Climate change has affected the phenology of a wide range of species but it remains difficult to interpret these shifts and to explain the variation among species and even among populations within species. We argue the need for a yardstick—some measure of how much a species should shift given the changes in its environment—to assess whether shifts in phenology are sufficient. We have brought together all examples we could find () and have shown that, in the majority of cases, the observed shifts do not seem to match the shifts that would be expected. It remains unclear how we should interpret the thousands of reported shifts in phenology for which we have no yardstick. We would like to encourage researchers to establish links with other researchers or institutions that work on other components of the food chain of their focal species. In many cases, data are available but are often collected by groups working in a different setting, for instance fisheries research may well have data on the phenology of fish needed to interpret shifts in phenology of piscivorous birds. Integration and linkages of long term databases of plant, insect and vertebrate species is both crucial and a major challenge.
In this review, we have considered a very simple form of yardstick: in most of our examples we have assumed that the selection acting on the phenology of a species comes from just a single selection agent: their food source. Furthermore, we have assumed that there is just a single activity (i.e. breeding, spawning) a year for which timing is important. Although we admit that this ‘single critical activity–single selection agent’ scenario is highly unlikely to be the case, we fear that it is the best possible yardstick at this moment. And even so, most examples we reviewed come from simple ecological situations, because more complex trophic interactions are more difficult to study, and long-time series on all relevant species within a food web are rarer than these simple food chains.
When we go beyond measuring the shifts in phenology of a single selection agent it becomes more difficult to define a yardstick, as we then need to integrate these different selection pressures. The one example where there are data on both food and predator phenology (the Macoma example, Philippart et al. 2003
) there was no change in food phenology but a strong shift in predator risk phenology, and it is unclear how these two selection pressures should be combined into a single yardstick. Another example where the phenology of predation may be an equally important selection pressure as the phenology of food is the frog (Rana temporaria
), and its predators (newts, Triturus
sp.). The newts have advanced their entry in ponds, whereas frogs have not substantially altered their reproductive phenology (Beebee 1995
). Therefore, embryos and larvae of early breeding frogs are now exposed to higher levels of newt predation (Walther et al. 2002
Ultimately, the way forwards is to measure selection on phenology and to assess whether there is increased directional selection (Visser et al. in press a
). For this however, long-term studies where individual fitness can be calculated are needed rather than just population means. The very few studies that have calculated whether there is increased directional selection are all on birds (Visser et al. 1998
; Both & Visser 2001
; Cresswell & McCleery 2003
) as only for this group such long-term studies are available. Clearly, individual fitness measures will not be available for the Macoma
system. But also for such systems, the ultimate way to assess whether their shift in phenology is sufficient is to measure the reproductive success of early and late spawning individuals. Even if we are able to measure the selection acting on the phenology, a yardstick is still essential as the changes in these fitness-based measures may also be caused by other changes in the environment. A full understanding of whether species are reacting sufficiently to the climate change-induced advance of its food requires therefore both these fitness estimates and the yardstick. In the case of great tits, the change in selection differential over the years is consistent with the improved (Cresswell & McCleery 2003
) or the deteriorated synchrony (Visser et al. 1998
) between food and reproduction.
The second critical assumption of our review is that there is just a single critical activity per year that is under selection. In reality, this will not be the case and a life cycle approach is more appropriate: the entire life cycle has to be fitted into the seasonal changes in suitability of the habitat. This is even more important as different life history stages may each be affected by climate change, as we have already discussed for migrant birds (Winkler et al. 2002
; Both & Visser 2005
). Such changes of multiple life-history traits have also been reported for resident bird species. The Hoge Veluwe great tits, which have not shifted their laying dates, have responded to climate change by no longer producing second clutches (Visser et al. 2003
). In the case of the Wytham Wood great tits, they have prolonged the time between the laying of their last egg and the hatching of their chicks. As a result the interval between hatch date and caterpillar peak has not changed over the years and hatching asynchrony has been reduced (Cresswell & McCleery 2003
). It is, therefore, very well possible that the shift in laying date in this population has been sufficient despite the fact that the shift in the phenology of their food, the peak caterpillar biomass date, was weaker than the shift in laying date, and hence we have classified this study as ‘sufficient’ rather than to ‘too much’ in . As for the ‘single selection agent’ assumption, also the ‘single critical activity’ assumption can only be lifted for a handful of studies, again mainly birds.
Finally, there are a few more complications with the assumption that shifts in food phenology is a useful yardstick. It may also be that more generalist species are less affected by climate change, because they can more easily switch to alternative prey if they are out of synchrony with one of their prey species. Another complication is that so far we have just considered changes in the timing of the optimal period, e.g. food peak, but also the width of the optimal window may change as climate changes. These changes have been only rarely mentioned in the literature (Buse et al. 1999
) and will make the use of a yardstick more difficult. However, changes in the width of the optimal period may be even more important than the actual date of the peak, because if the window becomes too narrow reproduction may become impossible, whatever the change in phenology.
Our review suggests that an insufficient response to climate change is the rule rather than the exception, and that only in a few cases has the consumer shifted its phenology to the same extent as its food. We, however, want to stress that it may well be possible that insufficient responses are published more frequently than cases where species have adjusted smoothly to the present climate change, i.e. there may be publication bias toward reports of mistiming. We urge researchers with long-tem datasets on phenology to link their data with those that can serve as a yardstick. Despite the complications discussed above, we believe that making a comparison of actual shifts with predicted shifts will be an important step forwards, even if the yardstick is not perfect, as it is crucial to assess the impact of climate change on the natural world. If indeed most species are becoming mistimed this will emphasize the need to take measure to reduce climate change because mistiming is likely to have detrimental effects on species persistence, and thereby on biodiversity.