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Synchronous timing of food resources triggers bears to switch from salmon to berries

We are in an era of phenological (seasonal timing) change (1). One of the most consistent fingerprints of climate change is the spring advancement of life history events of diverse taxa in the northern hemisphere, from flowers to butterflies to birds. As phenologies change, so too do potential interactions among species. The speed of phenological change can differ among interacting species (2, 3), potentially disrupting crucial interactions such as pollination, foraging, or predator–prey encounters. While there is growing appreciation that climate change may cause such trophic mismatches, the effect of climate-induced synchronization on food webs has been practically unexplored. Enter Deacy et al. (4).
Deacy et al. (4) study an iconic interaction: bears feeding on salmon. However, as any biologist who has walked along a salmon stream knows, bears do not feed exclusively on salmon during the salmon run; bear scat encountered along salmon streams often contains seeds from berries (Fig. 1). As mobile consumers, bears integrate across heterogeneous resource pulses that are available at different times (5, 6). For example, in the Karluk watershed of Kodiak Island, Alaska, where Deacy et al. (4) conducted their research, brown bears feed on stream-spawning sockeye salmon early in the summer and then switch to feeding on red elderberry late in the summer. The complementary timing of stream-spawning salmon and elderberry effectively prolongs the duration of high-quality foraging opportunities during the short Alaskan growing season.
Bear scat encountered along a salmon stream reveals a balanced diet. Image courtesy of Andrew Hendry (photographer).
However, with climate change and warmer springs, elderberry phenology is changing. Elderberries ripen earlier with warmer conditions, overlapping more with stream-spawning salmon. These stream-spawning salmon—in contrast to salmon spawning in larger rivers or lakes—are the most vulnerable to bear predation (7). Deacy et al. show that bears abandon stream-spawning salmon and shift to feeding on elderberry when both resources are available concurrently (4). Indeed, aerial surveys showed reduced bear counts on spawning streams in years with higher temporal overlap of salmon and elderberry. Once elderberry became available, camera traps documented reduced bear activity in the vicinity of salmon streams; scat surveys along stream margins revealed a higher proportion of scats with berry remnants; and GPS-collared females shifted their distributions from salmon streams to adjacent hillslopes where elderberry were common. These different lines of evidence paint a coherent picture of climate-induced diet switching due to synchronized resource availability. Why bears switched from salmon to berries is an open question, but the authors postulate that elderberries might have more suitable macronutrient content, hinting that food quality and costs associated with assimilation could be playing a role.
The synchronizing effect of climate is perhaps counterintuitive given that the growing season in northern temperate ecosystems is getting longer. On the one hand, we might expect increased duration of high-quality foraging opportunities for bears with longer growing seasons. On the other hand, Deacy et al. (4) show the schedule of availability of two key foods synchronized during warm years, which reduced the ability of bears to capitalize on the two resource pulses. Which is more important to bear fitness and demography—the overall duration of the feeding period or the schedule of availability of key diet items—is an open question. However, given that bears reach larger sizes, have larger litters, and generally higher population densities when they have access to salmon versus when they do not (8) hints that the pattern documented by Deacy et al. (4) might have consequences for bear fitness and population ecology. On a more positive note, bears do have access to other food options in these systems, albeit of lower quality, including sparser berries with lower protein (blueberries) and spawned-out carcasses of late-spawning beach and river populations of salmon. Perhaps the phenological variation among salmon populations or species can buffer bears from shifting elderberry phenologies?
Beyond the general implications for how climate change can alter food webs, the results of Deacy et al. (4) have two important implications for bear–salmon systems. First, while many organisms feed on live salmon or scavenge salmon carcasses, bears are special because they kill large numbers of salmon and are capable of transporting many salmon from streams to adjacent terrestrial areas, thereby vectoring marine-derived nutrients into terrestrial food webs and ecosystems. The prey switching documented by Deacy et al. (4) thus has potential to alter the magnitude and timing of energy flows through terrestrial ecosystems. How bear behavior and social dominance is altered by synchronization of key foods is unclear but an important topic for future research given that subdominant bears are especially important for moving salmon carcasses into the adjacent riparian zone; subdominant bears often haul salmon carcasses into the forest to avoid dominant bears in the stream channel (9). Moreover, male bears tend to have a more salmon-rich diet than females (10), possibly because females with spring cubs actively avoid salmon streams to reduce the risk of infanticide (11). If females switch from stream salmon to elderberry earlier than males, this might partially explain the results of previous studies (10, 11) and have consequences for cub growth and survival, particularly if cubs are more protein-limited than adult bears. These nuances surrounding bear social hierarchies suggest the need to more fully explore intrapopulation variation in the timing of the diet switch under different scenarios of resource overlap as well as the corresponding demographic consequences.
Second, bears not only kill large numbers of salmon, they can also kill a large proportion of salmon in stream-spawning populations, suggesting potential evolutionary implications of bear diet switching. Bears are agents of natural selection acting on salmon, influencing patterns of senescence and body size among salmon populations (7, 12, 13). Heavy predation on the early part of the salmon run generates natural selection on salmon run timing (Fig. 2). Specifically, strong selection on the early part of the run and relaxed selection on the late part of the run will favor late-arriving fish. Because arrival timing is a heritable trait in salmonid fishes (14), consistent selection across years favoring late-arriving fish could drive evolution toward later arrival. Indeed, strong fishery selection that favors fish arriving early (by capturing the late arrivers) has resulted in progressively earlier arrival of salmon (15). Evolution of delayed arrival in Karluk River salmon would act to further synchronize the timing that stream-spawning salmon and elderberry are available to the bears, creating potential for a feedback between evolution of salmon arrival timing and bear foraging ecology that further disrupts this iconic predator–prey interaction. However, the potential for evolutionary change is dampened by interannual variation in air temperature and berry phenology, which perhaps explains why no change in salmon arrival patterns have been observed to date.
Bears are potential agents of natural selection acting on salmon populations. (A) Under the “normal” scenario, bear predation is distributed throughout the salmon run because elderberry ripen later in the season. (B) Under this scenario, there is little potential for selection by bears on salmon arrival timing. (C) Under the “warming” scenario, when elderberry fruits early and overlaps more with salmon, bears feed on early-arriving salmon and then switch to elderberry. (D) This diet switch generates natural selection on salmon arrival timing that favors late-arriving fish, setting up the potential for evolution of progressively later arrival of salmon to the spawning grounds.
Beyond the ecological and evolutionary implications for coastal ecosystems around the Pacific rim, the results of Deacy et al. (4) call attention to the potential for climate change to synchronize resource pulses, thereby disrupting the ability of generalist consumers to capitalize on different resource pulses. Moreover, they emphasize that changes in relative phenology of prey—and not just their relative abundance—can drive diet switches of generalist consumers. Both results push the conversation of how climate change will impact food webs beyond pairs of interacting species, a refreshing step. A broader message is that that species will do better when they have multiple food options throughout the year. In the near-pristine watersheds studied by Deacy et al. (4), bears have other food options and the landscape connectivity needed to ride different resource waves. However, adding hatcheries, mines, or other perturbations could alter the temporal availability and abundance of different resources as well as the ability of mobile consumers to exploit them.
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