Climate-associated phenological advances in bee pollinators and bee-pollinated plants

Abstract

The phenology of many ecological processes is modulated by temperature, making them potentially sensitive to climate change. Mutualistic interactions may be especially vulnerable because of the potential for phenological mismatching if the species involved do not respond similarly to changes in temperature. Here we present an analysis of climate-associated shifts in the phenology of wild bees, the most important pollinators worldwide, and compare these shifts to published studies of bee-pollinated plants over the same time period. We report that over the past 130 y, the phenology of 10 bee species from northeastern North America has advanced by a mean of 10.4 ± 1.3 d. Most of this advance has taken place since 1970, paralleling global temperature increases. When the best available data are used to estimate analogous rates of advance for plants, these rates are not distinguishable from those of bees, suggesting that bee emergence is keeping pace with shifts in host-plant flowering, at least among the generalist species that we investigated. C limate warming over the past 50 y is associated with phenological advances in a wide variety of organisms including plants, birds, and insects (1-3). Responses to climate warming are particularly important to understand for species that provide critical ecological functions such as pollinators. Furthermore, many ecological functions result from interactions among species, and because not all species respond to climate warming in the same manner, this could potentially lead to phenological mismatches that result in the loss of function (4-6). Alternatively, the interacting species may be buffered against climate variation if they have evolved similar responses to environmental variation (7). Here we present an analysis of climate-associated shifts in the phenology of wild bee pollinators, and compare the rates of advance for bees to those of bee-pollinated plants from the same region.Bees (Hymenoptera: Apoidea: Anthophila) are the primary animal pollinators in most ecosystems (8). However, there is only one study of climate-associated phenological shifts in bees, and this focused on a single managed species, the honey bee (9). The honey bee (Apis mellifera L.) represents a special case relative to the ∼19,700 described species of bees existing worldwide (10), first, because it is a domesticated species, and second, because it is one of the minority of perennial bee species, meaning that adults remain active over the winter and regulate hive temperatures in temperate latitudes. In contrast, most wild bee species outside the tropics have annual cycles that include an obligatory larval or adult diapause before spring emergence. The development of bees and the environmental triggers regulating seasonal activity are largely unknown, and the few species studied show complex responses to both winter and spring temperatures (11,12). Thus, although we would predict phenological shifts in bee activity due to climate change, the directionality and magnitude of these shifts are difficult...

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“…Kudo & Ida, 2013;Petanidou et al, 2014), even if several empirical studies suggest that the large plant and insect biodiversity could mitigate the expected dramatic consequences (e.g. Bartomeus et al, 2011Bartomeus et al, , 2013bForrest & Thomson, 2011;Iler et al, 2013). Such changes in pollinator communities may not only affect wild plants but can also impact important agricultural crops (e.g.…”

“…Kuhlmann et al, 2012). On the other hand, the gradual changes can lead to modification of species' phenology (Polgar et al, 2013;Kharouba et al, 2014; for wild bees see Bartomeus et al, 2011). Indeed, in both cases, species can respond to gradual climate change by tracking spatially or temporally their climatic niche (e.g.…”

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