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Diet Can Predict Phenological Changes in Response to Climate Change

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Diet Can Predict Phenological Changes in Response to Climate Change Ecology Letters, (2010) 13: 1475–1484 doi: 10.1111/j.1461-0248.2010.01534.x LETTER Tell me what you eat and IÕll tell you when you fly: diet can predict phenological changes in response to climate change Abstract Florian Altermatt* Changes in phenology are correlated with climate change. However, we still struggle to Department of Environmental understand the traits making species susceptible to climate change, and the implications Science and Policy, University of of speciesÕ reactions for communities and food webs. Butterflies and moths are an California, 1 Shields Ave., Davis, ecologically important group that have shown pronounced phenological changes over CA 95616, USA the last decades. Tests using a > 150-year dataset from 566 European butterfly and moth *Correspondence: E-mail: species demonstrated that variation in phenological change was strongly related to traits [email protected] describing plant–herbivore interactions (larval diet breadth, diet composition), and the life cycle. The results indicate that climate change related shifts in phenology are correlated with the seasonal availability and palatability of food plants. Lepidopterans feeding on herbaceous plants showed smaller shifts in flight periods but larger increases in voltinism than lepidopterans feeding on woody plants. Consequently, the effect of herbivorous lepidopterans may increase in herb-rich grassland ecosystems under warmer conditions, and not in forest ecosystems. Keywords Butterfly, climate change, flight period, generation, Lepidoptera, moth, phenology, species traits, voltinism. Ecology Letters (2010) 13: 1475–1484 butterflies and moths have shifted from univoltinism INTRODUCTION towards bi- or multi-voltinism (Jo¨nsson et al. 2009; Alterm- Global climate change is altering the distribution, abundance att 2010). and phenotypes of species, worldwide (Walther et al. 2002; Many of these phenological changes are likely to have Parmesan & Yohe 2003; IPCC 2007). Phenological changes large consequences for local populations and interactions are among the best-studied warming-related changes in life- with other species. For example, the onset of flowering in history traits, because they are relatively easy to track, and a plants and first appearance dates of pollinators is evolu- direct causality is well-accepted (Walther et al. 2002). They tionarily well-synchronized, but temporal mismatches have been reported from many different taxonomic groups. among mutualistic partners have occurred during warming For example, plants shortened life cycles, flowering and seed (Hegland et al. 2009). Also, earlier onset of development set have advanced (Fitter & Fitter 2002; Steltzer & Post and increased voltinism may promote faster population 2009) and birds and other vertebrates have advanced their growth (Steinbauer et al. 2004), making outbreaks of pest breeding season (Walther et al. 2002). Some of the most species more likely (Steinbauer et al. 2004; van Asch & drastic phenological changes have been reported for insects Visser 2007). For herbivores, phenological shifts have (Parmesan & Yohe 2003; Mene´ndez 2007): since the late negative consequences when they do not match host–plant 1970s on various continents, seasonal appearance of many phenology, or when phenological mismatches result in the butterflies and other insects have advanced by up to several production of an inappropriate diapausing stage, as found in weeks (Roy & Sparks 2000; Walther et al. 2002; Forister & the true bug Nezara viridula: the species occurs nowadays Shapiro 2003); multibrooded species have prolonged their out of its historic range, yet females still lay eggs late in flight period (Roy & Sparks 2000), and bark beetles, autumn even though their offspring have no chance of Ó 2010 Blackwell Publishing Ltd/CNRS 1476 F. Altermatt Letter attaining adulthood or surviving the winter (Musolin 2007). a food resource. A difference in the diet spectrum of the Many of these observed phenological changes are due to herbivore can thus affect the ability for phenological phenotypic plasticity, but evolutionary changes are likely, changes. For example, plants may flush their leaves and may increase in importance (Bradshaw & Holzapfel simultaneously (such as many trees) or sequentially (such 2006). as many herbaceous plants). Only in the latter case, fresh Phenology in insects is closely related to environmental and potentially less defended leaves are available over most variables, and differs between species and populations. For of the season, while the leaves of most trees and shrubs are instance, Lepidoptera using larval food plants of poorly only palatable over a short time-window in spring (Feeny defended plants tend to be bi- or multi-voltine (Hunter & 1970). I therefore hypothesized that species feeding on McNeil 1997), whereas Lepidoptera using a restricted set of woody plants will shift their flight period to match the strongly defended food plants tend to be univoltine flushing of leaves, but may not be able to have a further (Shreeve et al. 2001; Cizek et al. 2006). Even within a generation (i.e., a change in voltinism), because the species, such as the cabbage white butterfly, Pieris rapae, the simultaneously flushed leaves will be less palatable for a speed of development depends on an intimate interaction second generation. Also, plants with year-round foliage or between environmental temperature and larval food type evergreen plants may be a more reliable food source for (Kingsolver et al. 2006). There is a large body of research herbivores, but the leaves may be more defended and less showing both a high interspecific and intraspecific variability palatable compared to plants with short-lived leaves (Feeny in phenological traits, such as development rates, number of 1976; Rhoades & Cates 1976). Finally, I hypothesized that instars or diapause induction and a dependence of pheno- species with a more flexible larval diet (i.e., oligo- or logical trait expression on ambient temperature (Gotthard polyphagous species) would show stronger changes in et al. 2000; Kingsolver 2007; Musolin 2007). phenology than species with a very restricted larval diet, as While changes in phenology along with increases in the latter are constrained to the phenology of their single ambient temperature are widely documented, the relation- host–plant. (3) Populations of species that occur over a wide ship between phenological changes in the context of climate geographic range are adapted or plastic to match a wide change and species traits seems to be largely unexplored in range of climates, and dispersal may introduce genetic natural systems. However, to generalize and eventually variability that is favourable in altered local conditions mitigate effects of climate change, we must understand (Bradshaw & Holzapfel 2006), whereas species with a species-specific variation in the reaction norm to climate narrow geographic range have less inherent variation to deal change. Three aspects are important: (1) comparing effects with altered local conditions. I therefore hypothesized that of climate change on a large number of species in natural species occurring over a wide geographic range would show communities, (2) attributing changes in phenology in the a stronger change in phenology compared to species which context of climate change to species traits and species are either rare or have a narrow geographic range. (4) ecology and (3) evaluating the evolutionary consequences Finally, I hypothesized that more closely related species (or potential) of climate change in whole communities. would show more similar changes in phenology than species I used extensive long-term data (> 150 years) on 566 belonging to different phylogenetic clades. butterfly and moth species from Central Europe for which There are good reasons to use Lepidoptera as a model I have documented changes in phenology and voltinism in system to study the interaction of species traits and climate an earlier study (Altermatt 2010). Here, I take an entirely change on phenology. First, Lepidoptera are one of the new approach by studying if species traits can explain largest insect orders and their physiological ecology with variation in different phenological changes. Thereby, I relate respect to phenology is reasonably well understood (Scoble biological changes in the context of climate change to 1995). Second, they have a high interspecific and intra- functional traits. I gathered species traits falling into four specific variation in phenological traits, which are both categories of speciesÕ life histories and ecology (Stearns under genetic and environmental control (Shapiro 1977; 1992), and which describe: (1) characteristics of the life Tauber et al. 1986; Va¨lima¨ki et al. 2008). Third, many cycle, (2) the larval diet spectrum, (3) geographical range and species showed pronounced phenological changes in abundance and (4) phylogenetic relationships among the parallel with climate change (Roy & Sparks 2000; Forister Lepidoptera species. The choice of these categories was & Shapiro 2003; Altermatt 2010). Finally, Lepidoptera are a motivated because they match a set of hypotheses describ- globally important component of primary consumers in ing species-specific changes in phenology: (1) changes in terrestrial ecosystems (Scoble 1995). Understanding the phenology are constrained by aspects of a speciesÕ life cycle, effects of environmental factors and species traits on such as the identity of the life stage that over-winters phenological changes is thus essential
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