual density the true effects at the individual level are probably larger index by 0.71. The resulting individual density index Id (in absolute value) than those found in our analysis. thus can be expressed as Id=ni/0.71, where ni is the The dispersal distances of the animals defined as number of genetically identified individuals surrounding dispersers were analysed by means of a linear mixed a radio-marked bear. We subtracted the area within the model. Dispersal distances were log-transformed (natu- 17.84 km radius around a bear that extended beyond the ral log) before analyses to meet assumptions of nor- borders of our study area, and extrapolated the number 2 mality and equal variance among groups of data (Sokal of bears to a density of 1,000 km , as in the northern and Rohlf 1995). The effects of density, area, sex, year study area. and age on the log-distances were estimated by means of Sæther et al. (1998) estimated a population growth restricted maximum likelihood to account for the ran- rate of about 16% annually in our southern study area dom effects in the model. As for the analysis of dispersal for the period 1985–1995. Population size and density probability in the logistic model, the random effect of estimates based on aerial capture-mark-recapture tech- mother was included to account for possible dependen- niques were carried out in the southern study area in cies among sibling. In addition the random effect of the 1993 (Swenson et al. 1995) and again in 2001 (Solberg individual bear was included, because there were re- et al. 2006). Both estimates yielded very similar results, peated observations of individuals. Due to this random suggesting that, although the population in the general effect, all observations on each animal will be equally area had increased in size and range, densities in the correlated. Two-tailed tests were used and an a level of intensive study area had stayed similar in the period 0.05 was selected for statistical significance. The model 1993–2001. To temporally correct the individual popu- fit was evaluated by investigating residual plots. lation density indices for this period, we assumed stable densities from 1993 to 2002. The temporally corrected individual population density index tId for an individual Results (1993–y) bear in year y (for y<1993) was then tId=Id/1.16 , where Id is the index for 2001–2002. Natal home ranges were calculated for 178 animals (89 females and 89 males) from 85 litters produced by 41 different mothers. These bears were followed for a total Statistical analysis of 595 bear-years (353 female and 242 male bear-years). An average of 48±19 (mean±SD) locations were used A logistic regression model for dispersal, including both for the calculation of 85 natal home ranges using 95% fixed and random effects, was fitted using the glmmPQL MCP and the average area of the natal home ranges was function in R (the MASS library) (R Development Core 257±157 km2. There was a tendency for the natal areas in the north to be larger than in the south, when con- positive effect of sex merely indicates that females dis- trolling for the identity of the mother (F1,39=2.61, perse farther than males at age 0, which is of no bio- P=0.08). Of the 178 animals, 54 (18 females and 36 logical interest. The significant negative interaction males) were classified as dispersers at some time during between sex and age indicates longer dispersal distances their first 4 years of life, whereas 75 (51 females and 24 for males than females for all ages above 1 year (Fig. 3). males) did not disperse before monitoring ceased. Forty- nine animals had too few locations to be classified as dispersers or non-dispersers. Discussion Cumulatively, 32% and 46% of the females and 81% and 92% of the males dispersed before reaching 5 years We found that the natal dispersal probability and dis- of age in the north and south, respectively (Table 1). The persal distances were inversely density dependent in average density index value for bears per year was brown bears in Scandinavia. Density-dependent dis- 11.1±8.9 bears/1,000 km2 in the north and persal has been observed in small mammals and ungu- 29.3±18.9 bears/1,000 km2 in the south. When con- lates (Boonstra 1989; Jones 1986; Lambin 1994a, b; trolling for all the other factors, density had a negative Linnell et al. 1998; Andreassen and Ims 2001), but this is effect on the probability of dispersal (Table 2). Bears in the first study to show that natal dispersal probability is the south were more prone to disperse than bears in the inversely density dependent also for a large carnivore. north and age had a positive effect on dispersal proba- Among badgers, a medium-sized carnivore, there seems bility (Table 2). There was a significant interaction be- to be a lower male dispersal rate (i.e. emigration into tween age and sex in the probability to disperse new groups) in populations with high density compared (Table 2), most likely because most males dispersed as 2- to low density populations, although female immigra- year-olds, whereas most females dispersed as 3-year-olds tion did not correlate with density (Woodroffe et al. (Fig. 2). The insignificant sex effect was retained in the 1995). The inverse density-dependent dispersal probably model, because the interaction between age and sex was contributes to an increased spatially heterogeneous significant. abundance of brown bears in the landscape. Because The longest dispersal distances recorded were 90 km brown bears are spatially structured in matrilinear for a female and 467 km for a male. When controlling assemblages (Støen et al. 2005), this might lead to a for all the other factors density had a significant negative spatial variation in population dynamics within the effect on the dispersal distances (Table 3). Separate population and among matrilines, as seen in other spe- analyses for the two study areas gave similar results cies and theoretical studies (Jost and Brandl 1997; Lec- (results not shown), indicating that the slight difference omte et al. 2004; Ims and Andreassen 2005). in methods for density estimation in the two study areas Theoretical models supported by empirical data pre- was not crucial for the conclusions in the global model. dict that dispersal should be density independent in non- The animals in the south had longer dispersal distances territorial mammals and inversely density dependent in than those in the north and there were significant effects territorial species (Wolff 1997). Dahle and Swenson of sex, age and the interaction between sex and age (2003a) found that home range sizes of both male and (Table 3). Due to the chosen coding of the sex variable female brown bears were inversely related to population (0 for males and 1 for females), the positive and signif- density in Scandinavia. Støen et al. (2005) found that icant age effect is the effect of age on dispersal distances overlap of home ranges in female brown bears in for males. The estimated interaction effect between age Scandinavia was positively related to relatedness, indi- and sex gives the additional contribution of females to cating that brown bears recognize kin and tolerate kin the age effect. Because the interaction effect is negative, more than non-kin. These results, in addition to the the age effect for females is smaller than for males. The results in this study, suggest that brown bears might be

Table 1 Observed and cumulative proportions of Scandinavian brown bears (Ursus arctos L.) dispersing by sex and age in two study areas in Sweden

Area Age (years) Dispersal at a given age (%) Cumulative dispersal (%)

Males (n) Females (n) Males Females

North 1 0.0 (25) 8.3 (24) 0.0 8.3 2 38.9 (18) 0.0 (19) 38.9 8.3 3 37.5 (8) 12.5 (16) 61.8 19.8 4 50.0 (2) 15.4 (13) 80.9 32.1 South 1 11.4 (35) 2.5 (40) 11.4 2.5 2 60.9 (23) 13.3 (30) 65.3 15.5 3 77.8 (9) 30.0 (20) 92.3 40.9 4 0.0 (0) 9.1 (11) 92.3 46.2 Table 2 Logistic regression model of the effects of density, study area, sex and age on the probability of dispersal by brown bears during ages 1 through 4 years, including both fixed and random effects

Explanatory variables b SE df t P

Density À0.0361 0.0144 310 À2.5039 0.012 Area 1.8489 0.5552 32 3.3303 0.002 Sex 0.4720 0.8966 310 0.5265 0.6 Age 1.9417 0.3235 310 6.0028 <0.001 Sex · age À1.0721 0.3759 310 À2.8518 0.005

The global model included: whether not dispersed or dispersed (0 or 1) as a response variable (n=348), density, study area (north = 0, south = 1), sex (male = 0 and female = 1), year, age, and all possible two-way interactions as explanatory variables, and mother identity as a random effect. After a successive exclusion of the least significant terms, but keeping main effects if included in a significant two-way interaction, the final model included the variables presented in the table

60 inbreeding, because of shorter distance between unre- Females n =18 lated animals and increased heterozygosity due to suc- Males n =36 50 cessful migration and fusion of demes. We found this pattern in both males and females. Following Cockburn (1985), this might be the reason for the effect for males, 40 but we do not believe the observed effect was due to inbreeding avoidance for females. Female dispersers 30 moved on average 27.6–28.4 km from the centre of their natal area as 2- to 4-year-olds, which is shorter than the 20 95% distribution of geographic distances between reproductive pairs, which approximated 40 km deduced 10 from parentage analysis (Bellemain et al. 2005a). This

Proportion of dispersing animals (%) means that females would not settle in areas outside the 0 reproductive reach of their father. However, males dis- 1 2 3 4 persed on average 118.9 km as 4-year-olds, which is Age (years) three times this distance, and most likely resulted in avoidance of inbreeding. Boonstra (1989), found a sim- Fig. 2 Age when dispersing Scandinavian brown bears perma- nently left their natal areas ilar effect, i.e. shorter dispersal distances at high density in female meadow voles (Microtus pennsylvanicus), and concluded that it was female–female competition for more territorial than previously thought, and that den- space that caused females in higher density areas to settle sity is regulated by social interactions. Emigration rates closer to their natal area. We suggest that this also oc- of juveniles from their natal sites over a range of den- curs in brown bears. sities have been documented in only a few studies of The dispersal distance could be biased towards territorial mammals and all have shown that emigration shorter distances due to the difficulty in following long rates decrease when densities are high (Wolff 1997). distance dispersers (Rehmeier et al. 2004). Ten (9 males This is the first study to show that density has a and 1 female) of the 54 dispersing brown bears were lost negative effect on dispersal distances in a large mammal. (i.e. lost collar or radio transmitter failure) and never Cockburn (1985) hypothesised that males in expanding located again during the study. Only four of these ani- populations should move shorter distances from their mals had moved longer than the average dispersal dis- natal site at high than at low densities to avoid tance for the sex and age when disappearing, indicating

Table 3 Linear mixed model of the effects of density, study area, sex and age on the dispersal distance by brown bears during ages 1 through 4 years, including both fixed and random effects

Explanatory variables b SE df t P

Density À0.0270 0.0042 124 -6.4916 <0.001 Area 0.5082 0.2078 20 2.4454 0.024 Sex 0.5549 0.2347 31 2.3645 0.025 Age 0.7607 0.0618 124 12.3050 <0.001 Sex · age À0.3992 0.0859 124 -4.6500 <0.001

The global model included: natural log of dispersal distance as a response variable (n=181), and density, study area (north = 0, south = 1), sex (male = 0 and female = 1), year, age, and all possible two-way interactions as explanatory variables, and mother identity and individual identity as random effects. After a successive exclusion of the least significant terms, but keeping main effects if included in a significant two-way interaction, the final model included the variables presented in the table 160 studies of brown bears (Glenn and Miller 1980; Blan- Males 15 chard and Knight 1991; McLellan and Hovey 2001; Females 140 28 Kojola et al. 2003). Even with our conservative criteria for defining dis- 120 persers, 32% and 46% of the females had left their natal area by the age of 4 years in the two study areas, 100 respectively (Table 1). This is in clear contrast to the strong female philopatry that has been reported in 80 North American populations of brown bears (Glenn and Miller 1980; Blanchard and Knight 1991; McLellan and 24 Hovey 2001). In Yellowstone National Park, USA, all

Distance (km) 60 three brown bear females tracked from family break-up had home ranges that overlapped with their natal areas 40 (Blanchard and Knight 1991). McLellan and Hovey 4 (2001) reported from British Columbia, Canada, that 20 6 14 14 ten female brown bears from known mothers that were 3 tracked to adulthood still had some locations inside their 0 1 2 3 4 mothers’ home ranges when 4 years of age. According to our criteria, these females would not have been classified Age (years) as dispersers. Fig. 3 Mean distance (±1 SE) from the centre of the natal area to McLellan and Hovey (2001) reported dispersal dis- annual locations of the Scandinavian brown bears that dispersed tances without distinguishing between dispersers and from the natal area. The numbers above and below error-bars give non-dispersers. To compare dispersal distances between the number of observations in each age and sex class Scandinavia and British Columbia, the distance between the arithmetic means of natal areas and annual locations that the loss of long distance dispersers due to detection for all bears (both dispersers and non-dispersers) were problems was probably not a major bias in this study. calculated. These calculations revealed that both males The detection probability was high, possibly because the and females dispersed farther in Scandinavia than in long dispersers often came into populated areas or areas British Columbia. Sixteen males and 31 females moved with livestock and were shot as part of the management an average of 108.3 km±27.4 (mean±SE) and regime. 15.7 km±2.4, respectively, in Scandinavia, compared to Bears in the south were more prone to disperse, and 23.5±1.7 for 5 males and 6.8±2.5 for 10 females in dispersed longer than bears in the north. The trend to- British Columbia (McLellan and Hovey 2001). The ob- wards larger natal home ranges in the north (P=0.08) served differences between Scandinavia and British might explain this effect, because our criteria for dis- Columbia may be due to differences in densities in persal assumed no overlap with the natal area. In areas relation to carrying capacity between the two areas. The with the same movement pattern but larger home ran- brown bear density in British Columbia was increasing ges, our criteria would result in fewer dispersers. The from an estimated 57/1,000 km2 in 1981 to 80/1,000 km2 shorter dispersal distances in the north can also be ex- in 1986, which is high for an interior population plained by poaching, because a large proportion of the (McLellan 1989) and more than twice the average den- bears moving outside the study area in the north are sity observed in this study in Scandinavia. The remark- killed illegally (Swenson and Sandegren 1999), thus ably high proportion of dispersing females in the biasing the dispersal distances towards shorter distances. Scandinavian populations might be due to the fact that The lower dispersal probability at a given density in the the population was expanding and unoccupied areas north may be explained by differences in carrying were available at the edges of the population. The longer capacity, which should be lower in the north due to dispersal distances in Scandinavian female brown bears lower primary productivity, i.e. less food per unit area might also indicate fewer social constraints on move- for brown bears, which is also suggested by the greater ments than for North American females. However, the home ranges. Thus, there might be less dispersal in the longer dispersal distances by Scandinavian males may be north with the same absolute density, because the area due to an increased searching for potential future mates might be saturated with bears in the north at a lower in peripheral areas, which have lower densities of fe- absolute density than in the south. males (Swenson et al. 1998). The Scandinavian brown bears showed a sex-biased dispersal, and the difference between sexes increased Acknowledgements This study was funded by the Norwegian with age, with more males dispersing than females and Directorate for Nature Management, the Swedish Environmental males moving farther. This is consistent with the general Protection Agency, the Swedish Association for Hunting and Wildlife Management, the Norwegian Institute for Nature Re- pattern in mammals, where females generally are search, WWF Sweden, the Research Council of Norway and the philopatric and males disperse (Greenwood 1980; Dob- Austrian Science Fund Project P16236-B06. We thank the per- son 1982; Pusey 1987). This has also been shown in other sonnel in the Scandinavian Brown Bear Research Project for their assistance in the field and Orsa Communal Forest for field support. Jost K, Brandl R (1997) The effect of dispersal on local population We thank Ole Wiggo Røstad and John Gunnar Dokk for technical dynamics. Ecol Model 104:87–101 assistance in data handling, and Jonas Kindberg for help with GIS Kojola I, Danilov PI, Laitala H-M, Belkin V, Yakimov A (2003) calculations. We also thank Andrew Derocher, Svein Dale, Per Brown bear population structure in core and periphery: analysis Wegge, Harry P. 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Paper II

Should I stay or should I go? Natal dispersal in the brown bear.

Andreas Zedrosser, Ole-Gunnar Støen, Solve Sæbø, and Jon E. Swenson

A. Zedrosser, Department of Integrative Biology, Institute for Wildlife Biology and Game Management, University for Natural Resources and Applied Life Sciences, Peter Jordan Str. 76, A - 1190 Vienna, Austria, and Department for Ecology and Natural Resource Management, Norwegian University of Life Sciences, Pb. 5003, NO - 1432 Ås, Norway. – O.- G. Støen, Department for Ecology and Natural Resource Management, Norwegian University of Life Sciences, Pb. 5003, NO - 1432 Ås, Norway. – S. Sæbø, Department for Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Pb. 5003, NO - 1432 Ås, Norway. – J. E. Swenson, Department for Ecology and Natural Resource Management, Norwegian University of Life Sciences, Pb. 5003, NO - 1432 Ås, Norway, and Norwegian Institute for Nature Management, Tungasletta 2, NO - 7485 Trondheim, Norway

Corresponding author: Andreas Zedrosser Department for Ecology and Natural Resource Management, Norwegian University of Life Sciences, Pb. 5003, NO - 1432 Ås, Norway Email: [email protected]

1 Abstract We studied the causes of natal dispersal of male and female brown bears in two study areas in northern and central Sweden. We found that males had a higher dispersal probability than females, and 94% of the males and 41% of the females dispersed from their natal area. In spite of differences in population density and sex ratio between the study areas, we found no difference in male dispersal probability, because almost all males dispersed. There was also no difference in mean male age of dispersal between the study areas. Additionally, the number of males around a subadult male did not significantly influence dispersal probability. These results support the inbreeding avoidance hypothesis as the cause for male natal dispersal. Female natal dispersal probability decreased with increasing maternal age and decreased with increasing body size. However an interaction between maternal age and body size suggested that the importance of body size for dispersal probability decreased with increasing maternal age. Non-dispersing females were closer to their mother than their dispersing sibling sisters in the period between weaning and dispersal. Female siblings from the same litter seemed to compete for philopatry, suggesting that a dominance hierarchy among female litter mates based on body size may cause the subdominant sister to disperse. However if juvenile females are born into matrilinear assemblages, surrounded mostly by related females, the competition for philopatry may not be as severe as if born into an area surrounded by mostly non-kin females. This is supported by our result that the importance of body size for dispersal decreases with increasing maternal age. We suggest that dispersal in juvenile female brown bears can be explained by the resident fitness hypothesis.

2 Introduction Dispersal is often a multi-cause phenomenon that is conditioned by different factors operating at different ontogenetic stages during an organism’s life cycle (Ims and Hjermann 2001). In general, dispersing individuals of most bird and mammal species are young (Greenwood 1980). In contrast to birds, where dispersal is usually female biased, dispersal in mammals is often male biased and females remain philopatric (Pusey 1987). Dispersal and philopatry can be viewed as behaviors of individual organisms that have demographic and genetic consequences for the population as a whole (Gaines and McLenaghan 1980, Armitage 1991, Byrom and Krebs 1999). Several hypotheses have been proposed to explain the ultimate causes of natal dispersal in a wide range of species: the inbreeding avoidance hypothesis, where individuals disperse to avoid inbreeding with close relatives (Greenwood 1980, Cockburn et al. 1985, Pusey 1987, Wolff 1993, 1994); the intrasexual mate competition hypothesis, where individuals disperse to avoid intrasexual mate competition (Dobson 1982, Moore and Ali 1984); the resource competition hypothesis, where individuals disperse to increase access to environmental resources (Greenwood 1980, Waser and Jones 1983, Pusey 1987), and the resident fitness hypothesis, where juveniles compete for philopatry (Anderson 1989). However causes of dispersal can differ among species, among populations, and between sexes (Waser and Jones 1983, Moore and Ali 1984, Lidicker and Stenseth 1992), and the various proposed hypotheses are not mutually exclusive (Dobson and Jones 1985). Our study species is a solitary large carnivore, the brown bear (Ursus arctos), a species with a polygynous mating system (Schwartz et al. 2003, Bellemain et al. 2006). Natal dispersal in brown bears has been reported to be sex biased, with highly philopatric females establishing their home ranges in or adjacent to their natal areas and males dispersing long distances from their mothers’ home range (McLellan and Hovey 2001, Støen et al. in press). Almost no female natal dispersal has been reported in brown bear populations in North America (e.g.: McLellan and Hovey 2001), but 32-46% of the natal females disperse from their natal home ranges in Scandinavian brown bear populations (Støen et al., in press). In this study we examine a data series from a long-term study (20 years) of brown bears in two study areas in Scandinavia. The study areas have different population densities (Zedrosser et al. in press), and human influence (poaching) has resulted in a skewed sexratio in one of the areas (Swenson 2001a). This and the large geographical distance (600 km) between the study areas has enabled us to use a “quasi-experimental design” for our study. We define a brown bear as a juvenile from ages 1-4 for both females and males, because

3 mean age of first successful litter was 5 years in both study areas (Swenson et al. 2001a, Støen et al. in press). We aim to investigate the causes of natal dispersal in brown bears, and also answer the question: “which life-history traits make individuals more prone to disperse?”

Hypothesis 1: Natal male brown bears disperse to avoid intrasexual mate competition (mate competition hypothesis) Because of the polygynous mating system of brown bears, it should be unlikely that females disperse to avoid mate competition, as has also been suggested in polygynous arctic ground squirrels (Spermohpilus spp.) (Dobson 1982, Byrom and Krebs 1999). The following predictions of the mate competition hypothesis therefore apply only for male brown bears: 1a) lower male dispersal probability in the area with lower density and with fewer males per female (northern study area); 1b) mean male dispersal age is higher in the area with the uneven sex ratio (northern study area); and 1c) dispersal probability of juvenile males in both study areas is positively related to the number of adult males in the vicinity of a given juvenile male.

Hypothesis 2: Juvenile male brown bears disperse to avoid inbreeding with close relatives (inbreeding avoidance hypothesis) Juvenile female brown bears disperse about 28 km from their natal area as 2-4 year olds in Scandinavia (Støen et al. in press). Bellemain et al. (2006) found that 95% of all reproductive brown bears pairs were located within a 40 km distance in Scandinavia. Hence dispersing juvenile females do not seem to settle in areas outside the reproductive reach of their father. However inbreeding between philopatric females and their fathers does not seem to be a major problem in brown bears, because in our study areas only 2% of all litters resulted from incestuous matings between father and daughter (Bellemain et al. 2006). The following predictions of the inbreeding avoidance hypothesis therefore apply only for male brown bears: 2a) no differences in male natal dispersal probability between the study areas, even with differences in density and sex ratio; 2b) mean dispersal age of juvenile males does not differ between the study areas; and 2c) dispersal probability of juvenile males in both study areas is not related to the number of adult males in the vicinity of a given juvenile male.

Hypothesis 3: Juvenile female brown bears compete for philopatry (the resident fitness hypothesis)

4 The prevalent hypothesis in the literature to explain the causes of female dispersal in mammals is the resource competition hypothesis, where individuals disperse to increase access to environmental resources, such as food or territories (Greenwood 1980, Waser and Jones 1983, Pusey 1987). However female brown bears show some dispersal characteristics that argue against this hypothesis; previous research has shown that related female brown bears form matrilinear assemblages, where members have more home-range overlap than unrelated females (Støen et al. 2005). This implies that there may be certain advantages for subadult females to remain philopatric, despite an increase in resource competition due to home range overlap. Anderson (1989) formulated the resident fitness hypothesis as an explanation for ultimate dispersal in rodents. According to this hypothesis, it is selectively advantageous for adult female rodents to retain their maturing daughters near the natal site and to behave cohesively towards them, provided competition for essential resources is below the point at which these resources become limiting to the mothers’ reproductive success. Sibling daughters should compete for philopatry, and the more dominant sibling should be expected to force the emigration of the subdominant sibling (Wiggett and Boag 1992). Although formulated specifically to explain dispersal in rodents, the resident fitness hypothesis may fit the expectations of female brown bear dispersal better than the resource competition hypothesis. Matrilinear assemblages in brown bears may be formed by philopatry or short- distance dispersal of juvenile female offspring (Støen et al. 2005). As more related females settle around a mother throughout time, this may decrease the competition with unrelated females. We therefore predict from the resident fitness hypothesis that 3a) the probability of juvenile females to disperse is negatively related to maternal age, while controlling for the effects of population density and environmental conditions; 3b) the dispersal probability of juvenile female is positively related to litter size and the number of female litter mates, because competition for philopatry should increase with increasing litter size of females. If female offspring compete for philopatry, then physical advantages may influence the outcome; we therefore predict that 3c) body size is negatively related to natal female dispersal probability. To assess if there is competition among female littermates for philopatry, we predict that 3d) in sibling pairs containing female dispersers and non-dispersers, the non- dispersing sibling is geographically more closely associated with the mother than the dispersing sibling after separation but before dispersal.

5 Material and Methods Study area The study was conducted in two study areas in Scandinavia, separated by 600 km. The southern study area, hereafter named the south, was in Dalarna and Gävleborg counties in south-central Sweden. The rolling landscape in the south is covered with coniferous forest, dominated by Scots pine (Pinus sylvestris) or Norway spruce (Picea abies) and contains a hunted bear population. The northern study area, hereafter named the north, was in Norrbotten County in northern Sweden (67º N, 18º E). The landscape is mountainous, with altitudes up to 2000 m with a subalpine forest dominated by birch (Betula pubescens) and willows (Salix spp.) below the tree line and a coniferous forest of Scots pine and Norway spruce below the subalpine forest. The north contains three national parks, where hunting is not allowed; however hunting is allowed in the surrounding forestlands. The areas differ also in the length of maternal care. In the south almost all cubs are weaned as yearlings, whereas in the north 40% of the litters are weaned as 2 year olds (Swenson et al. 1994, Dahle and Swenson 2003a). The two study areas differed in absolute population density (Zedrosser et al. in press, Støen et al in press). The average density index was 11.1 bears/1000km² in the north and 29.3 bears/1000km² in the south (Støen et al. in press). The study populations differed also in mortality regimes and in their male age structure (Swenson et al. 2001a). Bear hunting was allowed in during the autumn in both areas, except in national parks in the north. There was evidence of intensive poaching in the north (Swenson and Sandegren 1999). There were few adult males and very little male immigration in the northern area and a more evenly distributed male age structure in the south (Swenson et al. 2001a, Bellemain et al. 2006).

Capture, handling and radio telemetry Radiomarked female brown bears with yearling cubs were immobilized from a helicopter in mid-April in the southern study area and in early May in the northern study area, shortly after den emergence. We used 2.5 mg tiletamine, 2.5 mg zolazepam and 0.02 mg medetomidine per kg body mass to immobilize the bears. Atipamezol was used as an antidote for medetomidine (5 mg per 1 mg medetomidine) (Kreeger et al. 2002). A tissue sample was taken for genetic analysis. The head circumference (at the widest part of the zygomatic arch between eyes and ears) was measured with a tape measure and used as a measure of overall size of an individual. Because all bears were captured within a 2-week period in each study area, we did not adjust body size for capture date. Offspring of radiomarked females were first captured as yearlings. The bears were radiomarked and located weekly by telemetry using standard

6 triangulation methods from the ground during their nondenning period (Dahle and Swenson 2003b).

Definition of dispersal To identify individuals as dispersers or philopatrics, we defined a juvenile as a disperser if it left its natal area and did not return before reproducing or reaching reproductive age (i.e. 4 years), or did not return within a minimum of two years (for those followed to reproductive age) (see Støen et al. in press for a more detailed description). Natal areas of radiomarked bears were estimated as 95% minimum convex polygons (MCP) with the Ranges 6 computer package (Anatrack Ltd., 52 Furzebrook Rd., Wareham, Dorset, UK). The natal areas for the offspring were estimated based on all locations of the mother in the two first years of life and not only from positions when accompanied by the offspring. This was done for two reasons. 1) Relatively few locations were obtained annually for each litter due to the long time between successive locations, the prolonged period (5-7 months) spent in winter dens, and because using few locations underestimates home range sizes when using the MCP method (Macdonald et al. 1980). 2) We achieved a more reasonable estimate of the real home range the mother used when accompanied with the cubs by including all positions of the mother during the second year. To further limit underestimation of range size, only natal areas with >15 locations were used. To reduce the effect of autocorrelation in the data, only locations separated by at least 100 h were used (Støen et al. in press).

Individual population density index The population density around each individual (within a radius of 17.84 km, which corresponds to the density of bears per 1000 km2) was estimated in both the north and south, based on the high proportion of radiomarked bears and documented population growth rates (see Zedrosser et al. in press for a more detailed description). In the south, the population size was estimated based on a DNA analysis of scats collected throughout the area in 2001 and 2002 (Bellemain et al. 2005). The individual density index around each radiomarked individual in our analysis was based on the location of individuals genetically identified by the scat sampling (71% of the radiomarked bears were represented in the scats samples (Bellemain et al. 2005)), and the population growth rate (Sæther et al. 1998), which we used to temporally correct the density estimate. No corresponding population estimate was available for the north, but virtually every adult male and female and all subadult female bears were radiomarked (Swenson et al.

7 2001a). We used the locations of radiomarked bears, a correction to include the estimated number of subadult males, and data on growth rate of the population to calculate the individual density index as in the southern study area (Zedrosser et al., in press).

Environmental condition index We used spring body mass of yearlings in a given year and study area as the basis to construct an index of the general food condition of the study populations for each year. Rather than using the actual values and just controlling for sex (Garshelis 1994; Swenson et al. 2001b), we regressed yearling body mass as a function of maternal size, litter size, sex and individual population density. In this way we controlled for the variables that influence yearling mass independently of environmental conditions (Dahle et al., in press). The standardized residuals from this regression were sorted by study area and year, and the average value for each year and area was then used as the food condition index for the year before the yearlings were weighed (Zedrosser et al., in press). In order to estimate the effect of the individually experienced environmental conditions throughout the subadult period on dispersal behavior, we averaged the indices from age 1 to age 4 (Zedrosser et al. in press).

Statistical analysis Our first step was to fit a logistic regression model for the dispersal probability of both sexes, including both fixed and random effects, using the glmmPQL function in R 1.9.0 (R Development Core Team 2005). The logit function was used as a link function between the probability of dispersal and the linear expression of the regression variables. The fixed effects variables of interest were study area, sex, yearling body size, internal relatedness, environmental conditions, litter size and maternal age, while controlling for the effect of population density. In addition, the random effect of the mother was included to account for possible dependence in dispersal probability for siblings. This random effect induces a common positive correlation among all siblings. We used backward elimination for model identification. We used a t test to test whether there was a difference in mean dispersal age of males between the northern and the southern study area. A general linear model was used to test whether age at dispersal of males was influenced by the number of older males present within a 40 km radius around an individual male, while controlling for the effects of body size and population density. This radius was chosen because 95% of all reproductive pairs of brown bears were found within 40 km in our study areas (Bellemain et al. 2006). We therefore

8 considered a radius of 40 km as the potential area of influence by other males on natal male dispersal. We used a paired-samples t test to test whether females, which at age 4 were classified as non-dispersers, were geographically closer to their mother during their yearling year than their female siblings that were classified as dispersers at the age of 4 years. We chose the yearling year to assess potential sibling competition, because females start to disperse as 2- and 3-year-olds (Støen et al., in press). We compared the distance between radio-telemetry positions of the mother, the non-dispersing sibling and the dispersing sibling, taken on the same day. To reduce the effect of autocorrelation in the data, we only used locations separated by at least 100 h. We chose a level of Į” 0.05 for statistical significance, values of Į” 0.1 were considered statistically suggestive. Sample sizes differed among the tests and models due to different selection criteria and the availability of needed variables. The statistical software R 1.9.0 was used in all analyses.

Results We analyzed the dispersal probability of 48 individuals (16 males and 32 females) from 1989- 2002. Eighteen of those individuals were from the northern (5 males, 13 females) and 30 (11 males, 19 females) from the southern study area. Males had a higher dispersal probability than females (Table 1). Fifteen (94%) of the 16 males dispersed and 13 (41%) of the 32 females dispersed. Maternal age and body size as a yearling were negatively related to the probability to disperse, but the interaction between those two variables indicates that the effect of yearling body size became less prominent with increasing maternal age (Table 1). The importance of body size was not due to larger body size of yearling males, because almost all of the males dispersed. Instead our result that smaller individuals had an increased dispersal probability was dependent upon female dispersal patterns. The following variables were removed from the analysis in this order: number of same sex litter mates (ȕ = -0.208, P = 0.757), litter size (ȕ = 0.198, P = 0.832), environmental conditions (ȕ = 0.209, P = 0.794), study area (ȕ = 2.610, P = 0.213), population density (ȕ = -0.052, P = 0.196). There was no significant difference in mean male dispersal age between the north and the south (south: X = 2.08 ± 0.70 years (SD), north: X = 2.45 ± 0.69 years, t test, t = -1.483, P = 0.15, df = 34). The presence of older males did not influence juvenile male dispersal age significantly (general linear model, ȕ = -0.001, P = 0.99, df = 15), when controlling for body

9 size (ȕ = -0.002, P = 0.51), population density (ȕ = -0.0006, P = 0.48) and study area (ȕ = - 0.002, P = 0.62). Yearling females that were not to disperse were significantly closer to the mother on a given day than their yearling female siblings that were to disperse later (paired-samples t test: mean distance between non-dispersers and mother = 7.44 ± 3.69 km, mean distance between dispersers and mother = 10.08 ± 3.69 km, t = 4.10, P < 0.001; we used 67 simultaneous positions of 7 sister pairs from 5 litters with 12 individuals).

Discussion Male natal dispersal We found that males had a higher dispersal probability than females. All males, except one, dispersed from their natal area. The higher dispersal probability in males is consistent with dispersal behavior in other mammals (e.g.: Pusey 1987, Nunes et al. 1997, Ferreras et al. 2004), including ursids (e.g.: McLellan and Hovey 2003, Støen et al. in press). In spite of differences in population density and sex ratio between the study areas, we found no difference in male dispersal probability (support of prediction 2a as opposed to prediction 1a), because all males but one dispersed. There was also no difference in mean male dispersal age between the study areas (support of prediction 2b as opposed to prediction 1b). These results support the inbreeding avoidance hypothesis as the cause for male natal dispersal in brown bears. The mean dispersal distance of 4-year-old males in Scandinavia was 119 km (Støen et al., in press), which is sufficient for inbreeding avoidance, because 95% of the reproductive pairs in Scandinavia were within 40 km (Bellemain et al. 2006). Additionally, the number of males around a subadult male did not significantly influence dispersal probability (support of prediction 2c as opposed to prediction 1c). In roe deer (Capreolus capreolus), subadult males with large antlers experienced more agonism by resident males, and thus dispersed more often (Wahlström 1994). In solitary felids like the Florida panther (Puma concolor coryi) and the tiger (Panthera tigris) aggression of resident adult males toward subadults has been cited as the proximate cause of male dispersal (Maehr et al. 2002, Smith 1993). Our results suggest that male dispersal probability was not significantly influenced by male social structure. Also, antagonism by the mother and/or neighboring females, as documented for example in Columbian ground squirrels (Spermophilus columbianus) (Wigget and Boag 1993), is most likely also not a cause of dispersal in male brown bears, because family breakup in brown bears is most often associated with the presence of an adult male during the mating season (Dahle and Swenson

10 2003c). In addition, most offspring are weaned as yearlings in Scandinavian brown bears, but the mean male dispersal age is older than 2 years. Due to this time interval between weaning and dispersal, maternal aggression seems to be an unlikely stimulus for male dispersal in brown bears. Wolf (1993) reviewed 49 studies on natal dispersal in mammals, and found that it resulted from adult aggression in only four species. We were not able to reliably identify any extrinsic motivating factors for dispersal of subadult male brown bears. Instead much natal dispersal appears to have strong intrinsic components (Pusey 1987). It is interesting to note that the only non-dispersing male reproduced with his mother, and both of these individuals had the same father. This is the only known case of mother-son mating in our study among 107 known reproductive pairs based on reproductive analyses (Bellemain et al. 2006).

Female natal dispersal About 40% of the females in this study dispersed. As predicted from the resident fitness hypothesis, female natal dispersal probability decreased with increasing maternal age (prediction 3a) and decreased with increasing body size (prediction 3c), but the interaction between maternal age and body size suggested that the importance of body size for dispersal probability decreases with increasing maternal age. We found no support for the prediction that litter size and the number of same-sex litter mates influenced dispersal (prediction 3b). However, as predicted (prediction 3d), non-dispersing sisters were closer to their mother after weaning than their dispersing sister. We interpret these results as support for the resident fitness hypothesis as explaining the cause of dispersal in juvenile female brown bears. Our results suggest that female natal dispersal probability decreased with increasing maternal age, which may be related to the formation of matrilinear assemblages among brown bears. The increased overlap in a matriarchy indicates that related females are tolerant of each other (Støen et al. 2005), and related neighboring individuals should be more likely to facilitate philopatric behavior of juvenile females than neighboring non-kin females. This in turn should decrease female natal dispersal probability. Older mothers should be surrounded by a higher number of related females than younger mothers; therefore the daughters of older mothers may face less antagonism. This implies that brown bears can distinguish between related and unrelated individuals. The mechanism behind kin recognition in brown bears is not known, but Mateo (2002) showed that Belding’s ground squirrels produced odors that correlated with relatedness and Tegt (2004) showed that coyotes (Canis latrans) were able to recognize relatedness using odor cues in feces, urine, serum and anal sac secrets. The

11 described pattern may operate independently of density, because matrilinear assemblages were formed both in the core and the periphery of our study populations (Støen et al. 2005), which corresponded with high and low density areas of the brown bear distribution in Scandinavia (Swenson et al. 1998ab, Dahle and Swenson 2003b). Body size seems to be the factor deciding which females remain philopatric, because smaller individuals had a higher dispersal probability. Evidence from Columbian ground squirrels shows that daughters compete among themselves for access to the natal site, because among nonparous siblings, the subordinate sisters appeared ultimately to emigrate (Wiggett and Boag 1992). The authors did not describe which factor(s) caused dominance or subordination in their study, but our results suggest that in brown bears this dominance hierarchy is based on body size. Craighead et al. (1995) have observed dominance hierarchies based on body size in adult brown bears at garbage dumps in Yellowstone National Park. Several studies evaluating the effect of size and condition on dispersal in mammals have found that individuals in better condition or with larger body size were more likely to disperse. Nunes et al. (1996) reported that fat male Belding’s ground squirrels (Spermophilus beldingii) dispersed earlier than lean males. In red deer (Cervus elaphus) stags the birth weight of dispersers was heavier than those of non-dispersers (Clutton-Brock et al. 1982), and in roe deer dispersers were on average heavier than philopatrics (Wahlström and Liberg 1995). In contrast, Hanski et al. (1991) found that smaller individuals dispersed more frequently in the common shrew (Sorex araneus). However the importance of body size for female natal dispersal probability seems to decrease with increasing maternal age. This may be due to the already described pattern of matrilinear assemblages among brown bears. If juvenile females are born into an area surrounded mostly by related females, the competition for philopatry may be not as severe as if surrounded by mostly non-kin females. Contrary to our predictions under the resident fitness hypothesis (prediction 3b), we did not find an effect of litter size or the number of female littermates on dispersal probability in female brown bears. This result is similar to that of Gundersen and Andreassen (1998), who also were unable to show that dispersal rates in root voles (Microtus oeconomus) were associated with litter size. Our negative result may be related to the small litter size of brown bears (on average 1.6-2.4 cubs per litter, McLellan 1994, Schwartz et al. 2003). However, there is indirect evidence for intra-litter competition in brown bears. Dahle et al. (in press) found that the body mass in yearling litters varied up to 29.5% between the heaviest and the lightest individual. This suggests a competition for maternal milk, which may establish a hierarchy among female siblings. This is also suggested by the finding that, after yearlings left

12 their mother, the non-dispersing sibling stayed closer to the mother than the female sibling that later dispersed. Competition for philopatry implies that there is an advantage of philopatry. Dahle et al. (in press) found suggestive support that natural mortality of subadult brown bears increased with decreasing yearling body size, which according to our results would suggest that dispersing individuals were at a higher risk. Also, in a continuous bear population, dispersing daughters will experience competition from non-kin females. This could modify the cost-to-benefit ratio of philopatry versus dispersal and make the option of philopatry more attractive (Gundersen and Andreassen 1998). In addition, because bears are long-lived (Schwartz et al. 2003), territory vacancies in a continuous population should be rare, and a dispersing female may have problems to find a vacant area with sufficient habitat quality.

Acknowledgements The Scandinavian Brown Bear Research Project was funded by the Swedish Environmental Protection Agency, the Norwegian Directorate for Nature Management, the Swedish Association for Hunting and Wildlife Management, WWF Sweden and the Research Council of Norway. We thank the research personnel in the Scandinavian Brown Bear Research Project for their assistance in the field. E. Bellemain carried out the genetics work. P. Wegge and B. Dahle provided useful comments to earlier versions of the manuscript. AZ was financially supported by the Austrian Science Fund project P16236-B06.

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17 Table 1. Results of a logistic regression model, including fixed and random effects, of the probability to disperse in subadult brown bears. The fixed effects variables of interest were study area, sex, yearling body size, environmental conditions, litter size, number of same sex litter mates, and maternal age, while controlling for the effect of population density. The random effect of the mother was included to account for possible dependence in dispersal probability for siblings. Df is degrees of freedom, E is the slope, SE is the standard error, t denotes the t value, and P denotes the significance level. N = 48 (18 in the northern study area, 30 in the southern study area).

Explanatory variables Df E SE tP Sex 27 -10.333 3.835 -2.694 0.012

Body size 27 -2.859 0.934 -3.061 0.005

Maternal age 27 -8.299 3.079 -2.695 0.012

Body size*maternal age 27 0.215 0.079 2.731 0.011

18 Paper III

Correspondence author: Bjørn Dahle Department of Biology, Programme for Experimental and Population Ecological Research, University of Oslo, Postbox 1066, Blindern N-0316 Oslo Norway phone:+4722854588 fax: +47 e-mail: [email protected]

Running head: Home range size in subadult brown bears

FACTORS INFLUENCING HOME RANGE SIZE IN SUBADULT BROWN BEARS

Bjørn Dahle1, Ole-Gunnar Støen2, Jon E. Swenson 2,3

1 Department of Biology, Programme for Experimental and Population Ecological Research, University of Oslo, Postbox 1066 Blindern, N-0316 Oslo, Norway

2 Department for Ecology and Natural Resource Management, Norwegian University of Life Sciences, Postbox 5003, 1432 Ås, Norway

3 Norwegian Institute for Nature Research, Tungasletta 2, N-7485 Trondheim, Norway

1 ABSTRACT Most studies of animals’ home range sizes have focused on adults, and the home ranges of subadults are usually, at best, only mentioned anecdotally. In this paper we report home range sizes of 56 philopatric sexually immature (1.5 and 2.5 years old) brown bears (Ursus arctos) in two Swedish study areas and how size is influenced by sex, age, body size, food availability and population density. Home range size was larger in males than females and home range size increased with increasing body size, but was not related to individual age. Home range size decreased with increasing population density, but less so in females than males, a result consistent with the formation of matrilinear assemblages recently reported in brown bears. Although home ranges were larger in the less productive northern study area than in the southern one, home range size was not related to a general index of food availability.

Key words: body size, brown bear, home range, population density, sex, subadults, Ursus arctos

2 INTRODUCTION Home ranges are the areas in which animals acquire necessary resources and carry out biological requirements for life (Burt 1943). The size of these areas in mammals may be influenced by several factors, such as the mating system, which is strongly related to the spatial distribution of resources (e.g. Emlen and Oring 1977; Clutton-Brock and Harvey 1978; Litvaitis et al. 1986; Boutin 1990). In addition, body mass (Harestad and Bunnel 1979), age (e.g. Cederlund and Sand 1994), population density (e.g. Adler et al. 1997; Dahle and Swenson 2003a) and reproductive status (e.g. Rootes and Chabreck 1993; Dahle and Swenson 2003a, b) may play a significant role. However, most studies have focused on adults only, or the sample size of subadults has been too small to go beyond the purely descriptive stage. Thus, the factors influencing the size of home ranges of subadults are generally unknown. In this study we report home range size of subadult brown bears (Ursus arctos) in relation to 5 factors that are likely to affect home range size. Dispersal in brown bears is reported to be sex-biased, with philopatric females establishing their breeding home ranges in or adjacent to their natal areas and males generally dispersing from their mothers’ home range (Glenn and Miller 1980; Blanchard and Knight 1991; McLellan and Hovey 2001; Proctor et al. 2004). Previous studies using data from hunter-killed and radio-collared bears concluded that pre-saturation dispersal exists in both sexes in the Scandinavian population (Swenson et al. 1998). Dispersing individuals by definition do not possess home ranges (Burt 1943) so we restricted our analyses to philopatric subadult individuals. Sex.ʊ In polygynous and promiscuous species (including the brown bear) males usually have larger home ranges than females (Clutton-Brock 1989; Nugent 1994; Fisher and Lara 1999; Dahle and Swenson 2003a). Subadults (which by definition are not sexually mature) should not be expected to engage in reproductive activities, the main cause for sex differences in home range size of adults in a variety of mammalian species (Emlen and Oring 1977; Clutton-Brock 1989; Sandell 1989; Dahle and Swenson 2003b). For this reason we predicted no sex difference in home range size among subadults. Body mass and size.ʊAt the inter-specific level, home range size in mammals is positively related to body mass (e.g. Harestad and Bunnel 1979; Kelt and Van Vuren 2001). At the intra-specific level, the relationship between home range size and body size is less clear, as the relationship varies from positive (e.g. bobcats (Felis rufus), Knick 1990; male Egyptian mongooses (Herpestes ichneumon), Palomares 1994) to negative (e.g. female Egyptian mongooses, Palomares 1994), and other explanations than the body size hypothesis must explain differences in home range size between the sexes in many sexual dimorphic

3 species (e.g. mule deer (Odocoileus hemionus), Relyea et al. 2000; brown bears, Dahle and Swenson 2003a). To our knowledge, no one in the literature has questioned how body mass influences home range size of subadult mammals. Food resources are probably hard to defend in brown bears, due to their large home ranges (Dahle and Swenson 2003a) and subadults should be subordinate to adults, due to their smaller body size. Body mass is strongly condition dependent in brown bears (Hilderbrand et al. 2000), so body size might be a better measure of metabolic needs than body mass. Thus we predicted a positive relationship between body size and home range size. Age.ʊ Molsher et al. (2005) reported no relationship between age and home range size in feral cats (Felis catus), and Said et al. (2005) found that home range size in adult female roe deer (Capreolus capreolus) was not related to age. Cederlund and Sand (1994) on the other hand found a positive relationship between age and home range size in male, but not female moose (Alces alces). The positive relationship was explained by age-related dominance in males, enabling older males to ensure access to more females by using larger home ranges. Because the subadults we studied were sexually immature, and body size is highly variable within age classes (Dahle et al. in press), we predicted no difference in home range size between age classes, when controlling for body size. Food availability.ʊMcNab (1963) suggested that food controlled home range size through an animal’s size-dependent metabolic rate and the productivity of its habitat. Some studies e.g. Dussault et al. (2005) have reported that food availability has a greater effect on movement rates than the size of home ranges per se. However, usually, home range size decreases as food abundance increases, as individuals obtain sufficient resources in a smaller area (Litvatis et al. 1986; Ims 1987; Boutin 1990; Tufto et al. 1996; Said 2005). We predicted a negative relationship between food availability and home range size. Population density.ʊDahle and Swenson (2003a) reported a negative relationship between population density and home range size in adult brown bears, similar to that reported for other mammalian species, such as e.g. roe deer (Vincent et al. 1995), the Florida key deer (Odocoileus virginianus clavium) (Lopez et al. 2005) and feral hogs (Sus scrofa) (Kiefer and Weckerly 2005). Such a negative relationship may be attributed to food availability (Mares et al. 1982) or interactions among individuals restricting each other’s movement at higher densities, although in most studies it has been hard to separate these effects (Boutin 1990). We expected that subadults should be influenced by population density in the same way as adults and therefore predicted a negative relationship between population density and home range size.

4 MATERIALS AND METHODS Study area.ʊThe study was performed in Dalarna and Gävleborg counties, south central Sweden (61o N, 18o E) and Norrbotten County in northern Sweden (67q N, 18q E). In the southern study area (20,494 km2 hereafter named South) the landscape is covered with coniferous forest, dominated by Scots pine (Pinus sylvestris) or Norway spruce (Picea abies) mixed with deciduous trees in earlier successional stages. Although roads are common, the area is sparsely populated. The mean temperatures in January and July are -7° C and 15° C, respectively. Snow cover lasts from late October/early November until early May and the vegetation period is about 150-180 days (Moen, 1998). The northern study area (11,730 km2 hereafter named North) is covered by northern boreal forest dominated by Scots pine and Norway spruce, but there are extensive subalpine forests dominated by birch (Betula. pubescens) and willows (Salix spp.) and mountains rise to 2000 m. The mean temperatures in January and July are -13° C and 13° C, respectively. Snow cover lasts from beginning of October until late May, and the vegetation period is about 110-130 days (Moen, 1998). Capture and radiomarking.ʊFamily groups, consisting of the mother, usually radiomarked previously, and yearlings, were immobilized from a helicopter in late April-early May. We used 2.5 mg tiletamine, 2.5 mg zolazepam and 0.02 mg medetomidine per kg to immobilize the bears. Atipamezol was used as an antidote for medetomidine (5 mg per 1 mg medetomidine) (Kreeger, Arnemo & Raath, 2002). The age of offspring was known for most captured young from the reproductive pattern of the radiomarked mother. The age of offspring from unmarked mothers was determined from tooth eruption patterns (Jonkel, 1993). Body mass of immobilised bears was measured with a scale, and the head circumference (at the widest part of the zygomatic arch between eyes and ears) was measured with a tape measure and used as a surrogate measure of overall body size. Head circumference should reflect skeletal dimensions, independent of body condition, because fat deposition on the head is small (Derocher & Stirling, 1998b), especially after winter hibernation. Radiotransmitters, were either mounted on collars and placed on the bears, or implanted in the body cavity (Arnemo et al. in press). Bears were located from fixed-wing aircraft, helicopters or from cars about once a week during their active period lasting from April-May to October-November. All capture and handling conformed to the guidelines established by the American Society of Mammalogists (1998), the current laws regulating the treatment of animals in Sweden and were approved by the appropriate Swedish ethical committee (Djuretiska nämden i Uppsala).

5 Home range calculations.ʊ Because dispersing individuals do not posses home ranges while dispersing (Burt 1943), home range calculations of the subadults were based on the locations obtained after the permanent separation from the mother in the years when the bears were philopatric (i.e. frequently located within the natal area). A subadult was defined to have separated permanently when it stopped being together with the mother and the distance between the mother and the offspring were at least 500 m when located the same day. In the South, 95% of the litters are weaned as yearlings (Dahle and Swenson 2003c) whereas only 53% of the litters are weaned as yearlings in the North (Dahle and Swenson 2003d). Subadults were defined as individuals younger than 3 years old, because many females and also some males mate as 3-year-olds (Bellemain 2004). Home ranges were calculated as 95% minimum convex polygons (MCP) with the Ranges 6 computer package (Anatrack Ltd., 52 Furzebrook Rd., Wareham, Dorset, UK). We used 95% MCP to avoid the influence of unusual forays and because MCP is the most frequently reported home range estimate reported in brown bear literature (Schwartz et al. 2003) although they underestimate the home range size when the MCP is calculated from positions obtained at low frequency (Dahle and Swenson 2003a). To determine whether individuals were philopatric, natal areas were estimated as 95% MCP. Because using few locations underestimates home range sizes when using the MCP method (Macdonald et al. 1980) a minimum of 16 locations were used in both the home range and the natal area calculations. Only locations separated by at least 100 h were used in both calculations, which correspond to the minimum time between the weekly localizations of the bears. A bear was defined as philopatric until the year it left its natal area permanently. An underestimation of the size of a natal area could possibly underestimate the number of philopatric individuals using this criterion. We therefore estimated the natal areas based on all locations of the mother in the two first years of life for the offspring and not only from positions when accompanied by the offspring. This was done because of two reasons. 1) Relatively few locations were obtained annually for each litter due to the long time between successive locations and the prolonged period (5-7 months) spent in winter dens. 2) Because a 95% MCP underestimates the real home ranges of brown bears when they are based on positions obtained at a low frequency as in our study. Adult females have relatively stable home ranges between years (Støen et al. 2005) and by including all positions of the mother the second year, we achieved a more reasonable estimate of the real home range the mother used when accompanied with the cubs.

6 Food condition index.ʊWe used spring body mass of yearlings in a given year as the basis to construct an index of the general food condition of the study populations for each year. Like Garshelis (1994) and Swenson et al. (2001) we assume that the mass of yearlings in spring, shortly after den emergence should be strongly related to the food conditions the previous year (i.e. when the offspring were cubs-of-the-year). In addition yearling mass is related to other variables such as maternal size, litter size, sex and individual population density. (Dahle et al. in press). We made a regression with the yearling body mass as a function of maternal size, litter size, sex and individual population density. In this way we controlled for the variables that influence yearling mass independently of environmental conditions (Dahle et al. in press). The standardized residuals from this regression were sorted by study area and year and the average value for each year and area was then used as the food condition index for the year before the yearlings were weighed, i.e. when they were cubs. Thus, in analysis the food condition index based on body mass of yearlings in year n was used as a variable to explain variation in home range size in year n-1. Individual population density index.—The population density around each individual (within a radius of 17.84 km, which corresponds to the density of bears per 1000 km2) was estimated in both the North and South based on the high proportion of radio-marked bears and documented population growth rates (see Zedrosser et al. in press for a more detailed description). In the South, the population size was estimated based on a DNA analysis of scats collected throughout the area in 2001 and 2002 (Bellemain et al. 2005). The individual density index around each radio-marked individual in our analysis was based on the location of individuals genetically identified by the scat sampling, the location of the radio-marked bears (71% of the radio-marked bears were represented in the scats samples (Bellemain et al. 2005)) and the population growth rate (Sæther et al. 1998), which we used to temporally correct the density estimate. No corresponding population estimate was available for the North, but virtually every adult male and female and all subadult female bears were radio- marked (Swenson et al. 2001). We used the locations of radio-marked bears, a correction to include subadult males, and data on growth rate of the population to calculate an individual density index as in the South (Zedrosser et al. in press). Statistical analyses.ʊIn addition to the variables presented in the introduction, we controlled for the effect of study area as an independent variable in the statistical analysis, because the study areas were 600 km apart and brown bears in the North inhabit a less productive and mountainous area and occur at generally lower population densities. Because

7 estimates of home range size are related to the number of locations used (Macdonald et al. 1980), we also included the number of independent fixes as a covariate in the analyses. Home range estimates were transformed into their logarithms (log 10) before analyses to meet assumptions of normality and equal variance among groups of data (Sokal and Rohlf 1995). Because samples were not independent (several individuals had the same mother, and several individuals were measured twice, both at the age of 1.5 and 2.5 years), we used mixed linear models with the mother identity and the bear identity (nested within mother identity) as random variables to analyze variation in home range size. Based on the predicted relationship between the independent variables and home range size and likely interactions between independent variables, a global model was built. The final model was chosen by a stepwise backward elimination procedure of the least significant terms (p>0.05) in the global model. Cook’s distances (Montgomery et al. 2001) were obtained to check whether some individuals had a disproportionate influence on the results. The statistical package R 1.9.0 (R Development Core Team, http://www.R-project.org) was used in all statistical analyses.

RESULTS We estimated 90 annual home ranges from 68, 1.5 and 2.5 year old individuals that where philopatric according to our definition. Contrary to what we predicted, males had larger home ranges than females (Table 1, Figure 2). As predicted, home range size increased with increasing body size (Table 1), and was as predicted not related to age (t = 0.28, P = 0.78). Contrary to what we predicted, home range size was not related to the index of general food conditions in the study areas (t = -0.99, P = 0.34), but home ranges were larger in the less productive northern study area than in the southern study area (Table 1). As predicted, home range size decreased with increasing population density, but less so for females than for males (Table 1). Home range size was not related to the number of fixes used for home range calculation (t = -1.17, P = 0.26).

DISCUSSION We predicted (1) no difference between male and female home range sizes, because they were sexually immature. Our results did not support this prediction and contrast with the findings by Vangen et al. (2001), who reported no difference in home range size of juvenile male and female wolverines (Gulo gulo) before dispersal. The difference between the two species in this aspect might be due to a more male biased dispersal in brown bears than in wolverines (Vangen et al. 2001; McLellan and Hovey 2001), and that this behaviour was initiated earlier

8 in males than females. The larger male than female home ranges might also be related to some other sex specific difference in behaviour in brown bears. The finding that home range size was not related to age, but rather to body size implies that size rather than age influences home range size in subadult brown bears. Similarly Said et al. (2005) found that home range size in adult female roe was not related to age, but increased with increasing body size. The increase in home range size with increasing body size might be explained by increasing energetic demands with increasing body size. The body size hypothesis has been used to explain differences in home range size among different species, (e.g. Harestad and Bunnel 1979; Kelt and Van Vuren 2001), but rarely been tested within one species as an explanation for variation between sexes (Relyea et al. 2000) or among individuals (Knick 1990; Palomares 1994; Said et al. 2005). To our knowledge, this has only been done for adult individuals. An alternative explanation for the positive relationship between body size and home range size can be that large subadults might be dominant over smaller subadults and therefore able to use larger areas. Counter to predicted, home range size was not related to the index of general food availability in the study areas. This is hard to explain, as food availability is considered to be the single most important factor influencing animals’ home range size (e.g. Mares et al 1982; Ims 1987; Said et al. 2005), although food availability is found to influence movement rates more than home range size per se in species such as the moose (Dussault et al. 2005). Perhaps the food availability index did not reflect the actual food availability, as the food condition index is a general index for each study area and year, and thus does not take into account spatial patterns in food availability or general habitat quality within the study areas which might influence the home range size of individuals (McLoughlin et al. 2003). Unfortunately, we have no measurement of home range quality to evaluate this. Further, winter temperatures and thickness of the insulating snow covering the den may also influence yearling body mass (which was used as the basis for the food condition index) through weight loss during winter. Nevertheless, home ranges were larger in the northern study area, which is mountainous and with a shorter growing period and a lower primary production. This suggests that home range size in brown bears is generally related to the net primary production on a large geographical scale as reported by McLoughlin et al. (2000). Our finding that home range sizes decreased with increasing population density, as predicted, confirms the same pattern reported for adult brown bears (Dahle and Swenson 2003a) and for adults of many other solitary species (Vincent et al. 1995; Kiefer and Weckerly 2005; Lopes et al. 2005). Interestingly, home range size was less affected by

9 population density in females than males. This is consistent with the existence of matrilinear assemblages in female brown bears, where female kin have greater home range overlap than non-kin (Støen et al. 2005). This might restrict movement at high densities less for the females relative to males, which disperse away from kin. Because dispersal is inversely density dependent in brown bears (Unpublished data), exploratory movements by subadult males should be shorter when density increases. Body size of yearling brown bears also decreases with increasing population density (Dahle et al. in press), suggesting that population density affects subadult brown bears in similar ways as it affect adults. Our estimated home range sizes are probably underestimates because they are based on positions obtained at a low frequency (>100 h between successive locations). Dahle and Swenson (2003a) found that the 95% MCP for adult brown bears in the same study areas was 1.5 times greater when they were based on more frequently obtained positions (>75 positions with a minimum 12 h interval). However, they should be comparable indices of the actual home ranges and thus appropriate for analysis of the factors that influence the size of home ranges. The average home ranges reported for subadults in the south in this study, are somewhat smaller (t = 3.558, df = 74, P = 0.001) than the corresponding figures reported for adult females with cubs-of-the-year in the same study area (median 124 km2 ), whereas the average home ranges for subadult female sin the north did not differ significantly from those of adult females with cubs of the year (137 km2) (t = 0.646, df = 8, P = 0.537) (Dahle and Swenson 2003a). Subadult males in the north used home ranges that were comparable to the home ranges used by estrous females in that area (median = 280 km2, t = 0.40, df = 5, p = 0.712, one sample t-test), but they are considerably smaller than the home ranges used by adult males (median = 833 km2, t = 24.573, df = 5, p < 0.001) (Dahle and Swenson 2003a). Smith and Pelton (1990) also reported that home ranges of subadult American black bears were similar in size to those used by adults, whereas Glenn and Miller (1980) reported from a small sample size of coastal brown bears that seasonal range size was similar in adult and subadult females, but that subadult males used larger seasonal ranges than adult males. This difference was probably related to dispersal movements by subadult males in that study. We conclude that home range size of philopatric subadult brown bears was larger in males than females despite that they are not involved in reproductive activities. Home range size was not related to age, but increased with increasing body size and decreased with increasing population density. Home ranges were larger in the northern mountainous study

10 area with a lower primary production, but were not related to a general annual index of the food availability in the study areas.

ACKNOWLEDGEMENTS This study was funded by the Norwegian Directorate for Nature Management, the Swedish Environmental Protection Agency, the Norwegian Institute for Nature Research, the Swedish Association for Hunting and Wildlife Management, and World Wildlife Fund Sweden, The Norwegian University of Life Sciences and the Research Council of Norway. We thank personnel in the Scandinavian Brown Bear Research Project for their assistance in the field and A. Zedrosser for comments on a draft of the article.

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15 FIGURE CAPTION

Figure 1. Map of Sweden with the study areas defined by 100% minimum convex polygons of 702 and 3717 locations of 24 and 31 radio collared adult females in the North and the South, respectively.

Figure 2. Mean home range sizes for subadult brown bears in two study areas in Scandinavia. Error bars represent the standard deviation, and the numbers above the error bars represent the number of animals in each category.

16 Table 1. Mixed linear models with log home range size (km2) of 1.5- and 2.5- year-old brown bears (n = 90) in Scandinavia as the dependent variable, study area, sex, head circumference, age, population density and number of positions used to estimate home range size as explanatory variables. The individual subadults (nested within the mother identity) and their mother identity were used as random variables. Test statistics are given for the final model achieved by a stepwise backward elimination procedure of the least significant terms from a global model based on the predicted relationship and likely interactions.

Explanatory variables E SE t P df Intercept 1.039 0.345 3.01 0.0044 42 Study area (south - north) -0.187 0.088 -2.12 0.0458 21 Sex (female - male) -0.236 0.110 -2.15 0.0375 42 Head circumference 0.035 0.006 5.93 <0.0001 21 Population density -0.009 0.002 -4.04 0.0006 21 Sex (female)*population density 0.006 0.003 2.14 0.0447 21

17 Fig. 1

North

Sweden

South

N

100 0 100 200 Kilometers

18 Fig. 2

400 Males 6 Females

) 300 2 9

36 200 39

Home range size (km Home 100

0 North South

19

Paper IV

Behav Ecol Sociobiol (2005) 59: 191–197 DOI 10.1007/s00265-005-0024-9

ORIGINAL ARTICLE

Ole-Gunnar Støen · Eva Bellemain · Solve Sæbø · Jon E. Swenson Kin-related spatial structure in brown bears Ursus arctos

Received: 10 January 2005 / Revised: 12 May 2005 / Accepted: 2 June 2005 / Published online: 2 August 2005 C Springer-Verlag 2005

Abstract Kin-related social structure may influence re- blages exclusively using an area and dispersed matrilines productive success and survival and, hence, the dynamics spread over larger geographic areas. The variation in of populations. It has been documented in many gregarious matrilinear structure might be due to differences in com- animal populations, but few solitary species. Using petitive abilities among females and habitat limitations. molecular methods and field data we tested: (1) whether The influence of kin-related spatial structure on inclusive kin-related spatial structure exists in the brown bear (Ursus fitness needs to be clarified in solitary mammals. arctos), which is a solitary carnivore, (2) whether home ranges of adult female kin overlap more than those of Keywords Dispersal . Genetic distance . Matriline . Social nonkin, and (3) whether multigenerational matrilinear structure . Philopatry assemblages, i.e., aggregated related females, are formed. Pairwise genetic relatedness between adult (5 years and older) female dyads declined significantly with geographic distance, whereas this was not the case for male–male Introduction dyads or opposite sex dyads. The amount of overlap of multiannual home ranges was positively associated with Kin-related social structures have been documented in relatedness among adult females. This structure within many animal populations (Clutton-Brock et al. 1982; matrilines is probably due to kin recognition. Plotting of Gompper and Wayne 1996; Ishibashi et al. 1997). A kin- multiannual home-range centers of adult females revealed related social structure in females may influence reproduc- formation of two types of matrilines, matrilinear assem- tive success and survival and, hence, population dynamics, as demonstrated in microtines (Lambin and Krebs 1993). Matrilines, defined as individuals descending from the Communicated by C. Nunn same ancestral female, have been found to be functional O.-G. Støen () · J. E. Swenson demographic entities in animal populations (Johannesen Department of Ecology and Natural Resource Management, et al. 2000). Studies of kin-related social structures in mam- Norwegian University of Life Sciences, mals have been restricted mostly to group-living species P.O. Box 5003, NO-1432 As,˚ Norway e-mail: [email protected] (Smuts et al. 1987; Gompper and Wayne 1996). The recent Tel.: +47-64-96-58-00 development of highly polymorphic molecular markers has Fax: +47-64-96-58-01 provided the potential to study social structure in solitary species that, due to their elusive nature, would otherwise E. Bellemain Laboratoire d’Ecologie Alpine (LECA), Genomique´ des be difficult to study (e.g., for carnivores, see Waser et al. Populations et Biodiversite,´ Universite´ Joseph Fourier, 1994; Schenk et al. 1998; Ratnayeke et al. 2002). CNRS UMR 5553, BP 53, The brown bear (Ursus arctos) is a solitary carnivore with F-38041 Grenoble Cedex 9, France a promiscuous mating system (Schwartz et al. 2003). Males have larger home ranges than females, but both males and S. Sæbø Department of Chemistry, Biotechnology and Food Science, females have home ranges that overlap intra- and inter- Norwegian University of Life Sciences, sexually (Dahle and Swenson 2003a). Dispersal is sex- P.O. Box 5003 NO-1432 As,˚ Norway biased, with highly philopatric females establishing their breeding home ranges in or adjacent to their natal areas J. E. Swenson and males generally dispersing from their mothers’ home Norwegian Institute for Nature Research, Tungasletta 2, ranges (Glenn and Miller 1980; Blanchard and Knight N-7485 Trondheim, Norway 1991; McLellan and Hovey 2001; Proctor et al. 2004). 192 The mechanism for kin-related spatial structure seems to 41% (n=32) in 1988–1989 (Swenson et al. 1994)to69% be sex-biased dispersal, and should be common, because (n=42) in 2001–2002 (Solberg and Drageseth 2003). Thus the general pattern among polygynous mammals is female a large proportion of adult females were radio-marked dur- philopatry and male dispersal (Greenwood 1980; Waser ing the entire period. Bear hunters in Sweden must report and Jones 1983; Pusey 1987). The observed behaviors of killed bears to the authorities and to provide location of kill, brown bears indicate that this species should demonstrate sex, body mass and several biological samples, including kin-related social structure even if it is a solitary species. In a tissue sample and one premolar tooth. In the south about North American black bears (Ursus americanus), a solitary 95% of all adult bear mortality is caused by hunting (unpub- species with a mating system and dispersal patterns similar lished data). Hunting brown bears is illegal in Norway, so to the brown bear, Rogers (1987) found that adult females most of the bears in Norway were killed as a management recognize their weaned offspring and tolerate them in their action following depredation of domestic sheep (Swenson territories. In addition, adult females actively aided their et al. 1998). daughters in establishing territories by shifting their area The southern study area, hereafter named the south, of use away from the daughter as she approached maturity. was in Dalarna and Gavleborg¨ counties in south-central In contrast, a study using molecular techniques in the same Sweden and Hedmark County in south-eastern Norway species revealed no relationship between relatedness and (61◦N, 18◦E). The northern study area, hereafter named spatial proximity (Schenk et al. 1998). the north, was in Norrbotten County in northern Sweden Although several studies have reported sex-biased dis- (67◦N, 18◦E). The rolling landscape in the south is covered persal and philopatric behavior in female bears, whether with coniferous forest, dominated by Scots pine (Pinus kin-related spatial structure occurs and the extent to which sylvestris) or Norway spruce (Picea abies), whereas in the philopatry and dispersal influence social organization in north, the landscape is mountainous, with elevations up to bear populations remains to be assessed. Manel et al. (2004) 2000 m and sub alpine forest dominated by birch (Betula analyzed the genetic spatial structure of the Scandinavian pubescens) and willows (Salix spp.) below the tree line and brown bear population, using two independent methods coniferous forest below the sub alpine forest. Both study (neighbor joining tree and Bayesian assignment test). Both areas were described by Dahle and Swenson (2003a). methods identified local clusters of genetically related in- dividuals that suggested kin-related social structure. In this study, we assess the spatial kin-related social struc- Genetic data and relatedness index ture in brown bears using field data and molecular genetic techniques. Based on the observed female philopatry and We isolated DNA from 973 tissue samples taken from male dispersal in brown bears, we predict a positive rela- marked and hunter-killed bears (Waits et al. 2000; tionship between relatedness and spatial proximity in fe- Bellemain 2004). The DNA extractions and amplifications males. A consequence of female philopatry is increased were performed following the protocol described in proximity of related females (Waser and Jones 1982). This Waits et al. (2000). Individuals were genotyped using could result in multigenerational clusters of related fe- 18 microsatellite loci. We calculated basic genetic data (al- males, where successfully reproducing females form so- lelic frequencies; observed and expected heterozygosities called “matrilinear assemblages”, i.e., related females ag- and probabilities of identities) using the software Gimlet gregated within subpopulations. Thus we predict increased (Valiere` 2002). We calculated pairwise genetic relatedness home-range overlap with increasing relatedness of females. between pairs of individuals using Wang’s estimator Due to high dispersal rates, we do not predict this pattern (Wang 2002) and the software SPAGeDi 1.0 (Hardy and in males. Vekemans 2002). This estimator, recommended by Blouin (2003), appears to have the most desirable properties among all relatedness indices reviewed, including: (1) low Methods sensitivity to the sampling error that results from estimat- ing population allele frequencies; and (2) a low sampling Study area variance that decreases asymptotically to the theoretical minimum with increasing numbers of loci and alleles This study was based on data from brown bears radio- per locus. Pedigrees of adult female bears were deduced marked or killed by humans in Sweden and Norway. During from field data and genetic analysis using the software 1984–2002, 386 different bears were captured in two study PARENTE (Cercueil et al. 2002; Bellemain 2004). areas in Sweden, separated by 600 km (Dahle and Swenson 2003b). The bears were radio-marked and located approx- imately weekly in their active period using standard trian- Distance calculations and home-range overlap gulation methods from the ground or from the air (Dahle and Swenson 2003a, b). From 1995 to 2002, virtually every We calculated the pairwise geographical distance for each adult brown bear was radio-marked in the northern study dyad of animals using arithmetic centers of multiannual ra- area (Swenson et al. 2001). In the southern study area the dio locations for radio-marked individuals and kill locations proportion of estrous radio-marked females observed with for shot bears. We used multiannual home ranges because a radio-marked male during mating season increased from we had relatively few annual locations for some females 193 and because bears spend 5–7 months in winter dens. Using tween the center of natal area and last locations of 37 four- multiannual home ranges also is justified, because adult fe- year-old females was 15.7 km ± 15.2 (mean±SD) (unpub- males have high fidelity to their home range in successive lished data). Thus, we analyzed only dyads with arithmetic years. The average distance between the arithmetic centers centers <100 km apart for associations between geograph- of successive annual home ranges, based on a minimum of ical distance and relatedness. This also resulted in total 30 annual locations, was only 2.8 km for 16 adult female separation between the study areas. We also computed brown bears that we followed for an average of 5.75 years Spearman’s rank correlations between relatedness and (unpublished data). In the analyses we used only adult bears home-range overlap, and due to the same dependence prop- that had reached the reproductive age of 5 years, the mean erties as discussed, we used permutation tests to test the age at which adult females produce their first successful significance of the estimated correlations. We separately litter (Swenson et al. 2001). Using only adults avoided a analyzed all categories of dyads based on sex (female– false spatial structure due to young animals that had not yet female, female–male and male–male), data collection dispersed. We estimated ages of bears not followed from (radio-marked and shot) and study area (north and south). birth by counting the annuli in a cross-section of a pre- molar root, which is a relatively accurate method (Matson et al. 1993). All age determinations were done by Matson’s Results Laboratory, Milltown, Montana, USA. We calculated multiannual home-range overlap for each A total of 288 adult bears were considered for the dyad of adult radio-marked females within the two study analysis. The combined unbiased probability of identity areas. We estimated multiannual home ranges using ra- −17 dio locations computed as 95% adaptive kernels (Worton (Paetkau and Strobeck 1994) of the 18 loci was 2.098e , 1989), with the Ranges 6 computer package (Anatrack Ltd., meaning that the 18 loci are sufficient to provide a full 52 Furzebrook Road, Wareham, Dorset, UK) and default assessment of kinship relationships (Table 1). Pairwise settings for contours (fitted to locations), smoothing fac- geographic distance was calculated based on arithmetic tor (h=1) and grid size (40), which resulted in nonfrag- centers of localizations of 75 radio-marked females and 67 radio-marked males, and shot locations for 75 females mented ranges. To eliminate auto-correlated data, we used < only locations outside the winter den and separated by at and 71 males, giving a total of 9,566 dyads 100 km apart. least 100 h, which corresponds to the minimum time be- The average relatedness between mother–daughter dyads and grandmother–granddaughter dyads was 0.568±0.089 tween the weekly localizations of the bears (Dahle and ± = ± ± = Swenson 2003b). For kernel estimates, at least 30 locations (mean SD, n 51) and 0.357 0.107 (mean SD, n 21), are recommended to achieve stable size estimates (Seaman respectively. The minimum relatedness between mother– daughter dyads was 0.448. The average relatedness for et al. 1999), and incremental tests in Ranges 6 showed that > most ranges stabilized around 30 points. Thus, we used female dyads 100 km apart in the same study area and only dyads with a minimum total of 30 individual locations north–south dyads of adult radio-marked females, i.e., during a period of one or several years and monitored in the same years for both individuals in the overlap compar- Table 1 Observed number of alleles, observed heterozygosity (Ho), ison. The multiannual home-range overlap between dyads Nei’s estimated heterozygosity (He) and unbiased probability of iden- tity (PI unbiased) (Paetkau and Strobeck 1994) of adult female bears was expressed as a percentage cal- Locus Number of alleles Ho He PI unbiased culated by the formula: (Oij/(Ai+Aj))×2, where Oij is the area of overlap between bear i and bear j, and Ai and Aj G10B 8 0.71 0.69 0.121 are the areas of the multiannual home ranges of bear i and G10C 7 0.7 0.67 0.144 bear j, respectively (see Ratnayeke et al. 2002; Atwood and G10H 11 0.62 0.6 0.174 Weeks 2003). G10J 7 0.68 0.65 0.148 G10L 8 0.79 0.76 0.068 G10O 3 0.31 0.29 0.509 Statistical analysis G10P 8 0.8 0.76 0.070 G10X 7 0.66 0.57 0.182 We used Spearman’s rank correlation as a measure of asso- G1A 9 0.74 0.67 0.113 ciation between geographic distance and relatedness. The G1D 8 0.69 0.67 0.154 number of pairwise comparisons by far exceeded the num- Mu05 10 0.71 0.67 0.128 ber of individuals, resulting in dependent data. Due to Mu10 10 0.81 0.77 0.062 this dependence, conventional tests for testing the signifi- Mu15 5 0.61 0.6 0.209 cance of the correlation coefficient do not apply. Following Mu23 7 0.8 0.74 0.066 Ratnayeke et al. (2002), we tested a null hypothesis of no Mu50 10 0.79 0.72 0.080 association between distance and relatedness (Spearman Mu51 8 0.81 0.78 0.067 correlation equal to zero) with a nonparametric permutation test (Dietz 1983). The maximum natal dispersal distance Mu59 11 0.81 0.81 0.058 recorded for female brown bears in Scandinavia is 80– Mu61 4 0.66 0.55 0.186 90 km (Swenson et al. 1998), and the average distance be- Mean 7.83 0.71 0.67 – 194

Table 2 Permutation test statistics for correlations of relatedness (R) on distance for brown bears in two study areas in Scandinavia Sex Dyads N Spearmans P correlation Female–female All 2805 −0.2060 <0.0001 Radio- 1369 −0.2569 <0.0001 marked Shot 454 −0.1329 0.0055 North 2002 −0.1732 <0.0001 South 803 −0.3000 <0.0001 Female–male All 4768 −0.0254 0.0789 Male–male All 1993 −0.0206 0.3598 Note. N is the number of dyads unrelated females, was 0.210±0.152 (mean±SD, n=95) and −0.179±0.134 (mean±SD, n=1334), respectively. Pairwise genetic relatedness between female dyads declined significantly with increasing geographic distance, but this was not the case for male dyads or dyads of opposite sex (Table 2, Fig. 1). Among female dyads, this pattern was consistent in both study areas and among shot and radio-marked animals (Table 2). A 95% adaptive kernel home range was calculated for 37 different adult females forming 55 overlapping dyads. Be- cause some females overlapped with several other females in different years, we calculated a total of 110 multiannual home ranges, one home range for each animal in a dyad. The multiannual home ranges were estimated using an av- erage of 100±62 locations (mean±SD, range: 31–364), where the difference in number of locations between indi- viduals in the overlapping dyads was on average 13.6±16.9 locations (mean±SD, range: 0–89), collected concurrently on average during 4.6±2.5 years (mean±SD, range: 2– 13). The average home-range size was 437±309 km2 (mean±SD), and the 55 dyads overlapped on average 26.4±17.7% (mean±SD, range: 0.7–75.8%). The percent overlap was positively associated with relatedness based on the permutation test across all dyads (Spearman corre- lation = 0.4413, p=0.0012, Fig. 2), and in both study areas (south: Spearman correlation = 0.4029, p<0.0094, north: Spearman correlation = 0.5769, p<0.037). Mother–offspring combinations were known from field observations and confirmed genetically (n=314). Paternity was determined genetically for 242 of the marked individu- als. Using those pedigrees, we identified four matrilines of Fig. 1 Pairwise genetic relatedness between pairs of adult brown adult females consisting of more than three generations or bears (5 years and older) in relation to their geographic proximity, more than five individuals in the south and three such matri- (a) is dyads of females, (b) is dyads of the opposite sex and (c)is lines in the north. There were two types of matrilinear struc- dyads of males. For visualizations of the association between the ture: a matrilinear assemblage where the animals belonging variables, nonparametric regression curves (LOWESS) (Cleveland 1979) are fitted and shown with the data points. For illustrative to the same matriline used an area exclusively and a more purposes the dependent variable is on the x-axis dispersed type, with the members spread over larger geo- graphic areas and residing closer to nonkin than kin (Fig. 3). of males or dyads of the opposite sex. This pattern was similar in both study areas, and was also observed when Discussion only shot animals were considered (Table 2). Because the system of bear hunting in Sweden did not constrain the As predicted, relatedness was negatively correlated with location of kills (Swenson et al. 1998), shot animals are distance between dyads of females, but not between dyads randomly distributed. Consequently, the results are not an 195

Fig. 2 Average relatedness between pairs of adult female brown bears (5 years and older) in relation to the percentage home-range overlap. For visualizations of the association between the variables, nonparametric regression curves (LOWESS) (Cleveland 1979)are fitted and shown with the data points. For illustrative purposes the dependent variable is on the x-axis effect of a biased sampling due to the capturing regime, where offspring of radio-marked females are systemati- cally captured. These results indicate that females gen- erally are located geographically close to their relatives, whereas males are located at random compared to their relatives (Fig. 1). This is consistent with a sex-biased dis- persal, where females are mostly philopatric and males are Fig. 3 Centers of home ranges and shot locations of adult female mostly dispersers, as observed in most mammals and doc- brown bears (5 years and older) illustrating spatial structure of female matrilines in northern (a) and southern (b) Sweden. Home-range umented in brown bears and as well in other species of centers were calculated by 95% adaptive kernel for females with bears (Greenwood 1980; Schwartz and Franzmann 1992; >30 radio locations and as arithmetic mean for females with <30 McLellan and Hovey 2000). radio locations. Matrilines consisting of more than three generations The relationship between genetic relatedness and ge- or five individuals of radio-marked females are shown with open squares, closed squares, open triangles, and closed triangles. Radio- ographic distance between female dyads was strongest marked females belonging to other matrilines are shown with closed within a distance of 40 km (Fig. 1a) and then rapidly dis- circles and shot unmarked females are shown with a ×. Arrows show appeared. This distance probably reflects the geographic mother–daughter dyads, with the arrow pointing to the daughter. distribution of closely related females, i.e., mothers and Matrilinear assemblages are shown by shaded areas daughters, sisters, granddaughters and grandmothers, aunts and nieces. With an average dispersal distance of 15.7 km, relatedness and low relatedness had >50% home-range 40 km would represent approximately three generations. overlap (Ratnayeke et al. 2002). Contrary to observations The average relatedness values observed beyond 40 km dis- in raccoons, only brown bears with high relatedness on tance corresponds well with animals being more distantly the level of mother–daughter (R>0.45) overlapped >50% related than at least three generations. The 95% distribution (Fig. 2). Our results thus indicate that brown bears discrimi- of geographic distances between reproductive pairs, de- nated between kin and nonkin with regard to sharing space. duced from parentage analysis, is also approximately 40 km This also has been documented in gregarious species, (Bellemain 2004). Therefore, the relationship between ge- where kinship influences social behaviors and increases netic relatedness and distance could also be strengthened tolerance (Clutton-Brock et al. 1982; Gouzoules and to a certain degree by a male successfully breeding with Gouzoules 1987). The mechanism behind kin recognition several females within his range. is not well known, but Mateo (2002) showed that Belding’s As predicted, there was a positive relationship between ground squirrels (Spermophilus beldingi) produced odors home-range overlap and relatedness between adult females. that correlated with relatedness, and this could also be the In raccoons (Procyon loctor), individuals with both high case for brown bears. Another possible mechanism is that 196 mother–daughter pairs or siblings maintain familiarity thro- now in brown bears. Due to the few studies conducted on ugh continued social contact while sharing common space. solitary mammals and especially large mammals (Gompper Survival and recruitment have been shown to correlate and Wayne 1996), we still do not know how common spatial with relatedness in small mammals and birds. Female organization based on kinship is among solitary mammals. Townsend’s voles with at least one first-degree relative as a Our study demonstrates that long-term and large-scale stud- neighbor survived better than females without such a rela- ies that combine field data with molecular techniques are tive (Lambin and Krebs 1993), and the probability of young required to reveal these relations in solitary species. The male red grouse (Lagopus lagopus scoticus) establishing a lack of long-term studies might explain the variation in territory increased with the number of kin in his father’s findings among studies of relatedness and proximity in kin-cluster (MacColl et al. 2000). Whether the observed solitary species (Rogers 1987; Schenk et al. 1998). In gre- increased home-range sharing with related individuals has garious species of mammals, aggregation of kin can have a positive effect on the inclusive fitness of female brown a positive effect on the inclusive fitness of females (Pope bears remains unknown. 2000), but it is unknown whether this is also the case for The matrilines in the Scandinavian brown bear showed solitary species, such as brown bears, which also shows two contrasting spatial patterns. Some females formed ma- spatial social structure. trilinear assemblages where related females occupied ex- clusive areas, whereas other matrilines were dispersed, with Acknowledgements This study was funded by the Norwegian Di- females established among nonrelated females or between rectorate for Nature Management, the Swedish Environmental Pro- tection Agency, the Swedish Association for Hunting and Wildlife other matrilinear assemblages. A similar pattern, where Management, the Norwegian Institute for Nature Research, WWF some animals settle away from the kin clusters, has also Sweden and the Research Council of Norway. We thank the per- been observed in grey-sided voles (Clethrionomys rufo- sonnel in the Scandinavian Brown Bear Research Project for their canus) (Ishibashi et al. 1997). The formation of matrilinear assistance in the field and Orsa Communal Forest for field support. We also thank Pierre Taberlet, Shyamala Ratnayeke, Per Wegge, assemblages in the Scandinavian brown bear population Andreas Zedrosser, Bjørn Dahle and Andres Ordiz for commenting may be associated with the ongoing distributional expan- on earlier drafts of the manuscript, and Torbjørn Nielssen for help sion (Swenson et al. 1998). Dispersing females may settle with the graphics. All capture and handling of bears reported in this in areas not inhabited by other bears and then form matrilin- paper complied with the contemporary laws regulating the treatment of animals in Sweden and Norway and was approved by the appropri- ear assemblages through philopatric behavior of the female ate management agencies and ethical committees in both countries offspring. Matrilinear assemblages were also formed in ar- eas where members of several matrilines resided, both in the center and in the periphery of the study populations. Sev- References eral of the matrilinear assemblages were also surrounded by unrelated individuals and other matrilines. Because a high Atwood TC, Weeks HP (2003) Spatial home-range overlap and proportion of females were radio-marked (north: ∼100%, temporal interaction in eastern coyotes: the influence of pair south: ∼69%) and no bears were shot within the matrilin- types and fragmentation. 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Paper V

Socially induced delayed primiparity in brown bears Ursus arctos

Ole-Gunnar Støen, Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway

Andreas Zedrosser, Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway, and Institute for Wildlife Biology and Game Management, Department for Integrative Biology, University of Natural Resources and Applied Life Sciences, Peter-Jordan Strasse 76, A-1190 Vienna, Austria

Per Wegge, Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway

Jon E. Swenson, Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway, and Norwegian Institute for Nature Research, Tungasletta 2, NO-7485 Trondheim, Norway

Corresponding author: Ole-Gunnar Støen Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O.Box 5003, NO-1432 Ås, Norway e-mail: [email protected] Tel.: +47 64 96 58 00, Fax: +47 64 96 58 01

1 Abstract Reproductive suppression through behavioural or physiological means is common in group- living and cooperative breeding mammals, but to our knowledge this has not been shown in wild-living large carnivores other than those with a clear form of social organization. The brown bear (Ursus arctos) may be more social than previously assumed, because females form matrilinear assemblages with related females using a common and largely exclusive area. Behavioural reproductive suppression might develop due to a hierarchical system among females within a matrilinear assemblage or due to inbreeding avoidance, because male brown bears can overlap with their daughters. In this study we tested whether natal dispersal status influenced age of primiparity. We predicted that dispersed females geographically removed from maternal or paternal influence will reproduce earlier than philopatric females. The average age of primiparity was 4.3 years in females that dispersed outside their mother’s home range (n=8) and 5.2 years in philopatric females (n=10). Only overlap with their mother’s home range, and not body size, body mass, growth, local population density or overlap with their father’s home range had a significant influence on the age of primiparity. The ultimate role of reproductive suppression for brown bears is likely similar to that in other species, i.e. to avoid inbreeding or to minimize resource competition. Due to the low risk of inbreeding and frequent exposure of young females to unrelated males, we conclude that it is probably not inbreeding avoidance, but rather resource competition within female hierarchies that causes reproductive suppression in young females.

Key words: maturity, reproduction, reproductive success, reproductive suppression, social organization

2 Introduction Costs and benefits of dispersal or philopatry to young animals may vary due to differences in mortality, access to unrelated mates, possibility to find suitable offspring rearing space, familiarity with the local area and neighbours or benefits of kin selection, and suppression by dominant animals (see Wiggett and Boag 1990). Reproduction by young animals is suppressed by adults or dominant individuals in many group-living and cooperatively breeding mammals, leading to delayed primiparity and failed reproduction attempts in philopatric females (Wasser and Barash 1983, Creel and Creel 1991, Waterman 2002, Oli and Armitage 2003). The mechanism of reproductive suppression varies among species, but occurs through behavioural or physiological means (Wasser and Barash 1983, Brant et al. 1998, Clarke et al. 2001, Solomon et al. 2001, Hackländer et al. 2003). Reproductive suppression is common in group-living mammals, but to our knowledge this has not yet been shown in wild-living large carnivores other than those with a clear form of social organization (e.g. wolves Canis lupus, see Mech 1970). Reproductive suppression can occur in subdominant females as a result of behavioral dominance by older females (see review by Wasser and Barash 1983) or when young females are not exposed to unrelated males (Wolff 1992, Lambin 1994). Such intrinsic reproductive suppression has been documented in several mammalian species, especially among rodents and group-living carnivores (see Wolff 1997). Reproductive suppression in a young female can be adaptive if the individual is responding to its social environment and withholding reproductive effort would result in greater reproductive success later than if she attempted to breed under current conditions (Wasser and Barash 1983, Wolff 1997). The brown bear (Ursus arctos) is a large carnivore with a promiscuous mating system (Pasitschniak-Arts 1993, Schwartz et al. 2003, Bellemain et al. 2006). Natal dispersal is sex- biased, with males generally dispersing and philopatric females (Glenn and Miller 1980, Blanchard and Knight 1991, McLellan and Hovey 2001, Proctor et al. 2004). Both the probability of natal dispersal and natal dispersal distances are inversely density dependent (Støen et al. 2006). Among adults, males have larger home ranges than females, but both males and females have intra- and inter-sexually overlapping ranges (Pasitschniak-Arts 1993, Dahle and Swenson 2003a). Brown bears are generally not considered to be territorial (Pasitschniak-Arts 1993, Schwartz et al. 2003), but dominance hierarchies have been observed among brown bears (Pulliainen et al. 1983), especially when aggregating at garbage dumps and at salmon (Oncorhyncus spp.) spawning streams (see IGBC 1987 for a review, Craighead et al. 1995,

3 Gende and Quinn 2004). The distance between females decreases and the amount of overlap of their home ranges increases with increasing relatedness (Støen et al. 2005). This leads to the formation of matrilinear assemblages with related females using a common and largely exclusive area. Thus, although non-gregarious, brown bears may be more social than previously assumed (Støen et al. 2005). A hierarchical system, with dominant and subdominant animals, can develop within these matrilinear assemblages and provide a possibility for reproductive suppression. After their near extirpation around 1930, the Scandinavian brown bear population increased in numbers and expanded in range from four small remnant areas. Today it encompasses more than half of Sweden and parts of Norway (Swenson et al. 1994, 1995). This expansion in range, with both philopatric and dispersed females in the same geographical area (Swenson et al. 1998, Støen et al. 2006), provided us with a rare possibility to test whether young philopatric females are reproductively suppressed. In this study we examined whether dispersal status (philopatric or dispersed) influenced age of primiparity. In mammals, body size, body mass and population density may also influence sexual maturity (Festa-Bianchet et al. 1995, 1998, Svendsen and White 1997, Forchhammer et al. 2001, Bonenfant et al. 2002, Weladji et al. 2003, Neuhaus et al. 2004); thus we controlled for this in our analysis. Based on the recent finding of matrilinear assemblages in brown bears (Støen et al. 2005), we predict that dispersed females relieved from matrilineal influence will reproduce earlier than philopatric females. Because the home ranges of adult male brown bears can overlap with their daughters and provide a potential risk of inbreeding (McLellan and Hovey 2001, Dahle and Swenson 2003a), we predict that females relieved from paternal influence by dispersing outside their father’s home range will reproduce earlier than females living within their father’s home range.

Methods Study area, home range estimations and dispersal status The study area was in Dalarna and Gävleborg counties in south-central Sweden and Hedmark County in southeastern Norway (61º N, 18º E). The rolling landscape in this region is covered with coniferous forest, dominated by Scots pine (Pinus sylvestris) and Norway spruce (Picea abies). During 1986-2003 we captured, radiomarked and monitored 32 adult female bears that weaned 78 litters with 175 yearlings. Eighteen yearling daughters from 7 different females were successfully followed until primiparity. The fathers of the yearlings were determined from DNA analysis of shot and captured males (Bellemain 2004). We located the

4 bears approximately once a week during their active period for several years, using standard triangulation methods from the ground or from the air (Dahle and Swenson 2003a). The study area and the methods used to capture, collar and radiotrack bears are described by Dahle and Swenson (2003a, b) and Arnemo et al. (in press). A daughter was defined as a natal disperser if she left her natal area and was never again observed within her natal area or her mother’s multiannual home range after separation. Daughters that were always or periodically observed within their natal areas or their mother’s multiannual home range after separation were defined as philopatric. Natal areas were estimated as 95% minimum convex polygons (MCP), using the mother’s locations with the Ranges 6 computer package (Anatrack Ltd., 52 Furzebrook Rd., Wareham, Dorset, UK). A 95% MCP estimate was used to avoid the influence of unusual forays and because MCP estimates are the most frequent home range estimators reported in the brown bear literature (Schwartz et al. 2003). Family break-up normally occurs in the spring (May-June) at cub age of 17-18 months (Dahle and Swenson 2003b). An underestimation of the size of a natal area could overestimate the number of dispersers using this criterion. We therefore estimated the natal areas (95% MCP) based on all of the mother’s locations during the first two years of the daughter’s life and not only from the positions when the daughter accompanied the mother. This was done for two reasons: a) relatively few locations were obtained annually for each litter, due to long time intervals between successive locations and the prolonged period (5-7 months) spent in winter dens, and b) a 95% MCP can underestimate the real home range size of brown bears when using few locations (Macdonald et al. 1980). By including all of the mother’s positions in the second year of her daughter’s life, we obtained a more reasonable estimate of the home range that the mother used while accompanied by cubs, i.e. the natal area. The average number of locations used to estimate natal areas (n = 18) was 58 ± 13 (mean ± SD, range: 28 - 76). To reduce the effect of autocorrelation in the data, only locations separated by at least 100 h were used, which corresponds to the minimum time between successive locations of the bears (Dahle and Swenson 2003b). Using multiannual home ranges is also justified because adult females have high fidelity to their home range in successive years (Støen et al. 2005). The multiannual home ranges (95% MCP) were estimated differently for mother- daughter dyads of philopatric and natal dispersers. The multiannual home ranges of mothers of philopatric daughters were estimated using locations of the mother obtained in all the years from the time the daughter turned 2 years until (and including) the year of the daughter’s first reproduction. An inclusion of the mother’s positions in the years when the dispersing female

5 resided in the natal area would bias the multiannual area of the mother towards the natal area and thus overestimate the number of dispersers. Multiannual home ranges of mothers with dispersing daughters were therefore estimated from locations obtained during the first years the daughter was not observed within the natal area until (and including) the year of her first reproduction. The average number of locations used to estimate the multiannual home ranges of mothers with philopatric daughters (n = 10) in this study was 121 ± 50 (mean ± SD, range: 26 - 185). The corresponding annual number of locations of their philopatric daughters these years (n = 42) was 31 ± 10 (mean ± SD, range: 9 - 47). The mother of one disperser lost her radio collar prior to separation. The average number of locations used to estimate the multiannual home ranges of the other mothers with dispersing daughters (n = 7) was 61 ± 42 (mean ± SD, range: 26 - 144). The corresponding annual number of locations of their daughters after natal dispersal these years (n = 16) was 31 ± 10 (mean ± SD, range: 4 - 43). The spatial association between a young female and her father was estimated based on locations of the daughter within the father’s multiannual home range after weaning. The multiannual home ranges of fathers (95% MCP) were estimated using locations of the father obtained in all the years from the time the daughter turned 2 years until (and including) the year of the daughter’s first reproduction. The average number of locations used to estimate the multiannual home ranges of fathers (n = 11) in this study was 96 ± 43 (mean ± SD, range: 22 - 184). The corresponding annual number of locations of their daughters these years (n = 38) was 29 ± 11 (mean ± SD, range: 4 - 47).

Monitoring of reproduction The reproductive status of the daughters was determined by three methods; direct observations, live capture, and visits to den sites. We observed a family as soon as possible after it left the den, again around the end of the mating season in late June-early July, and again before they entered the den in the autumn. Immobilised daughters without cubs of the year were checked for lactation by signs of nursing (e.g., matted hair) or presence of milk in the udder. We visited dens to determine whether young had been present outside the den, based on tracks and markings from their climbing in nearby trees. A daughter was considered to have reproduced if she was observed with cubs, if she was lactating when captured soon after emerging from the den, or if tracks of small cubs were found at the den site. If none of these criteria were confirmed, she was considered to not have reproduced.

6 Body size measurement The head circumference (at the widest part of the zygomatic arch between eyes and ears) was measured with a tape measure and used as a measure of the overall body size of an individual (Zedrosser et al. in press). Head circumference was used because Derocher and Stirling (1998) suggested that head measurements rather than body length might provide the most useful measures to compare body size in different populations of polar bears (Ursus maritimus). Live weight was measured with a scale and used as a measure of the overall body mass of an individual. Because all bears were captured within the same 2-week period each year (late April), we did not adjust body size or body mass for capture date. Growth was measured as kilo body mass gained and as cm head circumference gained from 1 to 4 years old.

Individual population density index An individual density index (i.e. number of bears within a radius of 17.84 km around each radio-marked bear, which corresponds to the density of bears per 1000 km2) in our analysis was based on the locations of individual bears genetically identified by DNA analysis of scats collected throughout the study area in 2001 and 2002 (Bellemain et al. 2005). A population growth rate (Sæther et al. 1998) and the proportion of radio-marked bears represented in the scat samples (71%) were used to correct the density estimates (see Zedrosser et al. (in press), for a more detailed description).

Statistical analysis

We fitted quasi-Poisson regression models for age of primiparity, using the glm function in R (the MASS library) (R Development Core Team 2005). The variables of interest were dispersal status, i.e. philopatric or dispersed, body size, body mass and the individual population density index. All the variables used in the models were measured at the same age of the bears. In our initial model we chose 4 years of age, because this is the lowest age of first reproduction recorded in Scandinavian female brown bears (Sæther et al. 1997), and it gave the largest sample size. We used both body size and body mass in our models, because body size gives a measure of structural size, whereas body mass in addition reflects variations in body conditions (i.e. fat storage) and thus environmental conditions.

7 Results Ten daughters were located within their natal area or within their mother’s multiannual home range every year after separation, including the year when they had their first litters, and were defined as philopatric. Eight daughters left their natal area and were never again observed within the natal area, including the year of primiparity, and were defined as dispersers. The mean age of leaving the natal area was 2.25 ± 0.89 (mean ± SD, range: 1 – 3) years, which was a minimum of 1 year and an average of 2 years before primiparity. The mother of one natal disperser used in the analysis lost her radio collar prior to separation and could possibly have overlapped with her dispersed daughter in the years after separation, if she had shifted her home range along with the daughter. In the year of primiparity (5 years old), the dispersed daughter’s closest position was 52 km from the border of her natal area, whereas the mother was shot 4 years later within the natal area. The 7 other dispersing daughters were never observed within their mothers’ multiannual home ranges after leaving the natal area. The average age of primiparity of all daughters was 4.8 ± 0.7 years, and as 4-year-olds their average body size was 56.0 ± 2.2 cm, the average body mass was 77.9 ± 10.4 kg and the average individual population density index was 31.6 ± 18.4 bears/1000 km2. Age of primiparity was the only variable that was significantly different between philopatric daughters and dispersed daughters (Table 1). When controlling for body size, body mass and density when 4 years old, a generalized linear model (GLM) revealed that dispersal status was the only variable having a significant effect on age of primiparity (Table 2). Whereas dispersed daughters started to breed at a mean age of 4.3 years, philopatric daughters started at a mean age of 5.2 years (Table 1). Lactation is energetically costly for females (Farley and Robbins 1995, Hilderbrand et al. 2000). Because 7 (87.5%) of the 9 daughters that gave birth as 4-years-olds had dispersed, measuring body size and body mass approximately 4 months after parturition could bias our data towards smaller sizes of dispersing daughters. However, when using body size, body mass and individual population density index values of 14 of the daughters when they were measured as 3 year olds in a GLM model, dispersal status was still the only variable having a significant effect on age of primiparity (Table 2). Growth rate and nourishment as young has also been found to be important for primiparity in several species (Reiter and LeBoef 1991, Svendsen and White 1997, Hofer and East 2003; Weladji et al. 2003). However, there was no effect of yearling body size or yearling body mass (ȕ = -0.009, p = 0.160, df = 14 and ȕ = -0.011, p = 0. 477, df = 15, respectively) and growth in body size or body mass from 1 to 4 years of age (ȕ = -0.002, p =

8 0.504, df = 14 and ȕ = 0.002, p = 0.887, df = 15, respectively) on age of primiparity, when controlling for natal dispersal status in the GLM models. The individual population density index did not differ significantly between the natal area and the area where the daughters (n = 18) gave birth to their first litter (t = 0.002, p = 0.999). This was true both for philopatric daughters (n = 10, t = 1.206, p = 0.258) and dispersing daughters (n = 8, t = 1.208, p = 0.266). Some daughters had their first litter when older than 4 years (n = 9), but the individual population density index of those daughters did not differ significantly between the area they resided in as 4-year-olds (used in the GLM model) and the area where they had their first litter (t = 0.083, p = 0.94). We obtained multiannual home ranges of the fathers of 11 daughters. Five of these daughters did not have locations within their fathers multiannual home range at least 1 year before primiparity. The other 6 daughters were located within their father’s home range every year until primiparity. There was no significant difference in the age of primiparity between these two groups of females (GLM, ȕ = 0.057, p = 0.665, df = 6), when controlling for body size (ȕ = 0.033, p = 0.450), body mass (ȕ = 0.005, p = 0.571) and density (ȕ = 0.005, p = 0.272) when 4 years old.

Discussion As predicted, philopatry was associated with an increased age of primiparity. Only dispersal status was significant in the GLM, which suggests a social suppression of reproduction of philopatric daughters residing within their mother’s home range (Table 2). Reproductive suppression of young females has been shown in several gregarious species but, to our knowledge, this is the first time socially induced delayed primiparity has been documented in a large non-gregarious wild-living carnivore. Dalerum et al. (in press) found that reproductive failure in captive female wolverines (Gulo gulo) kept in a highly aggregated social environment was related to low social rank. Social tendencies and physiological mechanisms mediating this reproductive suppression may be viewed as reaction norms to the social environment in wolverines, indicating that the social flexibility of solitary carnivores might be greater than commonly observed (Dalerum et al, in press). The reasons for the reproductive suppression in brown bears could be similar as for many gregarious species i.e. to avoid inbreeding (Wolff 1992) or to minimize resource competition (Wasser and Barash 1983). Reproductive suppression as an inbreeding avoidance mechanism has been observed in several species, and occurs when subadult females remain in contact with male relatives and are not exposed to unrelated adult males (Wolff 1992, Lambin

9 1994, Clarke et al. 2001, Clark and Galef 2001, 2002). Contrary to our prediction there was no significant difference in the age of primiparity between females that dispersed outside their father’s home range and those that overlapped with their fathers until primiparity; however, due to the low sample size in our study we can not rule out the importance of the father’s influence. Because of the low risk of inbreeding shown by theoretical modelling (McLellan & Hovey 2001) and empirical data showing only 2% incestuous matings, i.e. reproduction between the daughter and her father (Bellemain et al. 2006), we believe that fathers probably have little influence on female primiparity in brown bears. In addition, extensive home range overlap among adult males and a promiscuous mating system, as shown by frequent occurrence of multi-paternal litters (Bellemain et al. 2005) indicate frequent exposure of young females to unrelated males. Frequent exposure of young females to unrelated males may counteract potential reproductive suppression from related males (McGuire and Getz 1991, Sillero-Zubiri et al. 1996). Due to the extensive overlap within matrilinear assemblages, dominance hierarchies can develop among related females and reproductive suppression can be seen as a means to reduce resource competition, as found in badgers (Meles meles) (Woodroffe and MacDonald 1995). Female brown bears have been observed killing the offspring of other females (Hessing and Aumiller 1994, McLellan 1994), thus the threat of infanticide for subdominant females could result in delayed reproduction until such time that the female could successfully rear offspring, as proposed for other species (Wasser and Barash 1983, Wolff 1997). Because the home ranges of unrelated females overlap less than those of related females (Støen et al. 2005), natal-dispersing females surrounded by unrelated females probably have less contact with other females. With less contact between the females, a hierarchy may not develop and these females may thus be relieved from reproductive suppression. Even if female brown bears in our study area reach 90% asymptotic size at a mean age of 4.1 years (Zedrosser et al. in press), brown bears may continue to grow throughout their life (Schwartz et al. 2003). Dominance hierarchies have been related to size in brown bears (Craighead et al. 1995). We suggest that the increased size with age may improve the status of subdominant females within a hierarchy, which again reduces the threat of infanticide and probably increases the possibility for successfully rearing offspring. The nutritional condition of females has been found to be important for the onset of reproduction in brown bear populations (Stringham 1980, 1990; Bunnel and Tait 1981), and several other species (Svendsen and White 1997, Weladji et al. 2003, Neuhaus et al. 2004). Neither body size nor body mass as yearlings, 3-year-olds and 4-year-olds influenced age of

10 primiparity in our GLM models. The reason might be because small Scandinavian brown bear females show compensatory growth (Zedrosser et al. in press), and thus may not have a disadvantage of small body size when reaching reproductive age. Growth rate has been reported to influence the age of primiparity in spotted hyenas (Hofer and East 2003), however, we did not find this in brown bear females, because there was no effect on age of primiparity when controlling for natal dispersal status in our GLM models. Population density, which has been found to be important for age of primiparity in several mammalian species (Festa-Bianchet et al 1995, 1998, Forchhammer et al. 2001, Bonenfant 2002), was not observed to significantly influence the age of primiparity in our generalised linear model, at least at the densities observed in our study area. The individual density indices were not significantly different in the natal area and in the area where the dispersing daughters had their first litter. This suggests that dispersing females settled in a vacant area rather than in an area with generally fewer bears. This result suggests the inference that it is the related females that suppress reproduction and not bear density per se. One reason why some females may not disperse even if being philopatric delays first reproduction might be that dispersal is determined by other factors than the delay in reproduction due to reproductive suppression. In Scandinavia 60% of the females do not disperse and brown bear natal dispersal is inversely density dependent (Støen et al. 2006) and in North America female dispersal is rare (McLellan and Hovey 2001). There might be a fitness advantage of remaining philopatric i.e., improved survival of the female or cubs, familiarity with the local area and neighbours, proven resource base and benefits of kin selection (see Wiggett and Boag 1990), that exceed the disadvantage of delayed primiparity . However it is unknown whether fitness is increased by philopatric behaviour in brown bears.

Acknowledgements This study was funded by the Norwegian Directorate for Nature Management, the Swedish Environmental Protection Agency, the Swedish Association for Hunting and Wildlife Management, WWF Sweden, the Research Council of Norway, and the Norwegian University of Life Sciences. Andreas Zedrosser was financially supported by the Austrian Science Fund Project P16236-B06. We thank the personnel in the Scandinavian Brown Bear Research Project for their assistance in the field and Orsa Communal Forest for field support. We thank Ali Nawaz and Bjørn Dahle for comments on an earlier draft and Solve Sæbø for statistical help. All capture and handling of bears reported in this paper complied with the contemporary

11 laws regulating the treatment of animals in Sweden and Norway and was approved by the appropriate management agencies and ethical committees in both countries.

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16 Table 1. Age of primiparity, body size (head circumference), body mass (live weight) and individual population density index (density) for philopatric and natal dispersed female brown bears in Scandinavia.

Philopatric Dispersed daughters daughters XSDn XSDn t*P Age of primiparity (years) 5.2 0.6 10 4.3 0.5 8 3.547 0.003 Head circumference (cm) 1 year old 39.4 2.2 10 40.3 2.0 6 0.886 0.394 3 years old 51.6 1.8 8 52.3 2.7 6 0.646 0.530 4 years old 55.8 2.5 10 56.4 1.9 8 0.537 0.599 Growth 1-4 years age 16.4 2.4 10 16.2 3.1 6 0.160 0.877 Live weight (kg) 1 year old 21.3 4.9 9 22.3 2.5 6 0.516 0.615 3 years old 57.4 8.3 8 60.8 7.6 6 0.781 0.450 4 years old 76.4 12.7 10 79.8 7.0 8 0.677 0.508 Growth 1-4 years age 54.2 9.6 9 58.7 8.6 6 0.935 0.369 Density (bears/1000 km2) Natal area 32.4 15.3 10 31.0 18.5 8 0.182 0.858 3 years old 41.5 21.0 8 28.5 13.4 6 1.328 0.209 4 years old 36.0 21.1 10 26.1 13.6 8 1.143 0.270 First litter 37.2 22.5 10 24.9 13.4 8 1.363 0.192 * Two-sample t test.

17 Table 2. Generalized linear model of the effects of natal dispersal status (philopatric or dispersed), body size (head circumference), body mass (live weight) and individual population density index (density) when 3 years of age (n = 14) and 4 years of age (n = 18), on the age of primiparity in female brown bears in Scandinavia 1986-2003. Explanatory variables ȕ SE df t P 3 years old Density (bear/1000km2) 0.0009 0.0027 9 -0.320 0.756 Head circumference (cm) 0.0316 0.0218 10 1.452 0.177 Live weight (kg) -0.0055 0.0044 11 -1.271 0.230 Natal dispersal status (Philopatric vs Dispersed) -0.1678 0.0675 12 -3.488 0.029 4 years old Density (bear/1000km2) 0.0009 0.0018 13 0.507 0.620 Head circumference (cm) 0.0267 0.0235 14 1.141 0.273 Live weight (kg) -0.0033 0.0026 15 -1.269 0.224 Natal dispersal status (Philopatric vs Dispersed) -0.2017 0.0564 16 -3.579 0.002 The models were run repeatedly after successively excluding the least significant term, until the models included only significant terms.

18 Paper VI

Primiparity, litter size and cub survival in a species with sexually selected infanticide, the brown bear.

A. Zedrosser,a,b B. Dahle,c O.-G. Støen,b and J. E. Swensonb,d a Department of Integrative Biology, Institute for Wildlife Biology and Game Management, University of Natural Resources and Applied Life Sciences, Vienna, Peter Jordan Str. 76, A- 1190 Vienna, Austria, b Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, Post Box 5003, NO-1432 Ås, Norway, c Department of Biology, Program for Experimental Behavior and Population Ecology Research, University of Oslo, Postbox 1066, Blindern, 0316 Oslo, Norway, d Norwegian Institute for Nature Management, Tungasletta 2, NO-7485 Trondheim, Norway.

Correspondence author: Andreas Zedrosser Department of Ecology and Natural Resource Management Norwegian University of Life Sciences Post Box 5003 NO-1432 Ås, Norway email: [email protected]

running title: Primiparity in brown bears

1 ABSTRACT We studied the effects of primiparity on litter size and cub loss in brown bears in two study areas in Scandinavia. Sexually selected infanticide (SSI) has been previously suggested as a major mortality factor in one of the study areas. We found that both the cub-of-the-year and yearling litter size of a primiparous mother was significantly smaller than when she was multiparous. A primiparous female also lost significantly more cubs than when she was multiparous; however a primiparous mother did not seem to invest less in her offspring than a multiparous mother, because the yearling offspring of primiparous females were not smaller than the yearlings of multiparous females. We found that the probability of cub loss was higher in the area where SSI was suggested (south), than in the area without SSI (north). The probability of cub loss of primiparous mothers increased with male turnover (a variable identifying SSI), but was not related to environmental conditions, their body size or population density. Primiparous mothers lost more offspring than multiparous mothers, which suggests that they are less able to/experienced in defending their offspring. In general, females in the south were primiparous earlier than females in the north, however females raised their first successful litter at the same age in both areas. We found suggestive evidence that females that were primiparous at age 4 in the south had the highest probability of cub loss, maybe due to their low level of experience with other bears in their area.

Key words: brown bear, litter size, litter survival, sexually selected infanticide, primiparity, Ursus arctos.

2 INTRODUCTION Primiparity is a key event in the life history of all animals (Stearns, 1992). Primiparous females usually wean fewer and smaller offspring than multiparous females (Clutton-Brock, 1991, Festa-Bianchet et al., 1995). The trade-offs between future and current reproduction (Williams, 1966) and between growth and reproduction (Festa-Bianchet et al., 1995; Millar 1975; Tuomi et al., 1983) are life-history concepts that provide a theoretical basis for the relative low performance of first-time breeders (Künkele, 2000). In addition, primiparous females may be smaller, i.e. not yet fully grown, than multiparous females, and larger females often produce larger and heavier offspring (Arnbom et al., 1997; Clutton-Brock et al., 1988; Myers and Master, 1983; Wauters et al., 1993;), and larger offspring may have higher survival (Dahle et al., in press). Inexperience may also cause primiparous females to be energetically less efficient in offspring production than multiparous females (Künkele, 2000); Lunn et al., 1994) resulting in a lower reproductive performance. In addition, first-time breeders may lack refined behavioral skills associated with foraging (Becker et al., 1998) and parental care (Wang and Novak 1994). Inexperience and lack of skills by the mother may be of special importance for defending offspring if males seek mating opportunities by killing dependent offspring that are not their own, i.e. sexually selected infanticide (SSI) (Hrdy, 1979). Empirical studies of behavioral strategies and life history of large mammals, especially large carnivores, are rare, because they usually occur at low densities, are long- lived and costly to follow over a long time. Nevertheless, a long-term study of brown bears (Ursus arctos) has enabled us to study behavioral strategies in this species. The earliest recorded age of primiparity in brown bears is 3 years (Zedrosser et al., 2004). Swenson et al. (2001) report that the mean age of primiparity was 4.5 and 5.4 years in two study populations in Scandinavia, whereas the average age of primiparity in the North American brown/grizzly bear is 6.6 years for interior and 6.4 years for coastal populations (McLellan, 1994). Litter size is variable in brown bears, ranging from 1 to 4 cubs-of-the-year (termed cubs here) per litter (McLellan, 1994). There is evidence that young and old females produce fewer cubs per litter than prime-age adults (Craighead et al., 1974; 1995; Sellers and Aumiller, 1994). Dahle et al. (in press) found that offspring size was positively related to maternal size and negatively related to litter size and population density. In addition there was a strong cohort effect, suggesting that environmental conditions may be important for yearling brown bear size (Dahle et al., in press). Several factors have been proposed as important for brown bear cub survival, including nutritional, social and disturbance factors, however Swenson et al. (1997; 2001) have suggested SSI (a social factor) to be the major agent of brown bear cub mortality

3 in parts of Scandinavia; 75% of all cub mortalities occurred during the mating season (Swenson et al., 1997). In this study we investigated if primiparity had an effect on litter size, offspring size and cub survival in the brown bear. We further analyzed litter survival of primiparous females in relation to the SSI hypothesis. Specifically, we predict that 1) the litter size of a primiparous mother is smaller than when she is multiparous; 2) the average body size of yearlings with a primiparous mother is smaller than the average body size of yearlings with multiparous mothers; and 3) survival of cubs of primiparous mothers is lower than survival of cubs of multiparous mothers. We further analyze the probability of loss of cubs with primiparous mothers and predict that it is 4a) positively correlated to population density and male turnover (a variable predicting SSI; Swenson et al. 1997; 2001) and 4b) negatively correlated to environmental conditions, female body size at primiparity, and age at primiparity.

METHODS Study areas, study populations and field methods Data for this study were collected in two areas in Scandinavia. The southern study area (south) was situated in Dalarna and Gävleborg counties in south-central Sweden (61º N, 18º E), and the northern study area (north) was situated in Norrbotten County in northern Sweden (67º N, 18º E). The mating season usually lasts from the second half of May until the first week of July in both areas. The snow cover is shorter, mean temperatures in January and July are higher, and the vegetation period is longer in the south than in the north. For a detailed description of the study areas see Zedrosser et al. (in press). The study populations differed in some demographic parameters (Sæther et al., 1998). Due to male biased juvenile dispersal (Støen et al., 2006) and low rates of male immigration from nearby areas, the numbers of adult males was low (Swenson et al., 2001). Illegal killing in the spring additionally reduced the number of adult males (Swenson and Sandegren, 1999). As a result the number of adult males was stable but low during most of the study period. In the southern study area adult males were killed on a regular basis by legal hunting (Swenson et al., 2001). Cub survival was significantly lower in the south, and Swenson et al. (1997; 2001) suggested that SSI was the main reason for this difference. Age of primiparity was 4.5 years in the south and 5.4 years in the north. However, the ages of the mothers with their first successful litter were very similar in both study areas, 5.4 years in the north and 5.2 years in the south (Swenson et al., 2001).

4 Brown bears were immobilized from a helicopter in mid-April in the south and early May in the north, shortly after den emergence. We used 2.5 mg tiletamine, 2.5 mg zolazepam and 0.02 mg medetomidine per kg body mass to immobilize the bears. Atipamezol was used as an antidote for medetomidine (5 mg per 1 mg medetomidine) (Kreeger et al., 2002). The head circumference (at the widest part of the zygomatic arch between eyes and ears) was measured with a tape measure and used as a measure of overall size of an individual. Because all bears were captured within a 2-week period in each study area, we did not adjust body size for capture date. Few female bears were captured in the year they gave birth. To estimate their body size in this particular year, we calculated their theoretical body size based on the growth curves published in Zedrosser et al. (in press), using the head circumference in the capture year that was closest in time to primiparity as basis. In this study we only used female brown bears of known age (i.e. they were captured as yearlings with their radio-collared mother). We measured the reproductive success by counting the cubs of radio-collared females from the air or the ground three times during the year; just after leaving the natal den, at the end of the mating season, and just prior to entering the den in fall (September) or during capture of the female and her then yearling cubs in April/May the following year. Based on observations in our study populations we define the pre-mating season as the time period after a bear had left the den until the second week of May, and the mating season as the time period from the third week of May until the first week of July (Dahle and Swenson, 2003). Brown bears rarely loose offspring during hibernation, thus yearling litter size represents an accurate measure of offspring surviving their natal year until hibernation.

Environmental condition index We used spring body mass of yearlings in a given year and study area as the basis to construct an index of the general food condition of the study populations for each year. Rather than using the actual values and just controlling for sex (Garshelis, 1994; Swenson et al., 2001), we regressed yearling body mass as a function of maternal size, litter size, sex and individual population density. In this way we controlled for the variables that influence yearling mass independently of environmental conditions (Dahle et al., in press). The standardized residuals from this regression were sorted by study area and year and the average value for each year and area was then used as the food condition index for the year before the yearlings were weighed (Zedrosser et al., in press).

5 Individual population density index The population density around each individual (within a radius of 17.84 km, which corresponds to the density of bears per 1000 km2) was estimated in both the north and south, based on the high proportion of radio-collared bears and documented population growth rates (see Zedrosser et al. in press for a more detailed description). In the south, the population size was estimated based on a DNA analysis of scats collected throughout the area in 2001 and 2002 (Bellemain et al., 2005). The individual density index around each radio-collared individual in our analysis was based on the location of individuals genetically identified by the scat sampling, the location of the radio-collared bears (71% of the radio-collared bears were represented in the scats samples (Bellemain et al., 2005)) and the population growth rate (Sæther et al., 1998), which we used to temporally correct the density estimate. No corresponding population estimate was available for the north, but virtually every adult male and female and all subadult female bears were radio-collared (Swenson et al., 2001). We used the locations of radio-collared bears, a correction to include subadult males, and data on growth rate of the population to calculate an individual density index as in the south (Zedrosser et al., in press).

Male turnover Since 1981, every hunter killing a bear in Scandinavia has had to report the sex and kill location and has to deliver a tooth for aging, as well as body measurements and tissue samples to the authorities. To estimate the number of adult males killed in the vicinity of a given mother with cubs, we calculated the arithmetic center of the 95% minimum convex polygon (MCP) home range for every female with cubs. Within a radius of 40 km from this center we counted the number of adult males dying 1.5 years previously. This included males killed during the hunting season or for other reasons (i.e. accidents) and radio-collared males (arithmetic center of the 95% MCP home range) suspected to have been killed. A 40-km radius was chosen, because Bellemain et al. (2006) have shown that 95% of all brown bear reproductive couples occurred within this radius. A time lag of 1.5 years was chosen, because Swenson et al. (1997) have shown that cub loss was highest 1.5 years after an adult male has been killed. We defined a male as adult when •3 years, because the first age of male reproduction is 3 in both study areas (Bellemain et al., 2006). The software package Ranges 6 (Anatrack Ltd., 52 Furzebrook Rd., Wareham, Dorset, UK) was used for home range calculation.

6 Statistical analyses To evaluate differences in cub and yearling litter sizes and litter survival when the mother was primiparous and multiparous, we used paired two-tailed t-tests (Zar, 1984). An D level of 0.05 was selected for statistical significance. The statistical software SPSS 13.0 was used in these analyses. Due to differences in data availability, the sample size differed between tests. The difference in yearling offspring body size between primiparous and multiparous mothers was analyzed with a general linear mixed model (GLMM) (McCullagh and Nelder, 1989). The response variable was mean body size (head circumference in cm) of yearlings in a mother’s litter, while controlling for random effects of maternal identity. Predictor variables were litter size and whether the mother was primiparous or multiparous. The statistical software R 1.9.1 (R Development Core Team 2004) was used in this analysis. The factors determining cub loss of primiparous females were analyzed with a general linear model. We chose "loss of one or more cubs" as the binary response variable. The following candidate predictors were available from 1987-2004: study area (south or north), male turnover, which is the number of adult male deaths in a radius of 40 km 1.5 years previously, age of primiparity of the female (4- 7 years), body size of the female and the population density and environmental condition indices. We selected the best model in a backward elimination procedure. Predictor variables were chosen according to their p-values (p ” 0.05); p-values ” 0.1 were considered suggestive. The statistical software SPSS 13.0 was used in this analysis.

RESULTS We obtained ages of primiparity for 37 females, 14 in the north and 23 in the south (Table 1). A female’s litter size when she was primiparous (mean = 2.05 r 0.65 (SD)) was significantly smaller than when she was multiparous (mean = 2.47r0.61) (paired t-test: t = 2.29, df = 21, p = 0.033). A primiparous female’s yearling litter size (mean = 1.23 r 1.11) also was significantly smaller than when she was multiparous (mean = 1.95 r 0.98) (paired t-test: t = - 2.28, df = 21, p = 0.007). A primiparous female lost significantly more cubs (mean loss = 0.86 r 0.99 cubs) than when she was multiparous (mean loss = 0.39 r 0.63 cubs) (paired t-test: t = 2.49, df = 28, p = 0.019). The yearling offspring of primiparous females were not smaller than the yearlings of multiparous females, when controlling for mean litter size (GLMM: status of female (primiparous/multiparous): ȕ = -0.781, P = 0.414; mean litter size: ȕ = -0.179, P = 0.804; N = 64, number of groups = 50)

7 The proportion of cubs lost during different times of the year varied between ages and study areas, however primiparous females were not observed to loose cubs after the mating season in our sample (Table 2). A binary model examining the probability of losing one or more cubs (0 = no cub loss, 1 = loss of one or more cubs) showed that, among primiparous females, there was a significant difference in the probability of losing cubs between study areas and that the probability of cub loss was significant and positively influenced by the number of males dying within 40 km 1.5 years previously (male turnover) (Table 3). There was a suggestive negative relationship between the probability of losing one or more cubs and the age when the female was primiparous (Table 3). The other variables and interactions tested were not significant (age: ȕ = -0.021, p = 0.976; condition index: ȕ = -1.653, p = 0.227, population density: ȕ = 0.059, p = 0.189). The temporal distribution of cub loss differed between the study areas. In the north cub loss only occurred towards the end of the study period, whereas cub loss was evenly distributed through the study period in the south (Fig.1).

DISCUSSION As predicted, a female brown bear had a smaller litter when primiparous than when she was multiparous (prediction 1). Patterns of lowered reproductive success by young and primiparious reproducers have been observed in birds (e.g.: Lack, 1966; Curio, 1983; Ollason and Dunnet, 1988) and mammals (e.g.: Clutton-Brock, 1988; 1991; Festa-Bianchet et al., 1995; Hellgren et al., 1995), including ursids (Craighead et al., 1974; 1995; Derocher and Stirling, 1994; Schwartz et al., 2003b, 2005). The causes for this lowered performance of primiparous individuals vary widely and can include (among others) physical maturation, lower reproductive experience and changes in dominance rank (Clutton-Brock, 1988). Female brown bears reach 90% of their asymptotic body size at approximately 4-5 years of age in Scandinavia (Zedrosser et al., in press), however they can continue to grow throughout life (Schwartz et al., 2003a). The smaller litter size at primiparity in brown bears therefore may be due to age-related changes in allocation of energy to growth and reproduction. This is supported by results from the closely related polar bear (Ursus maritimus), where litter size was affected by maternal age (Derocher and Stirling, 1994). However this trade off does not seem to involve offspring body size, because, in contrast to our prediction, the average yearling body size of offspring of primiparous females was not smaller than the average yearling body size of multiparous females (prediction 2). Dahle et al. (in press) found that body size and mass of yearling brown bears were positively

8 related to maternal size, however that the relationship between maternal age and offspring size was weak. This suggests that, whereas primiparous females may produce smaller litters, they do not seem to be less efficient in transferring energy to their cubs, which has been suggested in the guinea pig (Cavia procellus) (Künkel 2000). As predicted, a mother loses more offspring when primiparous than when multiparous (prediction 3). This loss was not related to offspring size, however, because the offspring of primiparous females are not necessarily smaller and thus not less fit than offspring of multiparous females. Instead, we found, as predicted, that the probability of cub loss of primiparous females was positively correlated to male turnover (prediction 4a), and suggestively negatively correlated to female age at primiparity (prediction 4b). Contrary to our predictions, the probability of cub loss was not related to environmental conditions or the body size of primiparous females. Population density did not influence cub loss. However we found a difference between the study areas; primiparous females lost significantly more cubs in the south than in the north. Several factors have been proposed as important for bear cub survival (Miller et al., 2003, Swenson et al., 1997; 2001). Our results showed large differences in cub mortality rates and annual mortality patterns between the study areas (Fig 1), but male turnover was the most important factor explaining cub loss of primiparous females. This suggests that SSI is the major mortality factor for cubs of primiparous females. This is also supported by the timing of cub loss, because most primiparous females lost their cubs during the mating season (Table 2). According to the SSI-hypothesis, an infanticidal male should not kill his own young (Hrdy, 1979). This has been confirmed in brown bears in the south (Bellemain et al., 2006). Thus, the death of adult males would likely promote the influx of immigrating males (Young and Ruff, 1982) and/or possibly realignment of the home ranges of adult males (Swenson, 2003). This would result in males coming into contact with litters that they did not father. The correlation between male turnover and cub mortality has been reported from the south earlier (Swenson et al., 1997; 2001). Our results show that primiparous mothers lose more cubs than multiparous females, which suggests that primiparous mothers are less experienced or efficient in defending their cubs against infanticidal males. High initial mortality of adult males and low male immigration rates, apparently due to illegal killing, kept numbers of adult males low (1-3 males) in the north until 1996. Then recruitment of locally produced young males and probably increased immigration from the increasing population from nearby areas increased the number of males by 3-4 times

9 (Swenson et al. 2001; Swenson JE, unpublished). This has probably has resulted in increased loss of cubs with primiparous mothers due to SSI in the north at the end of our study period. The probability of cub loss of primiparous females was suggestively negatively correlated to female age at primiparity. Our results suggest that females primiparous at age 4 lost cubs most often (Table 2). Only females in the south reached primiparity at this age, but the age of first successful litter in both study areas were very similar (Swenson et al., 2001). The differences in age of primiparity between the study areas may be related to the more favorable environmental conditions in the south, which may enable females to reach primiparity earlier. It is unclear why females primiparous at age 4 have a higher probability of cub loss. This result was not related to a larger body size of females that were primiparous at later ages, because body size at primiparity did not influence the probability of cub loss. In addition, observations in more southern parts of Europe show that females can successfully raise cubs already at age 3 (Frkoviþ et al., 2001; Zedrosser et al., 2004). It may be that in a population where SSI is a major source of cub mortality, an additional year of experience with other bears increases a young females chance of successfully raising a litter. From the point of view of lifetime reproductive success it may be of advantage for young female brown bears to reproduce as early as possible because male turnover is unpredictable in space and time. Differences in the reproductive performance of primiparous and multiparous seem to be independent of environmental conditions. The major cause of cub loss of primiparous females seems to be SSI, which should be independent of environmental conditions, as has also been found by Swenson et al. (2001). In contrast, Miller et al. (2003) suggested that variations in brown bear cub survivorship may be influenced by local environmental factors in Alaska. Experimental evidence in birds suggests that age-specific reproductive success is independent of environmental effects (Daunt et al., 1999). In our study, there was almost no cub loss in the north, whereas cub loss in the south was evenly distributed through the entire study period (Fig 1). This strongly suggests that the differences in cub mortality of primiparous females between our study areas must be independent of environmental fluctuations. The importance of SSI in brown bear populations remains under debate among biologists (e.g.: McLellan, 1994; 2005; Miller et al., 2003; Swenson et al., 1997; 2001; Wielgus and Bunnell, 2000). While researchers in Europe have found support for the SSI- hypothesis (Swenson et al., 1997; 2001), results from North America are not as clear (McLellan 2005; Miller et al., 2003; Wielgus and Bunnell, 2000). A possible explanation for

10 some of these differences may be the higher age of primiparity in North America, because our results suggest that females being primiparous at older ages lose fewer cubs. We conclude that cub loss of primiparous female is related to SSI, a pattern that has been confirmed before for females generally in Scandinavia (Swenson et al., 1997; 2001). In areas without SSI (north), primiparous females do not seem to loose cubs, whereas in areas with SSI (south), cub loss of primiparous females was high. Primiparous mothers lose more offspring than multiparous mothers, which suggests that they are less able/experienced in defending their offspring. Because cub loss in primiparous females was not related to environmental conditions, their body size or population density, this suggests that SSI is an even more important agent of cub mortality in primiparous than multiparous females. In general, females in the south were primiparous earlier than females in the north, however the ages of first successful litter were the same in both areas. We found suggestive evidence that females primiparious at age 4 in the southern study area had the highest probability of cub loss, maybe due to their low level of experience with other bears in their area. The probability of cub loss of primiparous females was not related to environmental conditions, their body size or population density.

ACKNOWLEDGEMENTS The Scandinavian Brown Bear Research Project (SBBRP) was funded by the Swedish Environmental Protection Agency, the Norwegian Directorate for Nature Management, the Swedish Association for Hunting and Wildlife Management, WWF Sweden and the Research Council of Norway. We thank the research personnel of the SBBRP for their assistance in the field. AZ was financially supported by the Austrian Science Fund project P16236-B06.

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13 Støen OG, Zedrosser A, Sæbø S, Swenson JE. 2006. Inversely density-dependent natal dispersal in brown bears Ursus arctos. Oecologia, DOI: 10.1007/s00442-006-0384-5.

Swenson JE. 2003. Implications of sexually selected infanticide for the hunting of large carnivores. In: Animal behavior and wildlife conservation. (Festa-Bianchet M., Apollonio M, eds). Washington DC, USA: Island Press; 171-190.

Swenson JE, Sandegren F, Söderberg A, Bjärvall A, Franzén R, Wabakken P. 1997. Infanticide caused by hunting of male bears. Nature 386: 450-451. Swenson JE, Sandegren F. 1999. Mistänkt illegal björnjakt i Sverige. In: Statens Naturvardsverket, editor. Bilagor till Sammanhållen rovdjurspolitik; Slutbetänkande av Rovdjursurstredningen. Statens offentliga utredningar 1999, 146., Stockholm, Sweden; 201-206. Swenson JE, Sandegren F, Brunberg S, Segerström P. 2001. Factors associated with loss of brown bear cubs in Sweden. Ursus 12: 69-80. Sæther B-E, Engen S, Swenson JE, Bakke Ø, Sandegren F. 1998. Assessing the viability of Scandinavian brown bear, Ursus arctos, populations: the effect of uncertain parameter estimates. Oikos 83: 403-416. Tuomi J, Hakkala T, Haukioja E. 1983. Alternative concepts of reproductive effort, costs of reproduction, and selection in life-history evolution. Am Zool 23: 25-34. Wang Z, Novak MA. 1994. Parental care and litter development in primiparous and multiparous prairie voles (Microtus ochrugaster). J Mammal 75: 18-23. Wauters L, Bijnens L, Dhondt AA. 1993. Body mass at weaning and local recruitment in the red squirrel. J Anim Ecol 62: 280-286. Wielgus RB, Bunnell FL. 2000. Possible negative effects of adult male mortality on female grizzly bear reproduction. Biol Conserv 94: 145-154. Williams GC. 1966. Natural selection, the cost of reproduction, and a refinement of Lack’s principle. Am Nat 100: 687-690. Young BF, Ruff RL. 1982. Population-dynamics and movements of black bears in east central Alberta. Journal of Wildlife Management 46: 845-860. Zar JH. 1984. Biostatistical analysis. New Jersey: Prentice Hall. Zedrosser A, Rauer G, Kruckenhauser L. 2004. Early primipairty in brown bears. Acta theriol 49: 427-432. Zedrosser A, Dahle B, Swenson JE. Population density and food conditions determine body size in female brown bears. J Mammal; in press.

14 Table 1 Mean age of first reproduction and proportion of female brown bears first giving birth at a given age in two study areas in Scandinavia in 1987-2004. SE = Standard error, N = sample size.

Study area Mean age of primiparity (± SE) 4 years 5 years 6 years N South 4.69 ± 0.70 0.435 0.435 0.13 23 North 5.00 ± 0 0 1.00 0 14

15 Table 2 Timing of cub loss in relation to age at primiparity for primiparous female brown bears in two study areas in Scandinavia in 1987-2004. The pre-mating season is the time period from leaving the den until the second week of May; the mating season is the time period from the third week of May until the first week of July. Primiparous females were not observed loosing cubs outside these two time periods. The proportion is given in parentheses, N = sample size.

Study area Age at primiparity Timing of cub loss No loss N Pre-mating season Mating season South 4 2 (0.20) 7 (0.70) 1 (0.10) 10 5 - 5 (0.50) 5 (0.50) 10 6 - 1 (0.33) 2 (0.66) 3 North 5 - 2 (0.28) 12 (0.72) 14

16 Table 3 Probability that a primiparous female brown bear lost at least on cub from a litter in two study areas in south-central and northern Sweden from 1987-2004. The binary response variable was the probability of "loss of one or more cubs". The predictor variables available were study area (south or north), male turnover (the number of adult male deaths in a radius of 40 km 1.5 years previously), age at primiparity, body size at primiparity, and environmental conditions, while controlling for population density (N: South = 23; North = 14). Only significant (p”0.05) and suggestive (p”0.1) predictors are shown.

Variable ȕ S. E. df p

Study area

South 0 0 North -2.441 1.108 1 0.029

Male turnover 1.480 0.751 1 0.049

Age at primiparity -1.588 0.909 1 0.081

17 Figure 1 Cub loss (No: no cub loss from spring to fall; Yes: loss of one or more cubs from spring to fall) of primiparous female brown bears in two study areas in Scandinavia from 1987-2004. Points are jittered to reduce overlap. Filled triangles indicate a litter with male turnover in the vicinity (at least 1 adult male dying within 40 km1.5 years previously), open triangles indicate litters without male turnover in the vicinity, “?” indicates litters with no information on male turnover in the vicinity (N: South = 23; North = 14).

South

Yes Cub loss

No 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 Year

North

Yes Cub loss

No ? 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 Year

18 Paper VII

Terrain use by brown bears in relation to resorts and human settlements

Christian Nellemann1, Ole-Gunnar Støen2, Jonas Kindberg3, Jon Swensson2,4, Ingunn Vistnes2 Göran Ericsson3, Jonna Katajisto5, Bjørn Kaltenborn6 and Jodie Martin7

1United Nations Environment Programme, GRID Arendal, Fakkelgården, Storhove, NO-2624 Lillehammer, Norway 2Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P. O. Box 5003, NO-1432 Ås, Norway 3Department of Animal Ecology, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden 4Norwegian Institute for Nature Research, Tungasletta 2, NO-7485 Trondheim, Norway 5Department of Biological and Environmental Sciences, PO Box 65, 00014 University of Helsinki, Finland 6Norwegian Institute for Nature Research, Fakkelgården, Storhove, NO-2624 Lillehammer, Norway 7 Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558 - Université Lyon 1, 43 Bd du 11 novembre 1918, 69622 Villeurbanne Cedex. France

Abstract: Brown bears (Ursus arctos) were once widespread across the Northern Hemisphere, but have been hunted to local extinction in large areas of their former range. In addition, human infrastructure and land use have fragmented bear habitats. Conservation efforts in Sweden have now increased the number of Scandinavian bears to about 2,200 individuals, but large areas remain unused, even in high-density bear regions. We analyzed habitat use of 106 radio-collared male (51) and female (55) brown bears in relation to terrain ruggedness, habitat type, and distance to towns and resorts in 1985-2003. In addition, distributions of 145 individual bears were derived from DNA analyses of bear scats collected independently by hunters during 2001. Habitat use derived from radio collar data and scat data revealed similar results. More than 74% of all female bear locations were in the 29% of the area classified as rugged and forested located >10 km from any town or resort, rugged forested habitat near towns or resorts was avoided. Over a twenty year period, only 9% of all female bear locations were located within 10 km from towns or resorts, although this represented 40% of the study area and in spite of bears emigrating from the area. This

1 suggests that towns and resorts were a negative and disturbing factor for bears. Males also preferred undisturbed rugged forested terrain types, but apparently also used bogs and flatter terrain > 10 km from towns and resorts more often than females did. Currently 1-5% of the forest area is protected against piecemeal development, and more than 7,000 new recreational cabins are built annually in Norway and Sweden. Because bears are sensitive to human disturbance, a coordination of ongoing recreational developments is needed to avoid further degradation of the brown bear habitat quality in Scandinavia

Introduction The brown bear (Ursus arctos) became locally extinct across large parts of Scandinavia in the 19th century, mainly as a result of state-sponsored extermination campaigns (Swenson et al., 1994; 1998). Extensive conservation and protection efforts in Sweden resulted in growth of the bear population from approximately 300 bears in 1930 to about 2200 in 2004 (Swenson et al., 1998; Kindberg et al., 2004). Although this has resulted in an increased distribution of bears, re-colonization, especially by females, has occurred in only a portion of the former range (Swenson et al., 1994; 1998). Throughout its circumpolar range, the brown bear has also been threatened by overhunting, habitat fragmentation and habitat loss (UNEP, 2001; Uotila et al., 2002; Waller and Servheen, 2005). During the 20th century, the development of roads, settlements, mineral exploration sites and more intensified forestry has resulted in dramatic reductions in wilderness areas and subsequent loss of undisturbed bear habitat (Gibeau et al., 2002; Kaczensky et al., 2003; Nielsen et al., 2004a; 2004b). Anthropogenic disturbance of bears has led to avoidance of areas close to disturbance (McLellan and Shackleton, 1988; Gibeau et al., 2002; Johnson et al., 2005) and displacement of home ranges (McLellan and Shackleton, 1989). Infrastructure has also been documented to act as semi-permeable barriers to bear movements (Chruszcz et al., 2003). However, little is known about how the large-scale development of outdoor recreational resorts and construction of second-home cabins may be influencing the availability and quality of bear habitat (Mattson et al, 1992; Elgmork, 1994; Mace and Waller, 1996; Gibeau et al., 2002; Boyce and Waller, 2003; Apps et al., 2004). This is a potential problem in Scandinavia, because more than 2,000 recreational cabins are constructed annually in Sweden (Statistics Sweden, 2003), and more than 5000 annually in Norway (Nellemann et al., 2003). Human-caused habitat fragmentation may potentially influence the recolonization of former bear habitat (Gaines, 2003; Apps et al., 2004; Johnson et al., 2004). Hence, an

2 understanding of bear habitat use in increasingly human-dominated landscape is important for conservation and efforts to further develop networks of protected areas (Powell et al., 1996). In this study we compare bear densities across various terrain and vegetation types in relation to distance from resorts and towns.

Methods Study area The study area was located in Dalarna and Gävleborg counties in south-central Sweden and Hedmark County in southeastern Norway (61º N, 18º E; Fig. 1). The outer boundary was delineated by municipality or county borders or natural terrain features such as ridges and hills. The rolling landscape in this area is covered with coniferous forest, dominated by Scots pine (Pinus sylvestris) and Norway spruce (Pica abies). Over 95% of the study area is forest covered. There is an extensive road system consisting of small, closely spaced graveled logging roads and paved public roads with more traffic. Six towns and settlement areas, ranging in size from 3000-11,000 inhabitants, and 2 major tourist resort areas with cabin resorts and down-hill skiing facilities, are located within the study area. The resorts have only 100-500 permanent residents, but a very large number of tourists. In 2001, the largest resort had 1,000,000 visitor nights, distributed throughout the year with peaks in late winter, mid- summer and fall (Statistics Sweden, 2003). Fulufjellet National Park (380 km2) was established adjacent to this cabin resort area in the north-western portion of the study area in 2002. The number of visitors to the park increased by 40% from 2001 to 2003 (53,000 visitors in summer 2003; European Tourism Research Institute, 2005). Bears have been abundant in the area for more than 30 years and the numbers have been fairly stable during the last decade, although increasing at the western, eastern and southern edges (Swenson et al. 1998, Solberg et al. 2006).

Habitat classification The study area was divided into 771 4x4 km squares. The size of the squares was chosen , because it was appropriate to describe the relative ruggedness of the area according to terrain sampling techniques (Nellemann and Fry, 1994). Thirteen squares covered by water and mountains above 1,000 m were excluded, leaving 758 squares with continuous Norway spruce (Picea abies), birch (Betula pubescens) and Scots pine (Pinus sylvestris) forest and bogs and semi-open meadows. Squares were classified as “forest or “bogs” if more than 50% of the coverage was forest or bogs, respectively. We further classified each square according

3 to terrain ruggedness indices (TRI; Nellemann and Thomsen, 1994). The method has been used to help explain habitat selection of large ungulates such as reindeer (Rangifer tarandus tarandus), caribou (Rangifer tarandus granti), muskoxen (Ovibos moschatus) and African elephants (Loxodonta africana) (Nellemann and Cameron, 1996; Nellemann and Reynolds, 1997; Vistnes and Nellemann, 2001; Nellemann et al., 2002), and small predators like the Arctic fox (Alopex lagopus; Eide et al., 2001). In brief, terrain ruggedness is calculated as a function of changes in terrain aspects (“ups and downs”) and contour densities along 4 km transects within each grid cell, using 1:100,000 scale maps and contour intervals of 10 m (see details in Nellemann and Thomsen, 1994). Sites were classified as rugged (TRI • 2.5, comparable > 5 “ups and downs” across a 4-km transect) or flatter terrain (TRI < 2.5). We also classified all areas according to distance from towns and tourist resorts in the area. Reviews of disturbance studies have revealed that the majority of animals impacted by human activity primarily are disturbed within 10 km from infrastructure (Nellemann et al., 2003). We therefore classified areas beyond 10 km from towns and resorts as relatively low disturbance areas. Hence, we could compare the use of habitat and terrain types >10 km from towns and resorts with comparable habitat nearer (< 10 km) towns and resorts, respectively.

Brown bear abundance To estimate the abundance of bears within the squares, we randomly selected locations of radio-collared brown bears within the study area. From 1985-2002 a total of 55 female and 51 male brown bears 2 years and older (i.e. post weaning) carried radio collars within the study area (Støen et al., 2005). We estimated ages of bears not followed from birth by counting the annuli in a cross-section of a premolar root, which is a relatively accurate method (Matson et al. 1993). All age determinations were done by Matson’s Laboratory, Milltown, Montana, USA. The radio-collared bears were located approximately weekly in their active period using standard triangulation methods from the ground or from the air (Dahle and Swenson 2003a). To eliminate auto-correlated data, we only used locations separated by at least 100 hours, which corresponds to the minimum time between the weekly localizations of the bears. To avoid locations influenced by denning behaviour, we only used positions from June, July, August and September. Using these criteria, we obtained 4,150 radio locations of female bears and 2,323 radio locations of male bears. From these locations we selected 10 positions randomly from each individual, i.e. 550 female locations and 510 male locations. Of these, 515 female locations and 324 male locations were within the 758 squares. A population-size estimate, based on a DNA analysis of non-invasive sampling of scats, was carried out in the

4 study area in 2001 (Bellemain et al., 2005). As an additional measure of bear abundance, we selected the location of one random scat from each identified individual, which gave 88 female and 57 male scat locations within the 758 squares.

Statistics Statistical analyses were performed in Sigmastat (Kuo et al., 1992). Data were first subjected to a Kolmogorov-Smirnov test for normality. Comparisons in abundance of bear locations were made using the non-parametric Kruskal-Wallis analysis of variance with Dunn’s tests for multiple comparisons. Use versus availability was tested using the chi-square test. If significant differences were found, the Bonferroni z-statistic test was use to determine differences in use versus availability of the individual habitat types (Neu et al., 1974). P- values less than 0.05 were considered statistically significant.

Results Selection of rugged terrain far from human settlements based on radio-telemetry Within areas > 10 km from towns and/or resorts, the abundance of radio-telemetry locations of female bears was significantly higher in rugged forested terrain (0.108 ± 0.008 locations/km2) than in flatter forested terrain (0,036 ± 0.006 locations/km2) or in bogs (0,016 ± 0.003 locations/km2), both P < 0.01. Use was significantly higher than expected from availability in rugged forested areas far from human settlements for both female and male bears (Figs 2 and 3a-b). These areas comprised 29% of the study area, but contained 74% of all female and 57% of all male bear locations. Flatter, forested terrain far from human settlements was used according to availability by both females and males (Fig. 3a-b). All areas dominated by bogs were used less than expected by both males and females.

Avoidance of human settlements and resorts by bears based on radio-telemetry The number of female and male bear locations in forested rugged terrain far from human settlements and resorts was significantly higher than in any other habitat type (P<0.05). Both males and females used all areas <10 km from both towns and resorts less than expected from availability (Fig. 3 a-b). The largest resort had 1 million visitor nights, but the abundance of bear locations was just as low within 10 km from this as from towns with 3- 10,000 permanent residents. There was no statistical difference between the abundance of bear locations in rugged forested terrain in areas near resorts compared to similar habitat near towns (P=0,11). Rugged, forested terrain near towns and resorts comprised more than 20% of

5 the study area, but contained less than 7% of all female bear locations and 10% of all male locations. Overall, 40% of the study area (4864 km2) was classified as <10 km from towns and resorts, but contained only 9% of the female bear locations and 15% of the male locations. Within rugged forested terrain, the abundance of female bear locations in <10 km from towns and resorts areas was 81-95% lower than for areas far (<10 km) from towns and resorts (0.021 ± 0.004 and 0.005 ± 0.002 locations/km2 <10 km from towns and resorts, respectively; compared to 0,108 ± 0,008 locations/km2 in areas far form them; P < 0.05). Hence, when excluding bogs, flatter forested terrain and areas <10 km from resorts or towns, the remaining patches of rugged terrain corresponded closely to the distribution of recorded bear locations (Fig. 4a-d). The abundance of male locations appeared to be somewhat higher than that of females for bog dominated and flatter forested terrain types . The abundance was as expected or lower than expected from availability (Figs 2 and 3a-b). Overall, males used areas >10 km from towns and resorts more than areas < 10 km from towns and resorts.

Results based on non-invasive sampling of scats Corresponding patterns of habitat use and avoidance of areas <10 km from human settlements also were found with the distribution of individual bears as determined from DNA in scats collected. Of 145 locations of individual bears, 61% of the females and 47% of the males were located in the 29% of the landscape constituting rugged forested terrain >10 km from towns and resorts, significantly greater than expected from availability (P < 0.05 for both females and males; Fig. 5). All other categories were used according to availability. Scat data revealed some variation between towns and resorts, with resorts tending to have a lower abundance of bears within 10 km than towns (Fig. 5) . There was no difference in abundance of bear scat locations between flat forested terrain and areas dominated by bogs, independent of distance from towns and resorts (all P-values > 0.05).

Discussion Use of rugged forested terrain Both radio-telemetry data and scat data revealed that rugged forested terrain >10km from towns and resorts was the most preferred habitat for both male and female bears in the study area. Males used areas >10 km from town and resorts more than any habitat <10 km from towns and resorts, even for flatter forested terrain. Rugged terrain may provide particular benefits to bears. Terrain ruggedness influences plant composition and plant phenology

6 (Nellemann and Thomsen, 1994). The frequent changes in aspect also may influence the availability of denning sites (Linnell et al., 2000), food plants and the abundance of ant hills by providing numerous south facing slopes (Lyons et al., 2003; Nielsen et al., 2004a; 2004b; 2004c). Previous studies have shown preferences for rugged terrain by bears (Apps et al., 2004; Nielsen et al., 2004b). Rugged terrain may also provide better cover and lower human access (Nielsen et al., 2004a).

Effects of human activity Towns and resorts were generally avoided by bears. Although resorts have only 5 - 30% permanent residents compared with towns in the area, most of the people visiting the resorts primarily go there for outdoor recreation activities. The number of visitor nights in the largest resort, was 1 million per year and corresponds to 2739 every day on average, but with peaks in later winter, mid-summer and early fall. The towns, in comparison, have 3-10,000 permanent residents, but quite different traffic patterns, particularly much lower off-road traffic, but higher on the roads due to workers, shoppers, and school children living outside the town centers and only coming in during daytime on the main roads. The traffic patterns around recreational resorts in summer and fall are in contrast a product of off-road activities such as hunting, fishing and hiking, a large share following an intensively used network of trails away from the actual cabins through the woods. Hence, the disturbance reaches far beyond that of the physical footprint of the actual resorts and cabins. Most traffic around towns tend to concentrate more in the vehicle transportation infrastructure and corridors, and around different types of utilities and settlement areas, which may explain why the seemingly much smaller resorts still have little bear use within 10 km. The large avoidance zone for both types of settlements, however, is a function of traditionally active outdoor-activities in both resorts and town, including berry-picking, hunting, fishing etc. While people go to resorts primarily for outdoor activity, there is also a certain amount of this activity around permanent settlements. Avoidance of the areas of greatest human activity or traffic is well known from North America (Mace and Waller, 1996; Gibeau et al., 2002; Boyce and Waller, 2003; Chruszcz et al., 2003; Waller and Servheen, 2005). The avoidance and low use by bears of areas surrounding major roads and human settlements has been described in numerous bear studies in recent years from North America, Asia and Europe (Clevenger et al., 1992; Mace et al., 1996; Vander Heyden and Meslow, 1999; Huygens et al., 2001; Wielgus et al., 2002; Kaczensky et al., 2003; Johnson et al. 2005; Preatoni et al., 2005). Avoidance of human

7 disturbance is also well known for some other species of wildlife, including birds and ungulates (Reijnen et al., 1996; Forman and Alexander, 1998; UNEP, 2001; Vistnes et al. 2001; Nellemann et al. 2003).

Sexual differences in sensitivity to disturbance Female brown bears were most often located in the most rugged terrain farthest from resorts and towns. Whereas this also was true for the male bears, males also used areas within 10 km from settlements as expected from availability, thus they exhibited a greater tolerance than females (Gibeau et al., 2002). The same was true for flatter forested terrain and terrain dominated by bogs. Correspondingly, as the rugged forested terrain likely offered better food conditions, such terrain types closer to disturbance are likely to be used by more disturbance- tolerant individuals, typically younger male bears (Mueller et al., 2004). However, in spite of the large availability of rugged forested terrain near human settlements, these habitats were still only used as available or less than available, generally below that of undisturbed flatter forested habitat (Fig. 2). For all habitat categories near human activity and flatter forested habitats, there was a trend towards higher abundance of male than female bears.

Implications for dispersal and population expansion Although the bear population has grown (Sæther et al. 1998), the density of brown bears has been fairly stable in the study area in the past 10 years (Solberg et al. 2006), suggesting that little expansion has taken place into the disturbed parts of the study area where development has increased, mainly in the resorts. Dispersal in brown bear populations is sex-biased, with most of the females establishing their breeding home ranges in or adjacent to their natal areas and males dispersing long distances from their mothers’ home range (Glenn and Miller, 1980; Blanchard and Knight, 1991; McLellan and Hovey, 2001). In Scandinavia, however, more than 40% of the females disperse away from their natal areas and the dispersal probability and dispersal distances are inversely density dependent in both males and females (Støen et al., in press). The net growth in the bear population in our study area has apparently largely resulted in emigration out of the study area, primarily by juveniles (Swenson et al., 1998; Solberg et al. 2006, Støen et al. 2006), not occupation of the more disturbed areas within the study area in spite of the bears travelling through these areas. Abundance of towns and farmland increases substantially to the south, east and west of the study area with few undisturbed corridors available to migrating bears. This may restrict population expansion in the future.

8 Implications for conservation Resorts apparently had significant influence on bear movements and habitat choice, as much as towns with many more permanent inhabitants. The selection of undisturbed rugged forested terrain by bears results in minimizing bear-human encounters and conflicts (Olson et al., 1997), and bears tend to abandon the study area rather than habituating. Currently, more than 7000 new recreational cabins are built in Norway and Sweden every year, although not all are within the range of brown bears. In many cases, they form resorts with shops, hotels and extensive trail systems, and in some cases, smaller previously disconnected resorts merge and generate long corridors of development, typically in the low-alpine zone and in the boreal forest. Most resort and town planning is left to municipalities with boundaries very seldom following those of bear habitats. If the degradation of brown bear habitat is to be avoided municipalities must coordinate their planning regarding establishment of resorts and recreational cabins in order to secure protection of large undisturbed patches of rugged forested terrain and potential bear migration routes between such patches. This will be necessary to fulfil the Swedish goal of establishing female bears throughout the present range of brown bears in Sweden. Unfortunately, there are presently few national policies in place to secure continuous undisturbed wildlife habitat against piecemeal development (UNEP, 2004).

Acknowledgements This study was funded by the Norwegian Directorate for Nature Management, the Swedish Environmental Protection Agency, the Swedish Association for Hunting and Wildlife Management, WWF Sweden, the Research Council of Norway, and the Norwegian University of Life Sciences. We thank the personnel in the Scandinavian Brown Bear Research Project for their assistance in the field and Orsa Communal Forest for field support. We also thank Pierre Taberlet and Eva Bellemain for the genetic results. All capture and handling of bears reported in this paper complied with the contemporary laws regulating the treatment of animals in Sweden and Norway and was approved by the appropriate management agencies and ethical committees in both countries.

9 References

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11 Mattson, D. J. Blanchard, B. M., and Knight, R. R. 1992. Yellowstone grizzly bear mortality, human habituation, and whitebark-pine seed crops. Journal of Wildlife Management 56, 432-442. McLellan, B. N., and Hovey, F. W. 2001. Natal dispersal of grizzly bears. Canadian Journal of Zoology 79, 838-844. Mueller, C., Herrero, S., and Gibeau, M. L. 2004. Distribution of subadult grizzly bears in relation to human development in the Bow River Watershed, Alberta. Ursus 15, 35-47. Nellemann, C., and Thomsen, M. G. 1994. Terrain ruggedness and caribou forage availability during snowmelt on the Arctic Coastal Plain, Alaska. Arctic 47, 361-367. Nellemann, C., and Cameron, R. D. 1996. Effects of petroleum development on terrain preferences of calving caribou. Arctic 49, 23-28. Nellemann, C., and Reynolds, P. E. 1997. Predicting late winter distribution of muskoxen using an index of terrain ruggedness. Arctic and Alpine Research 29, 334-338. Nellemann, C., Moe, S. R., and Rutina, L. P. 2002. Links between terrain characteristics and forage patterns of elephants (Loxodonta africana) in northern Botswana. Journal of Tropical Ecology 18, 835-844. Nellemann, C., Jordhøy, P., Vistnes, I., Strand, O., and Newton, A. 2003. Progressive impacts of piecemeal development. Biological Conservation 113, 307-317. Neu, C. W., Byers, C. R., and Peek, J. M. 1974. A technique for analysis of utilization- availability data. Journal of Wildlife Management 38, 541-545. Nielsen, S. E., Herrero, S., Boyce, M. S., Mace, R. D., Benn, B., Gibeau, M. L., and Jevons, S. 2004a. Modelling the spatial distribution of human-caused grizzly bear mortalities in the Central Rockies ecosystem of Canada. Biological Conservation 120, 101-113. Nielsen, S. E., Boyce, M. S., and Stenhouse, G. B. 2004b. Grizzly bears and forestry I. Selection of clearcuts by grizzly bears in west-central Alberta, Canada. Forest Ecology and Management 199, 51-65. Nielsen, S. E., Munro, R. H. M., Bainbridge, E. L., Stenhouse, G. B., and Boyce, M. S. 2004c. Grizzly bears and forestry II. Distribution of grizzly bear foods in clearcuts of west-central Alberta, Canada. Forest Ecology and Management 199, 67-82. Olson, T. L., Gilbert, B. K., and Squibb, R. C. 1997. The effects of increasing human activity on brown bear use of an Alaskan river. Biological Conservation 82, 95-99. Pasitschniak-Arts M (1993) Ursus arctos. Mammalian Species 439:1-10

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14 Figure 1. Location of the study area in the southern part of central Sweden and adjacent Norway.

15 Figure 2. Use (mean ± 95% C.I.) by 55 radio-collared female (closed dots) and 51 male brown bears (open triangles) and the proportion of nine different forest habitat types available in the study area (bars) (10 random positions per animal in June-September 1985-2003), Dalarna, Sweden.

1,0 Expected proportion 0,9 Observed proportion with 95 % C.I. 0,8

0,7

0,6

0,5

0,4

Proportion in area 0,3

0,2

0,1

0,0 Rugged terrain > 10 km from settlem from > 10 km Rugged terrain settleme terrain from Flatter > 10 km settlement from > 10 km Bogs towns from < 10 km Rugged terrain towns terrain from < Flatter 10 km Bogs < 10 km from towns resorts from < 10 km Rugged terrain Flatter terrain resorts < from 10 km resorts from < 10 km Bogs

16 Figure 3a-b. Relative use of rugged forested, flatter forested and bog-dominated terrain types by radio-collared male (n=51) and female (n=55) brown bears in three disturbance categories given as percent of expected from availability (presented as 0-line), June-September 1985- 2003, Dalarna, Sweden. * indicates significant difference using the Bonferrroni z-test..

Female bears

> 10 km from 0-10 from towns 0-10 km from cabin 300 settlement resorts a *

200 More - Less More

100

0

* -100 * * * * Use of habitat (%) versus availability * *

-200 Male bears 0-10 km from cabin > 10 km from 0-10 from towns 300 settlement resorts b

200 * More - Less More 100

0

* * -100 *

Use versus availability of habitat (%) of Use versus availability *

-200 Rugged terrainsettl. > 10 kmfrom Flattersettl. terrain > 10 kmfrom settlement from km 10 > Bogs towns from km < 10 terrain Rugged Flatter terrain from < 10 km towns from towns km 10 < Bogs resorts from km < 10 terrain Rugged Flatter terrain from< 10 km resorts resorts from km 10 < Bogs

*

17 Figure 4a-d. The locations of major roads, towns and tourist resorts (a), the location of undisturbed rugged terrain (high TRI) (b), and the distribution of random radio-telemetry locations from 51 male (c) and 55 female brown bears (d) (10 random positions per animal in June-September 1985-2003, Dalarna, Sweden).

18 Figure 5. Use (mean ± 95% C.I:) versus availability (bars) of 142 individual female (·) and male (ǻ) brown bears as determined from locations of individuals, based on DNA analysis of collected scats (Solberg et al. 2006) according to habitat categories in September-October 2001, Dalarna, Sweden.

1,0 Expected proportion 0,9 Observed proportion with 95 % C.I. 0,8

0,7

0,6

0,5

0,4

Proportion in area Proportion 0,3

0,2

0,1

0,0 Rugged terrain from settl. > 10 km settl. terrainFlatter from > 10 km from settlement 10 km Bogs> Rugged terrain from towns < 10 km towns terrainFlatter from < 10 km from towns < 10 km Bogs Rugged terrain from resorts < 10 km resorts terrainFlatter from < 10 km from resorts < 10 km Bogs

19 ISBN 82-575-0699-0 ISSN 1503-1667

Scandinavian Brown Bear Research Project Dept. of Ecology and Natural Resource Management Norwegian University of Life Sciences P.O.Box 5003 NO-1432 Aas, Norway Phone: +47 64 96 57 30 www.bearproject.info

Norwegian University of Life Sciences NO–1432 Aas, Norway Phone +47 64 96 50 00 www.umb.no, e-mail: [email protected]