Increasing phenological asynchrony between spring green-up and arrival of migratory birds
Understanding whether and how species are able to adjust and adapt to climate change has become one of the most urgent challenges facing ecology. Climate change is projected to drive hundreds of bird species to extinction and greatly reduce the ranges of others1, 2, and is already impacting species richness and composition3. Despite these impacts, in recent decades a majority of species examined have shifted the timing (phenology) of key ecological events, such as migration or reproduction4, consistent with expectations under climate change5. For instance, birds appear to be laying eggs earlier6, especially among populations experiencing greater increases in temperature7. Earlier arrival of migrants on breeding grounds has also been reported8, 9, mirroring advances in spring vegetation phenology10.
More important than whether birds are shifting their phenologies is whether these shifts adequately compensate for a changing climate and resulting shifts in avian food resources that drive fitness. Individuals and species might be able to adjust rapidly: phenotypically plastic behavioural responses can track environmental conditions closely11, and even evolutionary changes in migratory behaviour which are generally expected to be much slower can occur rapidly12. Migratory birds, given their ability to rapidly move long distances, might appear to be among the most adaptable animals to climate change. Migration itself is partly an adaptation to intra-annual changes in climate, so additional inter-annual climatic changes might seem not to pose a problem for further adaptation. However, onset of long-distance migration in birds is primarily cued by physiological responses to photoperiod—which is annually consistent—yet conditions at their breeding grounds depend on climate—which is annually variable13, 14. To maximize fitness, birds must time their breeding phenology (including arrival on breeding grounds, breeding, egg laying, and fledging) to coincide with optimal habitat conditions and food availability. This means there is evolutionary incentive to correctly anticipate breeding site conditions while birds are still at their winter grounds, often thousands of kilometers distant. As climate at the breeding grounds changes, birds may be unable to adjust wintering ground departure times and transit speeds sufficiently to match their arrival with altered breeding resource phenology, particularly leaf growth and the closely associated emergence of herbivorous insects.
Arriving too early at breeding grounds can bring risk of freezing (due to cold temperatures) and hatching chicks before peak resource abundance, whereas arriving too late can mean fewer nest sites, fewer mates with successfully guarded territories, and declining resource abundance15, 16. As such, the loss of synchrony between insect emergence and migrant bird arrival phenology17, 18 can be accompanied by negative fitness consequences including reduced reproductive output and juvenile survival19, 20. The decoupling of the phenology across trophic levels can ultimately lead to population declines and biodiversity loss20, 21. Beyond impacts on birds, phenological asynchrony between birds and their insect prey can generate novel trophic cascades: for instance, a lack of predation on insects can cause insect outbreaks and subsequently increase defoliation of trees22.