Recent changes in the seasonal timing (phenology) of familiar biological events have been one of the most conspicuous signs of climate change. However, the lack of a standardized approach to analysing change has hampered assessment of consistency in such changes among different taxa and trophic levels and across freshwater, terrestrial and marine environments. We present a standardized assessment of 25 532 rates of phenological change for 726 UK terrestrial, freshwater and marine taxa. The majority of spring and summer events have advanced, and more rapidly than previously documented. Such consistency is indicative of shared large scale drivers. Furthermore, average rates of change have accelerated in a way that is consistent with observed warming trends. Less coherent patterns in some groups of organisms point to the agency of more local scale processes and multiple drivers. For the first time we show a broad scale signal of differential phenological change among trophic levels; across environments advances in timing were slowest for secondary consumers, thus heightening the potential risk of temporal mismatch in key trophic interactions. If current patterns and rates of phenological change are indicative of future trends, future climate warming may exacerbate trophic mismatching, further disrupting the functioning, persistence and resilience of many ecosystems and having a major impact on ecosystem services.

This paper reviews information from ecological and physiological studies to assess how extrinsic factors can modulate intrinsic physiological processes. The annual cycle of birds is made up of a sequence of life-history stages: breeding, moult and migration. Each stage has evolved to occur at the optimum time and to last for the whole duration of time available. Some species have predictable breeding seasons, others are more flexible and some breed opportunistically in response to unpredictable food availability. Photoperiod is the principal environmental cue used to time each stage, allowing birds to adapt their physiology in advance of predictable environmental changes. Physiological (neuroendocrine and endocrine) plasticity allows non-photoperiodic cues to modulate timing to enable individuals to cope with, and benefit from, short-term environmental variability. Although the timing and duration of the period of full gonadal maturation is principally controlled by photoperiod, non-photoperiodic cues, such as temperature, rainfall or food availability, could potentially modulate the exact time of breeding either by fine-tuning the time of egg-laying within the period of full gonadal maturity or, more fundamentally, by modulating gonadal maturation and/or regression. The timing of gonadal regression affects the time of the start of moult, which in turn may affect the duration of the moult. There are many areas of uncertainty. Future integrated studies are required to assess the scope for flexibility in life-history strategies as this will have a critical bearing on whether birds can adapt sufficiently rapidly to anthropogenic environmental changes, in particular climate change.

Life-history theory proposes that costs must be associated with reproduction. Many direct costs are incurred during breeding. There is also evidence for indirect costs, incurred after breeding, which decrease survival and future reproductive success. One possible indirect cost identified in birds is that breeding activity in some way compromises plumage quality in the subsequent moult. Here we propose a mechanism by which this could occur. Breeding activity delays the start of moult. Birds that start to moult later also moult more rapidly - an effect of decreasing daylength. Could this result in poorer quality plumage? We kept two groups of male European starlings, Sturnus vulgaris, one on constant long days and the other on decreasing daylengths from the start of moult. Decreasing daylengths reduced the duration of moult from 103 ± 4 days to 73 ± 3 days (p < 0.0001). Newly grown primary feathers of birds that moulted fast were slightly shorter, weighed less (p < 0.05) and were more asymmetrical. They had a thinner rachis (p < 0.005), were less hard (p < 0.01) and less rigid (p < 0.05). They were also less resistant to wear so that differences in mass and asymmetry increased with time. There was no difference in Young's modulus. Poorer quality plumage will lead to decreased survival due to decreased flight performance and increased thermoregulatory costs. Thus, reproduction incurs costs through a mechanism that operates after the end of breeding.

The introduction and rapid dispersal of the African flavivirus West Nile virus (WNV) throughout North America, and the high fatality rate due to encephalitis in birds, horses, other wildlife species and humans, has attracted major attention worldwide. Usutu virus, another flavivirus, came to prominence in 2001, when it was identified as the agent responsible for a drop in the bird population in Austria; previously this encephalitic virus was found only in birds and mosquitoes in Africa. Sindbis virus, a pathogenic alphavirus that causes arthritis, is widespread throughout Africa, Europe, Asia and Australia, infecting a range of arthropods and vertebrates and is genetically related to encephalitic viruses in North America. Currently there is no evidence that any of these viruses cause disease in the UK. Here the presence of virus-specific neutralizing antibodies is reported in the sera of resident and migrant birds in the UK, implying that each of these viruses is being introduced to UK birds, possibly by mosquitoes. This is supported by nucleotide sequencing that identified three slightly different sequences of WNV RNA in tissues of magpies and a blackbird. The detection of specific neutralizing antibodies to WNV in birds provides a plausible explanation for the lack of evidence of a decrease in the bird population in the UK compared with North America. The potential health risk posed to humans and animals by these viruses circulating in the UK is discussed.

Timing of reproduction in temperate-zone birds is strongly correlated with spring temperature, with an earlier onset of breeding in warmer years. Females adjust their timing of egg laying between years to be synchronized with local food sources and thereby optimize reproductive output. However, climate change currently disrupts the link between predictive environmental cues and spring phenology. To investigate direct effects of temperature on the decision to lay and its genetic basis, we used pairs of great tits (Parus major) with known ancestry and exposed them to simulated spring scenarios in climate-controlled aviaries. In each of three years, we exposed birds to different patterns of changing temperature. We varied the timing of a temperature change, the daily temperature amplitude, and the onset and speed of a seasonal temperature rise. We show that females fine-tune their laying in response to a seasonal increase in temperature, whereas mean temperature and daily temperature variation alone do not affect laying dates. Luteinizing hormone concentrations and gonadal growth in early spring were not influenced by temperature or temperature rise, possibly posing a constraint to an advancement of breeding. Similarities between sisters in their laying dates indicate genetic variation in cue sensitivity. These results refine our understanding of how changes in spring climate might affect the mismatch in avian timing and thereby population viability.

The rhythm of life on earth is shaped by seasonal changes in the environment. Plants and animals show profound annual cycles in physiology, health, morphology, behaviour and demography in response to environmental cues. Seasonal biology impacts ecosystems and agriculture, with consequences for humans and biodiversity. Human populations show robust annual rhythms in health and well-being, and the birth month can have lasting effects that persist throughout life. This review emphasizes the need for a better understanding of seasonal biology against the backdrop of its rapidly progressing disruption through climate change, human lifestyles and other anthropogenic impact. Climate change is modifying annual rhythms to which numerous organisms have adapted, with potential consequences for industries relating to health, ecosystems and food security. Disconcertingly, human lifestyles under artificial conditions of eternal summer provide the most extreme example for disconnect from natural seasons, making humans vulnerable to increased morbidity and mortality. In this review, we introduce scenarios of seasonal disruption, highlight key aspects of seasonal biology and summarize from biomedical, anthropological, veterinary, agricultural and environmental perspectives the recent evidence for seasonal desynchronization between environmental factors and internal rhythms. Because annual rhythms are pervasive across biological systems, they provide a common framework for trans-disciplinary research.