Plant-pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations?

Anthropogenic climate change is widely expected to drive species extinct by hampering individual survival and reproduction, by reducing the amount and accessibility of suitable habitat, or by eliminating other organisms that are essential to the species in question. Less well appreciated is the likelihood that climate change will directly disrupt or eliminate mutually beneficial (mutualistic) ecological interactions between species even before extinctions occur. We explored the potential disruption of a ubiquitous mutualistic interaction of terrestrial habitats, that between plants and their animal pollinators, via climate change. We used a highly resolved empirical network of interactions between 1420 pollinator and 429 plant species to simulate consequences of the phenological shifts that can be expected with a doubling of atmospheric CO(2). Depending on model assumptions, phenological shifts reduced the floral resources available to 17-50% of all pollinator species, causing as much as half of the ancestral activity period of the animals to fall at times when no food plants were available. Reduced overlap between plants and pollinators also decreased diet breadth of the pollinators. The predicted result of these disruptions is the extinction of pollinators, plants and their crucial interactions.

The timing of life history traits is central to lifetime fitness and nowhere is this more evident or well studied as in the phenology of flowering in governing plant reproductive success. Recent changes in the timing of environmental events attributable to climate change, such as the date of snowmelt at high altitudes, which initiates the growing season, have had important repercussions for some common perennial herbaceous wildflower species. The phenology of flowering at the Rocky Mountain Biological Laboratory (Colorado, USA) is strongly influenced by date of snowmelt, which makes this site ideal for examining phenological responses to climate change. Flower buds of Delphinium barbeyi, Erigeron speciosus, and Helianthella quinquenervis are sensitive to frost, and the earlier beginning of the growing season in recent years has exposed them to more frequent mid-June frost kills. From 1992 to 1998, on average 36.1% of Helianthella buds were frosted, but for 1999-2006 the mean is 73.9%; in only one year since 1998 have plants escaped all frost damage. For all three of these perennial species, there is a significant relationship between the date of snowmelt and the abundance of flowering that summer. Greater snowpack results in later snowmelt, later beginning of the growing season, and less frost mortality of buds. Microhabitat differences in snow accumulation, snowmelt patterns, and cold air drainage during frost events can be significant; an elevation difference of only 12 m between two plots resulted in a temperature difference of almost 2 degrees C in 2006 and a difference of 37% in frost damage to buds. The loss of flowers and therefore seeds can reduce recruitment in these plant populations, and affect pollinators, herbivores, and seed predators that previously relied on them. Other plant species in this environment are similarly susceptible to frost damage so the negative effects for recruitment and for consumers dependent on flowers and seeds could be widespread. These findings point out the paradox of increased frost damage in the face of global warming, provide important insights into the adaptive significance of phenology, and have general implications for flowering plants throughout the region and anywhere climate change is having similar impacts.

Climate warming affects the phenology, local abundance and large-scale distribution of plants and pollinators. Despite this, there is still limited knowledge of how elevated temperatures affect plant-pollinator mutualisms and how changed availability of mutualistic partners influences the persistence of interacting species. Here we review the evidence of climate warming effects on plants and pollinators and discuss how their interactions may be affected by increased temperatures. The onset of flowering in plants and first appearance dates of pollinators in several cases appear to advance linearly in response to recent temperature increases. Phenological responses to climate warming may therefore occur at parallel magnitudes in plants and pollinators, although considerable variation in responses across species should be expected. Despite the overall similarities in responses, a few studies have shown that climate warming may generate temporal mismatches among the mutualistic partners. Mismatches in pollination interactions are still rarely explored and their demographic consequences are largely unknown. Studies on multi-species plant-pollinator assemblages indicate that the overall structure of pollination networks probably are robust against perturbations caused by climate warming. We suggest potential ways of studying warming-caused mismatches and their consequences for plant-pollinator interactions, and highlight the strengths and limitations of such approaches.