Winter Ethology of Free-Ranging Brown Bears (Ursus Arctos) in Central Sweden

Winter ethology of free-ranging brown bears (Ursus arctos) in central Sweden

Dissertation

zur Erlangung des Doktorgrades der Naturwissenschaften

vorgelegt beim Fachbereich 15 - Biowissenschaften der Goethe-Universität in Frankfurt am Main

von Andrea Friebe aus Frankfurt am Main Frankfurt 2014 D 30

Winter ethology of free-ranging brown bears (Ursus arctos) in central Sweden

Dissertation

zur Erlangung des Doktorgrades der Naturwissenschaften

vorgelegt beim Fachbereich 15 - Biowissenschaften der Goethe-Universität in Frankfurt am Main

von Andrea Friebe aus Frankfurt am Main Frankfurt 2014 D 30

vom Fachbereich 15 – Biowissenschaften der Goethe-Universität Frankfurt am Main als Dissertation angenommen.

Dekanin: Prof. Dr. A. Starzinski-Powitz

1. Gutachter: Prof. Dr. Günther Fleissner, Institut für Zellbiologie und Neurowissenschaften Goethe-Universität Frankfurt am Main

2. Gutachter: Prof. Dr. Manfred Kössl, Institut für Zellbiologie und Neurowissenschaften Goethe-Universität Frankfurt am Main

Datum der Disputation: 03. Februar 2015

To one of the most generous and wonderful persons in my life

My father

Contents:

1 Introduction ...... 1 1.1 The main goals of the thesis ...... 4 1.2 The brown bear (Ursus arctos) ...... 5 1.2.1 Hibernation ...... 5 1.2.2 Reproduction ...... 6 2 Focal areas of the thesis ...... 7 2.1 The factors affecting denning behavior and den abandonment (Paper I) ...... 7 2.2 How can we detect pregnancy in free-ranging brown bears? (Paper II) ...... 10 2.3 Determination of the gestation period of free-ranging brown bears (Paper III) ...... 11 2.4 Factors influencing the timing of parturition (Paper III) ...... 11 2.5 List of papers ...... 13 3 Materials and Methods: ...... 14 3.1 Study area and population ...... 14 3.2 Bear capture ...... 15 3.3 Sensors and data collection ...... 16 4 Summary of results ...... 18 4.1 Den entry behavior in Scandinavian brown bears implications for preventing human injuries (Paper I) ...... 18 4.2 Detection of pregnancy by means of activity data (Paper II) ...... 19 4.3 Factors affecting the dates of implantation, parturition, and den entry (Paper III) ...... 19 5 Discussion ...... 21 5.1 Denning of brown bears in central Sweden...... 21 5.2 Behavior prior to den entry and den abandonment ...... 22 5.3 Can we use activity data to detect pregnancy in bears? ...... 25 5.4 The use of activity and body temperature data to determine the gestation period ...... 27 5.5 Which factors influence the timing of parturition? ...... 29 6 Future research perspectives ...... 30 7 Abstract ...... 33 8 Zusammenfassung ...... 35 9 References ...... 41 10 Compilation of papers ...... 49 Paper I ...... 50 Paper II ...... 66

Paper III ...... 79 11 Acknowledgements ...... 91

1 Introduction

Why do some species hibernate? Winter is not only characterized by low temperatures and snow, but also by the lack of food and extreme changes in habitat conditions. Some animals, like birds, migrate to warmer climates, however, mammals are not able to carry out such long- distance migrations, but rather cope with these seasonal changes by physiological or behavioral adaptations; they develop an insulating winter fur, gain adipose tissue, reduce locomotive activities, or search for a hiding place and adapt their metabolism in the form of torpor or hibernation (prolonged torpor). Torpor is characterized by a controlled reduction of physiological functions, where the metabolic rate can be reduced to less than 1% of the normothermic resting metabolic rate, and body temperature can decrease below 0 °C (Geiser, 2004, Barnes, 1989). However, hibernators do not remain torpid throughout the entire hibernation season. The bouts of torpor often last several days or weeks and are interrupted by periodic short-time arousals where biochemical and physiological parameters return to the euthermal level, probably to recover from the physiological costs caused by metabolic depression, like e.g. oxidative stress or reduced immunocompetence (Humphries et al., 2003, Prendergast et al., 2002, Astaeva and Klichkhanov, 2009). Hibernation is one of the most efficient energy-saving mechanisms, and is regularly activated before the beginning of winter (Nelson, 1973). It is known to occur in several small (< 5kg) mammals, such as ground squirrels, marmots and bats and last several days to months, depending on the species, ambient temperature, time of year, and individual's body condition (Nelson, 1973, Geiser, 1998, Humphries et al., 2003). Hibernation is also found in tropical animals and desert species, and, occurs also in larger carnivores, like badgers (Meles meles) as well as bears (Ursids). Bears were earlier not considered as true hibernators, because their body temperature does not decrease as dramatically during hibernation (generally > 30°C), as it does in other hibernators (Geiser, 1998, Tøien et al., 2011, Tanaka, 2006, Heldmaier, 2011). A study of American black bears (Ursus americanus) additionally demonstrated that bears do not show periodical arousals to normothermic levels of body temperature, as small hibernators do, maybe due to their high basal body temperature level during hibernation. Instead, multiday cycles of body temperature with a variation of 2-6 °C have been recorded (Tøien et al., 2011). Hibernation is thus defined as comprehensive metabolic suppression, rather than only based on a decline in body temperature. Therefore, species such as bears are nowadays considered as true hibernators (Heldmaier et al., 2004, Heldmaier, 2011). Bears have

additionally an exceptional position among hibernators, because they are the only mammals with delayed implantation, gestation, parturition, and lactation during hibernation (Ramsay and Dunbrack, 1986, Nelson, 1973, Nelson et al., 1973).

Hibernation necessitates a variety of complex physiological and behavioral changes to cover needs both at the general species-specific level, as well as the individual level. This variability is necessary, due to variations in the life history of individuals, such as age or physiological state, but also due to variations in habitat, and local climate. Therefore, studies of factors affecting hibernation must clearly distinguish between general mechanisms and the effects of environmental variables on an individual’s physiology and behavior. It is of special interest to understand the underlying mechanisms which trigger the timing of hibernation. Therefore, studies of physiology, behavior, and ecology must be combined in an interdisciplinary approach to gain a general understanding of hibernation strategies.

In a larger context hibernation physiology of bears has gained special interest for medical science. Bears’ ability to prevent muscle atrophia, azotemia, and osteoporosis at near-normal body temperatures during hibernation makes the bear to a unique model species for advanced human medicine research. Humans would not survive even short periods of inactivity and anuria without lethal metabolic complications, such as renal failure or extensive muscle and bone loss (Stenvinkel et al., 2013). To learn about bears' hibernation physiology on the other hand implies basic knowledge about the mechanisms allowing free-ranging bears to withstand harsh winter conditions.

This thesis deals with the winter ethology of free-ranging brown bears (Ursus arctos) in central Sweden. In Sweden, all brown bears hibernate and spend 5-7 months in their dens, depending on sex, reproductive status, age, and latitude (Friebe et al., 2001, Manchi and Swenson, 2005). The process when bears enter their dens is called denning. In Sweden brown bears mainly choose four different den types: Anthill dens, stone dens (under a large rock or glacial boulder), soil dens, and basket dens (a nest of sticks on the ground) (Elfström and Swenson, 2009, Swenson et al., 1997). Dens are usually equipped with collected bed material that mainly contains moss, berry shrubs, heather lichens or grass (personal observation).

Denning is an essential part of the ecology and reproduction of brown bears, because pregnant females give birth to cubs during winter. In polar bears (U. maritimus), only pregnant females den (Lentfer and Hensel, 1980). However, not all brown bears den, as has been reported for males in Alaska and Italy (Van Daele et al., 1990, Roth et al., 1996), for brown bears of

undetermined sex in Croatia (Huber and Roth, 1997), and also for nonpregnant females in Spain (Nores et al., 2010). To my knowledge, nondenning has not been observed in pregnant females. Denning behavior of brown bears has been studied in many different parts of the world. The start of denning has often been defined as a mean date between two locations or observations when bears arrived and remained at their den sites (Friebe et al., 2001, Manchi and Swenson, 2005, Van Daele et al., 1990, Reynolds et al., 1976, Schoen et al., 1987). However, very little information is available about the timing when free-ranging brown bears physiologically start and end their hibernation and how this hibernation process is linked to denning behavior and physical activity. Bears might be physically active in their dens without hibernating, or, in contrast, the hibernation process may have started before the bears enter their dens. Likewise, the hibernation process may have ended before or after bears emerge from their dens. In a previous study on the denning chronology of female brown bears (Friebe et al., 2001), I observed tracks of females with cubs around their dens before the estimated emergence date. Females that gave birth during hibernation left their den sites on average 24 days later than lone females. When visiting den sites of females with cubs in spring, I often found several fresh day beds indicating that bears had been physically active around the den site (Friebe et al., 2001).

Most studies of hibernation in bears, especially physiological studies, have been conducted on bears in captivity, because free-ranging bears are vulnerable to disturbance at their dens (Swenson et al. 1997; Elfström and Swenson 2009). However, captive bears often do not decide themselves when to enter their artificial dens, and thus the potential differences between the physical and the physiological onset are difficult to study. Additionally, free- ranging bears must cope with more challenging environmental factors, such as limited food availability, harsh weather conditions, and disturbances by human activities, all of which can affect their winter behavior (e.g. (Craighead and Craighead, 1972b, Reynolds et al., 1976, Servheen and Klaver, 1983). The bears must trade-off between the energy costs and benefits to decide on an optimal timing of denning. Knowledge about the timing when bears enter their dens and start hibernation or when they give birth to young in winter can give us important information for bear conservation, such as how to minimize human disturbance during the critical hibernation period. Pregnant females play a crucial role in population dynamics (Sæther et al., 1998). Previous studies have shown that disturbance of pregnant female brown bears during winter can lower their reproductive success (Swenson et al., 1997). Information about denning behavior may also improve the safety of humans and bears.

Although the Scandinavian brown bear is not an aggressive bear, as long as it is not wounded, bears at dens are associated with higher levels of aggression (Swenson et al., 1999, Linnell et al., 2000, Moen et al., 2012). However, it is still unknown if the presence of the den or if the bears’ physiological condition is the reason for this higher aggression.

1.1 The main goals of the thesis

My main goals were to:

1. Evaluate which factors affect den entry of brown bears in Sweden (paper I). 2. Investigate whether activity and movement behavior prior and during the onset of denning can explain the higher risk of attacks on humans during this time period (paper I). 3. Evaluate if the frequency of den abandonment is caused by different hibernation strategies (paper I). 4. Develop and test a method to detect pregnancy in free-ranging hibernating bears based on activity recordings (paper II). 5. Investigate changes in activity and body temperature during the gestation period of free-ranging hibernating bears (paper III). 6. Evaluate which factors affect the timing of parturition in free-ranging hibernating brown bears (paper III).

Below I give a short general introduction of the brown bear and its hibernation and reproductive biology. Then I will describe how my results have contributed and increased our knowledge about these areas and about the brown bear in general.

1.2 The brown bear (Ursus arctos)

The brown bear is a large nonsocial carnivore that is distributed over much of the Northern Hemisphere in Europe, Asia, and North America. Brown bears live in a great variety of habitats, including treeless arctic tundra, grasslands, boreal forest, forested and alpine mountains, and deserts. Overharvest and habitat destruction are the major reasons why brown bear populations have declined or become fragmented in much of their range (Servheen, 1990, Zedrosser et al., 2001).

Brown bears are sexually dimorphic. Males are up to 2.2 times larger than females. Asymptotic spring body mass averages 115 ± 8.6 kg for females and 248 ± 24.9 kg for males in our study area in central Sweden (Swenson et al., 2007). In Sweden, annual home ranges overlap and male bears typically have larger home ranges (median: 1055 km2) than females (median: 124-217 km2, depending on reproductive status) (Dahle and Swenson, 2003). Brown bears are omnivorous and their diet varies among populations and seasons. In Scandinavia, the diet is mainly composed of graminoids, forbs, berries, ants, and ungulates (Dahle et al., 1998, Persson et al., 2001). During spring and early summer, adult brown bears accumulate lean mass reserves (Hilderbrand et al., 1999) from foods rich in protein (Swenson et al., 2007). The period of fat accumulation (hyperphagia) starts in August, when the bears consume mainly berries rich in carbohydrates to gain adipose fat tissue before entering the winter den (Dahle et al., 1998).

1.2.1 Hibernation

Brown bears in Sweden spend half of their life in winter dens and hibernate between 5 -7 months (Manchi and Swenson, 2005, Friebe et al., 2001). In contrast to other hibernating species, the body temperature of bears drops only 2° to 6°C below the summer core temperature of 37° - 38° C, (Hissa et al., 1994, Tøien et al., 2011, French, 1986). Heart rate during hibernation can be as low as 8-10 beats per minute (bpm), compared to the heart rate of 30 - 50 bpm of sleeping bears in summer (Folk et al., 1980, Folk et al., 2008, Folk et al., 1976, Folk et al., 1972, Nelson et al., 1973, Nelson et al., 2003). During hibernation, bears are largely inactive, they do not eat, drink, urinate, or defecate, but subsist on the energy

resources they gained during their active season. Their basal metabolic rate decreases by 40%, and their oxygen consumption by about 50% of normal levels (Hellgren, 1998). During hibernation, bears loose between 20% - 45% of their body weight, depending on several factors, e.g., duration of denning, sex, age, and reproductive status (Nelson, 1973, Nelson et al., 1973, Swenson et al., 2007, Kingsley et al., 1983, López-Alfaro et al., 2013). A low respiratory quotient has been documented for hibernating bears, which indicates a high fat combustion, whereas carbohydrates and proteins are conserved (Nelson et al., 1973, Nelson, 1980, Boyer and Barnes, 1999). Fat, with its high energy density, serves as an efficient caloric storage medium. Burning body fat produces water and carbon dioxide; the carbon dioxide is exhaled and the water stays in the blood (Nelson et al., 1973). Azotemia does not develop in hibernating bears, urea production is decreased, and urea is recycled and resynthesized into skeletal muscles and other body proteins, to preserve lean body mass (Nelson, 1989, Harlow et al., 2001, Nelson et al., 1983). Although bears exhibit little physical activity during hibernation, they do not develop osteoporosis (Donahue et al., 2006) and lose only little skeletal muscle mass, in contrast to humans, who would lose about 90% of their strength during the same period (Harlow et al., 2001, Shavlakadze and Grounds, 2006).

1.2.2 Reproduction

Bears are the only mammals with delayed implantation, gestation, parturition, and lactation during hibernation. The reproduction biology of ursids is controlled by a complex timing system, in which the chronological sequence is determined by seasonality and endogenous timing mechanisms (Palmer et al., 1988, Spady et al., 2007). Although photoperiod is an important regulator of the reproductive cycle, the mating season and the duration of embryonic diapause vary among ursid species and individuals (Spady et al., 2007, McMillin et al., 1976). The mating season of brown bears lasts approximately 2-2.5 months in Sweden, from mid-May to early July (Dahle, 2003, Steyaert, 2012). Both males and females mate with different partners (Bellemain et al., 2006, Spady et al., 2007, Steyaert et al., 2012, Zedrosser et al., 2007). Fertilized eggs undergo diapause at the blastocyst stage for 4–5 months until delayed implantation occurs in November-December (Wimsatt, 1963, Sato et al., 2000, Foresman and Daniel, 1983, Iibuchi et al., 2009). The duration of embryonic diapause varies

among and within the same bear species, because the time of implantation and birth is uncoupled from the mating season (Sandell, 1990, Spady et al., 2007). A minimum amount of body mass and fat content (about 19% in brown bears) prior to hibernation is necessary for reproduction (Beecham, 1980, Elowe and Dodge, 1989, Rogers, 1976, Atkinson and Ramsay, 1995, López-Alfaro et al., 2013). Dates of birth are independent of the dates of estrus and mating (Sandell, 1990, Dittrich and Kronberger, 1963, Spady et al., 2007).

Brown bears commonly give birth to 1 to 3 cubs, which are born in the den in January- February (Zedrosser et al., 2011). The neonates, which weigh about 500 g, are naked at birth, and are nursed by their mother with fat- and protein-rich milk in the winter den (Farley and Robbins, 1995, López-Alfaro et al., 2013). Gestation in ursids lasts approximately 60 days (Tsubota et al., 1987, Quest, 2001, Spady et al., 2007). This short period limits the energetic costs of reproduction by truncating embryonic development, which in turn reduces the size of offspring and thus the initial costs of lactation (Sandell, 1990, Spady et al., 2007). Lactation in brown bears lasts about 1.5-2.5 years (Farley and Robbins, 1995) and the mean litter interval varies among populations and lasts on average 2.8 years in European brown bears (Steyaert et al., 2012, Nawaz et al., 2008, Zedrosser et al., 2011). Longevity of free ranging brown bears is 25 to 30 years, and reproductive senescence in females occurs around 27 years (Schwartz et al., 2003).

2 Focal areas of the thesis

2.1 The factors affecting denning behavior and den abandonment (Paper I)

Hibernation enables survival during seasonal periods of resource and energy shortage. It requires physiological and behavioral adaptations in combination with prehibernal energy storage and hibernal metabolic depression (Humphries et al., 2003). Winter is associated with an abrupt decrease in available food resources for bears, and brown bears in Sweden respond to this resource shortage by hibernating in dens (Friebe et al., 2001, Manchi and Swenson, 2005). Various factors have been reported to influence the denning behavior of bears, including: reproductive status (i.e., pregnant vs. nonpregnant), body condition, age, annual

and seasonal variations in ambient temperature, food availability, snow conditions, latitude and photoperiod, as well as human activities (Servheen and Klaver, 1983, Schoen et al., 1987, Elfström et al., 2008, Craighead and Craighead, 1972b, Judd et al., 1986, Van Daele et al., 1990, Miller, 1990, Mace and Waller, 1997). Due to the multitude of factors and their interactions, it is difficult to generalize patterns of denning behavior from one study area to another. Additionally, behavioral patterns can vary among individuals in the same study area (Judd et al., 1986, Schoen et al., 1987, Manchi and Swenson, 2005, Friebe et al., 2001), and even for the same individual (Roth and Huber, 1986). For this reason, and perhaps due to the use of different methods, studies of winter behavior in bears have yielded variable results. Previous research on brown bears’ denning behavior was often based on radio telemetry data (Friebe et al., 2001, Huber and Roth, 1997, Craighead and Craighead, 1972b). This technique required that bears equipped with radio transmitters be located manually by foot, from car, or airplane. Because free-ranging brown bears are vulnerable to disturbance at their dens (Swenson et al. 1997; Elfström and Swenson 2009), the frequency of locations often was low and of poor quality, which resulted in low resolution of spatial, temporal, and behavioral data.

Although brown bears in Sweden generally are not aggressive, they do sometimes injure humans. The period of highest risk coincides both with brown bear den entry and the moose (Alces alces) hunting season, when large numbers of hunters and their hunting dogs are present in the forest (Moen et al., 2012, Friebe et al., 2001, Manchi and Swenson, 2005). Few incidents occur during bear hunting season, which ends 15 October, before the majority of bears in Sweden have entered their dens (Sahlén et al., in prep., Friebe et al., 2001, Manchi and Swenson, 2005). In order to understand how to reduce the rate of injury, it is important to evaluate if the bears’ behavior prior to denning might explain the higher risks of injuries at this time. In central Sweden, female bears start to reduce their daily movements about 6 weeks before den entry, and 2 weeks before they enter the dens, they reduce their movements by an additional 40% (Friebe et al., 2001). Craighead and Craighead (1972b) were the first to observe predenning behavior, which they described as reduced activity combined with lethargic behavior at the den site before the bears definitely enter their dens and start hibernation. Some researchers have documented that bears prepare their dens quite a while before the start of hibernation, often combined with a reduction of movements, food intake, and activity (Craighead and Craighead, 1972b, Judd et al., 1986, Servheen and Klaver, 1983).

Hibernating bears survive on the energy stores they have accumulated during the fall hyperphagic period. Disturbances during hyperphagia and hibernation may have a negative

effect on the bears' fitness (Ordiz et al., 2008, Welch et al., 1997, Elowe and Dodge, 1989). Disturbances of pregnant female brown bears during the winter can reduce their reproductive success (Swenson et al., 1997) and after females give birth, the cost of den relocation rises dramatically, because young cubs would be exposed to thermal stress. Thus, the choice of a safe place for the den is of vital relevance, particularly for reproducing females. In Scandinavia, human activity around the den site has been suggested to be the main reason why bears abandon their dens (Swenson et al., 1997). And indeed, several researchers have suggested that bears select their den sites to reduce such risks of disturbance (Elfström et al., 2008, Ciarniello et al., 2005, Goldstein et al., 2010, Elfström and Swenson, 2009).

New techniques, such as GPS collars with activity sensors, which record and store the data automatically, provide us today with more detailed information about the bears’ hibernation biology, without disturbing them during hibernation. This will allow us to identify general patterns of hibernation behavior that had been overlooked using radio telemetry data and other less accurate methods.

My goal was to gain more detailed knowledge of the winter behavior of free-ranging brown bears in Sweden and to evaluate how environmental, behavioral, and individual factors influence the denning process (paper I). I evaluated how sex, reproductive status, age, and environmental factors influenced the timing of den entry generally.

I documented activity and movement behavior prior to denning and evaluated whether bears built a den in a predetermined place. I also documented how often bears abandoned their dens, and suggested that bears that build their dens in known places abandon their dens less than bears that had not visited the den area before. Because the risk of human injury from an attacking bear is greatest during the end of September until mid-November, which coincides with brown bear den entry, I evaluated if the bears’ behavior near den entry explained higher risks of human injury at that time. So far, no detailed information about brown bears’ denning behavior is available, therefore the results of this study could help managers to improve the safety of both humans and bears, e.g. by developing appropriate hunting restrictions and informing the relevant public to minimize disturbances which can lead to injuries.

2.2 How can we detect pregnancy in free-ranging brown bears? (Paper II)

Detecting pregnancy and birth, as well as the abortion or early loss of young, is essential for studies of life history and population ecology (Stearns, 1992). Several methods exist to detect pregnancy or parturition in mammals. The most common invasive methods are blood serum analysis, radiography, ultrasonography, or ultrasound imaging, whereas noninvasive methods include fecal and urinary hormone metabolites (Schwarzenberger et al., 1996, Kähn, 1992, Bauman et al., 2008). Also, behavioral changes, such as restlessness, lethargy, nest building, aggression, and changes in appetite or foraging behavior can be used as efficient noninvasive methods to document pregnancy or parturition, because many species show specific behavioral patterns during pregnancy, imminent parturition, or lactation (Kleiman et al., 2010, Perrigo, 1987). No reliable noninvasive method presently exists to detect pregnancy in free- ranging bears during hibernation, although an indirect sign has been used to determine successful reproduction in bears, such as tracks, claw marks, or scats of neonates at the den site (Craighead and Craighead, 1972a, Friebe et al., 2001). The reproductive success of hibernators is often recorded by direct observation after a female has left the hibernaculum with or without offspring. Primiparous female brown bears lose their cubs more often at this time than older females (Zedrosser et al., 2009) and, thus, sometimes may be classified into the wrong reproductive class. This, especially, may be true for extraordinarily young mothers, which were not expected to give birth. Although hibernating mammals are mostly inactive during winter, they periodically wake up during hibernation and frequently make small movements (Hissa et al., 1994, Tøien et al., 2011, Humphries et al., 2003). I expected that pregnant females would show different activity patterns than nonpregnant individuals, because their physiology and behavior would be affected by pregnancy, birth, and nursing.

My aim was to test whether it would be possible to detect pregnancy in brown bears, based on winter activity patterns observed with activity sensors mounted in GPS neck collars (paper II). This would allow researchers to obtain important information about reproduction without disturbing the bear during hibernation.

2.3 Determination of the gestation period of free-ranging brown bears (Paper III)

The gestation period of bears has been estimated mainly with macroscopic and histological investigations of the ovaries and uteri of hunter-killed females or with blood serum analysis in captive and free-ranging bears (Wimsatt, 1963, Tsubota et al., 1987, Spady et al., 2007). Quest (2001) determined a 54-56-day gestation period in captive brown bears using ultrasonic examination, however no information about the exact gestation period of free-ranging brown bears is available. Examinations of the reproductive organs of free-ranging and captive brown and American black bears indicate that implantation occurs in late November and early December, and parturition occurs in late January and early February (Wimsatt, 1963, Dittrich and Kronberger, 1963, Tsubota and Kanagawa, 1993, Tsubota et al., 1990, Kordek and Lindzey, 1980, Hensel et al., 1969). The time of parturition has also been determined for American black bears by listening for vocalizations of cubs at the den sites (Alt, 1983, Bridges et al., 2002). Some researchers have observed that the body temperature of pregnant female brown and black bears in captivity is higher (~37°C) during the gestation period than during the rest of hibernation (32-34°C), because embryo development requires euthermia. Body temperature drops at parturition (Hissa, 1997, Tøien et al., 2011, Shimozuru et al., 2013, Laske et al., 2011).

I used this knowledge and my findings from paper II to determine if the raised activity levels during pregnancy and the body temperature data would yield the same dates of implantation or parturition. Based on this, I documented, for the first time, the gestation period of free- ranging brown bears (paper III).

2.4 Factors influencing the timing of parturition (Paper III)

Many aspects of the reproductive biology of ursids are still poorly understood, such as reproductive cycles, hormone and estrous cycling, and factors that trigger implantation and birth. Most of these studies have been carried out in captivity (Dehnhard et al., 2006, Schwarzenberger, 2007, Spady et al., 2007) and little information is available about the timing

of implantation and parturition in free-ranging bears. Several studies of bears have shown a strong correlation between a female’s body condition in fall and their reproductive success. Well-nourished females have larger litter sizes and shorter litter intervals (Rogers, 1987, Stringham, 1990, Bunnell and Tait, 1981, Welch et al., 1997, Ryan, 1997, McLellan, 2011). A minimum amount of body mass and fat content (19% in brown bears) prior to hibernation is necessary for reproduction (Beecham, 1980, Elowe and Dodge, 1989, Rogers, 1976, Atkinson and Ramsay, 1995, López-Alfaro et al., 2013). Thus, brown bears are able to vary both the birth date and growth rate of their cubs that are depending on their fat stores, which means that females in superior condition give birth earlier, lactate longer, and produce more and higher quality milk while in the den than females in poorer condition. This also accelerates cub growth relative to females in poorer condition (Robbins et al., 2012b, Atkinson and Ramsay, 1995). Knowledge about the timing of reproductive events is therefore important for conservation and management.

My goal was to determine which factors influence the timing of gestation in free-ranging brown bears and to evaluate whether age, primiparity, environmental conditions, weather conditions in autumn, and/or the start of hibernation influence the date of parturition (paper III).

2.5 List of papers

Paper I

Sahlén, V., A. Friebe, S. Sæbø, J. E. Swenson, O.-G. Støen. 2014. Den entry behavior in Scandinavian brown bears; implications for preventing human injuries (Journal of Wildlife Management, The Journal of Wildlife Management; DOI: 10.1002/jwmg.822)

Paper II

Friebe, A., A. Zedrosser, and J. E. Swenson. 2013. Detection of pregnancy in a hibernator based on activity data. European Journal of Wildlife Research 59:731-741.

Paper III

Friebe A., A. L. Evans, J. M. Arnemo, S. Blanc, S. Brunberg, G. Fleissner, J. E. Swenson, and A. Zedrosser. 2014. Factors affecting date of implantation, parturition, and den entry estimated from activity and body temperature in free-ranging brown bears. PLoS ONE 9(7): e101410. doi: 10.1371/journal.pone.0101410

3 Materials and Methods:

3.1 Study area and population

This PhD study was conducted in the northern boreal forest zone in Dalarna and Gävleborg counties, south-central Sweden (~61°N, 15°E, Figure 1), which is the southern study area of the Scandinavian Brown Bear Research Project. The area comprises about 13,000 km2, is hilly, and is covered with coniferous forests with interspersed lakes and bogs. Altitudes range from 200 m in the southeast to 1,000 m in the west, but are mostly (>90 %) below timberline, which is about 750 m (Dahle and Swenson, 2003). The forest is dominated by Norway spruce (Picea abies), Scots pine (Pinus sylvestris), and birches (Betula pendula, B. pubescens). Ground vegetation includes a variety of species of mosses, lichens, grass, heather and berries. Bilberries (Vaccinium myrtillus) and crowberries (Empetrum hermaphoditum) are the main autumn food resource of brown bears in this area (Opseth, 1998). The landscape is intersected by a dense network of logging roads (0.7 km/km2) and a few high- traffic roads (0.14 km/km2) (Martin et al., 2010).. The human population density is low, and only a few small villages exist in the study area. (Swenson et al., 1999). Snow cover lasts from the end of October until late April, and mean daily temperatures range from −7 °C in January to 15 °C in July (Swedish Meteorological and Hydrological Institute).

Fig 1. Map of Sweden and Norway with the southern study area (black area) of the SBBRP.

The size of the Swedish brown bear population size was estimated to be about 3300 individuals in 2008. Brown bears hibernate 5–6 months in this part of Sweden. They select denning habitats on the landscape scale by avoiding water and intermediate-sized roads and by denning more at lower altitudes (Elfström et al., 2008, Elfström and Swenson, 2009). The study area of the Scandinavian Brown Bear Research Project (SBBRP) is part of the southernmost core reproductive area for Scandinavian brown bears, with a population density of about 30 individuals per 1000 km2 (Kindberg et al., 2011, Bellemain et al., 2005, Solberg

et al., 2006). The brown bear is a game species and legal hunting is the single-most important cause of mortality for brown bears in Sweden (Bischof et al., 2009). The annual brown bear hunting spans from 21 August until quotas are filled (45–75 bears are harvested per year in the study area), but stops by no later than 15 October, in order to protect hibernating bears from disturbance.

3.2 Bear capture

Bears were localized from a helicopter and anestetized using a remote drug delivery system (Dan-Inject). Most captures were made in spring, shortly after bears had emerged from their dens. For anaestesia, a combination of tiletamine/zolazepam and medetomidine was used. Spring provides the best conditions for capture, when remaining snow cover and minimal vegetation make it easier to find the bear, open water in the terrain is limited, and ambient temperature is relatively low. Females with cubs of the year were not captured, only females with offspring older than one year and lone bears. During immobilization, we frequently recorded the bears’ health status parameters such as heart rate, body temperature, and respiration frequency. Body weight and body measurements were taken. From bears of unknown age, we removed a premolar tooth for age estimation. When a bear was captured for the first time, we marked the bear with a microchip under the skin and tattooed its ID number inside the lip. Blood, hair samples, and a biopsy were taken from all individuals. All bears received a motion-sensitive radio transmitter. A radio-tagged bear is generally recaptured at intervals of two to three years to replace its transmitter/receiver. For detailed capture and marking procedures, see Arnemo et al. (2012). The permission to capture and instrument bears was granted by the Swedish Environmental Protection Agency (permit Dnr 412-7327-09 Nv) and the Ethical Committee on Animal Experiments in Uppsala (approval C47/9).

Fig 2: Bears were anesthetized from a helicopter.

The SBBRP started to mark bears with radio-collars in 1984. Since 2003, bears received GPS- collars containing integrated activity acceleration sensors, which provide very accurate and frequent information about brown bears’ activity and movements without restrictions to specific periods. Since 2010, biologgers, such as body temperature sensors, have been implanted in bears to gain more knowledge about the brown bears’ physiology.

Below I describe the sensors that have been used in this study and their functions. For detailed descriptions of the methods and statistical analyses, see the respective papers.

3.3 Sensors and data collection

Radiotransmitter: All bears equipped with GPS radiocollars also received a motion-sensitive radiotransmitter that was implanted into the body cavity (Telonics Inc., Arizona, USA) (Arnemo et al., 2012). An integrated activity and mortality sensor changed the pulse rate of the transmitter. Animal movement activated the sensor to change the signal mode to a faster pulse rate for a fixed time interval or until further movements generated a new change in the pulse rate of the signal. The slow mortality pulse rate started after a transmitter had not been moved for 5 hours. Battery life length of the implant was 4-8 years, depending on the settings and model of the device.

Fig.3: Radiotransmitter (Telonics Inc., USA): VHF- implant 400L

GPS-GSM collar: The bears were equipped with a GPS-GSM collar (Vectronic Aerospace GmbH, Berlin) with an integrated activity sensor. The size and weight of a collar is adjustable and was based on the bear’s neck size and body weight. GPS location data were transmitted via the GSM network to a base station from which they can be downloaded remotely. The GPS collars were programed to collect GPS location fixes at 30-min intervals during the period 1 April until 30 November and once per day (at noon) from 1 December until 30 March.

The activity sensor measures true acceleration six to eight times per second in two orthogonal directions. The acceleration values were accumulated and averaged for each direction for a recording interval of 5 minutes, resulting in average acceleration values ranging from 0 to 255 for each axis. These averaged acceleration values were stored in the neck collar with the associated date and time until they were downloaded as a text file via Link Manager (Vectronic Aerospace GmbH, Berlin). Activity counters in the GPS collars provide an individual-based method to measure animal activity levels. However, the acceleration value measured by the sensor can be affected by several factors, such as collar placement and how tight the collar is on the neck.

Fig.4: GPS-GSM collar with integrated activity sensor (grey housing) and a round shaped battery pack (black housing) (Vectronic Aerospace GmbH, Berlin)

Body temperature implants Abdominal temperature data loggers (DST Centi, Star Oddi, Iceland) were implanted in bears that were included in the physiological hibernation study in paper III. The loggers were programed to record the body temperature every 30 mins (see Arnemo et al. (2012)) for further details on the implantation procedures). These temperature data were stored in the logger’s internal memory with a real-time clock reference for each measurement. After recapturing the bears, the temperature loggers were recovered and the body temperature data were uploaded with SeaStar software and the Communication Box (Star Oddi, Iceland), which served as a wireless interface between the logger and a PC.

Fig 5: Body temperature implant (Star Oddi, Iceland)

4 Summary of results

4.1 Den entry behavior in Scandinavian brown bears implications for preventing human injuries (Paper I)

Encounters between Scandinavian brown bears Ursus arctos and humans that result in human injuries and fatalities typically coincide with den entry in October/November, and commonly occur near a den. I determined when bears arrive at their dens, identified potential predictors of this event, documented behavior and activity associated with this period, and attempted to explain the increased risk of bear-caused human injuries in this period.

Bears reduced their activity gradually during the course of the autumn. They arrived at their den sites on average 24 October ± 11.4 days (range: 6 October until 1 December) and spent 4.0 ± 3.2 days at the den site before they started to hibernate (mean: 28 October ± 12.5 days, range: 6 October until 15 December). The timing of arrival at the den site varied with reproductive category and age and between years. Pregnant females, single females, and females accompanied by cubs of the year arrived at their dens earlier than males and females with yearlings, and older bears tended to arrive at their den sites earlier than younger bears. Bears abandoned their first dens in 22% of the denning events, and appeared to be more sensitive to disturbance during early denning period, because den abandonment rates were lower later in winter. Males abandoned their dens more frequently than females, especially those that had not visited their den sites before den entry. Predenning, which was defined as reduced activity level below the normal activity level, started on average 22 October ± 11 days, which was before the bears entered their final den sites in 58% of the cases. Many people associate dens with an increased risk of a bear responding aggressively to disturbance, but the results indicated that other behavioral and possibly physiological changes in this period also may be involved. Den entry occurred over a long period, with high variability and poor predictability of its timing. Therefore, restricting hunting or other recreation activities to reduce risk of injury by bears and disturbing bears would probably be both impractical and ineffective. Our findings can be used to educate hunters about bear behavior at this time of year to increase the awareness, about when the risk of disturbing, and being injured by a bear is greatest.

4.2 Detection of pregnancy by means of activity data (Paper II)

I developed a new method to confirm pregnancy and parturition in hibernating female brown bears using activity data from 30 individual bears in Sweden. For this purpose I analyzed data from 52 hibernation events. Pregnant females showed characteristic activity patterns during the period of pregnancy, with significantly higher daily activity levels and higher frequency of active periods during pregnancy than for nonpregnant bears. Pregnant females were active on average 2.2 times more often during the pregnancy period than during the postpartum period, compared with no difference between these periods for nonpregnant females. I developed a pregnancy index, defined as the average of the proportion of mean daily activity levels and the proportion of activity events during the pregnancy period divided by these values of the postpartum period. It averaged 2.61±1.73 (SD) for pregnant females and 0.94±0.24 for nonpregnant females, which was a highly significant difference. I evaluated this method using a group of adult females that had an unverified reproductive status, but were classified as not pregnant, because no cubs had been observed after den emergence. My results suggested that 35 % of those females had, in fact, been pregnant. This method is potentially important for future studies of the population ecology of bears and of factors affecting their reproductive success. At the same time it shows how unsecure conclusions based only on cub observations are.

4.3 Factors affecting the dates of implantation, parturition, and den entry (Paper III)

I used the knowledge about the activity levels of pregnant females during hibernation that I gained in paper II to investigate the factors affecting the dates of implantation, parturition, and den entry in paper III. Body temperature and activity were higher in pregnant brown bears during the gestation period than during the rest of hibernation and both dropped at parturition. Based on body temperature, the estimated mean date of implantation was 1 December ±12 days (median: 28 November, range: 29 days, from 19 November – 18 December). The mean date of parturition was 26 January ±12 days (median: 23 January, range: 29 days, from 12

January – 10 February). The mean duration of the gestation period lasted 56 ±2 days. The parturition dates calculated with activity and body temperature data did not differ significantly and were the same in 50 % of the females. However, the estimated implantation dates differed up to 17 (±5) days when comparing dates calculated from activity data and body temperature. The mean body temperature during the preimplantation, gestation, and lactation periods was 34.1 ±0.4 ˚C, 37.1 ±0.04 ˚C, and 34.6 ±0.3 ˚C. For nonpregnant bears during the corresponding periods it was 33.9 ±0.5 ˚C, 33.2 ±0.3 ˚C, and 33.1 ±0.4 ˚C, respectively. Although the body temperature of pregnant females decreased with the ongoing gestation period, it was the period with the highest body temperature compared to all other periods for both pregnant and nonpregnant females. The mean daily variation in body temperature was also lowest during this period for pregnant females.

The activity data during 46 hibernation events showed that the parturition date can range over 43 days (from 1 January – 13 February). The mean start of hibernation was 18 October, ranging 34 days, from 2 October – 5 November. The mean duration of denning prior to parturition was 95 days. The start of the hibernation was earlier when ambient temperatures in October were low. I tested whether age, litter size, primiparity, environmental conditions, or the start of hibernation influenced the timing of parturition. Older females started hibernation earlier. The start of hibernation was earlier during years with favorable environmental conditions. Dates of parturition were later during years with good environmental conditions, which was unexpected. I suggest that free-ranging pregnant brown bears in areas with high levels of human activities at the beginning of the denning period, as in our study area, might prioritize investing energy in early denning rather than in early parturition during years with favorable environmental conditions, as a strategy to prevent disturbances caused by humans.

5 Discussion

5.1 Denning of brown bears in central Sweden.

Den entry Bears arrived at their den sites on average 24 October, but den arrival date ranged over almost 2 months, from 6 October until 1 December (paper I). My study on pregnant females showed that the start of hibernation varied over 34 days (paper III), with a mean start on 18 October, which was similar to a previous study in our study area (Friebe et al., 2001). The blastocyst is not implanted in the uterus until the female is in the winter den (Tsubota et al., 1990, Hissa, 1997), which may be one reason for the early start of hibernation for pregnant female bears.

Environmental conditions affecting date of initiating hibernation In paper III, I showed that low ambient temperature was associated with an early start of hibernation (Servheen and Klaver, 1983, Reynolds et al., 1976). Male bears in northern Sweden, where the climate is colder, start to hibernate on average 20 days earlier than in central Sweden (Manchi and Swenson, 2005).

In paper III, I tested the effects of environmental conditions on the start of hibernation by using a yearly environmental condition index that had been used in former studies as a proxy for food conditions (Zedrosser et al., 2006). Environmental conditions were significantly correlated with the start of hibernation for pregnant females, with earlier hibernation following years of good conditions. Early start of hibernation has been observed previously as a strategy for extremely well nourished female bears (Servheen and Klaver, 1983). A trade-off in the ability to store additional fat and the energy used to consume the calories necessary to add additional fat can be a reason for an early start of hibernation during years with good environmental conditions (Humphries et al., 2003). In late autumn, when food availability decreases, the trade-off between energy expenditure and energy consumption might diminish (Humphries et al., 2003).

Sex, reproductive status and age as factors affecting date of arrival at the den site and initiation of hibernation We found that single females, pregnant females, and females with cubs of the year arrived at their den sites earlier than males and females accompanied by older offspring (paper I). The sex and the reproductive status of a bear have been identified as factors that influenced den entry behavior also in other study areas (Servheen and Klaver, 1983, Judd et al., 1986, Van Daele et al., 1990). However, females with cubs were reported to den first by Mace and Waller (1997). In the long-term study of 90 hibernation events (paper I), I detected a tendency for younger bears to arrive at their den sites later than older bears. Older pregnant females initiated hibernation earlier than younger pregnant females (paper III). An early start of hibernation has been hypothesized as a strategy for predator avoidance in small mammals (Bieber et al., 2014). Perhaps older females had experienced that hunting activities are high in autumn in our study area, and therefore started to hibernate earlier than younger, less experienced, pregnant females. Schooley et al. (1994) suggested that pregnant American black bears den after they have stored sufficient fat reserves for winter survival and reproduction in order to avoid being active during periods when food become less abundant. Manchi and Swenson (2005) observed that older males hibernated for a shorter time than younger males. They suggested that the surface area:volume ratio may explain the age-related differences they observed in denning behavior. Large bears probably can store more fat and might lose proportionally less weight per day than small bears. This might explain why older male bears could afford to be active for a longer time during winter and start to hibernate later.

5.2 Behavior prior to den entry and den abandonment

Bear behavior prior to den entry and risks of human injuries The bears spent 4.6 ± 3.8 days in the den area before reaching their hibernation activity level. How long a bear spent in the den area before the start of hibernation was mainly related to the age of the bear, with older bears spending less time in the den area than younger bears (paper I). This may be an effect of the older bears’ greater experience and familiarity with their home range. Manchi and Swenson (2005) documented that the distance between an individual’s

dens in successive years was short for adult males and females irrespective of age, indicating that the same general area tended to be used for denning year after year, but that young male bears had long distances between successive years’ dens, due to the subadult males’ dispersal behavior.

Hissa et al. (1994) reported that changes of blood parameters in early fall may indicate the development of a biochemical preparation for hibernation. We found that approximately half of the bears reduced their activity on average two days before reaching their den areas and when they still were several kilometers away from it, whereas the other half arrived in their den areas before they reached predenning activity levels. The bears reduced their activity gradually during the course of the autumn. These results were similar to my pilot study of predenning behavior of female brown bears, where I observed a reduction of movements of about 5% per week starting six weeks before den entrance (Friebe et al., 2001). Most human injuries in Scandinavia occur during the moose hunting season, which is concurrent with the den entry period. The vicinity of a den is one important factor that had been associated with human injuries (Sahlén, 2013). Bears arrived at their dens over the course of several weeks, with great variation in timing, which made it difficult to predict the onset of denning (papers I and III). One important finding was that bears do not have to be at their den site to begin predenning activity; in fact, half of the bears in our study were often kilometers away from their final den location when their activity levels dropped significantly. Thus, many bears moved in this lowered activity state for almost two days before arriving at their den area. This raises the question of whether a bear in this low activity state away from its den responds similarly to a bear in this state near its den when meeting a human. The fight response in rodents can be triggered when there is a limited ability to flee and/or the threat is close to the animal (Eilam, 2005). Thus, bears in a reduced predenning behavioral state may be more prone to attack a human who approaches it, not because they are defending themselves at or near a den, but because their physiological state prevents them from using escape as an effective defensive mechanism. Bears undergo a series of physiological changes during the hibernation period (Nelson et al., 1983), but the predenning reduction in activity we documented suggested that physiological changes affecting the bears’ behavior may begin before hibernation starts. More research on bears’ physiology prior to hibernation is necessary in order to confirm if the bears’ physiological state can explain higher risks of injuries during this time.

Den abandonment In paper I, we documented high den abandonment rates (22%) and that den abandonment was more common early in the denning period, which coincides with the moose-hunting season. The majority of documented den abandonments appeared to be the result of human disturbance (Swenson et al., 1997, Linnell et al., 2000). Male brown bears were more likely to abandon their dens than females, and had higher abandonment rates when they had not visited their den sites previously. Friebe et al. (2001) also documented that free-ranging female brown bears in central Sweden select predetermined places for denning by visiting their den areas on average more than once a month during season, which was more often than expected. All dens were constructed inside, rather than at the periphery of the home range. Thus, they suspected that female bears chose a known place for the winter den. Bears that had visited the den area previously may be aware of some of the regular disturbances that occur there and are therefore either accustomed to them, or have already selected against such disturbances when choosing their den site. We know from small- and large-scale studies that adult males avoid human activity to a greater extent than females or young males (Nellemann et al., 2007, Elfström et al., 2008, Steyaert et al., 2013a). Additionally, males are more likely to den in open “nest dens”, which could also make them more vulnerable to disturbance (Elfström and Swenson, 2009). The greater likelihood of males to abandon their dens may also be an effect of their better ability to tolerate the cost of abandonment (Beale and Monaghan, 2004), due to their greater body size and fat reserves.

Denning is essential for the reproductive success of female brown bears. Previous studies have shown that disturbances during hyperphagia and hibernation has a negative effect on the bears' fitness and reproductive success (Ordiz et al., 2008, Welch et al., 1997, Elowe and Dodge, 1989, Linnell et al., 2000, Swenson et al., 1997). In central Sweden, 60% of the presumed pregnant females that had abandoned their dens emerged from their new dens without cubs (Swenson et al., 1997). Pregnant females are not protected from hunting, however, they play a crucial role in population growth and start to hibernate earliest (Friebe et al., 2001, Judd et al., 1986, Miller, 1990, Van Daele et al., 1990). Our study of pregnant females showed that 47% of the females started hibernation before the 15 October, the last day when hunting is still permitted if the quota has not been filled (paper III). Therefore, an early start of hibernation could also be a strategy to avoid disturbance and loss of energy during the hunting season. Restricted use of their home range, combined with reduced movements, are known strategies of female brown bears with cubs of the year to avoid male

bear encounters during the mating season (Dahle and Swenson, 2003, Martin et al., 2013, Steyaert et al., 2013a). Several studies have shown that bears try to avoid human disturbance during hibernation, e.g., by selecting den sites far from roads or in concealed and rugged terrain (Sahlén et al., 2011, Elfström et al., 2008, Goldstein et al., 2010, Ordiz et al., 2012, Ordiz et al., 2013, Ordiz et al., 2011). Additionally, pregnant females choose better concealed den types, like anthill, soil, and rock dens, than male bears (Elfström and Swenson, 2009). Further research is necessary to determine whether early denning combined with tactically wise denning strategies help pregnant females to avoid disturbances.

5.3 Can we use activity data to detect pregnancy in bears?

Our results in paper III showed that activity recordings with dual-axis motion sensors in GPS neck collars can be used to document pregnancy in hibernating brown bears. Pregnant females showed, on average, activity levels that were three times higher and had been active on average, 2.2 times more frequently during the pregnancy than in the postpartum period. In contrast, nonprengnant bears showed no changes in activity over comparable periods of time, neither in the mean daily activity levels nor in the mean daily activity events.

Distinct differences in activity behavior during and after the time of pregnancy were clearly visible to the unaided eye from a plot of the activity data in 85 % of the cases. I suggest that the sudden drop in activity I observed in late January or early February was related to parturition. In 15 % of the cases, the decline was more gradual, and activity was reduced for only a short period after parturition, but my calculated pregnancy index confirmed pregnancy status also for these cases. Therefore, I recommend calculating the pregnancy index as described in paper II in order to detect pregnancy, even in females whose characteristic pregnancy activity patterns are more difficult to detect visually.

Nonpregnant bears generally showed the lowest activity levels in January and February. The duration and period of hibernation varies among bear populations (Servheen and Klaver, 1983, Schoen et al., 1987, Miller, 1990, Judd et al., 1986, Roth and Huber, 1986). Therefore, the periods of pregnancy and postpartum used in this study may have to be changed for similar studies elsewhere. Nevertheless, it could be difficult to determine pregnancy with my

method for females that lose their cubs immediately after parturition, because typical pregnancy patterns are easiest to detect when comparing activity data during pregnancy with postpartum periods. The raised activity during pregnancy may be caused by the physiological changes during pregnancy. Several studies on different species have shown that changes in sex hormones during mating, pregnancy, and lactation can alter an animal's circadian activity rhythm (Kiddy, 1977, Labyak and Lee, 1995, Wollnik and Turek, 1988, Lightfoot, 2008). Studies on female golden hamsters (Mesocricetus auratus) have shown that changes in hormone levels (estradiol and progesterone) during pregnancy impact the circadian locomotor rhythms (Takahashi and Menaker, 1980). Changes in estradiol and progesterone hormone levels during pregnancy have also been documented in brown bears (Sato et al., 2000). Hellgren (1998) suggested that female American black bears may remain active after implantation. However, after birth, when hormone concentrations change, the mothers may remain still in order to warm their newborns, which are dependent upon their mother's body heat. Robbins et al. (2012a) observed that captive pregnant female brown bears in artificial dens were less active after birth, as they did not stand during the first 3 weeks postpartum. Laske et al. (2011) also suggested that a decrease in heart rate and activity during hibernation occurs with parturition in American black bears. This supports my conclusion that the observed decrease in activity indicates the birth of cubs. Hissa et al. (1994) reported that positional movements and head lifting are less frequent during midwinter than during the beginning or end of hibernation. I also observed that bears were less active during midwinter. However, the level of activity of nonpregnant bears did not decrease during midwinter to the same extent as that of pregnant females after parturition and should, therefore, not be mistaken as a sign of pregnancy for females with low basal activity levels. Because January and February are the coldest months in our study area (SMHI, Swedish Meteorological and Hydrological Institute), reduced physical activity during this time may save energy.

Most female brown bears reach sexual maturity at the age of 5, but in some populations, 4- year-old and even 3-year-old females give birth (Zedrosser et al., 2004, Zedrosser et al., 2009, Frković et al., 2001). These primiparous mothers lose their cubs more often during the premating and mating seasons than older females (Zedrosser et al., 2009). This fact can complicate the classification of a young female into the correct reproductive class using conventional methods of detecting pregnancy, which are often based primarily on cub observations after they leave the den. My activity-based method suggests that the method based on postdenning behavior observations may have underestimated pregnancy in 35 % of

the cases when cubs had not been observed, probably due to early cub loss. Therefore, I recommend calculating pregnancy indices also for young female bears that are not expected to be pregnant. My method can facilitate demographic studies of GPS-marked animals, because it provides reliable information about whether a female has given birth or not. In addition, the use of this method does not require human intervention during the sensitive periods of pregnancy and postpartum, when animals are vulnerable to disturbance. My method may help to obtain better information about the age of primiparity or the phenomenon of mixed-age litters.

5.4 The use of activity and body temperature data to determine the gestation period

My study was the first to document the timing of gestation in free-ranging brown bears. The body temperature data clearly identified the dates of implantation and parturition. The calculated gestation periods ranged between 54 – 59 days and were similar to early reports for black and brown bears in other studies. Mean body temperature was significantly higher during the gestation period than during the preimplantation and lactation periods for pregnant females and nonpregnant female bears. Besides the energetic costs of lactation, the maintenance of a high body temperature during gestation may be an additional reason why pregnant females lose more body mass during hibernation than nonpregnant bears (López- Alfaro et al., 2013). The variation of mean daily body temperature during gestation was lower compared to the periods before and after the gestation and compared to the variation in body temperature of nonpregnant females. Multiday cycles of body temperature have been documented for nonpregnant hibernating bears (Tøien et al., 2011, Ruby, 2003). I did not observe this in pregnant females during the gestation period. Instead, the mean daily body temperature was stable and did not fall below 35.9 ˚C, as also was observed in one pregnant American black bear (Tøien et al., 2011). Fetal development might be intolerant of high variations in body temperature. Raised hormone levels during pregnancy could be another reason for the low variation of body temperature during gestation (Tsubota et al., 1987).

I also observed that the body temperature of pregnant females decreased during the course of gestation. Studies have shown that the maximum serum progesterone level of pregnant brown bears occurs approximately 60 days before parturition and decreases during gestation (Tsubota et al., 1987). The decrease in body temperature during gestation that I observed might be caused by changes in progesterone or other hormone levels. A drop in body temperature at parturition has been reported previously for American and Asiatic black bears and brown bears; in both species of black bears, the body temperature decreased to the level of nonpregnant bears after parturition (Tøien et al., 2011, Shimozuru et al., 2013). However, my results for brown bears showed that the body temperature during lactation did not fall as low as that of nonlactating bears, as also reported by Hissa (1997) for brown bears. The data showed that the body temperature of pregnant females during the preimplantation period did not differ significantly from that during lactation. However, nonpregnant females had lower body temperature levels than pregnant females during the lactation period. Body temperature is probably lowest during midwinter, as it is for activity (Friebe et al., 2013, Hissa, 1997). Metabolic activity during lactation might require or result in higher body temperature levels.

Activity The estimated parturition dates using activity and body temperature data differed by only one or two days and were the same for 50% of the females. Thus, I consider that either activity data or body temperature can be used to determine dates of parturition. However, because of the high variation in mean daily activity during the early hibernation period, it was more difficult to estimate the dates of implantation using activity data. I used the moving 5th-order average, because in some cases, activity did not reach the mean hibernation level for more than a few days before implantation, in other cases activity rose before the implantation calculated from the body temperature. Raised activity during this period could be caused by hormonal changes prior implantation, or because activity is in general higher during the beginning of the hibernation period than during midwinter (Friebe et al., 2013, Hissa et al., 1994). The calculated dates of implantation varied 17 ±5 days between body temperature and activity recordings. I can therefore not recommend using activity recordings to determine the date of implantation. However, because the gestation period lasted on average 56 days and showed little variation, I recommend estimating the date of implantation using activity data by subtracting 56 days from the calculated date of parturition.

5.5 Which factors influence the timing of parturition?

My findings in paper III showed that parturition dates ranged over a period of 43 days, which demonstrates a high flexibility in the timing of gestation. Whereas dates of parturition have not been recorded in wild-living brown bears before, Bridges et al. (2011) documented that parturition dates of 150 litters of wild-living American black bears ranged over 53 days from late December to mid-February (39 days excluding an outlier). Robbins et al. (2012b) reported only a 17-day range of parturition in January for a smaller sample of 13 captive brown bear births, perhaps due to similar conditions among bears in captivity. Because the date of denning did not correlate with the date of parturition, I suggest that other factors trigger implantation. Age had a minor effect on the timing of parturition, as there was only a tendency for older females to give birth earlier. Bridges et al. (2011) observed later parturition in pregnant female American black bears that were younger than 5 years old. However, in my study, only 2 females were younger than 5 years. A larger dataset of young pregnant females might be necessary to document an effect of age on the date of parturition.

Studies on captive brown bears have shown that larger females give birth earlier during winter than smaller females (Robbins et al., 2012b). However, in my study, favorable environmental conditions correlated with late parturition. Although we had no information about the females’ body mass prior to denning, I expected that food availability was the most important factor affecting the environmental condition index (Zedrosser et al., 2006) and that the females were heavier when the environmental conditions had been favorable. With this reasoning, my results differed from those found in captive bears (Robbins et al., 2012b). It is possible that free-ranging females might budget their energy resources differently than captive females (Steyaert et al., 2013b, Steyaert et al., 2013c). In this study, during years with good environmental conditions, pregnant females began hibernating earlier rather than using energy reserves for early parturition and lactation, which would have maximized offspring weight at den emergence. More information about the relationship between female body condition prior to hibernation and the timing of gestation is needed for wild-living bears.

6 Future research perspectives

Johan Wolfgang Goethe:

"So eine Arbeit wird eigentlich nie fertig, man muss sie für fertig erklären, wenn man nach der Zeit und den Umständen das Möglichste getan hat."

This statement is probably applicable for all research. This thesis has delivered many new insights on hibernation, denning strategies and timing, and detection of parturition during hibernation in free-ranging brown bears. Nevertheless, many aspects of the physiological changes that occur during hibernation are still poorly understood. The results presented in this thesis showed that a variety of factors influence hibernation and denning behavior, some of which are: environmental conditions, age, sex, reproductive status, human activity, year, and individual. In order to understand the nexus of all these parameters, longtime studies of bears in different reproductive groups under different environmental conditions are necessary. Although the results are based on long-term studies with sufficient group size of bears with different reproductive status, the study was conducted within only one study area. Although this was important in order to gain a general knowledge of bears’ winter behavior, it would have been interesting to compare some of the results in this thesis with the winter behavior of brown bears in other study areas, where the photoperiod, climate, vegetation period, body size of bears and hunting season are different.

Because the SBBRP now equips bears with biologgers to record body temperature and heart rate, it will be important to compare the time course of activity and physiological parameters during den entry, hibernation, and den exit. Physiological changes may explain the higher rate of injuries during the denning period and also can give us more knowledge about how bears react physiologically to disturbances during hibernation. These parameters will also provide us with more detailed knowledge about factors that might trigger the start of hibernation. Special endocrine mechanisms have been implicated in the regulation of seasonal changes in the physiology and behavior of animals. Some of these mechanism are directly involved in annual time keeping, particularly through the photoperiodic mechanism (DeCoursey et al., 2004). Circannual rhythms are excellent adaptions for species that inhabit a severe and regularly changing environment, where each event in an animal’s life must occur at an exact

time in order to survive. A circannual rhythm guarantees, e.g., that emergence from hibernation occurs at the proper time, i.e., early enough for successful reproduction and late enough to avoid unfavorable conditions in late winter or early spring (Gwinner, 1986). During the active season, brown bears show diurnal activity patterns with activity peaks during crepuscular hours. Their circannual activity rhythm is affected by the photoperiod and their reproduction status, but also by the season, e.g., the mating, foraging, or hunting season (Friebe et al. in prep.). However, during hibernation, bears show neither chronological periodical arousals nor circadian activity patterns. It would therefore be of great importance to study the seasonal behavioral patterns of bears and their biological pacemakers, and then the transition period from the active to the hibernation stage, to detect physiological and ecological factors that may induce the start and end of hibernation. Although bear dens are covered by snow in the middle of the winter, daylight might reach into the dens in early winter and late spring while bears are still hibernating. Light sensors mounted on the GPS collars might help to clarify if the photoperiod triggers the start and end of hibernation. The results in paper I have shown that the start of hibernation and denning do not necessarily occur at the same time and that the activity starts to decrease some time before bears enter their dens. Further analyses of activity data, in combination with data on movement, body temperature, and heart rate will provide us with more knowledge about the chronological order of physiological and behavioral changes during the transition period from active to hibernation stage, and vice versa. These analyses would enable us to advance one step further in the understanding of the biological time keeping processes of hibernation.

In paper III, I used activity and body temperature data to detect implantation and parturition. Unfortunately I had no information about the females’ body weight prior to hibernation, but my results for free-ranging bears showed different results regarding the effect of female condition on the timing of parturition than for bears in captivity. The determination of parturition dates was a pilot study and never had been done on free-ranging bears before. Further studies of hibernating free-ranging pregnant brown bears are necessary in order to gain more reliable knowledge about which factors influence the timing of parturition. Comparable studies on pregnant captive bears in our study area could be conducted in order to determine if the start of denning and the time females had spent in the den prior to parturition affect the timing of parturition. Those factors were not included in previous studies on captive pregnant females, because animal keepers often decide the timing of hibernation by caging bears in their artificial dens and ceasing to feed them.

Pseudopregnancy has been documented and is common in captive ursids (Shimozuru et al., 2013, Sato et al., 2001, Tsubota et al., 1987, Dehnhard et al., 2006). Several researchers have demonstrated, that body temperatures and hormone levels are similar during gestation (or “pseudogestation”) for pregnant and pseudopregnant bears. It is therefore extremely difficult to distinguish between a free-ranging pregnant and pseudopregnant female, if the female had lost its cubs soon after parturition, before we were able to document that cubs had been born. When I compared the body temperature patterns between pregnant and nonpregnant bears during the gestation period (paper III), none of the nonpregnant bears showed high body temperature levels during hibernation, and I could confirm that cubs had been born for all pregnant bears. However, sooner or later we will receive body temperature data from pregnant females that lose their cubs before we observe them and which will not be captured (to confirm lactation and used nipples). Then, we will not be able to determine if this female had been pregnant or pseudopregnant. However, vaginal implants that document birth events and communicate with GPS collars in combination with implanted body temperature loggers might be a future method to document if pseudopregnancy occurs often in free-ranging brown bears or if this is a more common phenomenon in captive bears.

7 Abstract

This thesis deals with several aspects of the hibernation biology of bears. Hibernation is an essential feature of the ecology and reproduction of brown bears (Ursus arctos). It necessitates a variety of complex physiological and behavioral changes and the ability to adapt to environmental changes and anthropogenic influences. Furthermore, the bears’ needs during hibernation differ according to the physical condition and reproductive state of the individual. Many hibernation studies, especially physiological studies, have been conducted on bears in captivity; however, free-ranging bears must cope with more challenging factors. Thus, environmental, individual, and behavioral factors need to be included when studying winter behavior. In Sweden, hunting activities are high in autumn and bears are reported to be more aggressive at their den sites. Disturbance of pregnant female brown bears during winter can lower their reproductive success, because pregnant females give birth to cubs during hibernation. Pregnant females are not protected from the bear hunting. Thus, the knowledge of the timing when brown bears enter hibernation and when they give birth to offspring can supply us with important information for bear conservation, and may additionally improve the safety of both humans and bears. I documented the denning behavior of brown bears in central Sweden, with an emphasis on which environmental and behavioral factors influence den entry to gain a general understanding of the hibernation process in bears. Additionally I investigate bear’s activity and movement behavior prior and during denning to evaluate whether behavioral changes can explain the higher risks of injuries at this time. I also studied physiological and behavioral alterations of pregnant females during hibernation to document for the first time the timing of gestation and parturition in free-ranging brown bears. I developed a new noninvasive method to detect pregnancy and parturition in hibernating brown bears using activity data and evaluated which factors influenced the timing of hibernation and parturition in pregnant bears.

Brown bears arrived at their den sites from 6 October until 1 December. The mean den entry date for all bears was 28 October, but it varied with reproductive category, bear age, and among years. Solitary females, pregnant females, and females with cubs of the year arrived at their den sites earlier than males. Younger bears tended to arrive at their den sites later than older bears. However, older pregnant females started hibernation earlier and their start of hibernation was also earlier during years with favorable environmental conditions.

Bears gradually reduced their movements and activity several weeks before entering the den and appeared to be more sensitive to disturbance in this period. Den abandonment during hibernation was high (22%), but female brown bears had a lower den abandonment rate and visited their den areas during season more often than males. Although bear-caused injuries to humans peak during October and November, we could not confirm that the vicinity of a den was an important factor associated with these injuries. Half of the bears reduced their activity level significantly before they had arrived at their den sites, so some of the human injuries may have been associated with the bears’ prehibernation behavior. I suggest that physiological changes during prehibernation may affect the bears’ behavior. More research on bears’ physiology prior to hibernation is necessary in order to confirm if physiological changes can explain higher risks of injuries.

Pregnant females showed higher activity levels and were more frequently active during pregnancy than during the postpartum period, in contrast to nonpregnant females. I created a pregnancy index based on activity data that can be used to determine if a female brown bear had given birth during hibernation. I used the rise and drop in body temperature and activity levels during hibernation to determine the gestation period of pregnant females. Body temperature and activity were higher during the gestation period than during the preimplantation and lactation periods. The gestation period averaged 56 days in free-ranging brown bears. The mean date of parturition calculated with activity data was 21 January, with a range of 43 days which demonstrates a high flexibility in the timing of gestation. The dates of parturition were later during years with good environmental conditions, which was unexpected, because captive pregnant females in excellent condition give birth to young earlier than females that are lean. Further studies of hibernating free-ranging pregnant brown bears are necessary in order to gain more knowledge about which factors influence the timing of parturition. My new noninvasive method to detect pregnancy in bears can facilitate demographic studies of GPS-marked animals because it delivers reliable information about gestation and parturition. It may also help to obtain better information about the age of primiparous females and to detect phenomenons of mixed-age litters.

8 Zusammenfassung

Diese Dissertation beschäftigt sich mit verschiedenen Aspekten der Winterruhe von Bären. Die Winterruhe ist ein wesentlicher Bestandteil in der Ökologie und Reproduktion von Braunbären (Ursus arctos). Sie erfordert eine Vielzahl von komplexen physiologischen Umstellungen und Verhaltensänderungen und beruht auf der Fähigkeit, auf veränderte Umweltbedingungen und anthropogene Einflüsse reagieren zu können. Nahrungsangebot und Klima, insbesondere die Temperatur, können sowohl den Beginn als auch die Dauer der Winterruhe beinflussen. Da Bären während der Winterruhe keine Nahrung zu sich nehmen, haben diese Umweltfaktoren einen direkten Einfluß auf deren Fittness. Bären haben während der Winterruhe unterschiedliche Ansprüche, welche sich je nach körperlicher Kondition und reproduktivem Zustand des Individuums unterscheiden. Große Bärenmännchen halten zum Beispiel kürzer Winterruhe, da sie mehr Fett anlegen können und proportional zum Körpergewicht weniger Gewicht verlieren als kleine Bären. Trächtige Weibchen verbrauchen während der Winterruhe im Durchschnitt etwa doppelt so viel Energie wie andere Bären, da die Jungen während der Winterruhe geboren und mit einer fetthaltigen Milch gesäugt werden. Bisher wurde die Winterruhe, insbesondere in physiologischen Studien häufig an Bären in Gefangenschaft erforscht. Freilebende Bären müssen jedoch weitaus mehr und anspruchsvollere Umweltfaktoren bewältigen. Aus diesem Grund müssen bei der Erforschung der Winterruhe in Freilandstudien stets auch Umweltbedingungen, individuelle Eigenschaften und die Verhaltensweisen der Bären mit einbezogen werden. Zusätzlich können anthropogene Faktoren die Winterruhe beeinflussen. In Schweden finden viele Jagdaktivitäten, wie zum Beispiel die Großwildjagd, im Herbst statt, zu einer Zeit, in der Braunbären ihre Winterhöhlen aufsuchen. Berichten zufolge zeigen Bären in Schweden in der Nähe ihrer Winterhöhlen ein erhöhtes Aggressionsverhalten. Studien haben zudem gezeigt, daß trächtige Braunbärweibchen, die im Winter gestört werden, einen geringeren Fortpflanzungserfolg haben. Braunbären sind bei der Geburt blind und nackt, sie wiegen nur 300-500g und sind auf die Wärme der Mutter angewiesen. Ein Wechseln der Winterhöhle kann deshalb zum Verlust der Jungen führen insbesondere, wenn diese noch sehr jung sind.

In Schweden leben ca. 2800 freilebende Braunbären (Stand2013). Ich studierte das Winterverhalten der Braunbären in Mittelschweden, mit dem Schwerpunkt, die Umwelt- und Verhaltensfaktoren zu identifizieren, welche die Winterruhe beeinflussen, um

charakteristische Erkenntnisse über den Prozess der Winterruhe bei Braunbären zu gewinnen. Zusätzlich studierte ich das Aktivitäts- und Wanderverhalten der Bären vor und während dem Eintritt in ihre Winterhöhlen, um bewerten zu können, ob Verhaltensänderungen die vermehrten Angriffe auf Menschen in dieser Zeit erklären können. Frühere Freilandstudien über das Winterverhalten von Bären basierten meist nur auf Positionsdaten und nicht auf Aktivitätsdaten. Aktivitätsdaten können uns jedoch detailliertere Informationen über den Verlauf der Winterruhe liefern, wie z.B. ob ein Bär noch einige Zeit aktiv am Winterhöhlenplatz ist, oder ob die Winterruhe unmittelbar nach dem Aufsuchen der Winterhöhle eintritt. Bären in Schweden graben jedes Jahr eine neue Winterhöhle, werden sie während der Winterruhe gestört, so verlassen sie ihre Höhle und bauen sich ein neues Winterquartier. Ich untersuchte, ob Bären strategisch einen Platz für die Winterhöhle wählen, der schon vorher während der aktiven Saison aufgesucht wurde oder ob die Wahl der Höhlenplätze spontan erfolgt. Zudem dokumentierte ich, wie viele Bären im Winter ihre Höhlen wechselten.

Mit dem Ziel, zum ersten Mal die Periode der Tragzeit und die Zeitpunkte der Geburten bei frei lebenden Braunbären zu dokumentieren, untersuchte ich physiologische Modifikationen und Verhaltensänderungen von trächtigen Braunbärenweibchen während der Winterruhe. Früheren Studien haben dokumentiert, daß bei Bären die Einnistung der Blastozysten etwa im November/Dezember und die Geburten im Januar/Februar stattfinden. Detaillierte Informationen für freilebende Braunbären sind nicht vorhanden. Da Braunbären während der Winterruhe sehr störanfällig sind, entwickelte ich mit Hilfe von Aktivitätsmessungen eine neue, nicht invasive Methode, um die Trächtigkeit und Geburt während der Winterruhe bei Braunbären zu bestimmen. Zudem untersuchte ich bei trächtigen Bären, welche Faktoren den Beginn der Winterruhe und den Zeitpunkt der Geburt beeinflussen.

Zwischen 2004-2013 haben wir von einem Helikopter aus insgesamt 55 freilebende Bären in verschiedenen Geschlechts- und Alterskategorien betäubt und mit einem GPS-GSM Halsband, in dem ein Aktivitätssensor integriert ist, für mehrere Jahre besendert. Die GPS- Sender lokalisierten die Bären während der aktiven Phase alle 30 min und während der Winterruhe 1-mal täglich. Die Aktivitäten wurden 6-8 mal pro Sekunde gemessen, im 5 Minuten Intervall gemittelt und auf einer Skala von 0-255 aufgezeichnet. Alle Winterhöhlen wurden im darauffolgenden Frühjahr, nachdem die Bären ihre Höhlen verlassen hatten, aufgesucht und vermessen. Um die Tragzeit und den Zeitpunkt der Geburt dokumentieren zu

können, wurden 16 adulten, weiblichen Braunbären zusätzlich ein Temperatursensor abdominal implantiert, der die Körpertemperatur alle 30 min aufzeichnete.

Braunbären suchten den Platz der Winterhöhlen zwischen dem 6. Oktober und 1. Dezember auf. Sie betraten die Winterhöhlen im Durchschnitt am 28. Oktober, das Eintrittsdatum variierte jedoch mit der reproduktiven Kategorie, dem Alter des Bären, und zwischen den Kalenderjahren. Solitäre Weibchen, trächtige Weibchen und Bärenweibchen mit Jungtieren, suchten die Plätze der Winterhöhlen früher auf als Bärenmännchen. Jüngere Bären suchten ihre Höhlenplätze früher auf als ältere Bären. Ältere trächtige Bärenweibchen hingegen, gingen früher zur Winterruhe insbesondere in Jahren mit günstigen Umweltbedingungen. Die Bären begannen bereits mehrere Wochen vor dem Eintritt in die Winterhöhlen ihre täglichen Wanderungen und Aktivitäten zu reduzieren und sie schienen in diesem Zeitraum empfindlicher auf Störungen zu reagieren. Während der Winterruhe wechselten 22% der Bären die Winterhöhle. Weibliche Bären wählten ihren Winterhöhlenplatz in bekannten, zuvor aufgesuchten Gebieten und flüchteten aus ihren Winterhöhlen seltener als Männchen, die ihren Höhlenplatz spontan gewählt hatten. Obwohl Unfälle mit Bären vorwiegend im Oktober und November stattfinden, konnte ich nicht bestätigen, daß die Nähe einer Winterhöhle ein wichtiger Faktor bei diesen Verletzungen war. Die Hälfte der Bären reduzierte ihr Aktivitätsniveau schon deutlich vor dem Aufsuchen der Winterhöhle, so daß einige der Angriffe auf Menschen mit den Verhaltensänderungen vor der Winterruhe in Verbindung gebracht werden können. Ich vermute, daß physiologische Veränderungen schon vor der Winterruhe einsetzen, die das Verhalten der Bären beeinflussen können. Einige Studien berichten über lethargisches Verhalten und Ende der Nahrungsaufnahme noch bevor sich Bären zur Winterruhe begeben. Weitere Forschung über die Physiologie der Bären vor der Winterruhe ist erforderlich, um zu bestätigen, ob und welche physiologischen Veränderungen ein höheres Aggressionsverhalten erklären können.

Der Beginn der Winterruhe spiegelte sich bei den Bären in einem drastischen Abfall der täglichen Aktivitäten wieder. Während der Winterruhe wechseln Bären mehrmal täglich ihre Körperposition in der Winterhöhle. Aus diesem Grund sind nur sehr niedrige Aktivitäten meßbar. Dennoch konnte ich bei trächtigen Bärenweibchen typische Aktivitätsmuster während der Winterruhe erkennen. Die tägliche Durchschnittsaktivität viel bei trächtigen Weibchen wie auch bei anderen Bären bei Beginn der Winterruhe drastisch ab, doch stieg die Aktivität gegen Ende November wieder leicht an und sank erst im Januar oder Februar wieder

ab. Während der Tragzeit hatten trächtige Bärenweibchen im Durchschnitt 3-mal höhere Aktivitätslevel und sie waren doppelt so oft aktiv wie während der postpartalen Phase. Bei nicht-trächtigen Weibchen war kein signifikanter Unterschied zwischen diesen Perioden nachweisbar. Trächtige Weibchen waren während der Tragzeit aktiver und während der postpartalen Phase passiver als nicht-trächtige Weibchen. Da neugeborene Bärenjungen auf die Wärme der Mutter angewiesen sind, liegen diese wahrscheinlich still, um die Jungen vor dem Auskühlen zu schützen. Ich habe eine Formel für einen Trächtigkeits-Index erstellt. Dieser Index basiert auf den unterschiedlichen Aktivitätslevel während der Tragzeit und postpartalen Phase und kann verwendet werden, um festzustellen, ob eine Braunbärin während der Winterruhe Jungtiere geboren hat. Um die Qualität des Trächtigkeits-Index zu testen, wurden in dieser Studie nur Daten von Tieren verwendet, deren Reproduktionsstatus anhand von Observationen von Jungtieren und anhand von Information über Laktation bestätigt werden konnten. Bärinnen wurden als trächtig eingestuft, wenn wir sie im Frühjahr mit Jungtieren beobachten konnten, oder wenn die Bärin laktierte. Bärinnen wurden als nicht trächtig eingestuft, wenn die Bärin nicht laktierte und auch keine neugeborenen Jungen bei sich hatte. Ich testete meinen Trächtigkeits-Index bei einer Bärengruppe, die von meiner Analyse ausgeschlossen wurde, um zu bewerten, wie hoch die Wahrscheinlichkeit ist, dass mit der üblichen Observationsmethode ein Weibchen in die falsche Reproduktionskategorie eingeordnet wird. Bei den Weibchen dieser Testgruppe beobachteten wir keine Jungtiere, wussten jedoch nicht, ob die Bärinnen laktierten. Der Trächtigkeits-index zeigte, dass 35% der Tiere dieser Testgruppe in der Tat trächtig waren. In Schweden ist Infantizid durch Bärenmännchen während der Paarungszeit die häufigste Todesursache von Bärenjungen. Wahrscheinlich hatten diese Weibchen ihre Jungen sehr früh verloren, noch bevor wir die Familiengruppen beobachten konnten. Ich befürworte, die Trächtigkeit von Bären in Zukunft mit Hilfe von Aktivitätsdaten und dem Trächtigkeits-index zu bestimmen. In meiner Studie bestimmte der Index den Reproduktionsstatus zu 98% richtig und erkannte zusätzlich Trächtigkeiten, die mit reinen Observationsmethoden nicht endeckt wurden. Diese Methode vermeidet zusätzlich das Stören von Bären während der Winterruhe oder im Frühjahr, was mit Observationsmethoden unvermeidlich ist.

Ich vermutete, daß der beobachtete Abfall der Aktivitäten im Januar/Februar die Geburt der Jungen anzeigte. Da ich jedoch keinen Beweis erbringen konnte, dass die Jungen tatsächlich zu diesem Zeitpunkt geboren wurden, habe ich in der folgenden Studie die Körpertemperaturdaten der Bären miteinbezogen. Es ist bekannt, dass trächtige Bären

während der Tragzeit eine höhere Körpertemperatur haben. Ich habe den Anstieg und Abfall der Körpertemperatur mit den Aktivitätsdaten während der Winterruhe verglichen und mit Hilfe dieser Daten die Tragzeit von trächtigen Weibchen bestimmt. Die Körpertemperatur und auch die Aktivität waren wie erwartet während der Tragzeit höher als während der Präimplantations- und Laktationsphase. Ich ermittelte anhand der Körpertemperaturdaten die Daten der Implantation sowie die Daten der Geburt und errechnete eine durchschnittliche Tragzeit von 56 Tagen bei frei lebenden Braunbären. Die Daten der Geburten konnte auch mit den Aktivitätsdaten errechnet werden, sie unterschieden sich nicht signifikant von den errechneten Geburtsdaten mit den Körpertemperaturdaten; die maximale Differenz betrug 2 Tage. Die errechneten Daten der Implantation mit Aktivitäts- und Körpertemperaturdaten waren nur knapp statistisch signifikant gleich. Aus diesem Grund berechnete ich für Bären, bei denen nur Aktivitäts- und keine Körpertemperaturdaten vorgenommen wurden lediglich die Zeitpunkte der Geburten. Das mit Aktivitätsdaten berechnete durchschnittliche Datum der Geburt war der 21. Januar, mit einer Spanne von 43 Tagen. Diese enorme Spanne lässt auf eine hohe Flexibilität in der zeitlichen Planung der Tragzeit schließen. Braunbären gebaren ihre Jungen in den Jahren mit guten Umweltbedingungen (z.B. hohe Nahrungsverfügbarkeit) später. Dieses Ergebnis war unerwartet. In Tierparks gebären trächtige gutgenährte Braunbärweibchen früher als magere Weibchen, was zur Folge hat, das die Jungen beim Verlassen der Winterhöhle älter, schwerer und grösser sind. Meine Ergebnisse zeigten jedoch auch, dass trächtige Bären in Jahren mit hoher Nahrungsverfügbarkeit die Winterruhe früher begannen. In Tierparks entscheiden oft die Tierpfleger, wann die Bären in ihre künstlichen Winterhöhlen gebracht werden. In meiner Freilandstudie hatte der Beginn der Winterruhe keinen Einfluss auf den Zeitpunkt der Geburt, was darauf schliessen lässt, dass andere Faktoren, den Zeitpunkt der Implantation induzieren. In Schweden begannen 47% der trächtigen Bärenweibchen die Winterruhe vor dem 15. Oktober, dem offiziellen Ende der Bärenjagd. Ein frühzeitiger Beginn der Winterruhe kann eine Strategie sein, menschliche Störungen und potentielle Energieverluste während der Jagdzeit zu meiden. Frühere Studien haben gezeigt, daß trächtige Weibchen besser geschützte Winterhöhlen konstuieren. Unsere Studie zeigte zusätzlich, daß Bärenweibchen ihre Höhlenplätze strategisch wählen. Weitere Forschung über die Winterruhe von frei lebenden trächtigen Braunbären ist notwendig, um zu erfahren, welche Faktoren die zeitliche Organisation der Tragzeit und Geburt beeinflussen.

In Schweden sind trächtige Weibchen während der Bärenjagd nicht geschützt. Das Wissen, wann Braunbären die Winterruhe beginnen und wann die Weibchen ihren Nachwuchs

gebären, kann somit wichtige Informationen für den Bärenschutz liefern und zusätzlich zur Sicherheit von Menschen und Bären während dieser empfindlichen Periode beitragen. Meine neue, nicht-invasive Methode zur Erkennung der Trächtigkeit von Bären kann demografische Studien von GPS-markierten Tieren erleichtern, da sie zuverlässige Informationen über die Tragzeit und Geburt liefert. Insbesondere kann sie zur Aufklärung beitragen wann Bärenweibchen das erst Mal gebären und wie häufig Phänomene wie z.B. altersgemischte Würfe wirklich vorkommen.

9 References

ALT, G. L. 1983. Timing of parturition of black bears (Ursus americanus) in northeastern Pennsylvania. Journal of Mammalogy, 64, 305-307. ARNEMO, J. M., EVANS, A. L. & FAHLMAN, Å. 2012. Biomedical protocols for free-ranging brown bears, gray wolves, wolverines and lynx. Hedmark University College. Evenstad, Norway. ASTAEVA, M. D. & KLICHKHANOV, N. K. 2009. Oxidative modification of proteins and blood antioxidant activity of ground squirrels during induced awakening from hibernation. Biology Bulletin, 36, 562-567. ATKINSON, S. N. & RAMSAY, M. A. 1995. The effects of prolonged fasting of the body composition and reproductive success of female polar bears (Ursus maritimus). Functional Ecology, 9, 559-567. BARNES, B. M. 1989. Freeze avoidance in a mammal: body temperatures below 0 degree C in an Arctic hibernator. Science, 244, 1593-1595. BAUMAN, J. E., CLIFFORD, D. L. & ASA, C. S. 2008. Pregnancy diagnosis in wild canids using a commercially available relaxin assay. Zoo Biology, 27, 406-413. BEALE, C. M. & MONAGHAN, P. 2004. Behavioural responses to human disturbance: a matter of choice? Animal Behaviour, 68, 1065-1069. BEECHAM, J. J. 1980. Population characteristics, denning, and growth patterns of black bears in Idaho. Dissertation, University of Montana. BELLEMAIN, E., SWENSON, J. E., TALLMON, D., BRUNBERG, S. & TABERLET, P. 2005. Estimating population size of elusive animals with DNA from hunter-collected feces: Four methods for brown bears. Estimación del tamaño poblacional de animales elusivos con ADN de heces colectadas por cazadores: Cuatro métodos para osos pardos. Conservation Biology, 19, 150- 161. BELLEMAIN, E., ZEDROSSER, A., MANEL, S., WAITS, L. P., TABERLET, P. & SWENSON, J. E. 2006. The dilemma of female mate selection in the brown bear, a species with sexually selected infanticide. Proceedings. Biological sciences / The Royal Society, 273, 283-91. BIEBER, C., LEBL, K., STALDER, G., GEISER, F. & RUF, T. 2014. Body mass dependent use of hibernation: why not prolong the active season, if they can? Functional Ecology, 28, 167-177. BISCHOF, R., SWENSON, J. E., YOCCOZ, N. G., MYSTERUD, A. & GIMENEZ, O. 2009. The magnitude and selectivity of natural and multiple anthropogenic mortality causes in hunted brown bears. The Journal of animal ecology, 78, 656-65. BOYER, B. B. & BARNES, B. M. 1999. Molecular and Metabolic Aspects of Mammalian Hibernation: Expression of the hibernation phenotype results from the coordinated regulation of multiple physiological and molecular events during preparation for and entry into torpor. BioScience, 49, 713-724. BRIDGES, A. S., OLFENBUTTEL, C. & VAUGHAN, M. R. 2002. A mixed regression model to estimate neonatal black bear cub age. Wildlife Society Bulletin, 30, 1253-1258. BRIDGES, A. S., VAUGHAN, M. R. & FOX, J. A. 2011. American black bear estrus and parturition in the Alleghany Mountains of Virginia. Ursus, 22, 1-8. BUNNELL, F. L. & TAIT, D. E. N. 1981. Population dynamics of bears - implications. In: FOWLER, C. W. & SMITH, T. D. (eds.) Dynamics of large mammal populations. John Wiley and Sons, New York, USA. CIARNIELLO, L. M., BOYCE, M. S., HEARD, D. C. & SEIP, D. R. 2005. Denning Behavior and Den Site Selection of Grizzly Bears along the Parsnip River, British Columbia, Canada. Ursus, 16, 47-58. CRAIGHEAD, F. C., JR. & CRAIGHEAD, J. J. 1972a. Data on grizzly bear denning activities and behavior obtained by using wildlife telemetry. Proceedings of the International Conference on Bear Research and Management, 2, 84-106.

CRAIGHEAD, F. C., JR. & CRAIGHEAD, J. J. 1972b. Grizzly Bear Prehibernation and Denning Activities as Determined by Radiotracking. Wildlife Monographs, 3-35. DAHLE, B. 2003. Reproductive strategies in Scandinavian brown bears. Ph.D. dissertation, Norwegian University of Science and Technology, Trondheim, Norway. DAHLE, B. & SWENSON, J. E. 2003. Seasonal range size in relation to reproductive strategies in brown bears Ursus arctos. Journal of Animal Ecology, 72, 660-667. DAHLE, B., SØRENSEN, O. J., WEDUL, E. H., SWENSON, J. E. & SANDEGREN, F. 1998. The diet of brown bears Ursus arctos in central Scandinavia: effect of access to free-ranging domestic sheep Ovis aries. Wildlife Biology, 4, 147-158. DECOURSEY, P., DUNLAP, J. & LOROS, J. 2004. Chronobiology: biological timekeeping. Sunderland, MA: Sinauer Associates Inc. DEHNHARD, M., HILDEBRANDT, T. B., KNAUF, T., JEWGENOW, K., KOLTER, L. & GORITZ, F. 2006. Comparative endocrine investigations in three bear species based on urinary steroid metabolites and volatiles. Theriogenology, 66, 1755-1761. DITTRICH, L. & KRONBERGER, H. 1963. Biologischanatomische Untersuchungen über die Fortpflanzungsbiologie des Braunbären (Ursus arctos L.) und anderer Ursiden in Gefangenschaft. Zeitschrift für Säugetierkunde, 28, 129-192. DONAHUE, S. W., GALLEY, S. A., VAUGHAN, M. R., PATTERSON-BUCKENDAHL, P., DEMERS, L. M., VANCE, J. L. & MCGEE, M. E. 2006. Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis. The Journal of experimental biology, 209, 1630-8. EILAM, D. 2005. Die hard: A blend of freezing and fleeing as a dynamic defense—implications for the control of defensive behavior. Neuroscience & Biobehavioral Reviews, 29, 1181-1191. ELFSTRÖM, M. & SWENSON, J. E. 2009. Effects of sex and age on den site use by Scandinavian brown bears. Ursus, 20, 85-93. ELFSTRÖM, M., SWENSON, J. E. & BALL, J. P. 2008. Selection of denning habitats by Scandinavian brown bears Ursus arctos. Wildlife Biology, 14, 176-187. ELOWE, K. D. & DODGE, W. E. 1989. Factors affecting black bear reproductive success and cub survival. The Journal of Wildlife Management, 53, 962-968. FARLEY, S. D. & ROBBINS, C. T. 1995. Lactation, hibernation, and mass dynamics of American black bears and grizzly bears. Canadian Journal of Zoology, 73, 2216-2222. FOLK, G. E., DICKSON, E. W., HUNT, J. M., NILLES, E. J. & THRIFT, D. L. 2008. QT intervals compared in small and large hibernators and humans. Biological Rhythm Research, 39, 427-438. FOLK, G. E., JR., FOLK, M. A. & MINOR, J. J. 1972. Physiological Condition of Three Species of Bears in Winter Dens. Bears: Their Biology and Management, 2, 107-124. FOLK, G. E., JR., HUNT, J. M. & FOLK, M. A. 1980. Further Evidence for Hibernation of Bears. Bears: Their Biology and Management, 4, 43-47. FOLK, G. E., JR., LARSON, A. & FOLK, M. A. 1976. Physiology of Hibernating Bears. Bears: Their Biology and Management, 3, 373-380. FORESMAN, K. R. & DANIEL, J. C. 1983. Plasma progesterone concentrations in pregnant and nonpregnant black bears (Ursus americanus). Journal of Reproduction and Fertility, 68, 235- 239. FRENCH, A. R. 1986. Patterns of thermoregulation during hibernation. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold. Elsevier, New York, 393-402. FRIEBE, A., SWENSON, J. E. & SANDEGREN, F. 2001. Denning chronology of female brown bears in central Sweden. Ursus, 12, 37-45. FRIEBE, A., ZEDROSSER, A. & SWENSON, J. E. 2013. Detection of pregnancy in a hibernator based on activity data. European Journal of Wildlife Research, 59, 731-741. FRKOVIĆ, A., HUBER, D. & KUSAK, J. 2001. Brown Bear Litter Sizes in Croatia. Ursus, 12, 103-105. GEISER, F. 1998. Evolution of daily torpor and hibernation in birds and mammals: Importance of body size. Clinical and Experimental Pharmacology and Physiology, 25, 736-740.

GEISER, F. 2004. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annual review of physiology, 66, 239-74. GOLDSTEIN, M. I., POE, A. J., SURING, L. H., NIELSON, R. M. & MCDONALD, T. L. 2010. Brown bear den habitat and winter recreation in South-Central Alaska. The Journal of Wildlife Management, 74, 35-42. GWINNER, E. 1986. Circannual rhythms: Endogenous annual clocks in the organization of seasonal processes Berlin and New York, Springer-Verlag Zoophysiology, 18. HARLOW, H. J., LOHUIS, T., BECK, T. D. I. & IAIZZO, P. A. 2001. Muscle strength in overwintering bears. Nature, 409, 997-997. HELDMAIER, G. 2011. Life on Low Flame in Hibernation. Science, 331, 866-867. HELDMAIER, G., ORTMANN, S. & ELVERT, R. 2004. Natural hypometabolism during hibernation and daily torpor in mammals. Respiratory Physiology & Neurobiology, 141, 317-329. HELLGREN, E. C. 1998. Physiology of hibernation in bears. Ursus, 10, 467-477. HENSEL, R. J., TROYER, W. A. & ERICKSON, A. W. 1969. Reproduction in the female brown bear. The Journal of Wildlife Management, 33, 357-365. HILDERBRAND, G. V., JENKINS, S. G., SCHWARTZ, C. C., HANLEY, T. A. & ROBBINS, C. T. 1999. Effect of seasonal differences in dietary meat intake on changes in body mass and composition in wild and captive brown bears. Canadian Journal of Zoology, 77, 1623-1630. HISSA, R. 1997. Physiology of the European brown bear (Ursus arctos arctos). Ann. Zool. Fennici, 34, 267–287. HISSA, R., SIEKKINEN, J., HOHTOLA, E., SAARELA, S., HAKALA, A. & PUDAS, J. 1994. Seasonal patterns in the physiology of the European brown bear (Ursus arctos arctos) in Finland. Comparative Biochemistry and Physiology Part A: Physiology, 109, 781-791. HUBER, D. & ROTH, H. U. 1997. Denning of Brown Bears in Croatia. Proceedings of the International Conference on Bear Research and Management, 9, 79-83. HUMPHRIES, M. M., THOMAS, D. W. & KRAMER, D. L. 2003. The role of energy availability in mammalian hibernation: A cost benefit approach. Physiological and Biochemical Zoology, 76, 165-179. IIBUCHI, R., NAKANO, N., NAKAMURA, T., URASHIMA, T., SHIMOZURU, M., MURASE, T. & TSUBOTA, T. 2009. Change in body weight of mothers and neonates and in milk composition during denning period in captive Japanese black bears (Ursus thibetanus japonicus). Japanese Journal of Veterinary Research, 57, 13-22. JUDD, S. L., KNIGHT, R. R. & BLANCHARD, B. M. 1986. Denning of grizzly bears in the Yellowstone National Park area. Proceedings of the International Conference on Bear Research and Management, 6, 111-117. KIDDY, C. A. 1977. Variation in physical activity as an indication of estrus in dairy cows. Journal of Dairy Science, 60, 235-243. KINDBERG, J., SWENSON, J. E., ERICSSON, G., BELLEMAIN, E., MIQUEL, C. & TABERLET, P. 2011. Estimating population size and trends of the Swedish brown bear Ursus arctos population. Wildlife Biology, 17, 114-123. KINGSLEY, M. C. S., NAGY, J. A. & RUSSELL, R. H. 1983. Patterns of Weight Gain and Loss for Grizzly Bears in Northern Canada. Bears: Their Biology and Management, 5, 174-178. KLEIMAN, D. G., THOMPSON, K. V. & BAER, C. K. 2010. Wild Mammals in Captivity: Principles and Techniques for Zoo Management, University of Chicago Press. KORDEK, W. S. & LINDZEY, J. S. 1980. Preliminary analysis of female reproductive tracts from Pennsylvania black bears. Proceedings of the International Conference on Bear Research and Management, 4, 159-161. KÄHN, W. 1992. Ultrasonography as a diagnostic tool in female animal reproduction. Animal Reproduction Science, 28, 1-10. LABYAK, S. E. & LEE, T. M. 1995. Estrus- and steroid-induced changes in circadian rhythms in a diurnal rodent, Octodon degus. Physiology & Behavior, 58, 573-585.

LASKE, T. G., GARSHELIS, D. L. & IAIZZO, P. A. 2011. Monitoring the wild black bear's reaction to human and environmental stressors. BMC Physiology, 11, 13. LENTFER, J. W. & HENSEL, R. J. 1980. Alaskan Polar Bear Denning. Bears: Their Biology and Management, 4, 101-108. LIGHTFOOT, J. T. 2008. Sex hormones' regulation of rodent physical activity: a review. International Journal of Biological Sciences, 4, 126-32. LINNELL, J. D. C., JON, E. S., ANDERSEN, R. & BARNES, B. 2000. How vulnerable are denning bears to disturbance? Wildlife Society Bulletin, 28, 400-413. LÓPEZ-ALFARO, C., ROBBINS, C. T., ZEDROSSER, A. & NIELSEN, S. E. 2013. Energetics of hibernation and reproductive trade-offs in brown bears. Ecological Modelling, 270, 1-10. MACE, R. D. & WALLER, J. S. 1997. Denning ecology of grizzly bears in the Swan Mountains, Montana. Final report: Grizzly bear ecology in the Swan Mountains. Montana Department of Fish, Wildlife and Parks, Helena, Montana, USA. MANCHI, S. & SWENSON, J. E. 2005. Denning behaviour of Scandinavian brown bears Ursus arctos. Wildlife Biology, 11, 123-132. MARTIN, J., BASILLE, M., VAN MOORTER, B., KINDBERG, J., ALLAINÉ, D. & SWENSON, J. E. 2010. Coping with human disturbance: spatial and temporal tactics of the brown bear (Ursus arctos). Canadian Journal of Zoology, 88, 875-883. MARTIN, J., VAN MOORTER, B., REVILLA, E., BLANCHARD, P., DRAY, S., QUENETTE, P.-Y., ALLAINÉ, D. & SWENSON, J. E. 2013. Reciprocal modulation of internal and external factors determines individual movements. Journal of Animal Ecology, 82, 290-300. MCLELLAN, B. N. 2011. Implications of a high-energy and low-protein diet on the body composition, fitness, and competitive abilities of black (Ursus americanus) and grizzly (Ursus arctos) bears. Canadian Journal of Zoology, 89, 546-558. MCMILLIN, J. M., SEAL, U. S., ROGERS, L. & ERICKSON, A. W. 1976. Annual testosterone rhythm in the black bear (Ursus americanus). Biology of Reproduction, 15, 163-167. MILLER, S. D. 1990. Denning ecology of brown bears in Southcentral Alaska and comparisons with a sympatric black bear population. Proceedings of the International Conference on Bear Research and Management, 8, 279-287. MOEN, G. K., STØEN, O.-G., SAHLÉN, V. & SWENSON, J. E. 2012. Behaviour of solitary adult Scandinavian brown bears (Ursus arctos) when approached by humans on foot. PLoS ONE, 7, e31699. NAWAZ, M. A., SWENSON, J. E. & ZAKARIA, V. 2008. Pragmatic management increases a flagship species, the Himalayan brown bears, in Pakistan’s Deosai National Park. Biological Conservation, 141, 2230-2241. NELLEMANN, C., STØEN, O.-G., KINDBERG, J., SWENSON, J. E., VISTNES, I., ERICSSON, G., KATAJISTO, J., KALTENBORN, B. P., MARTIN, J. & ORDIZ, A. 2007. Terrain use by an expanding brown bear population in relation to age, recreational resorts and human settlements. Biological Conservation, 138, 157-165. NELSON, O. L., MCEWEN, M. M., ROBBINS, C. T., FELICETTI, L. & CHRISTENSEN, W. F. 2003. Evaluation of cardiac function in active and hibernating grizzly bears. J Am Vet Med Assoc, 223, 1170-5. NELSON, R. 1989. Nitrogen turnover and its conservation in hibernation., In: Malan A, Canguilhem M (eds) Living in the Cold. Libby Eurotext: Montrouge, France. NELSON, R., WAHNER, H., JONES, J., ELLEFSON, R. & ZOLLMAN, P. 1973. Metabolism of bears before, during, and after winter sleep. American Journal of Physiology - Legacy Content, 224, 491- 496. NELSON, R. A. 1973. Winter sleep in the black bear: a physiologic and metabolic marvel. Mayo Clinic Proceedings, 48, 733-737. NELSON, R. A. 1980. Protein and fat metabolism in hibernating bears. Fed Proc, 39, 2955-8.

NELSON, R. A., FOLK, G. E., JR., PFEIFFER, E. W., CRAIGHEAD, J. J., JONKEL, C. J. & STEIGER, D. L. 1983. Behavior, Biochemistry, and Hibernation in Black, Grizzly, and Polar Bears. Bears: Their Biology and Management, 5, 284-290. NORES, C., BALLESTEROS, F., BLANCO, J., GARCÍA-SERRANO, A., HERRERO, J. & PALOMERO, G. 2010. Evidence of non-hibernation in Cantabrian brown bears. Acta Theriologica, 55, 203-209. OPSETH, O. 1998. Brown bear (Ursus arctos) diet and predation on moose (Alces alces) calves in the southern taiga zone in Sweden. Candidatus Scientarum Thesis, Norwegian University of Science and Technology, Trondheim, Norway. ORDIZ, A., STOEN, O. G., DELIBES, M. & SWENSON, J. E. 2011. Predators or prey? Spatio-temporal discrimination of human-derived risk by brown bears. Oecologia, 166, 59-67. ORDIZ, A., STOEN, O. G., SWENSON, J. E., KOJOLA, I. & BISCHOF, R. 2008. Distance-dependent effect of the nearest neighbor: spatiotemporal patterns in brown bear reproduction. Ecology, 89, 3327-35. ORDIZ, A., STØEN, O.-G., SÆBØ, S., KINDBERG, J., DELIBES, M. & SWENSON, J. E. 2012. Do bears know they are being hunted? Biological Conservation, 152, 21-28. ORDIZ, A., STØEN, O.-G., SÆBØ, S., SAHLÉN, V., PEDERSEN, B. E., KINDBERG, J. & SWENSON, J. E. 2013. Lasting behavioural responses of brown bears to experimental encounters with humans. Journal of Applied Ecology, 50, 306-314. PALMER, S. S., NELSON, R. A., RAMSAY, M. A., STIRLING, I. & BAHR, J. M. 1988. Annual changes in serum sex steroids in male and female black (Ursus americanus) and polar (Ursus maritimus) bears. Biology of Reproduction, 38, 1044-1050. PERRIGO, G. 1987. Breeding and feeding strategies in deer mice and house mice when females are challenged to work for their food. Animal Behaviour, 35, 1298-1316. PERSSON, I. L., WIKAN, S., SWENSON, J. E. & MYSTERUD, I. 2001. The diet of the brown bear Ursus arctos in the Pasvik Valley, northeastern Norway. Wildlife Biology, 7(1), 27-37. PRENDERGAST, B. J., FREEMAN, D. A., ZUCKER, I. & NELSON, R. J. 2002. Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. American Journal of Physiology. Regulatory, integrative and comparative physiology, 282, R1054-62. QUEST, M. 2001. Untersuchungen zur Fortpflanzungsphysiologie und Geburtenkontrolle bei in Menschenhand gehaltenen Bären (Ursidae). doctoral dissertation, Freie Universität Berlin Germany. RAMSAY, M. A. & DUNBRACK, R. L. 1986. Physiological constraints on life history phenomena: The example of small bear cubs at birth. The American Naturalist, 127, 735-743. REYNOLDS, H. V., CURATOLO, J. A. & ROLAND, Q. 1976. Denning ecology of grizzly bears in Northeastern Alaska. Bears: Their Biology and Management, 3, 403-409. ROBBINS, C. T., LOPEZ-ALFARO, C., RODE, K. D., TØIEN, Ø. & NELSON, O. L. 2012a. Hibernation and seasonal fasting in bears: the energetic costs and consequences for polar bears. Journal of Mammalogy, 93, 1493-1503. ROBBINS, C. T., MERAV, B.-D., FORTIN, J. K. & NELSON, O. L. 2012b. Maternal condition determines birth date and growth of newborn bear cubs. Journal of Mammalogy, 93, 540-546. ROGERS, L. Effects of mast and berry crop failures on survival, growth, and reproductive success of black bears. Transactions of the North American Wildlife and Natural Resource Conference, 1976. 431-438. ROGERS, L. L. 1987. Effects of food supply and kinship on social behavior, movements, and population growth of black bears in Northeastern Minnesota. Wildlife Monographs, 3-72. ROTH, H. U., BOSCAGLI, G. & GENTILE, L. 1996. Movements, activity and hibernation of brown bears in the Abruzzo National Park as revealed by radiotelemetry. F. Bourlière, compiler. Management and restoration of small and relictual bears populations. Museum d’Historie Naturelle, Grenoble, France. ROTH, H. U. & HUBER, D. 1986. Diel activity of brown bears in Plitvice Lakes National Park, Yugoslavia. Bears: Their Biology and Management, 6, 177-181.

RUBY, N. F. 2003. Hibernation: When good clocks go cold. Journal of Biological Rhythms, 18, 275-286. RYAN, C. W. 1997. Reproduction, survival, and denning ecology of black bears in Southwestern Virginia. Master of science. SAHLÉN, E., STØEN, O.-G. & SWENSON, J. E. 2011. Brown bear den site concealment in relation to human activity in Sweden. Ursus, 22, 152-158. SAHLÉN, V. 2013. Encounters between brown bears and humans in Scandinavia – contributing factors, bear behavior and management perspectives. doctoral dissertation, Norwegian University of life sciences. SAHLÉN, V., STØEN, O.-G., ORDIZ, A., ARNEMO, J. M., BRUNBERG, S., KRISTOFFERSSON, M. & SWENSON, J. E. in prep. Human injuries and fatalities caused by brown bears in Scandinavia 1977-2012. SANDELL, M. 1990. The evolution of seasonal delayed implantation. The Quarterly Review of Biology, 65, 23-42. SATO, M., TSUBOTA, T., KOMATSU, T., WATANABE, G., TAYA, K., MURASE, T., KITA, I. & KUDO, T. 2001. Changes in sex steroids, gonadotropins, prolactin, and inhibin in pregnant and nonpregnant Japanese black bears (Ursus thibetanus japonicus). Biol Reprod, 65, 1006-13. SATO, M., TSUBOTA, T., YAMAMOTO, K., KOMATSU, T., HASHIMOTO, Y., KATAYAMA, A., HAZUMI, T., KITA, I. & KUDO, T. 2000. Serum progesterone and estradiol-17beta concentrations in captive and free-ranging adult female Japanese black bears (Ursus thibetanus japonicus). Journal of Veterinary Medical Science, 62, 415-20. SCHOEN, J. W., BEIER, L. R., LENTFER, J. W. & JOHNSON, L. J. 1987. Denning ecology of brown bears on Admiralty and Chichagof Islands. Proceedings of the International Conference on Bear Research and Management, 7, 293-304. SCHOOLEY, R. L., MCLAUGHLIN, C. R., MATULA, G. J., JR. & KROHN, W. B. 1994. Denning chronology of female black bears: Effects of food, weather, and reproduction. Journal of Mammalogy, 75, 466-477. SCHWARTZ, C. C., KEATING, K. A., REYNOLDS, H. V., III, BARNES, V. G., JR., SELLERS, R. A., JON, E. S., MILLER, S. D., MCLELLAN, B. N., KEAY, J., MCCANN, R., GIBEAU, M., WAKKINEN, W. F., MACE, R. D., KASWORM, W., SMITH, R. & HERRERO, S. 2003. Reproductive maturation and senescence in the female brown bear. Ursus, 14, 109-119. SCHWARZENBERGER, F. 2007. The many uses of non-invasive faecal steroid monitoring in zoo and wildlife species. International Zoo Yearbook, 41, 52-74. SCHWARZENBERGER, F., MÖSTL, E., PALME, R. & BAMBERG, E. 1996. Faecal steroid analysis for noninvasive monitoring of reproductive status in farm, wild and zoo animals. Animal Reproduction Science, 42, 515-526. SERVHEEN, C. 1990. The status and management of the bears of the world. International Conference on Bear Research and Management, Monography Series, 2. SERVHEEN, C. & KLAVER, R. 1983. Grizzly bear dens and denning activity in the Mission and Rattlesnake Mountains, Montana. Proceedings of the International Conference on Bear Research and Management, 5, 201-207. SHAVLAKADZE, T. & GROUNDS, M. 2006. Of bears, frogs, meat, mice and men: complexity of factors affecting skeletal muscle mass and fat. BioEssays : news and reviews in molecular, cellular and developmental biology, 28, 994-1009. SHIMOZURU, M., IIBUCHI, R., YOSHIMOTO, T., NAGASHIMA, A., TANAKA, J. & TSUBOTA, T. 2013. Pregnancy during hibernation in Japanese black bears: effects on body temperature and blood biochemical profiles. Journal of Mammalogy, 94, 618-627. SOLBERG, K. H., BELLEMAIN, E., DRAGESET, O.-M., TABERLET, P. & SWENSON, J. E. 2006. An evaluation of field and non-invasive genetic methods to estimate brown bear (Ursus arctos) population size. Biological Conservation, 128, 158-168. SPADY, T. J., LINDBURG, D. G. & DURRANT, B. S. 2007. Evolution of reproductive seasonality in bears. Mammal Review, 37, 21-53.

STEARNS, S. C. 1992. The evolution of life histories. Oxford University Press. STENVINKEL, P., JANI, A. H. & JOHNSON, R. J. 2013. Hibernating bears (Ursidae): metabolic magicians of definite interest for the nephrologist. Kidney Int, 83, 207-212. STEYAERT, S. M. 2012. The mating season of the brown bear in relation to the sexually seleted infanticide theory. doctoral thesis, Norwegian University of Life Sciences. STEYAERT, S. M. J. G., ENDRESTØL, A., HACKLÄNDER, K., SWENSON, J. E. & ZEDROSSER, A. 2012. The mating system of the brown bear Ursus arctos. Mammal Review, 42, 12-34. STEYAERT, S. M. J. G., KINDBERG, J., SWENSON, J. E. & ZEDROSSER, A. 2013a. Male reproductive strategy explains spatiotemporal segregation in brown bears. Journal of Animal Ecology, 82, 836-845. STEYAERT, S. M. J. G., REUSCH, C., BRUNBERG, S., SWENSON, J. E., HACKLÄNDER, K. & ZEDROSSER, A. 2013b. Infanticide as a male reproductive strategy has a nutritive risk effect in brown bears. Biology letters, 9. STEYAERT, S. M. J. G., SWENSON, J. E., KINDBERG, J., BRUNBERG, S. & ZEDROSSER, A. 2013c. Making the best of a bad situation: sexual segregation of a non-social mammal in a risky landscape. Journal of Animal Ecology Accepted. STRINGHAM, S. F. 1990. Grizzly bear reproductive rate relative to body size. Bears: Their Biology and Management, 8, 433-443. SWENSON, J. E., ADAMIC, M., HUBER, D. & STOKKE, S. 2007. Brown bear body mass and growth in northern and southern Europe. Oecologia, 153, 37-47. SWENSON, J. E., FRANZÉN, R., WIKAN, S. & WABAKKEN, P. 1999. Interactions between brown bears and humans in Scandinavia. Biosphere Conservation, 2, 1-9. SWENSON, J. E., SANDEGREN, F., BRUNBERG, S. & WABAKKEN, P. 1997. Winter den abandonment by brown bears Ursus arctos: causes and consequences. Wildlife Biology, 3, 35-38. SÆTHER, B.-E., ENGEN, S., JON, E. S., BAKKE, Ø. & SANDEGREN, F. 1998. Assessing the Viability of Scandinavian Brown Bear, Ursus arctos, Populations: The Effects of Uncertain Parameter Estimates. Oikos, 83, 403-416. TAKAHASHI, J. S. & MENAKER, M. 1980. Interaction of estradiol and progesterone: effects on circadian locomotor rhythm of female golden hamsters. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 239, R497-R504. TANAKA, H. 2006. Winter Hibernation and Body Temperature Fluctuation in the Japanese Badger, Meles meles anakuma. Zoological Science, 23, 991-997. TSUBOTA, T. & KANAGAWA, H. 1993. Morphological characteristics of the ovary, uterus and embryo during the delayed implantation period in the Hokkaido brown bear (Ursus arctos yesoensis). Journal of Reproduction and Development, 39, 325-331. TSUBOTA, T., KANAGAWA, H., MANO, T. & AOI, T. 1990. Corpora albicantia and placental scars in the Hokkaido brown bear. Bears: Their Biology and Management, 8, 125-128. TSUBOTA, T., TAKAHASHI, Y. & KANAGAWA, H. 1987. Changes in serum progesterone levels and growth of fetuses in Hokkaido brown bears. Proceedings of the International Conference on Bear Research and Management, 7, 355-358. TØIEN, Ø., BLAKE, J., EDGAR, D. M., GRAHN, D. A., HELLER, H. C. & BARNES, B. M. 2011. Hibernation in black bears: Independence of metabolic suppression from body temperature. Science, 331, 906-909. VAN DAELE, L. J., BARNES, V. G., JR. & SMITH, R. B. 1990. Denning characteristics of brown bears on Kodiak Island, Alaska. Proceedings of the International Conference on Bear Research and Management, 8, 257-267. WELCH, C. A., KEAY, J., KENDALL, K. C. & ROBBINS, C. T. 1997. Constraints on Frugivory by Bears. Ecology, 78, 1105-1119. WIMSATT, W. A. 1963. Delayed implantation in the Ursidae, with particular reference to the black bear. In: Enders, A.C. Ed., Delayed Implantation, University of Chicago Press, Chicago IL, 49- 76.

WOLLNIK, F. & TUREK, F. W. 1988. Estrous correlated modulations of circadian and ultradian wheel- running activity rhythms in LEW/Ztm rats. Physiology & Behavior, 43, 389-396. ZEDROSSER, A., BELLEMAIN, E., TABERLET, P. & SWENSON, J. E. 2007. Genetic estimates of annual reproductive success in male brown bears: the effects of body size, age, internal relatedness and population density. The Journal of animal ecology, 76, 368-75. ZEDROSSER, A., DAHLE, B., JON, E. S. & GERSTL, N. 2001. Status and Management of the Brown Bear in Europe. Ursus, 12, 9-20. ZEDROSSER, A., DAHLE, B., STOEN, O. G. & SWENSON, J. E. 2009. The effects of primiparity on reproductive performance in the brown bear. Oecologia, 160, 847-54. ZEDROSSER, A., DAHLE, B. & SWENSON, J. E. 2006. Population density and food conditions determine adult female body size in brown bears. Journal of Mammalogy, 87, 510-518. ZEDROSSER, A., RAUER, G. & KRUCKENHAUSER, L. 2004. Early primiparity in brown bears. Acta Theriologica, 49, 427-432. ZEDROSSER, A., STEYAERT, S. M. J. G., GOSSOW, H. & SWENSON, J. E. 2011. Brown bear conservation and the ghost of persecution past. Biological Conservation, 144, 2163-2170.

10 Compilation of papers

Paper I

Sahlén, V., A. Friebe, S. Sæbø, J. E. Swenson, O.-G. Støen. 2014. Den entry behavior in Scandinavian brown bears; implications for preventing human injuries. The Journal of Wildlife Management; DOI: 10.1002/jwmg.822.

Paper II

Friebe, A., A. Zedrosser, and J. E. Swenson. 2013. Detection of pregnancy in a hibernator based on activity data. European Journal of Wildlife Research 59:731-741.

Paper III

11 Acknowledgements

The first time I visited the SBBRP was in 1998 as a volunteer, at the end of my biology studies. I soon understood how fascinating it was to study the behavior of brown bears, but I was especially motived to study brown bears’ winter behavior after I read more about the miracle of how brown bears survive the winter and reproduce during hibernation. I am very thankful to Prof. Jon Swenson and Sven Brunberg and also to Prof. Günther Fleissner, who accepted me as a MSc student and enabled me to study the denning chronology of bears. Already during my time at the field station in Kvarnberg, I learned much about bears, field work, life, and how to survive the Swedish winters. After the master thesis, my interest for bears did not allow me to move back to Germany. In 2000 I started the company Björn & Vildmark in Sweden, which still works with brown bear excursions, presentations, and guided tours in the wild. My partner Gunther moved to Sweden and during the following years we expanded our family (with two wonderful children) and the company’s success (with international customers), before I finally started my PhD in 2010 and continued with the research on brown bear hibernation.

I could not have been more satisfied with the supervision of my PhD. Many thanks to Dr. Andreas Zedrosser and Prof. Dr. Jon Swenson from the SBBRP, and Prof. Dr. Günther Fleissner and Prof. Dr. Manfred Kössl from the Goethe University for taking me as a PhD student. Being a PhD student in the SBBRP was one of my best educational experiences. It was amazing to work in this network of excellently cooperating, open-minded specialists, who brilliantly supervised my PhD, by simultaneously giving me the trust and opportunity to develop my own personality and research ideas. Jon and Andreas, thank you for all the creative discussions, your critical reviews that improved my manuscripts, for your positive feedback, your motivation, and for always being there when needed. Andreas, I also thank you for torturing me with statistics (Believe it or not, “Discovering Statistics Using SPSS” was fun to read! ). Sven, field work would have been impossible without you. Thank you for all the support and fieldwork you enabled me to experience. You are probably not only the world’s most experienced fieldwork supervisor for bear research, you are also a fantastic team leader with the skills to bring out the best of each person. Today, you are not only my first line manager, but also a best friend. I also thank Veronica Sahlén, Ingela Jansson, Alina Evans, Shane Frank, Marcus Elfström, Andrés Ordiz, Sam Steyaert, Jon Arnemo, Ole-

Gunnar-Støen, Jonas Kindberg, Stéphane Blanc, Ole Fröbert, and many others for all creative talks and unforgettable fieldwork memories in Tackåsen.

Günther, you always motivated me about starting the PhD. Thank you and also Dr. Gerta Fleissner for all constructive talks about chronobiology and activity. The working group NCR (Neurobiologie Circadianer Rhythmen) is like a big family, I will remember the manifold parties, with delicious Indian dinners at your house. Gerta, I will not forget the days and nights we spent in Okarben with writing applications for financial support for my studies. At this, I thank the Verein der Freunde und Förderer der Goethe Universität and the Wilkomm Stiftung for their financial support. I also thank Mrs Margot Toledano from the Dekanat FB15 for all her help.

Last but not least, I will first say thank you (partly in German) to my entire beloved family. Gunther without your love, patience and support I had never been able to complete my PhD. Thank you for all the good conversations during days and nights, taking care of the children and the company when I was absent and thank you for always being there for me. Elvis und Kaj, ich danke Euch für all Eure Geduld, Unterstützung und Liebe (und für alle am Bett servierten Kaffees am Morgen  ). Ihr seid mein schönstes, liebstes und grösstes Abenteuer. Meine lieben Eltern Uschi und Albrecht, vielen Dank für Eure wohl niemals endende Unterstützung. Uschi, wie wäre ich nur ohne Deine monatelangen Besuche und Hilfe in Schweden ausgekommen? Danke auch an meine süsse Schwester Moni, an Alex, Nike und Charly, an meine Eltern und Schwiegereltern Hanne und Günter, dass unsere Kindern so tolle Urlaube mit Euch verbringen durften. Ihr seid alle wunderbar!

CURRICULUM VITAE Andrea Friebe Backvägen 21 79433 Orsa, Schweden Email: [email protected] & [email protected]

Persönliche Daten geboren am 16.02.1971 in Frankfurt Staatsangehörigkeit deutsch

Schulausbildung / Berufliche Weiterbildung 1977 – 1990 mit Abiturabschluss im Wöhler-Gymnasium, Frankfurt 1991-1993 Kaufmännische Ausbildung zur Verischerungskauffrau bei der Allianz-Versicherungs AG in Frankfurt 1993 – 2000 Hochschulstudium Biologie (Diplom) an der Goethe-Universität in Frankfurt, Fachrichtung Zoologie 1999-2000 Diplomarbeit: “Das Winterverhalten und die täglichen Wanderungen von weiblichen Braunbären in Zentralschweden.” (Betreuung Prof.Dr.Günther Fleissner) Diplomhauptprüfung in den Prüfungsfächern Zoologie, Mikrobiologie und Biochemie 1998-2011 Mitarbeit im Skandinavischen Braunbärforschungsprojekt

Berufstätigkeit 2000- 2014 Gründung und Leitung der Firma Björn & Vildmark in Orsa Schweden. 2008- 2014 Öffentlichkeitsarbeit für das schwedische Naturschutzamt. Erstellung von Ausstellungen, Vorlesungen und Exkursionen zum Thema Bärenbiologie und Bärenforschung. 2010-2014 Halbtagsanstellung im Skandinavischen Braunbärforschungsprojekt

Dissertation 2000 - 2001 Beginn der Promotionsarbeit mit dem Thema "Winterverhalten der Braunbären in Schweden" an der Johann-Wolfgang-Goethe-Universität, Arbeitsgruppe Neurobiologie Circadianer Rhythmen, Betreuer: Prof. Günther Fleissner 2001 Veröffentlichung des Papers: “Denning chronology of female brown bears (Ursus arctos) in central Sweden” in Ursus 12: 37-46 als Erstautor. 2000 Poster präsentation (Lillehammer) 2001-2010 Unterbrechung der Promotionsarbeit aus beruflichen und familiären Gründen. 2010 - 2014 Wiederaufnahme der Promotionsarbeit mit dem Thema: ”Winter ecology of brown bears in Sweden”. 2013 Veröffentlichung der Publikation: “Detection of pregnancy in a hibernator based on activity data” in European Journal of Wildlife Research 59:731-741als Erstautor. 2013 Posterpräsentation der IBA Conference 2013 in Utah (International Bear Association) 2014 Veröffentlichung der Publikation: “Factors affecting date of implantation, parturition, and den entry estimated from activity and body temperature in free-ranging brown bears in PLoS ONE 9(7): e101410. doi: 10.1371/journal.pone.0101410, als Erstautor. 2014 Fachgutachter für: „Journal of Mammalogy“ und für „Mammalian Review“ 2014 2. Review der Publikation: “Den Entry Behavior in Scandinavian Brown Bears; Implications for Preventing Human Injuries (minor revisions) in Journal of Wildlife Management and Wildlife Monographs als Coautor 2014 Abgabe der Dissertationsarbeit