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Energetic and Fitness Costs of Mismatching Resource Supply and Demand in Seasonally Breeding Birds

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Science  30 Mar 2001:
Vol. 291, Issue 5513, pp. 2598-2600
DOI: 10.1126/science.1057487

Abstract

By advancing spring leaf flush and ensuing food availability, climatic warming results in a mismatch between the timing of peak food supply and nestling demand, shifting the optimal time for reproduction in birds. Two populations of blue tits (Parus caeruleus) that breed at different dates in similar, but spatially distinct, habitat types in Corsica and southern France provide a unique opportunity to quantify the energetic and fitness consequences when breeding is mismatched with local productivity. As food supply and demand become progressively mismatched, the increased cost of rearing young pushes the metabolic effort of adults beyond their apparent sustainable limit, drastically reducing the persistence of adults in the breeding population. We provide evidence that the economics of parental foraging and limits to sustainable metabolic effort are key selective forces underlying synchronized seasonal breeding and long-term shifts in breeding date in response to climatic change.

Matching the timing of breeding with the local peak in food abundance is crucial to reproductive success for income breeders such as small passerine birds (1–3), which must forage daily to cover breeding costs. Many insectivorous birds show a seasonal decline in nestling growth, condition, and survival that can be attributed to a falloff in prey abundance (4,5), resulting in a progressive mismatching between food supply and nestling demand. By advancing the phenology of budding, leaf production, and food supply, climatic warming exacerbates such mismatching (6). Any mismatch between nestling demand and food supply must be mediated by parents, affecting both foraging costs and provisioning rates.

We hypothesize that the economics of parental foraging is a key selection pressure shaping the evolution of highly seasonal breeding in birds and underlying the tracking of climate change. Energetic and fitness consequences of mismatching cannot easily be measured in wild populations because strong stabilizing selection drives the frequency of early- and late-breeding phenotypes to low levels, making it impossible to quantify the performance of “maladapted” phenotypes. However, two populations of blue tits (Parus caeruleus) that breed at different dates relative to the local peak in prey abundance, due to differences in gene flow from adjacent habitats (7,8), offer a unique opportunity to expose energetic and fitness costs when breeding is mismatched with food supply. Here, we show that parental foraging costs increase and that adult survival and nestling condition decrease with the degree of mismatching.

In the Mediterranean region, blue tits exhibit extreme variation in breeding date (9) mediated by interpopulation differences in photoperiod response (10–12). Differences in the timing of breeding between populations appear to be genetic and adaptive, acting to match the period of peak nestling food demand with the brief spring peak in caterpillar abundance in the forest type that dominates the local landscape (7, 8). Because the spring flush in new foliage supports caterpillar production, the phenology of prey abundance changes between forest types as a function of interspecific differences in the timing of leaf growth (13). In Corsica, the local landscape is dominated by forests of evergreen Holm oak (Quercus ilex), which renew about 30% of leaves in early June. Here, blue tits time breeding such that peak nestling demand coincides with the early June peak in caterpillar abundance (14). At the same latitude and altitude in continental southern France, the local landscape is dominated by deciduous Downy oak (Q. pubescens) forest where the spring leaf flush occurs in early May. Here, blue tits breed nearly 4 weeks earlier than in Corsica, again matching peak nestling demand with food supply (7, 8).

In continental southern France, however, the May-breeding phenotype of blue tits overflows from deciduous oak forest into less common patches of evergreen oak, where pairs breed about 3 weeks too early relative to the local peak in caterpillar abundance (8). This phenotype overflow creates two blue tit populations that occupy the same evergreen oak habitat, yet differ in the degree of matching between nestling food demand and the local peak in caterpillar abundance. These two populations, which we refer to as matched (Corsican evergreen oak population) and mismatched (continental evergreen oak population), allow us to test for energetic and fitness costs when breeding is mismatched with food supply.

For selection to act on the timing of breeding via parental energy budgets, two conditions must be met. First, the degree of matching between peak nestling demand and the local peak in caterpillar abundance must affect the field metabolic rate (FMR) of breeding adults, with the most mismatched individuals making the greatest metabolic effort. Second, mismatched individuals must have lower lifetime reproductive output (measured either directly as survival or indirectly as persistence in the breeding population) than matched individuals. We show that Mediterranean blue tits meet both conditions.

Caterpillar abundance (15) showed a repeatable seasonal peak with similar timing and amplitude in both Corsican and continental evergreen oak habitats (Fig. 1) (Julian dates, i.e., days since 1 January: Corsica peak, 156.8 ± 8.0; continent peak, 157.9 ± 6.1). In Corsica, breeding dates for our study nests were well matched with caterpillar abundance (16), with all nesting dates falling within the 13-year range in peak caterpillar abundance (Julian dates: nesting, 163 to 172; caterpillar peak, 151 to 172). In the continental population, most birds bred before the 10-year range in caterpillar peak (nesting, 132 to 149; caterpillar peak, 148 to 172). Brood size was not significantly correlated with breeding date in either the matched Corsican population or the mismatched continental population (Table 1). However, in the continental population, total brood mass declined and daytime FMR for adults (FMRday) (17) rose as the offset between breeding date and caterpillar peak increased (Table 1and Fig. 2). The daily unit cost for rearing young (per gram of nestling) rose from a mean of 1.01 ± 0.49 kJ day−1 adult−1 in Corsica and 1.27 ± 0.16 kJ day−1 adult−1 in the three most matched continental nests to 2.59 ± 0.59 kJ day−1 adult−1 in the four least matched continental nests, an increase of more than 100%. Metabolic effort of adults, measured as FMR24-h/BMR (24-hour FMR divided by basal metabolic rate), rose from 4.91 ± 0.54 × BMR in the three most matched to 6.96 ± 1.27 × BMR in the four most mismatched continental nests, but averaged only 3.45 ± 0.88 in Corsica. The metabolic effort exhibited by the most mismatched pairs is among the highest reported to date for breeding birds (18–20). The relation between metabolic effort and breeding date (effort = 27.96 – 0.16 · date) was such that effort in the continental population would fall to the Corsican level of 3.45 × BMR at Julian date 156—exactly when the breeding date is matched with the interannual peak in food supply (Fig. 1).

Figure 1

Caterpillar prey abundance in continental and Corsican evergreen oak (Q. ilex) forests. The vertical arrow indicates the interannual mean in peak caterpillar abundance; the horizontal bar indicates the timing of breeding for study pairs.

Figure 2

Brood mass and energetic costs for blue tit parents as a function of breeding date. (A) Summed mass of all nestlings at 14 days of age. (B) Cost to individual parents rearing nestlings, in terms of kJ day−1adult−1 per gram of nestling (calculated from FMRday/brood mass). (C) Metabolic effort for adults, measured as FMR24-h/BMR. Slight variations in date between panels are due to random jitter induced so as to separate overlapping data points.

Table 1

Contrasts in brood parameters and parental energetics between matched and mismatched populations of breeding blue tits. Results are for regressions of parameters against breeding date. Response direction indicates the direction of response for the mismatched population as breeding date approaches the peak in caterpillar prey abundance.

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If there is a tradeoff between current metabolic effort and future survival and reproductive prospects, as postulated by the prudent parent hypothesis (21), then one would expect lower persistence of breeding pairs in mismatched populations compared with matched populations, reflecting a difference in survival. Mean persistence (22) was significantly lower for both males and females in mismatched continental evergreen oak compared with matched Corsican evergreen oak forest [females: continent, 1.35 ± 0.66 years; Corsica, 2.16 ± 1.44 years; analysis of variance (ANOVA):F = 18.71, P < 0.001; males: continent, 1.35 ± 0.75 years; Corsica, 2.23 ± 1.62 years; ANOVA: F = 15.29, P < 0.001]. The proportion of females that bred more than 1 year in the local population fell from 52.7% in the matched population to only 25.0% in the mismatched population, and for males it fell from 49.6% to 22.2% (females: χ2 = 13.2, P < 0.001; males: χ2 = 14.9, P < 0.001).

The following pattern emerges: When breeding date is matched with the peak in food supply, blue tits work at levels typical of other breeding birds when provisioning their young (18–20). Brood size and nestling demand appear to be adjusted to the level of prey abundance such that parental metabolic effort lies at 3 to 4 × BMR, which the prudent parent hypothesis associates with the highest metabolic effort that does not compromise survival and future reproductive success (21). Individuals who fail to match breeding date with local food supply, as a result of either gene flow from habitats with a different resource phenology or insufficient phenotypic plasticity, face low prey densities. The consequent mismatching between nestling demand and prey abundance forces parents to increase foraging effort beyond their sustainable limit, resulting in a tradeoff between immediate metabolic effort and persistence in the breeding population. The reduction in adult persistence and the decline in nestling size that result from mismatching act together to constitute stabilizing selection, setting photoperiod response and the chronology of the ensuing reproductive events.

The combination of lower metabolic effort and higher persistence in the matched Corsican population and higher metabolic effort and lower persistence in the mismatched continental population supports the prudent parent hypothesis. By interacting with nestling number and quality, the tradeoff between foraging cost and persistence sets the optimal level for metabolic effort at 3 to 4 × BMR, beyond which individuals face a decline in fitness. The fitness cost of excessive metabolic effort also provides the physiological mechanism by which a broad spectrum of terrestrial birds have responded to global warming by advancing their breeding date (23).

  • * To whom correspondence should be addressed. E-mail: d.thomas{at}courrier.usherb.ca

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