Observed changes in seasons: an overview - Wiley Online Library

INTERNATIONAL JOURNAL OF CLIMATOLOGY Int. J. Climatol. 22: 1715–1725 (2002) Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/joc.821

OBSERVED CHANGES IN SEASONS: AN OVERVIEW T. H. SPARKSa, * and A. MENZELb NERC Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton, Huntingdon, Cambridgeshire PE28 2LS, UK Lehrstuhl für Bioklimatologie und Immissionsforschung, Technical University of Munich, Am Hochanger 13, 85354 Freising, Germany a

b

Received 18 February 2002 Revised 5 April 2002 Accepted 17 June 2002

ABSTRACT Within the last decade the study of phenology has taken on a new legitimacy in the area of climate change research. A growing literature reveals that a change in the timing of natural events is occurring in a wide range of locations and affecting a wide range of species. Changes in spring have been those most commonly reported, with the emphasis on an advance in spring linked to an increase in temperature. Detection of change in autumn is hampered by a smaller pool of available data, events that are harder to define (such as leaf coloration), and various influencing environmental factors triggering autumnal phases. Despite this, the general pattern may be towards a delay in autumn. Plant, animal and abiotic responses, especially in spring, are quite similar. Thus, it would appear that winter is being squeezed at both ends, and this effect, of increasing the growing season, should become more pronounced in the face of predicted global warming. Copyright  2002 Royal Meteorological Society. KEY WORDS:

phenology; spring; autumn; climate change; temperature response; trends

1. INTRODUCTION Phenology can be described either as the study of natural events, or of biological events, in relation to climate (Schnelle, 1955). The former definition allows the study of ice events associated with high latitudes and continental climates (e.g. Magnuson et al., 2000; Sagarin and Micheli, 2001). In Europe, phenology has a history going back to the early 1700s and, as such, is probably the longest written biological data in existence (e.g. Sparks and Carey, 1995). In Japan, data stretch back to the eighth century (Lauscher, 1978). During the 100 years 1850–1950, phenology was universally popular with most developed countries having a scheme, usually with an emphasis on plant phenology and often coordinated by a meteorological agency or society (see Schnelle, 1955). In the subsequent 40 years there was a shrinkage of plant phenological activity towards central Europe. Within the last decade the scientific community’s view of phenology as a harmless pastime of natural historians has changed dramatically, because the value of phenological data in climate change research has been recognized (Menzel, 2002). Faced with the prospect of global warming, information has been needed about how natural systems may respond. Because of the volume of data, phenology has proved extremely useful in this respect. Examining how species have responded in the past to temperature gives clues as to how they may respond in the future to a warming planet. This has led to a resurgence of activity in examining existing data sets for evidence of change and for temperature response (Menzel and Estrella, 2001). It has also re-emphasized the value of long-term data, often collected at considerable effort in terms of time and money. The 1990s proved to be the warmest decade on record, and this has helped enormously in revealing how change has happened in recent decades. The low-tech approach offered by phenology is now being * Correspondence to: T. H. Sparks, NERC Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton, Huntingdon, Cambridgeshire PE28 2LS, UK; e-mail: [email protected]

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linked with the high-tech by comparing satellite observations with those on the ground (e.g. Duchemin et al., 1998, 1999). We believe that phenology is the most responsive aspect of nature to warming and the simplest to observe. While it is anticipated that global warming will affect species distributions, population sizes and community composition (Hughes, 2000; Parmesan et al., 2000; Walther et al., 2001), changes in these will be much harder and more expensive to detect. The timing of events is a very simple concept to understand and is popular with the general public and with the media. Phenology, therefore, is an ideal vehicle to demonstrate that warming may already be having an influence on the natural world. It also provides a means whereby the general public can get motivated to contributing to monitoring and discussing climate change issues. Its popularity is confirmed by its inclusion in existing and proposed lists of climate change indicators (e.g. Cannell et al., 1999; proposed also by the European Topic Centre on Air and Climate Change (ETC-ACC) of the European Environment Agency (EEA), personal communication). In recent decades there have been marked changes in environmental variables other than temperature, including the North Atlantic oscillation (NAO) (Jones et al., 1997), CO2 levels (Houghton et al., 2001), and nitrogen deposition levels. These, and other variables such as genetic adaptation, influence the timing of natural events, although temperature, either directly or indirectly, is by far the most influential. In this paper we provide examples of (i) the responsiveness of natural events to temperature using archive data and (ii) examples from a wide range of locations and covering a wide range of species demonstrating the extent of change in recent decades and how this relates to changes in temperature.

2. HISTORIC EXAMPLES To demonstrate the value of historic data we have selected examples of ground flora, bird migration, tree flowering, and harvest timing. Within Europe there is evidence of phenological recording from the early 1700s. While coordinated schemes did not get under way until the second half of the 19th century, many very useful data exist from an earlier period. One such data set, possibly unique in its longevity, is that of the Marsham family from Norfolk in the UK (Sparks and Carey, 1995). This record of spring events commenced in 1736 and continued until 1958. One of the recorded events was the flowering date of wood anemone Anemone nemorosa whose response over 154 years to early spring temperatures is shown in Figure 1. Regression analysis suggests that the response to a 1 ° C rise in temperature would be to advance flowering by 7 days. In contrast, an examination of data from the whole of the British Isles (Sparks et al., 2000) suggested that the wood anemone response was of the order of 4 days/° C. Wood anemone is one of a range of species that are present throughout much of Europe and, as such, may be a candidate for pan-European coordination of phenological monitoring. Ahas (1999) reported a trend towards earliness for wood anemone in Estonia (17 days earlier over 78 years) and that the trend varied according to region, being more pronounced in coastal areas than in the interior. For many countries, one of the most eagerly sought first signs of spring is the return of birds from their wintering grounds to their breeding territories. As with plants, there are records from the early 1700s including at least both the UK and Finland (Esa Lehikoinen, personal communication). For many of these series a correlation between arrival time and temperature is apparent, but this is typically only of the order of 2 days/° C, i.e. less than that for plants. Unlike plants, where a direct mechanistic response to temperature is likely, responses of birds to temperature is likely to be indirect through the availability of invertebrate prey. The influence of tail winds and the effect of temperatures en route remain largely unexplored, although Huin and Sparks (1998) demonstrated an influence of migration route temperature on the UK arrival date of the swallow Hirundo rustica. We are not convinced that we yet fully comprehend the magnitude of the historic data resource. It is still relatively easy to discover unexploited, often substantial, data sets that are residing as paper records in obscure locations. How much might have been destroyed in recent decades as being of little importance we do not know. Because early phenological work often fails to appear on electronic cataloguing, detection is labour intensive. The importance of preserving historical data is now being recognized, and there is a Copyright  2002 Royal Meteorological Society

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Jan-Mar mean temperature Figure 1. The relationship between flowering date of Anemone nemorosa in Norfolk, UK, and January–March mean temperature

growing urgency to ensure protection of early phenological data. As collaborating phenological researchers working with all the technical advantages of the early 21st century, we are deeply impressed by the extent of collaboration that was evident before World War II (e.g. Southern, 1938). If we go even further back we note that Professor Ihne of Darmstadt was collecting phenological data from European colleagues from the 1880s onwards. Figure 2 displays his collated data for pear Pyrus communis flowering in 1882 in relation to latitude. A latitudinal trend is very evident; the three-month span in dates through Europe suggesting flowering is delayed by 4 days for every degree of latitude. Current-day recording of production systems (forestry, horticulture, viticulture, agriculture) are only compatible if systems are relatively stable with respect to cultivar and management techniques. In Western Europe the turnover of wheat cultivars is so rapid that any examination of harvest records will need very careful interpretation. However, if we go back to the period before modern machinery and before intensive

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Latitude Figure 2. The relationship between latitude and flowering date of Pyrus communis in Europe. Data are from 1882 and cover locations from the Iberian Peninsula in the south to the Baltic in the north Copyright  2002 Royal Meteorological Society

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Mean May-July temperature Figure 3. The relation between harvest date in Sussex, UK, and mean May–July temperature

plant breeding activity these records may be valuable. Figure 3 is prepared from data abstracted from a graph displaying 141 years of harvest records from Sussex, UK, in relation to May–July mean temperature (Russell, 1921). From this it can be seen that a wide range of harvest dates, as large as 50 days, existed and that a very strong relationship with temperature is apparent: each degree warmer advancing the harvest date by 8 days. 3. CONTEMPORARY EXAMPLES 3.1. Plants Tree leafing and flowering dates are amongst the easiest to record because of the prominence of trees in the landscape. There are many examples of substantial records that continue until the current time. One of the most famous examples is the leafing date of horse chestnut Aesculus hippocastanum in Geneva, Switzerland (Defila and Clot, 2001). This has shown an extreme range of values from the latest, 23 April, to the earliest, 3 January. The general impression is of an advance of some 40 days over the two centuries of this record. It should be emphasized that the record is taken in an urban area and, therefore, is subject to warming associated with human activity (‘heat islands’). Roetzer et al. (2000) demonstrated that urban areas were, on average, 4 days earlier than their rural neighbours. Defila and Clot (2001) also report a long record for full flowering of cherry trees in Liesthal (1894–2000), where the change has been less prominent (latest appearance, 4 May; earliest appearance, 16 March). In Germany there are numerous long-term records of tree phenological phases. One of these concerns the flowering date of wild cherry Prunus avium at Geisenheim. Not only has this displayed a trend in recent years, but also a very strong relationship with early spring temperatures is evident (R 2 = 0.69) (Menzel and Testka, 2002) (Figure 4). This clearly demonstrates that most of the variability experienced in flowering date (about 40 days between earliest and latest recorded dates) can be accounted for by temperature. One series from Surrey, UK, has shown a remarkable trend towards earlier leafing of oak Quercus robur, which is now some 3–4 weeks earlier than in the 1950s (Cannell et al., 1999). A strong relationship with temperature is evident in this series, and this response has been shown to be nearly identical to the historic Marsham series (Sparks, 2000). Menzel and Fabian (1999) and Menzel (2000) have revealed a lengthening of the growing season by analysing the data from the International Phenological Gardens, a network currently of 49 gardens covering Europe based on cloned plant material. Here, we reproduce the summary of results for spring events (Figure 5), which emphasizes a trend towards earlier spring, particularly in central and northern Europe. Copyright  2002 Royal Meteorological Society

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year Figure 4. The relationship between flowering date of Prunus avium at Geisenheim and Frankfurt and February–March mean temperature (black line) at Frankfurt a.Main, Germany 300

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slope of trends [day / year ] Figure 5. Frequency of slopes of linear regressions (trends in days/year) for spring phases in the International Phenological Gardens (1959–1996; only records with more than 20 years of observation included) (after Menzel and Fabian, 2001) Copyright  2002 Royal Meteorological Society

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In North America, the limited number of articles point towards a trend towards earlier events. In Canada, Beaubien and Freeland (2000) have gathered together data on the first flowering date of aspen poplar Populus tremuloides. This has shown a marked trend towards earlier flowering: 26 days earlier over the period 1900–1997. Schwartz and Reiter (2000) reported a trend towards earlier phenology of lilac from across the USA. Bradley et al. (1999) reported that the majority of events in Wisconsin had a negative trend over time (i.e. earlier) and there is a clear pattern with a greater response for events earlier in the year than for later ones. This feature is repeated many times. The analysis of first bloom of lilac and honeysuckle data in the western USA by Cayan et al. (2001) revealed earlier spring onsets since the late 1970s, which reflects the unusual spell of warmer-than-normal springs during this period. Abu-Asab et al. (2001) reported that 89 of 100 species examined in the Washington, DC, area had developed earlier in a 30 year period and the overall pattern was of an advance in direct correlation with temperature increases. This paper also provides data that demonstrate that early events tend to be more variable than those later in the year (Figure 6). This feature is also evident in many other data sets (e.g. Roetzer et al., 2000; Menzel et al., 2001). It is not only terrestrial species and not only first events that are occurring earlier. In Cumbria, UK, a long-term record on the peak bloom date of the algae Asterionella has shown an advance of some 30 days over the last 30 years (Stephen Maberly, personal communication). 3.2. Birds There is evidence that birds are also responding to warmer conditions by having earlier phenophases. This relationship is despite the fact that the phenology of animals tends to be more variable than that of plants. The Cambridge naturalist Leonard Jenyns recognized this over 150 years ago, when he wrote ‘. . .the appearance of birds and insects. . . cannot be watched with the same exactness as plants’ (Jenyns, 1846). To counter this problem there are extensive data relating to the arrival dates of birds, as these are seen as traditional harbingers of spring and there is far greater interest in birds than most other aspects of natural history. The pattern seen for plants, that earlier events are more variable, is also repeated in observations of bird migration (e.g. Tryjanowski et al., 2002). A temperature response in bird migration timing has been reported from across Europe, e.g. UK (Sparks and Mason, 2001), Russia (Sokolov et al., 1998), Poland (Tryjanowski et al., 2002), Slovakia (Sparks and Braslavská, 2001), and Bradley et al. (1999) summarize some changes in Wisconsin, USA. An example of the change in recent times is provided by the arrival dates of the sand martin Riparia riparia in Essex,

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Mean date (day of year) Figure 6. The relationship between variability and mean flowering date for 100 plant species in the Washington, DC, area, USA. Derived from data tabulated in Abu-Asab et al. (2001) Copyright  2002 Royal Meteorological Society

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Year Figure 7. The arrival dates of sand martin in Essex, UK (after Sparks and Mason, 2001)

UK (Figure 7). This is now some 20 days earlier than it was 50 years ago, and a strong response to March temperature of 4 days/° C is apparent. This is greater than that recorded for many bird species, and there is a suggested differential response between species that may lead to changed competition for resources. This was also evident in Poland, where the advance of short-distance (European) migrants was more marked than that for long-distance (African) migrants (Tryjanowski et al., 2002). There is also substantial evidence of changes to breeding times of birds in relation to temperature. As with migration timing, this is probably an indirect response through the altered availability of invertebrate food items, whose development times are shortened under warmer conditions (see later). Crick and Sparks (1999) report the majority of species examined in the UK to be nesting earlier and a high degree of correlation with temperature. Both and Visser (2001) and Koike and Higuchi (2002) give strong evidence for temperaturerelated advances in nest timing in single species in the Netherlands and Japan respectively. There is evidence that changes in bird arrival and hatching in pied flycatcher Ficedula hypoleuca in northern Germany correspond well to plant phenological phases in spring. Both are correlated with spring air temperature and the NAO of spring months (Figure 8). In contrast, in the Netherlands, Both and Visser (2001) detected a trend towards earlier nesting in pied flycatcher but not in earlier arrival, and suggested that the former was constrained by the latter. A great deal more work remains to be done on the interrelationships between the phenologies of birds, invertebrates, and plants. 3.3. Insects Virtually all the UK butterfly fauna seem to have already been affected by warming. Trends to earlier first and peak appearance have been noted, and flight periods have been lengthened in multibrooded species, suggesting additional generations achieved in a year, and most of this correlates well with temperature (Roy and Sparks, 2000). In the Netherlands, Ellis et al. (1997) have reported an average 11 day shift in peak flight dates of micromoths over a 20 year period. Changes in insect timing can be very marked: Zhou et al. (1995) reported that a 1 ° C increase in temperature could advance aphid migration by up to 19 days. Despite the huge number of species, there are few recording schemes that supply phenological data on insects. In the south of the UK, there are some suggestions of earlier activity of hoverflies (Morris, 2000). The influence of climate on invertebrates is an area where we anticipate that a great deal more research will be published in the coming decade. Copyright  2002 Royal Meteorological Society

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May shoot of Picea abies flowering of Forsythia NAO (FebMar)

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spring arrival in birds flowering of Galanthus nivalis

Figure 8. Selected phenological spring phases and spring air temperature and NAO of corresponding months in Germany (plant phenological data and temperature data from the DWD; NAO index from Jones, http:/www.cru.uea.ac.uk/cru/data/nao.htm; hatching in pied flycatchers from Bairlein and Winkel (2001); spring arrival from Institute for avian research, Dr O. Hüppop, unpublished)

3.4. Autumn We would anticipate that warmer autumns would lead to earlier fruit ripening but delayed leaf senescence. In contrast to spring, there is much less information available on autumn phenology for both plants and animals. Autumn plant events also tend to be more difficult to define and are subject to sudden individual weather events such as a single frost or high winds. What data are available suggest a delay in autumn events in recent years. Menzel (2000) and Menzel and Fabian (2001) summarized the autumn responses from the International Phenological Gardens (Figure 9), where the trends towards lateness are more marked for central and southern Europe. Indeed, there is some localized evidence from the Kola Peninsula in arctic Russia that autumns may be advanced in the face of slightly colder autumn weather (Kozlov and Berlina, 2002).

4. DISCUSSION There is evidence from a wide range of taxa and across a wide range of geographic locations that events in spring have been happening earlier in recent decades. It is also obvious that the changes have been most profound in those events which occur earlier in the year. This does not mean that later events are unaffected by temperature and are unchanging under climate warming. Rather, it emphasizes that the changes in temperature experienced so far have been more pronounced in the winter and early spring period. Looking at year-to-year variability, it is also apparent that early events are generally more variable than those later in the year, and this reflects on the greater variability in temperatures which influence those events. As an example of the variability in monthly temperatures, the standard deviations of the central England temperature series 1951–2000 for the months January–March range from 1.5 to 2.0 ° C (mean 1.8 ° C) compared with those for April to September, which range from 1.0 to 1.3 ° C (mean 1.1 ° C). Yet, despite this inherent greater variability, there are numerous examples of the detection of significant trends towards earliness. It is also apparent that the length of the series and its start and end dates are critical in determining whether trends can be detected. Thus, series that include the whole of the 1990s benefit from that decade being the warmest on record. This influences earlier phenology and enhances the likelihood of detecting trends. In contrast, series ending a decade earlier will not have been so lucky. Though it is obvious, it is worth Copyright  2002 Royal Meteorological Society

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slope of trend [day / year] Figure 9. Frequency of slopes of linear regressions (trends in days/year) for autumn phases in the International Phenological Gardens (1959–1996; only records with more than 20 years of observation included) (after Menzel and Fabian 2001)

re-emphasizing that it is easier to detect trends in longer time series and we recommend that 20 years be considered as the minimum acceptable length for detection of change. A good example for the influence of the length of the record analysed is given by Scheifinger et al. (2002). For one site, he determined the slopes of linear regression of all possible time periods within 1951–1998. Only those time series ending in the 1990s reveal strong advancing trends. Some changes already experienced have been very marked despite the relatively modest warming so far. This suggests that we need to seek additional information to explain the magnitude of such changes. This may include the need for daily data, minimum and maximum rather than mean temperature, grass and soil temperatures, the degree of urbanization of a site, and the consequences of elevated CO2 , ozone, atmospheric nitrogen, and other pollutants. Alternatively, we may be too na¨ıve in believing that the response to temperature is linear and that within part of a species temperature range a relatively modest temperature increase can result in a big change in phenology. Phenology is very simple to record and is very responsive to temperature. But, ultimately, it is not the timing that is our main interest. We want on know what the consequential effects of earlier phenology may be to production (in agriculture, horticulture, viticulture, and forestry), on human health (e.g. through earlier pollen release and insect infestations), and on the distribution of species, their community composition, and their life cycles following climate warming. A changing phenology does not just affect wildlife; it may have serious economic and social implications. REFERENCES Abu-Asab MS, Peterson PM, Shetler SG, Orli SS. 2001. Earlier plant flowering in spring as a response to global warming in the Washington, DC, area. Biodiversity and Conservation 10: 597–612. Ahas R. 1999. Long-term phyto-, ornitho- and ichthyophenological time-series analyses in Estonia. International Journal of Biometeorology 42: 119–123. Copyright  2002 Royal Meteorological Society

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Schwartz MD, Reiter BE. 2000. Changes in North American spring. International Journal of Climatology 20: 929–932. Sokolov LV, Markovets MYu, Shapoval AP, Morozov YuG. 1998. Long-term trends in the timing of spring migration of passerines on the Courish spit of the Baltic sea. Avian Ecology and Behaviour 1: 1–21. Southern HN. 1938. The spring migration of the swallow over Europe. British Birds 32: 4–7. Sparks T. 2000. The long-term phenology of woodland species in Britain. In Long-term Studies in British Woodland, Kirby KJ, Morecroft MD (eds). English Nature Science Series, vol. 34. English Nature: Peterborough; 98–105. Copyright  2002 Royal Meteorological Society

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Sparks TH, Braslavská O. 2001. The effects of temperature, altitude and latitude on the arrival and departure dates of the swallow Hirundo rustica in the Slovak Republic. International Journal of Biometeorology 45: 212–216. Sparks TH, Carey PD. 1995. The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. Journal of Ecology 83: 321–329. Sparks TH, Mason CF. 2001. Dates of arrivals and departures of spring migrants taken from Essex Bird Reports 1950–1998. Essex Bird Report 1999 154–164. Sparks TH, Jeffree EP, Jeffree CE. 2000. An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. International Journal of Biometeorology 44: 82–87. Tryjanowski P, Ku´zniak S, Sparks T. 2002. Earlier arrival of some farmland migrants in western Poland. Ibis 144: 62–68. Walther G-R, Burga CA, Edwards PJ (eds). 2001. “Fingerprints” of Climate Change — Adapted Behaviour and Shifting Species Ranges. Kluwer Academic/Plenum Publishers: New York. Zhou XL, Harrington R, Woiwod IP, Perry JN, Bale JS, Clark SJ. 1995. Effects of temperature on aphid phenology. Global Change Biology 1: 303–313.

Copyright  2002 Royal Meteorological Society

Int. J. Climatol. 22: 1715–1725 (2002)