Phenological responses to climate change differ across trophic levels, which may lead to birds failing to breed at the time of maximal food abundance. Here we investigate the population consequences of such mistiming in the migratory pied flycatcher, Ficedula hypoleuca. In a comparison of nine Dutch populations, we find that populations have declined by about 90% over the past two decades in areas where the food for provisioning nestlings peaks early in the season and the birds are currently mistimed. In areas with a late food peak, early-breeding birds still breed at the right time, and there is, at most, a weak population decline. If food phenology advances further, we also predict population declines in areas with a late food peak, as in these areas adjustment to an advanced food peak is insufficient. Mistiming as a result of climate change is probably a widespread phenomenon, and here we provide evidence that it can lead to population declines.
Climate change has led to shifts in phenology in many species distributed widely across taxonomic groups. It is, however, unclear how we should interpret these shifts without some sort of a yardstick: a measure that will reflect how much a species should be shifting to match the change in its environment caused by climate change. Here, we assume that the shift in the phenology of a species' food abundance is, by a first approximation, an appropriate yardstick. We review the few examples that are available, ranging from birds to marine plankton. In almost all of these examples, the phenology of the focal species shifts either too little (five out of 11) or too much (three out of 11) compared to the yardstick. Thus, many species are becoming mistimed due to climate change. We urge researchers with long-term datasets on phenology to link their data with those that may serve as a yardstick, because documentation of the incidence of climate change-induced mistiming is crucial in assessing the impact of global climate change on the natural world.
Spring temperatures in temperate regions have increased over the past 20 years, and many organisms have responded to this increase by advancing the date of their growth and reproduction. Here we show that adaptation to climate change in a long-distance migrant is constrained by the timing of its migratory journey. For long-distance migrants climate change may advance the phenology of their breeding areas, but the timing of some species' spring migration relies on endogenous rhythms that are not affected by climate change. Thus, the spring migration of these species will not advance even though they need to arrive earlier on their breeding grounds to breed at the appropriate time. We show that the migratory pied flycatcher Ficedula hypoleuca has advanced its laying date over the past 20 years. This temporal shift has been insufficient, however, as indicated by increased selection for earlier breeding over the same period. The shift is hampered by its spring arrival date, which has not advanced. Some of the numerous long-distance migrants will suffer from climate change, because either their migration strategy is unaffected by climate change, or the climate in breeding and wintering areas are changing at different speeds, preventing adequate adaptation.
In seasonal environments, the main selection pressure on the timing of reproduction (the ultimate factor) is synchrony between o¡spring requirements and food availability. However, reproduction is initiated much earlier than the time of maximum food requirement of the o¡spring. Individuals should therefore start reproduction in response to cues (the proximate factors), available in the environment of reproductive decision making, which predict the later environment of selection. With increasing spring temperatures over the past decades, vegetation phenology has advanced, with a concomitant advancement in the reproduction of some species at higher trophic levels. However, a mismatch between food abundance and o¡spring needs may occur if changes in the environment of decision making do not match those in the environment of selection. Date of egg laying in a great tit (Parus major) population has not advanced over a 23-year period, but selection for early laying has intensi¢ed. We believe that this is the ¢rst documented case of an adaptive response being hampered because a changing abiotic factor a¡ects the environment in which a reproductive decision is made di¡erently from the environment in which selection occurs.
The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity.The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions.Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.
Theoretical and laboratory research suggests that phenotypic plasticity can evolve under selection. However, evidence for its evolutionary potential from the wild is lacking. We present evidence from a Dutch population of great tits (Parus major) for variation in individual plasticity in the timing of reproduction, and we show that this variation is heritable. Selection favoring highly plastic individuals has intensified over a 32-year period. This temporal trend is concurrent with climate change causing a mismatch between the breeding times of the birds and their caterpillar prey. Continued selection on plasticity can act to alleviate this mismatch.
Timing of reproduction has major fitness consequences, which can only be understood when the phenology of the food for the offspring is quantified. For insectivorous birds, like great tits (Parus major), synchronisation of their offspring needs and abundance of caterpillars is the main selection pressure. We measured caterpillar biomass over a 20-year period and showed that the annual peak date is correlated with temperatures from 8 March to 17 May. Laying dates also correlate with temperatures, but over an earlier period (16 March-20 April). However, as we would predict from a reliable cue used by birds to time their reproduction, also the food peak correlates with these temperatures. Moreover, the slopes of the phenology of the birds and caterpillar biomass, when regressed against the temperatures in this earlier period, do not differ. The major difference is that due to climate change, the relationship between the timing of the food peak and the temperatures over the 16 March-20 April period is changing, while this is not so for great tit laying dates. As a consequence, the synchrony between offspring needs and the caterpillar biomass has been disrupted in the recent warm decades. This may have severe consequences as we show that both the number of fledglings as well as their fledging weight is affected by this synchrony. We use the descriptive models for both the caterpillar biomass peak as for the great tit laying dates to predict shifts in caterpillar and bird phenology 2005-2100, using an IPCC climate scenario. The birds will start breeding earlier and this advancement is predicted to be at the same rate as the advancement of the food peak, and hence they will not reduce the amount of the current mistiming of about 10 days.
Summary 1.Climate change has been shown to affect the phenology of many organisms, but interestingly these shifts are often unequal across trophic levels, causing a mismatch between the phenology of organisms and their food. 2. We consider two alternative hypotheses: consumers are constrained to adjust sufficiently to the lower trophic level, or prey species react more strongly than their predators to reduce predation. We discuss both hypotheses with our analyses of changes in phenology across four trophic levels: tree budburst, peak biomass of herbivorous caterpillars, breeding phenology of four insectivorous bird species and an avian predator. ) have advanced, whereas raptor hatching dates showed no trend. 4. The caterpillar peak date was closely correlated with budburst date, as were the passerine hatching dates with the peak caterpillar biomass date. In all these cases, however, the slopes were significantly less than unity, showing that the response of the consumers is weaker than that of their food. This was also true for the avian predator, for which hatching dates were not correlated with the peak availability of fledgling passerines. As a result, the match between food demand and availability deteriorated over time for both the passerines and the avian predators. 5. These results could equally well be explained by consumers' insufficient responses as a consequence of constraints in adapting to climate change, or by them trying to escape predation from a higher trophic level, or both. Selection on phenology could thus be both from matches of phenology with higher and lower levels, and quantifying these can shed new light on why some organisms do adjust their phenology to climate change, while others do not.
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