IPCC Fourth Assessment Report: Climate Change 2007
Climate Change 2007: Working Group II: Impacts, Adaptation and Vulnerability Changes in phenology

Phenology – the timing of seasonal activities of animals and plants – is perhaps the simplest process in which to track changes in the ecology of species in response to climate change. Observed phenological events include leaf unfolding, flowering, fruit ripening, leaf colouring, leaf fall of plants, bird migration, chorusing of amphibians, and appearance/emergence of butterflies. Numerous new studies since the TAR (reviewed by Menzel and Estrella, 2001; Sparks and Menzel, 2002; Walther et al., 2002; Menzel, 2003; Walther, 2004) and three meta-analyses (Parmesan and Yohe, 2003; Root et al., 2003; Lehikoinen et al., 2004) (see Section 1.4.1) concurrently document a progressively earlier spring by about 2.3 to 5.2 days/decade in the last 30 years in response to recent climate warming.

Although phenological network studies differ with regard to regions, species, events observed and applied methods, their data show a clear temperature-driven extension of the growing season by up to 2 weeks in the second half of the 20th century in mid- and high northern latitudes (see Table 1.7), mainly due to an earlier spring, but partly due also to a later autumn. Remotely-sensed vegetation indices (Myneni et al., 1997; Zhou et al., 2001; Lucht et al., 2002) and analysis of the atmospheric CO2 signal (Keeling et al., 1996) confirm these findings. A corresponding longer frost-free and climatological growing season is also observed in North America and Europe (see Section This lengthening of the growing season might also account for observed increases in productivity (see Section The signal in autumn is less pronounced and more homogenous. The very few examples of single-station data indicate a much greater lengthening or even a shortening of the growing season (Kozlov and Berlina, 2002; Peñuelas et al., 2002).

Table 1.7. Changes in length of growing season, based on observations within networks.

Location Period Species/Indicator  Lengthening (days/decade) References 
Germany 1951-2000 4 deciduous trees (LU/LC) 1.1 to 2.3 Menzel et al., 2001; Menzel, 2003 
Switzerland 1951-1998 9 spring, 6 autumn phases  2.7* Defila and Clot, 2001 
Europe (Int. Phenological Gardens) 1959-1996 1969-1998 Various spring/autumn phases (LU to LC, LF) 3.5 Menzel and Fabian, 1999; Menzel, 2000; Chmielewski and Rotzer, 2001 
Japan 1953-2000 Gingko biloba (LU/LF) 2.6 Matsumoto et al., 2003 
Northern Hemisphere 1981-1999 Growing season by normalised difference vegetation index (NDVI) 0.7 to 1 Zhou et al., 2001 

LU = leaf unfolding; LC = leaf colouring; LF = leaf fall. * indicates mean of significant trends only.

Altered timing of spring events has been reported for a broad multitude of species and locations; however, they are primarily from North America, Eurasia and Australia. Network studies where results from all sites/several species are reported, irrespective of their significance (Table 1.8), show that leaf unfolding and flowering in spring and summer have, on average, advanced by 1-3 days per decade in Europe, North America and Japan over the last 30 to 50 years. Earlier flowering implies an earlier start of the pollen season (see Section There are also indications that the onset of fruit ripening in early autumn has advanced in many cases (Jones and Davis, 2000; Peñuelas et al., 2002; Menzel, 2003) (see also Section Spring and summer phenology is sensitive to climate and local weather (Sparks et al., 2000; Lucht et al., 2002; Menzel, 2003). In contrast to autumn phenology (Estrella and Menzel, 2006), their climate signal is fairly well understood: nearly all spring and summer changes in plants, including agricultural crops (Estrella et al., 2007), correlate with spring temperatures in the preceding months. The advancement is estimated as 1 to12 days for every 1°C increase in spring temperature, with average values ranging between 2.5 and 6 days per °C (e.g., Chmielewski and Rotzer, 2001; Menzel, 2003; Donnelly et al., 2004; Menzel et al., 2006b). Alpine species are also partly sensitive to photoperiod (Keller and Korner, 2003) or amount of snowpack (Inouye et al., 2002). Earlier spring events and a longer growing season in Europe are most apparent for time-series ending in the mid-1980s or later (Schaber, 2002; Scheifinger et al., 2002; Dose and Menzel, 2004; Menzel and Dose, 2005), which matches the turning points in the respective spring temperature series (Dose and Menzel, 2006).

Table 1.8. Changes in the timing of spring events, based on observations within networks.

Location Period Species/Indicator  Observed changes (days/decade)  References 
Western USA  1957-1994 Lilac, honeysuckle (F) -1.5 (lilac), 3.5 (honeysuckle) Cayan et al., 2001  
North-eastern USA  1965-2001 1959-1993 Lilac (F, LU) Lilac (F)  -3.4 (F) -2.6 (U) -1.7  Wolfe et al., 2005 Schwartz and Reiter, 2000 
Washington, DC  1970-1999 100 plant species (F)  -0.8 Abu-Asab et al., 2001 
Germany 1951-2000 10 spring phases (F, LU)  -1.6  Menzel et al., 2003  
Switzerland 1951-1998 9 spring phases (F, LU) -2.3 (*) Defila and Clot, 2001 
South-central England 1954-2000 385 species (F) -4.5 days in 1990s Fitter and Fitter, 2002 
Europe (Int. Phenological Gardens) 1959-1996 1969-1998 Different spring phases (F, LU) -2.1 -2.7 Menzel and Fabian, 1999; Menzel, 2000; Chmielewski and Rotzer, 2001 
21 European countries 1971-2000 F, LU of various plants -2.5 Menzel et al., 2006b 
Japan 1953-2000 Gingko biloba (LU)  -0.9 Matsumoto et al., 2003 
Northern Eurasia 1982-2004 NDVI -1.5 Delbart et al., 2006 
UK 1976-1998 Butterfly appearance -2.8 to -3.2 Roy and Sparks, 2000 
Europe, N. America Past 30-60 years Spring migration of bird species -1.3 to -4.4 Crick et al., 1997; Crick and Sparks, 1999; Dunn and Winkler, 1999; Inouye et al., 2000; Bairlein and Winkel, 2001; Lehikoinen et al., 2004 
N. America (US-MA) 1932-1993 Spring arrival, 52 bird species +0.8 to -9.6 (*) Butler, 2003 
N. America (US-IL) 1976-2002 Arrival, 8 warbler species +2.4 to -8.6 Strode, 2003 
England (Oxfordshire) 1971-2000 Long-distance migration, 20 species +0.4 to -6.7 Cotton, 2003 
N. America (US-MA)  1970-2002  Spring arrival,16 bird species -2.6 to -10.0 Ledneva et al., 2004 
Sweden (Ottenby) 1971-2002 Spring arrival, 36 bird species +2.1 to -3.0 Stervander et al., 2005 
Europe 1980-2002 Egg-laying, 1 species -1.7 to -4.6 Both et al., 2004 
Australia 1970-1999 11 migratory birds 9 species earlier arrival Green and Pickering, 2002 
Australia  1984-2003 2 spring migratory birds 1 species earlier arrival Chambers et al., 2005 

F = flowering; LU =, leaf-unfolding; - advance; + delay. * indicates mean of significant trends only.

Records of the return dates of migrant birds have shown changes in recent decades associated with changes in temperature in wintering or breeding grounds or on the migration route (Tryjanowski, 2002; Butler, 2003; Cotton, 2003; Huppop and Huppop, 2003). For example, a 2 to 3 day earlier arrival with a 1°C increase in March temperature is estimated for the swallow in the UK (Sparks and Loxton, 1999) and Ireland (Donnelly et al., 2004). Different measurement methods, such as first observed individual, beginning of sustained migratory period, or median of the migratory period, provide different information about the natural history of different species (Sokolov et al., 1998; Sparks and Braslavska, 2001; Huppop and Huppop, 2003; Tryjanowski et al., 2005).

Egg-laying dates have advanced in many bird species (Hussell, 2003; Dunn, 2004). The confidence in such studies is enhanced when the data cover periods/sites of both local cooling and warming. Flycatchers in Europe (Both et al., 2004) provide such an example, where the trend in egg-laying dates matches trends in local temperatures. Many small mammals have been found to come out of hibernation and to breed earlier in the spring now than they did a few decades ago (Inouye et al., 2000; Franken and Hik, 2004). Larger mammals, such as reindeer, are also showing phenological changes (Post and Forchhammer, 2002), as are butterflies, crickets, aphids and hoverflies (Forister and Shapiro, 2003; Stefanescu et al., 2003; Hickling et al., 2005; Newman, 2005). Increasing regional temperatures are also associated with earlier calling and mating and shorter time to maturity of amphibians (Gibbs and Breisch, 2001; Reading, 2003; Tryjanowski et al., 2003). Despite the bulk of evidence in support of earlier breeding activity as a response to temperature, counter-examples also exist (Blaustein et al., 2001).

Changes in spring and summer activities vary by species and by time of season. Early-season plant species exhibit the strongest reactions (Abu-Asab et al., 2001; Menzel et al., 2001; Fitter and Fitter, 2002; Sparks and Menzel, 2002; Menzel, 2003). Short-distance migrating birds often exhibit a trend towards earlier arrival, while the response of later-arriving long-distance migrants is more complex, with many species showing no change, or even delayed arrival (Butler, 2003; Strode, 2003). Annual plants respond more strongly than congeneric perennials, insect-pollinated more than wind-pollinated plants, and woody less than herbaceous plants (Fitter and Fitter, 2002). Small-scale spatial variability may be due to microclimate, land cover, genetic differentiation, and other non-climate drivers (Menzel et al., 2001; Menzel, 2002). Large-scale geographical variations in the observed changes are found in China with latitude (Chen et al., 2005a), in Switzerland with altitude (Defila and Clot, 2001) and in Europe with magnitude of temperature change (Menzel and Fabian, 1999; Sparks et al., 1999). Spring advance, being more pronounced in maritime western and central Europe than in the continental east (Ahas et al., 2002), is associated with higher spatial variability (Menzel et al., 2006a).

As the North Atlantic Oscillation (NAO) is correlated with temperature (see Trenberth et al., 2007), the NAO has widespread influence on many ecological processes. For example, the speed and pattern (Menzel et al., 2005b), as well as recent trends of spring events in European plants, has also changed consistently with changes seen in the NAO index (Chmielewski and Rotzer, 2001; Scheifinger et al., 2002; Walther et al., 2002; Menzel, 2003). Similarly, earlier arrival and breeding of migratory birds in Europe are often related to warmer local temperatures and higher NAO indices (Hubalek, 2003; Huppop and Huppop, 2003; Sanz, 2003). However, the directions of changes in birds corresponding to NAO can differ across Europe (Hubalek, 2003; Kanuscak et al., 2004). Likewise, the relevance of the NAO index on the phenology of plants differs across Europe, being more pronounced in the western (France, Ireland, UK) and north-western (south Scandinavia) parts of Europe and less distinct in the continental part of Europe (see Figure 1.4a; Menzel et al., 2005b). In conclusion, spring phenological changes in birds and plants and their triggering by spring temperature are often similar, as described in some cross-system studies; however, the NAO influence is weaker than the temperature trigger and is restricted to certain time periods (Walther et al., 2002) (Figure 1.4b).


Figure 1.4. (a) Differences between the mean onset of spring (days) in Europe for the 10 years with the highest (1990, 1882, 1928, 1903, 1993, 1910, 1880, 1997, 1989, 1992) and the lowest (1969, 1936, 1900, 1996, 1960, 1932, 1886, 1924, 1941, 1895) NAO winter and spring index (November to March) drawn from the period 1879 to 1998. After Menzel et al. (2005b). (b) Anomalies of different phenological phases in Germany (mean spring passage of birds at Helgoland, North Sea; mean egg-laying of pied flycatcher in Northern Germany; national mean onset of leaf unfolding of common horse-chestnut (Aesculus hippocastanum) and silver birch (Betula pendula) (negative = earlier)), anomalies of mean spring air temperature T (HadCRUT3v) and North Atlantic Oscillation index (NAO) (http://www.cru.uea.ac.uk/cru/data/). Updated after Walther et al. (2002).