Oecologia (2011) 165:237–248 DOI 10.1007/s00442-010-1789-8 GLOBAL CHANGE ECOLOGY Environmental controls on the phenology of moths: predicting plasticity and constraint under climate change Anu Valtonen • Matthew P. Ayres • Heikki Roininen • Juha Po¨yry • Reima Leinonen Received: 26 April 2010 / Accepted: 25 August 2010 / Published online: 30 September 2010 Ó Springer-Verlag 2010 Abstract Ecological systems have naturally high inter- should be most immediately responsive in phenology to annual variance in phenology. Component species have climate warming, but variably so depending upon the presumably evolved to maintain appropriate phenologies minimum temperature at which appreciable development under historical climates, but cases of inappropriate phe- occurs and the thermal responsiveness of development rate. nology can be expected with climate change. Understand- Photoperiodic modification of thermal controls constrains ing controls on phenology permits predictions of ecological phenotypic responses in phenologies to climate change, but responses to climate change. We studied phenological can evolve to permit local adaptation. Our results suggest control systems in Lepidoptera by analyzing flight times that climate change will alter the phenological structure of recorded at a network of sites in Finland. We evaluated the the Finnish Lepidoptera community in ways that are pre- strength and form of controls from temperature and pho- dictable with knowledge of the proximate physiological toperiod, and tested for geographic variation within spe- controls. Understanding how phenological controls in cies. Temperature controls on phenology were evident in Lepidoptera compare to that of their host plants and ene- 51% of 112 study species and for a third of those thermal mies could permit general inferences regarding climatic controls appear to be modified by photoperiodic cues. For effects on mid- to high-latitude ecosystems. 24% of the total, photoperiod by itself emerged as the most likely control system. Species with thermal control alone Keywords Lepidoptera Á Light-trap Á Photoperiod Á Temperature Á Thermal sum Communicated by Je´rome Casas. Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00442-010-1789-8) contains supplementary material, which is available to authorized users. Ecological systems have naturally high interannual vari- ance in phenology, i.e., in the seasonal timing of periodic A. Valtonen (&) Á H. Roininen life cycle events (Rathcke and Lacey 1985). These events Department of Biology, University of Eastern Finland, are strongly influenced by interannual variation in envi- P.O. Box 111, 80101 Joensuu, Finland e-mail: anu.valtonen@uef.fi ronmental conditions, especially temperatures. Populations are generally well adapted in their phenological adjust- M. P. Ayres ments to interannual climatic variation. The eggs of many Department of Biological Sciences, Dartmouth College, herbivorous insect species tend to hatch when their host Hanover, NH 03755, USA plants leaf out (van Asch and Visser 2007), insectivorous J. Po¨yry birds tend to breed as their prey become abundant (Perrins Research Programme of Biodiversity, and McCleery 1989), insects enter and break diapause as Finnish Environment Institute, 00251 Helsinki, Finland appropriate for the progression of season (Denlinger 2002), R. Leinonen and adult moths typically emerge at the appropriate time Rauhalantie 14 D 12, 87830 Nakertaja, Finland for oviposition (e.g., Tammaru et al. 2001). 123 238 Oecologia (2011) 165:237–248 Plastic responses to environmental cues can help indi- meaningful development occurs (developmental threshold) viduals synchronize their life cycle to interannual variation and of the slope of development rate versus temperature in climate and resources. Phenotypic plasticity is the pro- above the threshold (Trudgill et al. 2005). The phenology duction of alternative phenotypes by the same genotype of species whose development is temperature driven will under different environmental conditions (Nylin and be predictably responsive to interannual temperature vari- Gotthard 1998), for example changes in the growth rate and ation, including directional climate change. However, therefore timing of reproduction depending upon temper- species within a community could vary in their respon- ature. Natural selection on phenotypic plasticity can siveness due to differences in their developmental thresh- enhance the fit between an organism and its environment. olds, differences in their temperature sensitivity when However, in some cases, climate change is already above the threshold, and differences in the extent to which exceeding the range of climatic conditions under which photoperiod modifies the thermal response. adaptive phenological plasticity has evolved (Post and Photoperiod is another well-known modifier of insect Forchhammer 2008), and there are increasing examples of development and therefore phenology since it frequently phenological disruptions of populations, communities, and provides the primary signal for initiation of diapause ecosystems (Visser and Holleman 2001; Willis et al. 2008; (Bradshaw and Holzapfel 2010). Photoperiodically enforced Post et al. 2009). A challenge is to understand and predict diapause in fall is presumed to be adaptive by preventing which species are most susceptible to disruption of inappropriate development in the late fall or winter, even appropriate phenological patterns and which species will when temperatures are permitting (Danilevskii 1965; tend to be most robust in their capacity for adaptive Tauber et al. 1986; Leather et al. 1993). Some insect species plasticity. require a critical photoperiod to terminate diapause in spring Lepidoptera are a good model system to study the nature or early summer (Tauber et al. 1986; Danks 1987; Leather of phenological plasticity because they are diverse, abun- et al. 1993). Some species also display a period of devel- dant, reasonably well understood with respect to their opmental inactivity during summer (aestivation), the ter- physiological ecology, and a globally important component mination of which can likewise be subject to photoperiodic of primary consumers in terrestrial ecosystems (Stamp and control (Masaki 1980; Tauber et al. 1986). Irrespective of Casey 1993; Scoble 1995). During the past decades, climatic variation, complete photoperiodic control leads to Lepidoptera have experienced both advanced phenology invariant interannual phenology with respect to Julian date. (Kuchlein and Ellis 1997; Forister and Shapiro 2003) and Temperature and photoperiod can be co-determinants of increased voltinism (Altermatt 2010). We studied the phenology. For example, temperature can be the dominant diverse community of Finnish nocturnal moths to evaluate driver of development rate and therefore phenology after patterns in the prevalence of four general theoretical pos- the critical photoperiod to terminate diapause is reached. sibilities for environmental controls on phenology: (1) However, many diapausing species seem to exhibit a temperature, (2) Photoperiod, (3) temperature and photo- gradual loss during late autumn and early winter in sensi- period together, and (4) regional adaptation of populations tivity to factors that maintain diapause (Tauber et al. 1986; in the form of their responses to temperature and/or Danks 1987), in which case development can proceed in photoperiod. spring as soon as temperatures rise above the develop- Temperature is frequently a dominant driver of pheno- mental threshold. logical state in insects because their development rate is Finally, there can be divergence among populations in strongly temperature-dependent (Gillooly et al. 2002). The different regions in the form of their responses to temper- generalized function, which is explicable in terms of ature and/or photoperiod. This is the least well studied of thermodynamics and enzyme function, is for development our general models of phenological controls, but geo- rate to be imperceptibly low at low temperatures, increase graphical variation in insect seasonal cycles has been with increasing temperatures across a range that is typically recorded across different latitudes, altitudes, and proximity broad with respect to realized temperatures during the to the center of large land-masses (Danilevskii 1965; growing season, and then decelerate and decline at tem- Leather et al. 1993) and can involve both continuously peratures that are warm with respect to that to which the varying characteristics (for example, diapause-inducing population is adapted (Davidson 1944; Logan et al. 1976; photoperiods or diapause duration) and disjunctly varying Sharpe and DeMichele 1977; van der Have 2002). Since traits (e.g., voltinism) (Tauber et al. 1986). Evidence for the time of Re´aumur (Egerton 2006), it has been recog- population differentiation in the controls on phenology nized that a linear approximation of this relationship can implies a capacity for adaptive adjustments to climate explain much of the interannual variation in phenological change. events. At their simplest, such thermal sum models only We exploited historical records from across Finland of require an estimate of the minimum temperature at which the flight phenology of 112 species of moths to test the 123 Oecologia (2011) 165:237–248 239 applicability of these alternative models of controls on the phenology of high-latitude Lepidoptera. We asked what proportion of species have phenologies