Phenological shifts drive biodiversity loss in plant--pollinator networks

Plant-pollinator interactions are key for ecosystem maintenance and world crop production, and their occurrence depends on the synchronization of life-cycle events among interacting species. Phenological shifts observed for plant and pollinator species increase the risk of phenological mismatches, threatening community stability. However, the magnitudes and directions of phenological shifts present a high variability, both among communities and among species of the same community. Community-wide consequences of these different responses have not been explored. Additionally, variability in phenological and topological traits of species can affect their persistence probability under phenological changes. We explored the consequences of several scenarios of plant-pollinator phenological mismatches for community stability. We also assessed whether species attributes can predict species persistence under phenological mismatch. To this end, we used a dynamic model for plant-pollinator networks. The model incorporates active and latent life-cycle states of species and phenological dynamics regulating life-cycle transitions. Interaction structure and species phenologies were extracted from eight empirical plant-pollinator networks sampled at three locations during different periods. We found that for all networks and all scenarios, species persistence decreased with increasing magnitude of the phenological shift, for both advancements and delays in flowering phenologies. Changes in persistence depended on the scenario and the network being tested. However, all networks exhibited the lowest species persistence when the mean of the expected shift was equivalent to its standard deviation and this shift was greater than two weeks. Conversely, the highest species persistences occurred when earlier-flowering plants exhibited stronger shifts. Phenophase duration was the most important attribute as a driver of plant persistence. For pollinator persistence, species degree was the most important attribute, followed by phenophase duration. Our findings highlight the importance of phenologies on the stability and robustness of mutualistic networks. Author summaryPlant-pollinator interactions involve a great number of species and are essential for the functioning of natural and agricultural systems. These interactions are facing a great number of threats. In both plants and pollinators, life-cycle events including flowering and adult emergence are triggered by environmental cues such as temperature and snowmelt. Climate change has the potential to alter the timing of these events. These phenological shifts generate mismatches in the timing of interacting species. Thus, plants and their pollinators may not match in time and/or space, leaving flowers unpollinated and disrupting pollinator feeding. Given that natural communities are composed of multiple species interacting in complex ways, experimentally assessing the effects of this kind of perturbation is difficult. To tackle this challenge, we simulated different scenarios of phenological shifts for several empirical communities. Our results indicate that strong shifts in the timing of life-cycle events may represent a greater risk of community collapse. Likewise, plants with short blooming periods and pollinators with short activity periods or high specialization face a greater risk of extinction.