PHENOLOGY IN A CHANGING CLIMATE

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PHENOLOGY IN A CHANGING CLIMATE TIM SPARKS, PHIL CROXTON AND NICK COLLINSON Introduction The word “phenology” isn’t familiar to the general public. However, it is probably known by naturalists and has been in use for over 150 years.

Phenology, for those that don’t know, is the study of the timing of natural events. Since it is an –ology, Maureen Lipman would class it as a science. So would we.

The collection of the dates when things happen, such at the first flowering of plants, the first swallow of spring and the first frog spawn, has a long history and isn’t just a trait of the British. In Britain the oldest records we are aware of date back to 1703. The systematic collection of phenological records commenced in 1736 when Robert Marsham of Stratton Strawless in Norfolk began to collect 27 indications of spring; generally flowering, leafing and migration dates. After his death, successive generations of the same family continued to take these observations until 1958. Elsewhere in the World, some records are astonishingly long. The Chinese have peach blossom records going back to the sixteenth century, there are some grape harvest records in Europe going back to the 1400s. But the oldest we know of are the cherry flowering records of Kyoto, the former Japanese capital, which date back to 705 AD. Phenological recording began to get organised in the late Victorian period.

In Britain, the Royal Meteorological Society started a coordinated scheme in 1875 which was to run until 1947. In Germany, Professor Hoffman of Giessen started a compilation of records of plant phenology from across Europe in 1883 that continued until the Second World War. In 1905 the British Naturalists’ Association started to report phenology, and still does. After the Second World War, large scale phenological recording ended in Britain but was started up by the Hydrometeorology Institutes of many countries, including the Czech and Slovak Republics, Germany, Austria, Slovenia and Switzerland.

Recent long-term records of phenology in Britain have been largely uncoordinated, and undertaken independently by individuals. Foremost in this category may be the late Richard Fitter who recorded the first flowering of several hundred plant species from 1954 to 2000. For migrant birds, regular observations of first arrivals are undertaken by bird observatories and through county bird reports, such as the Suffolk Bird Reports. These tend not be centrally coordinated or routinely analysed.

Phenological data can also often be derived from schemes which are principally devised to monitor populations. These include the many BTO schemes, such as the Nest Record Scheme, and monitoring of butterfly, moth and aphid populations. Such schemes were not devised with phenology in mind, but phenology has become a useful by-product.

In 1998 the UK Phenology Network was started with the aim of a creating a large scale network of phenology recorders and also to preserve as much historical data as possible. The UKPN is jointly run by the Woodland Trust and the Centre for Ecology and Hydrology. We seek to engage people in recording in their own environment in separate spring and autumn campaigns.

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Table 1. A summary of the phenological records of Orlando Whistlecraft from Thwaite, Suffolk 1819–1864 Mean Range SD Response R2 date Earliest Latest (days) (days) (days/°C) (%) Hawthorn leaf Horse chestnut leaf Sycamore leaf Cuckoo sang Willow leaf Cowslip flower Tall poplar leaf Maple leaf Hawthorn flower Oak leaf Wych elm leaf Ash leaf Dog rose flower Suffolk harvest began Suffolk harvest finished

30 Mar 13 Apr 15 Apr 17 Apr 18 Apr 19 Apr 30 Apr 4 May 14 May 14 May 16 May 17 May 7 Jun 4 Aug 1 Sep

26 Feb 20 Mar 16 Mar 6 Apr 14 Mar 13 Mar 4 Apr 6 Apr 30 Apr 26 Apr 28 Apr 28 Apr 24 May 18 Jul 12 Aug

25 Apr 2 May 4 May 29 Apr 14 May 17 May 25 May 21 May 5 Jun 1 Jun 5 Jun 3 Jun 22 Jun 17 Aug 19 Sep

58 43 49 23 61 65 51 45 36 36 38 36 29 30 38

13Â4 10Â0 10Â8 5Â4 13Â0 14Â8 12Â3 12Â2 9Â3 9Â6 10Â2 9Â0 7Â4 7Â4 9Â3

-9Â0 -5Â8 -8Â0 -4Â3 -7Â6 -8Â5 -7Â7 -6Â3 -8Â6 -6Â8 -7Â1 -6Â3 -4Â9 -5Â7 -5Â2

57Â9 35Â5 54Â1 57Â0 32Â6 32Â4 33Â4 21Â8 59Â5 37Â8 38Â9 35Â6 26Â2 54Â1 31Â9

For each of the 15 events the mean, earliest and latest dates are given. Events are arranged in order of increasing mean date. The range of dates from earliest to latest and the standard deviation (SD) of dates are given in the subsequent two columns.

The final two columns indicate by how much each event responded to a 1°C increase in temperature in the three months up to and including the month in which the mean occurred, and a measure (R2) of how well the timing of the event could be explained by these three months’ temperatures.

Data can be recorded on record sheets, but we prefer the speed and efficiency of online recording (at www.phenology.org.uk).

We are aware of more phenological records from Norfolk than from Suffolk, but hope that this article will encourage readers to correct this balance by informing us of long term records that we are currently unaware of. In this article we provide examples from three Suffolk sources and reveal how these can tell us which species are sensitive to climate. These species should be those that have shown most change in recent years as British temperatures have slowly increased. They will also tend to be the species that will change most in the future as the temperature increases become more pronounced.

Orlando Whistlecraft We know little of this gentleman, other than he kept records at Thwaite in Suffolk from 1819–1864. His records were published in 1926 in the Quarterly Journal of the Royal Meteorological Society (Margary, 1926). His records involve nine first leafing events, three first flowering events, the first cuckoo of spring and the beginning and end of harvest (“in Suffolk generally”). A Trans. Suffolk Nat. Soc. 42 (2006)

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summary of his observations is given in Table 1. We can learn a lot from historical records such as these. For instance we can see that early spring events are more variable, sometimes called more phenologically plastic, than later spring events and there is some suggestion (albeit based on only two events) that autumn records become more variable again (Figure 1). The event that doesn’t fit well in this pattern is the only zoological event; the first cuckoo. The overall pattern is very encouraging as it is one we still see in modern observations from the UK and across Europe.

The final two columns of Table 1 are based on multiple regression of the Whistlecraft data against monthly Central England Temperatures for the three months up to and including the month in which the mean date occurred. Each event shows a good response to temperature which in every case, except maple leafing (p = 0Â015), is significant at p<0Â01. In each case increased temperature is associated with earlier phenology; so, for example, a 1°C increase in temperature would be associated with a 9 day advance in hawthorn leafing.

Responsiveness ranges from about 5 days earlier to about 9 days earlier for a 1°C increase in temperature. It is interesting to note that the early spring events are the most responsive (Figure 2), which is, to some extent, to be expected from the variability shown in Figure 1.

It is likely that this differential responsiveness arises because the species need to be adaptive to their own environment. Figure 3 shows that temperatures are more variable in the early and late months of the year.

Species whose development is dependent on temperatures in these months must have flexibility in order to survive.

standard deviation of dates

15 14 13 12 11 10 9 8 7 6

cuckoo

5 100

150

200

250

mean date (day of year) mean date (day of the year) Figure 1. A plot of standard deviation against mean date for the Whistlecraft records.

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response to a 1°C increase in temperature

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-5

-6

-7

-8

-9 100

150

200

250

meanmean datedate (day of year) (day of year)

standard deviation of temperatures

Figure 2. The predicted response of the 15 Whistlecraft events to a 1°C increase in temperatures in the three months up to and including the month in which the mean date occurred.

month Figure 3. Year-to-year variability (as measured by standard deviation) in monthly Central England Temperatures 1819–1864.

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The Whistlecraft harvest records correlate very highly (r>0Â8, p<0Â001) with contemporary records from Surrey and Sussex (Sparks et al., 2005).

It may come as a surprise that cuckoo appears to be correlated with temperatures in the UK. On first reflection this may appear odd since one might anticipate a greater influence of African and migration route temperatures. However, there are several reasons why UK temperatures are important. Warm springs will encourage the invertebrates on which the species depends. Warm springs in the UK tend to be warm across Europe and will give the cuckoo some advance notice of UK conditions. Warm springs are also associated with warm southerly airstreams which will aid migration from the south.

Lottie Riches From Lottie Riches’ diaries, currently held by the Ipswich Natural History Society, we have abstracted all phenological records. During 1942–1981 these relate to records whilst she was living in Ipswich. For this article we abstracted events for which at least 20 years of data were available. Some events appear to be poorly defined since they are highly variable, so we also eliminated events with a standard deviation greater than 25. This will eliminate events with a range of dates of 100+ days. These may include insect records where the first brood may have been overlooked in some years. This leaves 46 events to assess.

Table 2 summarises these records. About one third of the bird and insect events show a significant relationship with temperature whilst that figure is much higher for plants (>80%). The response to temperature also differs between taxonomic groups, appearing much higher for insects and plants. This may reflect the fact that these species are resident throughout the year whilst many of the bird events are of migratory animals that spend part of the year in other countries. However, as we saw with the Whistlecraft cuckoo record, some of the migrant bird events are correlated with temperature. Figure 4 shows the Riches’ sand martin records against April temperature. It is also interesting to note that sand martin is one of the species that shows a consistent advance in recent years across the UK, as would be expected by a temperature responsive species in a warming climate.

Table 2. A summary of Lottie Riches’ records 1942–1981 by three different taxonomic groups.

No. of events Birds Insects Plants

26 6 14

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No. of significant Mean response responses to (days/1°C) temperature 9 2 12

-3Â3 -9Â2 -7Â1

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date first seen

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April temperature

date first seen

Figure 4. Lottie Richesâ&#x20AC;&#x2122; sand martin observations plotted against April Central England Temperature.

March temperature Figure 5. Lottie Richesâ&#x20AC;&#x2122; bumblebee observations plotted against March Central England Temperature.

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January–March temperature Figure 6. Lottie Riches’ blackthorn flowering observations plotted against January–March mean Central England Temperature.

Figure 5 shows a similar pattern for bumblebee and Figure 6 a very strong relationship for blackthorn flowering. Using older and historical records such as these and the Whistlecraft records gives us a very good idea about which species are good to monitor. If a species is temperature responsive then we would expect its phenology to accurately reflect changes in temperature. From Figure 6 we can see that we would expect blackthorn flowering to be a very good indicator since the relationship with temperature is extremely tight. In practice, blackthorn flowering is indeed a very good phenological event to monitor, providing that there is no confusion with cherry plum, Prunus hybrids, or hawthorn!

At the UK Phenology Network we are always pleased to learn of additional long term records such as these, especially if they are of ten years duration or longer. If any reader knows of such records and is willing to let us add them to our database, then please get in touch.

Suffolk Bird Reports We have recently abstracted the arrival and departure dates from the Suffolk Bird Reports. Since we intend to publish the analyses of these data in the Report here we only give a taster of what will be in that article.

We thought it would be interesting to examine sand martin arrivals since Lottie Riches’ records suggested that this was a temperature responsive species. Figure 7 confirms the earlier arrival of sand martin in Suffolk (p<0Â001) and a comparison with temperatures in January, February and March suggests that the species responds to a 1°C increase in temperature by arriving some 4Â9 days earlier (p<0Â001).

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first observation date

A species of a very different habitat, the tree pipit, also shows considerably earlier arrival in recent years (Figure 8, p<0Â001). A comparison with temperatures in February, March and April suggests that the species responds to a 1°C increase in temperature by arriving some 4Â4 days earlier (p<0Â01).

year

first observation date

Figure 7. Sand martin first observation dates 1950–2002 as reported in the Suffolk Bird Report.

year Figure 8. Tree pipit first observation dates 1950–2002 as reported in the Suffolk Bird Report.

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Conclusions The British passion for collecting records has left us with a legacy that we can examine for signs of change in the natural world as a consequence of a warming climate. Records of any age can be examined to see if they provide evidence that species are responsive to temperature. From the results presented here we know that not all species respond at the same rate, for example early spring species seem to be most responsive. This gives us information on which species we should monitor. But the differential response between species also warns us that essential synchronisation within communities and within food webs are not guaranteed. Already we are being warned of serious disruption as a consequence of differentially changing phenology.

Older records also provide us with a baseline against which we can assess current phenology. For example, the average first flowering date of hawthorn in Suffolk in ten of the years between 1930 and 1941 was May 11, in the last seven years (1998–2005) it has been April 28. A t-test on annual average dates would tell us that it is now flowering significantly earlier (p = 0Â002). Where we have records of several decades duration that are still being maintained then we can easily see how much change has already occurred. Records like those of Richard Fitter and others clearly show an advancing phenology in recent decades as temperatures, particularly in the winter and early spring period, have risen. Phenological changes are much easier to detect than distributional, community or population change and yet may forewarn us of changes in these.

Acknowledgements We would like to thank all those who contributed to collecting the records reported here.

References Margary, I. D. (1926). The Marsham phenological record in Norfolk, 1736– 1925, and some others. Quarterly Journal of the Royal Meteorological Society, 52: 27–52.

Sparks, T. H., Croxton, P. J., Collinson, N. & Taylor, P. W. (2005). Examples of phenological change, past and present, in UK farming. Annals of Applied Biology, 146: 531–537.

Tim Sparks and Phil Croxton† ‡ †NERC Centre for Ecology and Hydrology Monks Wood Abbots Ripton, Huntingdon Cambridgeshire PE28 2LS e-mail: ths@ceh.ac.uk Nick Collinson‡ Woodland Trust Autumn Park Dysart Road Grantham Lincolnshire NG31 6LL ‡

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