Mating, Reproduction, 
and Fitness

Mating system

Brown bears have a polygamous mating system, meaning males may mate with several females and females may mate with several males (1-3). However, females are the sole care givers once cubs are born, and males show no paternal investment and do not help to raise their young. Brown bears are a long-lived species that reproduce relatively slowly, i.e., they have a slow life history. They take several years to reach sexual maturity (4, 5), and their cubs require between 1 and 2 years of maternal care during which time the female does not reproduce (6). Their reproductive cycle is flexible; some females remain with their cubs for 1 ½ years while others remain with them for 2 ½ years (6, 7). Females have the ability to reproduce again if they lose their newborn cubs before or during mating season (1, 8). Because females can come into reproductive readiness (estrous) when they lose their cubs during the mating season, infanticide (the killing of cubs by adult males) can be influential in their mating system and reproductive behavior (1, 3, 9).

Sexually selected infanticide: Research in Scandinavia suggest that brown bears exhibit sexually selected infanticide, in which adult males kill unrelated cubs in order to increase their chances of fathering more cubs during their lifetime (1). Although it is possible males kill young for reasons other than facilitating reproduction, e.g., to decrease competition, our research has shown that the main requirements for cub killing as mating strategy are met: First, killing all cubs results in the mother coming into estrous sooner than she would have otherwise, 2) the males killing the cubs are not the cubs father, 3) the infanticidal male is likely to be the father of the next litter, and 4) infanticide only occurs during mating season (1, 8). Sexually selected infanticide is relatively common in the bear population in Scandinavia, with males killing young cubs to induce the female into estrous sooner, and both resident and immigrant males commit infanticide with cubs they have not fathered (1, 8).

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Because of this, females have several counter strategies to protect their cubs of the year from male infanticide. First, mating with multiple partners, especially with partners who have more overlapping home ranges, may help hide the fathers identity (1). Although it remains uncertain, delayed implantation (described below) may also further help hide paternity (10). Finally, they move through and use the habitat in their home range during the mating season in a way that avoids males (11). For example, females with cubs of the year restrict their movement, and use areas that are closer to humans, and in less rugged and more open areas, which is opposite of what males select for during this time (11). This creates a type of ‘human-shield’ effect whereby females with cubs of the year trade off risks associated with close proximity to humans, presumably to decrease the chances of losing their cubs (12). Indeed, females appear to change movement strategies after the loss of their cubs; females who lose all of the cubs prior to or during mating season start the roaming behavior typical of mating females within 1 or 2 days of cub loss (8). However, protecting their young comes at a cost for female bears (13). Females who have cubs of the year have a lower quality diet during the mating season than other females, but not during other times of year (13), further reinforcing that females trade-off foraging for the safety of their cubs (13). Bear hunting has huge implications for patterns of infanticide in Scandinavia’s bear population, for more on this subject please see The effects of hunting on the population, behavior, and evolution.

Mate choice: The mating season begins in late May and lasts through early July (14). During this time, both males and females will roam more (i.e., increase their travel distance and area used) to find mates (14). Males tend to mate with multiple partners to increase their chances of fathering more cubs, while females have multiple partners to decrease the chances of male-induced infanticide (15). For example, females tend to mate with males that are larger and whose home ranges overlap more with theirs (15). Interestingly, between 14% to 28% of litters with ≤3 cubs had cubs with different fathers (1), which likely further reduces the chances of cub loss to infanticidal males (1). Only about 2% of the cubs are the result of incestuous mating in Scandinavia.

Sexual maturity and age of last reproduction: The average age that females reproduce for the first time (i.e., age at primiparity) was estimated at 4.7 years old in the Southern Study Area and 5.3 years old in the Northern Study Area, with a range between age 4 and 7 (4, 5). Interestingly, females that disperse farther away from their mothers home range reach sexual maturity almost a year earlier than females that remain nearby; at 4.3 compared to 5.2 years old (16). This reproductive suppression is likely due to increased competition between females, i.e., older dominant females have better access to resources than younger subordinate females, but young females who move to newer areas with a lower bear density may have better access to food (16). The probability of having cubs declines sharply after the age of 28 or 29 (2).

Reproduction

Estrous: Female bears are sexually receptive, or in estrous, between mid-May and early July each year. However, only solitary females or females who will wean their cubs that year are sexually receptive, although as previously mentioned, females with cubs of the year may enter estrous if they lose their cubs before or during the mating season (3). The majority (91%) of females that lose all of their cubs before or during mating season re-enter estrous and produce cubs the following year (8).

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Implantation: Bears are the only mammals for which delayed implantation, active gestation, parturition, and lactation have been reported during hibernation, a period when they do not eat, drink, urinate or defecate for several months. After mating, the female experiences an obligatory ‘embryonic diapause’, which is when the embryos halt development very early on (at the blastocyst stage) and remain free-floating in the uterus rather than attaching to the uterine wall (17, 18). The termination of embryonic diapause is marked by the reactivation of the corpus luteum (a mass of cells that forms in the ovaries during estrous which is responsible for progesterone production early in pregnancy), leading to a surge in progesterone (19, 20). Following this, embryo implantation typically occurs in November-December, after the female has entered her den (10, 21). In carnivores exhibiting delayed implantation, a period known as the ‘secretory phase’, lasting several days, intervenes between corpus luteum reactivation and blastocyst implantation, during which the uterus prepares to receive the fertilized eggs. The duration of the secretory phase in bears remains unknown, hindering precise determination of active gestation length. In our Southern Study Area, the mean date of implantation was 1 December, and the mean date of birth for mature females was 12 January (21).

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Excluding the secretory phase, the active gestation in brown bears is estimated to last between 56 and 60 days based on body temperature and progesterone levels (10, 19, 21). The active gestation phase is characterized by heightened metabolism due to sustained high progesterone levels and the presence of fetuses (22). During gestation, body temperature is elevated and stable, ranging between 37–38°C compared to the typical 34–36°C, and drops to near hibernation levels around parturition (10, 21). Gestation onset is presumed to occur in November-December when progesterone levels and body temperature (10) begin to rise. Implantation is improbable before body temperature stabilizes at near-active levels, as various studies indicate the necessity of a high and stable body temperature for embryo development during the active gestation phase in both hibernating and non-hibernating mammals (23-25). Thus, a recalculated gestation length in the Scandinavian brown bear is 49-53 days (21).

Birthing in the den: Parturition typically occurs around January-February in the den with the cubs weighing between 350 to 500 g, depending on the size of the mother and the number of cubs (10). Bears demonstrate a sharp drop in body temperature and activity levels coinciding with parturition (10, 21). These activity and thermal patterns provide distinctive markers facilitating parturition determination in free-ranging populations. The females lactate and provide food for their young in the den for 3-4 months before emerging in spring (3). Unlike the mother, the newborn cubs are awake, physically active, have normal physiological functions, and have sleep cycles similar to other mammalian young (10).

Litter size: In Scandinavia, females reproduce every 2-3 years, (depending on how long females keep their cubs) (6, 26), giving birth to an average of 2.4 - 2.7 cubs (range = 1 to 4) (3, 27, 28). Litter size (i.e., the number of cubs) is related to the age of the mother; older mothers tend to have larger litters (28). On average, females that give birth for the first time tend to have slightly smaller litters; 1.9 cubs compared to 2.4 cubs for females that had already reproduced once (4). In general, prime aged-females, or females between the ages of 9 and 20 years old, produce the most offspring (2). There are two documented occurrences of mixed-age litters in Scandinavia, which appear to have occurred when the mother thought her cubs died, subsequently mated, and then were subsequently reunited with their cubs (29).

Reproductive success: Reproductive success in female brown bears is tied to body weight and condition, which is linked to food availability, especially the availability of important fall food such as berries (21, 30). Bear body weight increases when blueberries are more abundant, and female body weight plays an important role in cub production (30). For example, lighter females have lower reproductive success compared to heavier females in poor blueberry years, but reproductive success is stable for all bears when blueberry abundance is high (30). Interestingly, this seems to be more important for younger females (< 8 years old), which unlike older adult females, delayed giving birth, spent less time in the den with their cubs, and subsequently had lower reproductive success in years with low blueberry abundance (21). In other words, “some bears are more vulnerable to food shortages than others” (30). This is important in the context of climate change, as decreased fall berry production could negatively affect their hibernation patterns and subsequently, their reproductive success in general (21).

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There is a trade-off between litter size and cub body mass that likely affects overall cub survival (28, 31). Evidence suggests that mothers invest more in their heavier cubs, while smaller cubs suffer the consequences of having more siblings (31). Cub survival increases when adult male mortality is higher in the previous years, probably because of decreased chances of sexually selected infanticide (32). First-time mothers have a greater chance of losing their cubs compared with females who have been a mother before, although this is slightly tempered if the first time mother is older when she reproduces for the first time (4). First time mothers are most likely to lose their cubs either directly after den emergence, especially when food is less available, or during mating season due to infanticidal males (4). We have also observed female-female reproductive suppression in females living near one another (33, 34). Females who settle closer to their mother’s home range appear to have lower reproductive success, possibly due to delayed primiparity or reproductive suppression by their mothers (34). Interestingly, a female’s probability of having cubs is influenced by whether or not the female closest to them had cubs; when the neighboring female also had cubs, the females chances of having cubs that year decreased (33). Finally, cub survival was greater when yearlings (1 ½) stayed with their mother an extra year, i.e., they were weaned at 2 ½ (35). This is likely in part because hunters are prohibited from harvesting family groups (35). For more on cub survival within the population see Population ecology and current status.

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In Scandinavia, male reproductive success has been shown to increase with population density, likely because there is greater access to more females as female densities are lower near the population expansion front (5). In general, older and larger males generally seem to sire more cubs, or have greater reproductive success, then younger smaller males, possibly because they are better competitors (5). Inbred males appear to have lower reproductive success than males with a more diverse genetic makeup (5). Interestingly, individual male reproductive success was higher in the Northern Study Area than in the Southern Study Area (5). In the North, age was more important while body size was more important in the South. This is likely because one older male dominated reproduction in the North at the time, while in the South where there are more bears, body size related to competition likely was key for access to females (5).

Cub rearing

In Scandinavia, female bears care for their cubs for between 1 ½ to 2 ½ years, after which the cubs are ‘weaned’ and gain independence from their mother who may then reproduce again (3, 6). Mothers usually separate from their cubs early in the mating season when her estrous begins, and family breakup is often associated with the presence of an adult male (36). Our research has previously shown that 95% of cubs are weaned as yearlings (i.e., at 1 ½ years) in our Southern Study Area (36). In the Northern Study Area, however, only 47% are weaned as yearlings while the remaining 53% move away from their mother as two year olds (i.e., 2 ½ years) (6). Why some females keep their cubs an extra year is an important question because the length of maternal care directly affects the timing of reproduction and subsequently population growth rate and size. In the Northern Study Area, where the environment is harsher and more limiting, it appears that yearling body mass, and factors that affect yearling body mass such as litter size and the mothers body mass, directly affected how long the cubs stayed with the mother. In this area, smaller cubs stayed with their mother an extra year (7). However, how long cubs stayed with their mother in the Southern Study Area is not affected by yearling growth, but may be more correlated with other activities such as hunting pressure (7). Indeed, hunting pressure may be driving longer maternal care, as family groups are protected from hunting, and keeping cubs an extra year provides a buffer from hunting pressure (26). For more information on the effects of hunting see The effects of hunting on the population, behavior, and evolution.

References