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.
Spring temperatures have increased over the past 25 years, to which a wide variety of organisms have responded. The outstanding question is whether these responses match the temperature-induced shift of the selection pressures acting on these organisms. Organisms have evolved response mechanisms that are only adaptive given the existing relationship between the cues organisms use and the selection pressures acting on them. Global warming may disrupt ecosystem interactions because it alters these relationships and micro-evolution may be slow in tracking these changes. In particular, such shifts have serious consequences for ecosystem functioning for the tight multitrophic interactions involved in the timing of reproduction and growth. We determined the response of winter moth (Operophtera brumata) egg hatching and oak (Quercus robur) bud burst to temperature, a system with strong selection on synchronization. We show that there has been poor synchrony in recent warm springs, which is due to an increase in spring temperatures without a decrease in the incidence of freezing spells in winter. This is a clear warning that such changes in temperature patterns may a¡ect ecosystem interactions more strongly than changes in mean temperature.
Summary 1.Traffic affects large areas of natural habitat worldwide. As a result, the acoustic signals used by birds and other animals are increasingly masked by traffic noise. Masking of signals important to territory defence and mate attraction may have a negative impact on reproductive success. Depending on the overlap in space, time and frequency between noise and vocalizations, such impact may ultimately exclude species from suitable breeding habitat. However a direct impact of traffic noise on reproductive success has not previously been reported. 2. We monitored traffic noise and avian vocal activity during the breeding season alongside a busy Dutch motorway. We measured variation in space, time and spectrum of noise and tested for negative effects on avian reproductive success using long-term breeding data on great tits Parus major. 3. Noise levels decreased with distance from the motorway, but we also found substantial spatial variation independent of distance. Noise also varied temporally with March being noisier than April, and the daytime being noisier than night-time. Furthermore, weekdays were clearly noisier than weekends. Importantly, traffic noise overlapped in time as well as acoustic frequency with avian vocalization behaviour over a large area. 4. Traffic noise had a negative effect on reproductive success with females laying smaller clutches in noisier areas. Variation in traffic noise in the frequency band that overlaps most with the lower frequency part of great tit song best explained the observed variation. 5. Additionally, noise levels recorded in April had a negative effect on the number of fledglings, independent of clutch size, and explained the observed variation better than noise levels recorded in March. 6. Synthesis and applications. We found that breeding under noisy conditions can carry a cost, even for species common in urban areas. Such costs should be taken into account when protecting threatened species, and we argue that knowledge of the spatial, temporal and spectral overlap between noise and species-specific acoustic behaviour will be important for effective noise management. We provide some cost-effective mitigation measures such as traffic speed reduction or closing of roads during the breeding season.
Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. We tested the direct effect of temperature on laying dates in great tits (Parus major) using climatized aviaries in a 6-year experiment. We mimicked the temperature patterns from two specific years in which our wild population laid either early ('warm' treatment) or late ('cold' treatment). Laying dates were affected by temperature directly. As the relevant temperature period started three weeks prior to the mean laying date, with a range of just 48C between the warm and the cold treatments, and as the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. We furthermore show a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. Our results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.
Climate change has led to an advance in phenology in many species. Synchrony in phenology between different species within a food chain may be disrupted if an increase in temperature affects the phenology of the different species differently, as is the case in the winter moth egg hatch -oak bud burst system. Operophtera brumata (winter moth) egg hatch date has advanced more than Quercus robur (pedunculate oak) bud burst date over the past two decades. Disrupted synchrony will lead to selection, and a response in phenology to this selection may lead to species genetically adapting to their changing environment. However, a prerequisite for such genetic change is that there is sufficient genetic variation and severe enough fitness consequences. So far, examples of observed genetic change have been few. Using a half-sib design, we demonstrate here that O. brumata egg-hatching reaction norm is heritable, and that genetic variation exists. Fitness consequences of even a few days difference between egg hatch and tree bud opening are severe, as we experimentally determined. Estimates of genetic variation and of fitness were then combined with a climate scenario to predict the rate and the amount of change in the eggs' response to temperature. We predict a rapid response to selection, leading to a restoration of synchrony of egg hatch with Q. robur bud opening. This study shows that in this case there is a clear potential to adapt -rapidly -to environmental change. The current observed asynchrony is therefore not due to a lack of genetic variation and at present it is unclear what is constraining O. brumata to adapt. This kind of model may be particularly useful in gaining insight in the predicted amount and rate of change due to environmental changes, given a certain genetic variation and selection pressure.
Summary1. Annual variation in the timing of avian reproduction is associated with predictive cues related to ambient temperature. Understanding how these cues affect timing, and estimating the genetic variation in sensitivity to these cues, is essential to predict the micro-evolutionary changes in timing which are needed to adapt to climate change. 2. We carried out a 2-year experiment with great tits Parus major of known genetic background, which were kept in pairs in climate-controlled aviaries with simulated natural photoperiod and exposed to a seasonal change in temperature, where the two treatments differed by 4°C. We recorded the dates of laying the first and last eggs and timing of moult, as well as physiological proxies associated with reproduction: plasma luteinizing hormone (LH), prolactin, and gonadal size at four-weekly intervals. 3. The temperature treatments did not affect first-egg dates, nor gonadal growth or plasma LH and prolactin concentrations. However, birds terminated egg laying, regressed their testes and started their moult earlier at higher temperatures. 4. There were marked family differences in both the start of egg laying, with sisters from early laying maternal families laying early, and in the termination of laying, indicating that there is heritable variation in sensitivity to cues involved in timing. 5. Our experiment, the first to use genetically related individuals in an experimental design with a natural change in photoperiod and biologically realistic temperature differences, thus shows that genetic adaptation in cue sensitivity is possible, essential for species to be able to adapt to a warming world.
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