Phenology

Alison Donnelly

Phenology is a branch of science focused on the timing of growth and development of plants and animals and the relationship with climate. In temperate latitudes, where Ireland sits, a rise in temperature in spring triggers the growth and development of many organisms across the country. Dormant buds develop into leaves on deciduous trees, birds, such as swallows and swifts, return from sub-Saharan Africa where they spend the winter and caterpillars emerge from their protective cocoons where they spend the cool winter months. These seasonal biological events, also called phenophases, occur at roughly the same time every year and are activated by environmental conditions, in particular, rising temperature. Similarly, in autumn, decreasing temperature and shorter days, trigger leaves to lose their colour and fall to the ground, migratory birds depart to warmer climates and some small animals, such as hedgehogs and bats hibernate. Also in autumn, birds, such as the Whooper swan, arrive from colder climates, like Iceland, to spend the winter in Ireland and later return to their breeding grounds further north in spring when temperatures in Iceland are less hostile. Other common examples of phenophases include, the date of flowering of shrubs and trees, the date of pollen release, the first flight date of butterflies and moths, the date of egg-laying of birds, the date of tadpole emergence, etc.

A brief history of phenological monitoring

This scientific discipline of phenology has a long history, as knowing when and how plants respond to seasonal changes in climate was important to early farmers. Understanding how climate influenced the life-cycle of crops meant they knew the best time to plant seeds to ensure high yields. Early records of phenological events provide clues to seasonal temperature. The date of the Japanese cherry blossom festival can be traced back more than 1,200 years while the harvest dates of grapes, in France, was recorded by monks as far back as 1370. Since 1736, the UK naturalist, Robert Marsham, systematically recorded the first dates of a range of activities in his garden in Norfolk, including, budburst and flowering of plants and trees, emergence of insects, arrival of migratory birds, etc. Subsequently, his family continued to record these ‘in- dications of spring’ up until 1958. Robert Marsham is considered to be the founder of modern day phenological monitoring. Together, these long-term records of phenology have proven invaluable in tracking the impact of current climate change on natural ecosystems as the data can be related to variations in temperature and other climatic parameters. The date of the cherry blossom festival in Japan was determined by spring temperature – so when the festival was early in spring the temperature was relatively warm and vice versa. A relatively late date for grape harvest indicated a relatively cool summer. Similarly, a gradual earlier date of oak leaf out dates between 1850 and 1950 from the Marsham records tracks a corresponding warming of the climate.

Establishing phenology networks around the world

Given the usefulness of long-term phenological observations in detecting changes in the natu- ral environment a number of phenological networks have been established around the world. One of the earliest networks was the International Phenologial Gardens (IPG) established by the German Weather Service in the 1950s. They distributed a number of genetically identical trees, such as beech, birch, poplar and cherry, to more than 50 locations throughout Europe and the timing of a range of phenophases, such as budburst, leaf unfolding, flowering, fruiting, leaf colouring and leaf fall, were systematically recorded each year. Today, the Pan European Phenology project, focused on plant phenology, collects data from across Europe. The USA-National Phenology Network collects, stores and makes freely available phenological data on all types of organisms from across the US. There are many other similar networks in Cana- da, Australia, China and a very recently established network in Africa. The importance of these networks can be gauged by the increasing number of scientific publications citing their data.

Phenological recordings began in Ireland in the 1960s as part of the IPG network. Four sites were established by Dr. Austin Burke, former director of the Irish Meteorological Service, in cooperation with the National Botanic Gardens, the Department of Agriculture and Dr. F Schnelle of the German Weather Service. These gardens were located at Valentia Observatory, Co. Kerry; JFK Arboretum, New Ross, Co. Wexford; JohnstownCastle also in Co. Wexford and the National Botanic Gardens, in Dublin. Two additional IPGs have been established in recent decades, the first in Armagh Observatory (2003) and the second in Glenveagh National Park, Co. Donegal (2007). Observations are made using a standard protocol, and up until 2006, Met Éireann managed the collection and submission of observation data after which Humboldt University rolled out their data submission web interface. Little attention was paid to analyzing the Irish data until relatively recently. In 2001 a study on ‘Indicators of Climate Change’ was commissioned by the Irish Environmental Protection Agency and renewed interest in phenological data was established as the relationship between spring phenophases and spring temperature was recognized. The data from the Irish IPG sites were used as an indicator of spring warming in Ireland and also contributed to a study which showed that phenological events closely matched climate warming across Europe. The importance of phenological research as a tool by which to determine and communicate the impact of climate change on ecosystems was demonstrated by the inclusion of European phenological data in the IPCC (Intergovernmental Panel on Climate Change) 4th Assessment Report on Impacts, Adaptation and Vulnerability (2007) thus illustrating the strength of these data in convincing policy makers that climate change was having a detectable impact on the environment.

Phenology and climate change

When spring temperature is warmer than usual, the timing of phenophases such as, leaf-out and flowering of trees and shrubs, arrival of migratory birds, and insect activity can be ob- served earlier in the season than expected. Likewise, when spring temperature is cooler than usual these events are delayed and occur later in the season. Therefore, the timing of pheno- phases is very sensitive to climate and responds to changes in temperature by occurring earlier or later in the season. This sensitivity to temperature coupled with the fact that these events are easy to observe and monitor make them ideal indicators of climate change.

It is well established that climate change is resulting in rising temperatures, which in turn is causing many plants and animals around the world to be active earlier in spring. Initially, this may sound like it would be beneficial but it also increases the risk of damage from late frost events. A number of fruit growers have reported earlier flowering of trees in recent years but that severe frost damages the delicate flowers resulting in significantly reduced yields in late summer.

Analysis of the data from the IPGs network of sites across Ireland revealed that many of the tree species are leafing-out earlier now than when monitoring began in the 1960s. For example, birch, beech, poplar and small leaf lime, all common deciduous trees in the Irish landscape, were leafing out on 23, 30, 28 and 30 April respectively in the late 1960s whereas in recent years they are now leafing out on 30 March, 20 April, 22 April and 17 April respectively. This results in an earlier leafing of 3 weeks, 10 days, 6 days and 2 weeks respectively. These results are very interesting and show clearly that not all species are responding to spring warming at the same rate, which is to be expected as all species behave differently. However, it indicates that the gen- eral trend for deciduous species is for earlier leafing. These earlier dates for leaf unfolding are driven by rising spring temperatures as a result of climate change.

In addition to evidence from trees, birds and insects have also been impacted by rising spring temperature. Over a 40-year period (1967-2004), the timing of leaf unfolding of a suite of deciduous trees advanced by up to 3 weeks, as mentioned above. Furthermore, the arrival time of a selection of sub-Saharan migrant birds also advanced significantly over the period 1969-1999, while the timing of spring departure of a short-distance winter visitor, the Whooper Swan was also significantly earlier. Likewise, sightings of a range of moth species across the country have become significantly earlier since records began in 1980 indicating earlier emergence times.

Even though an earlier start to spring has been established for each of these groups of organisms there has, as expected, been considerable variation in phenological response to temperature. Studies have shown that not all groups responded to the same environmental stimulus (i.e. rise in temperature) at the same rate. The need to understand an ecosystem-wide response to rising temperature has guided studies towards examination of the timing of key pheno- phases between interdependent species. For example, any mismatch in phenology between a predator and its food source owing to differing abilities to respond to rising temperature could have far-reaching implications throughout an ecosystem. Mismatch occurs when a dependent partnership is disrupted resulting in partial or complete trophic decoupling, any such decou- pling of food web phenology may result in a change in species composition. For example, moth caterpillars feed on newly emergent leaves for food and migratory birds depend on moth caterpillars as their primary food source. If caterpillars emerge before leaves have unfolded, a mismatch between the food source and caterpillars will develop and many caterpillars will perish. Furthermore, if birds arrive after the peak timing in availability of caterpillars, a mismatch between the food source and when it is needed will develop, fewer chicks will survive and more leaves will be consumed by the caterpillars. There are many other examples of partnerships that may be disrupted by rising temperature, for example, between plants and pollinators, predators and prey, and host and parasites. Predicting how this intricate web of synchrony/asynchrony may respond to further increases in temperature is clearly a challenging task. There will be winners and losers across all ecosystems and a change in species composition is inevitable but exactly which species will dominate remains to be seen.

Timing of the pollen season

Many trees, grasses and wildflowers produce allergenic pollen from spring right through to autumn, which causes misery to many hay fever sufferers. Across Europe, the pollen season is starting 10 days earlier than in the 1960s and has become more intense which has major im- plications for those who are allergic to grass and tree pollen. This earlier start to pollen release is directly related to warmer temperatures in spring and has resulted in a longer pollen season. As temperatures are expected to continue to warm in the coming decades the spring season is predicted to get earlier which will have further consequences for hay fever sufferers.

Phenology has a long history and, in recent decades, has proven to be an invaluable indicator of anthropogenic climate change. It is a simple and effective communication tool as the underly- ing principles are easy to understand. Therefore, it will be important to keep monitoring wild- life phenology to help identify which species and ecosystems may be at greatest risk of climate change.

Alison Donnelly, Associate Professor of Geography at the University of Wisconsin-Milwaukee, USA