Climate change is predicted to become a major threat to biodiversity in the 21st century, but accurate predictions and effective solutions have proved difficult to formulate. Alarming predictions have come from a rather narrow methodological base, but a new, integrated science of climate-change biodiversity assessment is emerging, based on multiple sources and approaches. Drawing on evidence from paleoecological observations, recent phenological and microevolutionary responses, experiments, and computational models, we review the insights that different approaches bring to anticipating and managing the biodiversity consequences of climate change, including the extent of species' natural resilience. We introduce a framework that uses information from different sources to identify vulnerability and to support the design of conservation responses. Although much of the information reviewed is on species, our framework and conclusions are also applicable to ecosystems, habitats, ecological communities, and genetic diversity, whether terrestrial, marine, or fresh water.

Beyond Predictions: Biodiversity Conservation in a Changing Climate

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.

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Climate change and population declines in a long-distance migratory bird

There is ample evidence for ecological responses to recent climate change. Most studies to date have concentrated on the effects of climate change on individuals and species, with particular emphasis on the effects on phenology and physiology of organisms as well as changes in the distribution and range shifts of species. However, responses by individual species to climate change are not isolated; they are connected through interactions with others at the same or adjacent trophic levels. Also from this more complex perspective, recent case studies have emphasized evidence on the effects of climate change on biotic interactions and ecosystem services. This review highlights the ‘knowns’ but also ‘unknowns’ resulting from recent climate impact studies and reveals limitations of (linear) extrapolations from recent climate-induced responses of species to expected trends and magnitudes of future climate change. Hence, there is need not only to continue to focus on the impacts of climate change on the actors in ecological networks but also and more intensively to focus on the linkages between them, and to acknowledge that biotic interactions and feedback processes lead to highly complex, nonlinear and sometimes abrupt responses.

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Community and ecosystem responses to recent climate change.

The effects of climate change on biodiversity are increasingly well documented, and many methods have been developed to assess species' vulnerability to climatic changes, both ongoing and projected in the coming decades. To minimize global biodiversity losses, conservationists need to identify those species that are likely to be most vulnerable to the impacts of climate change. In this Review, we summarize different currencies used for assessing species' climate change vulnerability. We describe three main approaches used to derive these currencies (correlative, mechanistic and trait-based), and their associated data requirements, spatial and temporal scales of application and modelling methods. We identify strengths and weaknesses of the approaches and highlight the sources of uncertainty inherent in each method that limit projection reliability. Finally, we provide guidance for conservation practitioners in selecting the most appropriate approach(es) for their planning needs and highlight priority areas for further assessments.

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Assessing species' vulnerability to climate change

Species are the unit of analysis in many global change and conservation biology studies; however, species are not uniform entities but are composed of different, sometimes locally adapted, populations differing in plasticity We examined how intraspecific variation in thermal niches and phenotypic plasticity will affect species distributions in a warming climate We first developed a conceptual model linking plasticity and niche breadth, providing five alternative intraspecific scenarios that are consistent with existing literature Secondly, we used ecological niche-modeling techniques to quantify the impact of each intraspecific scenario on the distribution of a virtual species across a geographically realistic setting Finally, we performed an analogous modeling exercise using real data on the climatic niches of different tree provenances We show that when population differentiation is accounted for and dispersal is restricted, forecasts of species range shifts under climate change are even more pessimistic than those using the conventional assumption of homogeneously high plasticity across a species' range Suitable population-level data are not available for most species so identifying general patterns of population differentiation could fill this gap However, the literature review revealed contrasting patterns among species, urging greater levels of integration among empirical, modeling and theoretical research on intraspecific phenotypic variation

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The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change

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. 3. In our long-term study, we show that between 1988 and 2005, budburst advanced (not significantly) with 0.17 d yr(-1), while between 1985 and 2005 both caterpillars (0.75 d year(-1)) and the hatching date of the passerine species (range for four species: 0.36-0.50 d year(-1)) 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.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-2656.2008.01458.x

Climate change and unequal phenological changes across four trophic levels: constraints or adaptations?

One consequence of climate change is an increasing mismatch between timing of food requirements and food availability. Such a mismatch is primarily expected in avian long-distance migrants because of their complex annual cycle, and in habitats with a seasonal food peak. Here we show that insectivorous long-distance migrant species in The Netherlands declined strongly (1984–2004) in forests, a habitat characterized by a short spring food peak, but that they did not decline in less seasonal marshes. Also, within generalist long-distance migrant species, populations declined more strongly in forests than in marshes. Forest-inhabiting migrant species arriving latest in spring declined most sharply, probably because their mismatch with the peak in food supply is greatest. Residents and short-distance migrants had non-declining populations in both habitats, suggesting that habitat quality did not deteriorate. Habitat-related differences in trends were most probably caused by climate change because at a European scale, long-distance migrants in forests declined more severely in western Europe, where springs have become considerably warmer, when compared with northern Europe, where temperatures during spring arrival and breeding have increased less. Our results suggest that trophic mismatches may have become a major cause for population declines in long-distance migrants in highly seasonal habitats.

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Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats

Climate change has advanced the breeding dates of many bird species, but for few species we know whether this advancement is sufficient to track the advancement of the underlying levels of the food chain. For the long-distance migratory pied flycatcher Ficedula hypoleuca the advancement in breeding time has been insufficient to maintain the synchrony with their main food sources. The timing of arrival in the breeding areas from their African wintering grounds is likely to constrain the advancement of breeding date. We hypothesise that this is because in Africa they cannot predict the advancement of spring in their breeding habitat. However, long-distance migrants may advance their arrival time by migrating faster when circumstances en route are favourable. In this study we show that both arrival and breeding date depend on temperatures at their main North African staging grounds, as well as on temperature at the breeding grounds. Male arrival and average laying date were not correlated, but the positive effect of temperature in North Africa on breeding dates suggests that breeding date is indeed constrained by arrival of females. Long-distance migrants thus are able to adjust arrival and hence breeding by faster spring migration, but the degree of adjustment is probably limited as timing schedules in spring are tight. Furthermore, as climate change is affecting temperatures differently along the migratory flyway and the breeding areas, it is unlikely that arrival dates are advanced at the same rate as the timing of breeding should advance, given the advancement of the underlying levels of the food chain.

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Climatic effects on timing of spring migration and breeding in a long‐distance migrant, the pied flycatcher Ficedula hypoleuca

Investigating food-limitation in generalist predators is difficult, because they can switch to alternative prey, when one of their staple prey becomes scarce. Apart from data on the dynamics of the predator population, a robust study requires: (i) a documentation of the predator's entire prey base; and (ii) an experimental or natural situation, where profitable dietary shifts are impossible, because several preferred prey species decline simultaneously. Here, we provide a detailed description of how food-supply has limited a generalist avian top predator, the northern goshawk Accipiter gentilis. In our study area, populations of several principal goshawk prey species crashed simultaneously during 1975-2000, whereas other extrinsic factors remained essentially unchanged. The breeding and non-breeding segments of the local goshawk population declined markedly, associated with a significant increase in nest failures. Brood size of successful pairs remained unaffected by changes in prey availability. Breeding recruitment ceased at a time when potential replacement birds ('floaters') were still present, providing a rare empirical demonstration of an 'acceptance threshold' in raptor territory choice. To investigate how goshawk diet changed in response to varying food-supplies, we make novel use of an analytical tool from biodiversity research-'abundance-biomass-comparison curves' (ABC curves). With increasing levels of food-stress, the dominance of principal prey species in the diet decreased, and the number of small-bodied prey species increased, as did intra-guild predation. Our finding that breeder and non-breeder segments declined in concert is unexpected. Our results carry the management implication that, in food-limited raptor populations, externally induced breeder mortality can rapidly depress population size, as losses are no longer buffered when floaters reject breeding opportunities.

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Rob G. Bijlsma

Papers

Climate change and unequal phenological changes across four trophic levels: constraints or adaptations?

Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats

Climatic effects on timing of spring migration and breeding in a long‐distance migrant, the pied flycatcher Ficedula hypoleuca

Food-limitation in a generalist predator.

Population limitation in the Northern Goshawk in Europe: A review with case studies