Phenomena in phenology and population dynamics

Phenology models and techniques

Among the phenology models and techniques, plant development models are considered as the most important. The history of these models dates back to 1735 and is associated with Reaumur. Reaumur recorded the dates of different phenophases and the mean temperatures of arbitrary days of a given phase.

A great upswing in modelling could have been observed in the 20^th century, along with the development of computer science and the growing popularity of analyses related to climate change. Most predominantly the correlation of increase n temperature and the changes in phenophases has been studied. Most phenology models are able to predict budburst, flowering and fruit maturation, but no model can predict the date of canopy leaf coloration so far.

Reaumur observed that grain and grape was harvested later in 1735 when the heat sum in April, May and June had been lower than in the year of 1734. Hence, he deducted that plants grains develop faster if the temperature is higher in the period between sowing and harvest, and grapes develop faster if the temperature is higher in the period between flowering and harvest.

Phenology models can be classified into 3 main types:

• theoretical models: in case of the leaves produced by the plants, these models are based on a cost/benefit ratio.
• statistical models: study the correlations between climatic factors and the time of phenophases. E.g. the Spring index model (Schwartz and Marotz 1986, 1988; Schwartz 1997) considers the heat degree days, mean temperatures, intensity and the number of synoptic weather phenomena.
• mechanistic models: describe plant phenology with the known or assumed “cause-effect relationships“ between biological processes and key driving variables. E.g. the spring warming model contains also the development rates along with mean temperatures and heat sum. However, this model has a fundamental problem: our knowledge on the biochemical and biophysical processes taking place in the dormancy periods are quite incomplete.

Importance of plant phenology models:

• prediction of impacts of global warming on wild and cultivated plants
• improvement of crop productivity models
• forecasting the presence of pollens for people suffering in allergic disorders
• forecasting frost damages for foresters and farmers.

Impact of climate change on the growth of forests is described by the FORGRO (Forest Growth) model. This model simulates tree growth, productivity (Mohren 1987) and considers the phenophases appearing at the end of the vegetation period (Vesala et al. 1998). The increase of CO₂ and temperature in the model impact the processes in forest trees.

Models describing the life-cycles of animals primarily deal with ectotherm (cold-blooded) animals, since the adaptation of endotherm (warm-blooded) animals to different seasons or periods is not so definite (Régnière et al. 2003). These models also include temperature-dependent models that describe the correlation between the development of insects and temperature (Logan and Powell 2001).

The four factors affecting the climate of a given unit of territory are as follows: geographical latitude, elevation above sea level, continentality and the layout of local circulations (Bolstad et al.)

There are also daily weather generators that depict realistic data on daily rainfall, insolation, monthly mean temperature and precipitation. These also simulate extreme impacts like drought and frost.

The paper of Brügger (2003) is about the phenological variations of forest trees. PEI (Phenological Emergence Index) gives an estimation of spring sprouting and autumn colouration of the leaves. Phenophase indicates which development stage the plants have been observed in. Different phenological development stages mark distinguishable processes when a special morphological structure is developed. Development of Fagus sylvatica and Picea abies has been studied in Swiss forests between 1990 and 1999. It has been found that colouration and fall of leaves is affected by temperature, photoperiod, precipitation, drought and also the wind. Sprouting of beech leaves took 1-19 days, colouration 6-36 days.

BBCH scale determines the phenological growth stage in case of mono- and dicotyledonous plants (Meier, 2003). The scale contains 99 codes classified into groups of 10’s. Code 00 marks seed stage before the plant starts to sprout; code 99 is for postharvest operations and storage.

Groups of the BBCH scale are as follows:

• 00-09: Germination, bud development and sprouting. Code 07 marks the stage of the beginning of sprouting or bud breaking; code 09 marks the stage when the bud shows its green tips.
• 10-19: Development of the leaf.
• 20-29: Formation of shoots.
• 30-39: Stem elongation or rosette growth, shoot development (main shoot).
• 40-49: Harvestable vegetative plant parts or vegetatively propagated organs begin to develop.
• 50-59: Inflorescence emergence. E.g.: code 51 – inflorescence or flower buds visible, code 55- first individual flowers visible, code 59- first flower petals visible.
• 60-69: Flowering (main shoot). E.g.: code 60 – first flower opens, code 65 – full flowering: 50% of the flowers open, first petals may be fallen, code 67 – flowering finishing: majority of petals are fallen or dry, code 69 – end of flowering: fruits set visible.
• 70-79: Development of fruit.
• 80-89: Ripening or maturity of fruit and seed.
• 90-99: Senescence, beginning of dormancy. E.g. beginning of leaf-fall.

In case of apple, pear, quince, strawberry and currant, a special scale is used (Meier et al. 1994):

• Bud development.
• Development of the leaves.
• Development of the shoot.
• Emergence of flowers.
• Flowering.
• Development of the fruit.
• Ripening of the seeds and fruit.
• Senescence, beginning of dormancy.

There are some so-called phenological calendars that describe the starting date and period of seasonal natural phenomena and their interrelations. Environmental conditions, ecosystems and various species provide a help for this task. If phenophases are compared to climate, a very colourful picture will be obtained. This is why it is so important in studies related to climate change. In the European program named POSITIVE (Menzel et al. 2001) more than 400 phases have been collected in flora and fauna, and also the environment of the observatory stations has been studied. The calendar also contains daily mean temperatures.

Important parameters were as follows:

• phenophase, e.g. budburst, leaf sprouting
• physical environment conditions, e.g. snow, ice
• climatic parameters e.g. temperature, precipitation, wind

Calendar types:

• descriptive: describes the emergence and succession of phenophases,
• relative: compares the phases and their ecological conditions.

In Central European phenological calendars, environmental limits determine the start and the end of a season. When mean daily temperature exceeds 0°C, it marks the beginning of early spring, when temperature exceeds 5°C it marks the start of spring and if 13°C is exceeded, summer is going to begin. And when the daily mean temperature falls below 0°C, this shows the start of winter, falling below 5°C is the indication of late autumn, and falling below 13°C marks the start of autumn (Jaagus and Ahas 2000).

By studying the data from the calendars of various nations, POSITIVE program has yielded the following results:

• Germany and around: earliest dates, longest vegetation period, longest transitional seasons, most definite trends and strong, 8-year long fluctuation cycles
• Baltic region: oceanic climatic impact (late summer, more rain), strong trends, visible 8-year long cycles.
• Ukraine: earliest middle spring, longest summer, late precipitation, low-normal differences.
• Russia: latest starting dates, shortest vegetation period, continental climate (long winter and short summer), short transitional seasons, no trends in the Eastern and Southern regions, 8-13-year long fluctuating trends in the fragments.

Fingerprints of plant phenology are the indicator plants that show the changes for us (Menzel 2003). Spring phenophases have mostly been studied in the last 3-5 decades e.g. in case of the lilac, with the following results: phenophases commenced 0.12-0.31 days earlier every year in Europe and 0.08-0.38 days earlier every year in North-America. Autumn phases have been studied in a less intensive manner, but these commenced 0.03-0.16 days later every year. A significant change in leaf-fall was demonstrated in North-Eastern Spain: leaves fell 13 days later in 2000 than in 1952 (Peñuelas et al. 2002). Fruit bearing commenced in the case of Sambucus nigra and Aesculus hippocastanum 9 days earlier in 2000 than in 1974.

The use of phenophases as bioindicators is also very useful in studies related to climate change. E.g. a 100-year long series of data is recorded on the flowering of the Prunus avium of Gresheim. These data has been displayed and trends fitted in three periods: 1900-2000, 1951-2000 and 1982-2000. The steepness of the resulting trends was increasingly greater, which shows that the change of phenology is becoming faster, phenophases are emerging earlier and earlier every year. This phenomenon is associated with the increase in temperature. The colouring of the leaf is affected by the late, warm summer (delaying it) and the high temperatures in May and June, hurrying it (Menzel 2003).

The impact of precipitation is most expressed in the Mediterranean vegetation (Peñuelas et al. 2002), species with lesser drought tolerance and non-irrigated cultivated crops are in close correlation with precipitation. In the future, some additional factors can prove to be important in determining the change of phenophases: photoperiodic regulation, the impact of CO2, irrigation, fertilization, action of agricultural producers (Menzel1998; Peñuelas et al. 2002).

Not only the plants can mark the change of seasons, but also the first song of birds, earlier arrival of migratory birds or earlier emergence of butterflies.

Since the beginning of the 20^th century, mean temperature of the Northern hemisphere increased by 0.6°C. Daily minimum temperature has increased in a greater extent than maximum (IPCC 2007). The length of vegetation period was lengthened by 18 +/- 4 days in Eurasia and 12 +/- 5 days in North America.

Continental-scale phenology modeling utilizes sums of heat-degree days and observes plant-climate relations (Schwartz 2003). The model studies exclusively indigenous plants. Spring index considers data resulting from the first leaf sprouting of lilac and two species of honeysuckle bushes. Second generation models studying the first leaf and first flower formulated by Schwartz (1997) contained the following data:

• First -2.2 °C freeze date in autumn
• Composite chill date (all frosty days)
• First leaf date (early spring)
• First bloom date
• Last -2.2 °C freeze date in spring
• -2.2°C freeze period (number of frosty days)
• Damage index value (elapsed time between the sprouting of the first leaf and the last frosty day)
• Average annual, average seasonal, and twelve average monthly temperatures

A study observing the data of the period of 1959-1993 reported that the first leaf indicating spring emerged 5.4 days earlier, the first flower appeared 4.2 days sooner and the last frosty day commenced 4.2 days earlier (Menzel and Fabian 1999).

Plant phenological phenomena

Studies in phenology play an important role in researching climate change. Phenology data collected by monitoring systems set up at various spots of the world provide us help to create models. With the statistical analysis of these data, forecasts can be given on the extent of impacts of global warming and changes in weather.

Global plant phenology data, networks and research

In China, the CAS (Chinese Academy of Sciences) network studies the change of various phenophases. Among the studied 127 species there are soft stem (herbaceous) and woody stem (arboreal) plants like Paeonia lactiflora or Ginkgo biloba. The dates of the various phenological phases of these plants are observed, such as budburst or leaf colouring. These dates are used to study correlations with weather parameters (Wan and Liu 1979). CMA network (Chinese Meteorological Administration) collects the necessary meteorological data from the 587 stations located at various locations of the country (Cheng et al.1993). Also historical records can provide a great help in the work of climate change researchers, since written materials on phenological observations are available from the 11th century BC. Various models formulated in the country show the difference in the flowering date of the observed plant species in different regions of China, which can be associated with the different temperatures a CO2-concentration of these areas.

The meteorological network of Japan, the JMA (Japanese Meteorological Agency) has been established in 1953 (Chen 2003). It has nearly 100 stations country-wide which are also dealing with the observation of phenophases and measurement of meteorological data. 12 plant and 11 animal species are observed in different regions. Phenological models are concentrating on the extent of warming in urban regions, and the extent of changes climate change causes in the dates of phenophases. One of these models studies the relation between main inflorescence and geographical coordinates, and another model tracks the relation between temperature and flower bearing. The most important among the observed plants is the Prunus yedoensis. It has been observed that 1°C increment in the March mean temperature causes the flowering to commence 3-4 days earlier. Other important studied plant species are Prunus mume, Acer palmatum and Taraxacum officinale.

The exploration of the flora and fauna of Australia started practically in 1788 (Keatley 2003). In this work, the continent has been divided into the following regions: Western Australia, Northern Region, Southern Australia, Queensland, New South Wales, Victoria and Tasmania. Mostly the observation of eucalyptus species are conducted in these regions, but Araucaria cumminghamii, Corymbia maculata or the indigenous Pinus species are also studied.

The first phenology network in Europe has been established by Carl von Linné, who made his observations in Sweden (Menzel 2003). The IPG (International Phenological Garden) is a unique network in Europe established in 1957 by F. Schnelle and E. Volkert. This network studies 7 phenophases of 23 plant species. Length of vegetation period, amount of CO2, changes of spring temperature are observed and tracked. ICP Forests (International Co-operative Programme) is a programme observing the impacts of air pollution to forests.

There are also national networks in Europe, in Albania, Austria, the Czech Republic, Estonia, Germany, Poland, Russia, Slovakia, Slovenia, Spain and Switzerland (Schnelle 1955). There are also networks in some countries that are incomplete or not fully operational, like in Portugal and Greece.

Research in the United States has been conducted mainly in the 20^th century. From 1851 to 1859 a relatively short observational project took place when 86 plant, bird and insect species have been observed in 33 different places of the country. Phenological research became important in the 1950’s for agriculture (Schwartz 1994). Besides the observations of Syringa and Lonicera species, study of Cercis canadensis, Cornus florida and Acer rubrum can be mentioned as significant observations (Reader et al. 1974). Eventually, these plants indicate earlier springs from 1970 on.

Observation in Canada has been conducted from as early as 8-10 thousand years before (Schwartz 2003). The first nations and the Inuits made natural calendars that were based mainly on the flowering date of Thermopsis rhombifolia, the ripening of Rubus spectabilis and the flowering of several Rose species and Holodiscus discolour. Nowadays the flowering of wildflowers, phenological examination of birds, frogs and the freezing dates of lakes and rivers are conducted.

In South America, the examination of the flowering of indigenous tropical trees, coffee and cacao is conducted. Impacts of El Niño and CO₂ emission on the phenology of plants are also studied. This region is inhabited by a huge number of different types of climatic and plant communities. The emergence of the flower and the maturity of the fruit of a given plant species on different locations are also studied.

Researchers started to show interest towards phenology during the 1990’s. They were motivated by the recently increased temperature and the changes taking place in the development of plants and animals. In 1993, the Phenology Study Group of the International Society for Biometeorology (ISB) has been established in Canada, and in 1996, the GPM (Global Phenological Monitoring) was formed. GPM is one of the most important systems currently operating at the Northern hemisphere. The most important factors determining the starting date and duration of phenophases are: temperature, precipitation, soil type, soil humidity and insolation. Among these, temperature has the most important influence, therefore the GPM is focused mainly to this factor. The selection of the species is based on the following criteria:

• Plants should have phenophases that are easy to observe.
• The start of the phenophases should be sensitive to air temperature.
• Plants should be economically important.
• Plants should have a broad geographic distribution or ecological amplitude.
• Plants should be easy to propagate.
• Blooming should last several months during the growing period.

These criteria are met particularly by fruit trees, bushes in parks and spring flowers. There are special standardized observation programmes when plants are grown in a closed place, watered and eliminating weather effects. In these cases, only temperature effects are examined. Trees and bulbous plants do not need to be grown in special places. Observations are done at the starting day of the given phenophase, at least 3-4 hours after the sun has passed its peak position.

GPM utilizes the so-called BBCH (Biologische Bundesanstalt, Bundessortenamt, Chemische Industrie) codes, where abbreviations are attached to the various phenophases:

• SL: The buds begin to open in at least 3 places on the object under observation. In the case of flower buds (bud burst) the green leaf tips enclosing flowers are visible; in the case of leaf buds (bud break) the first green is visible.
• UL: Beginning of the unfolding of the leaves, first leaf surfaces visible. In at least 3 places on the object under observation, first leaves have pushed themselves completely out of the bud or leaf sheath and have unfolded completely, so that the leaf stalk or leaf base is visible. This phase is sometimes only recognizable by bending back the young leaf. The individual leaf has taken on its ultimate form, but has not yet reached its ultimate size.
• BF: First flowers open, Beginning of flowering, blossom. In at least 3 places the first flowers have opened completely.
• FF: full flowering. Approximately 50% of the flowers are open.
• EF: end of flowering. Approximately 95% of the total petals have fallen.
• RP: fruit ripe for picking. The fruits show the colouring characteristic for their variety and can be removed easily from the fruiting lateral.
• RF: first ripe fruits. The first ripe fruits fall from the tree naturally.
• CL: colouring of leaves. Approximately 50% of the leaves have taken on the colours of autumn.
• FL: leaf fall. Approximately 50% of the leaves have fallen off.

Phenological data are utilized in numerous programmes. There are data providers who record which day and where the phenological activity of the given species has taken place. In the process of research, observations, data analyses, modelling, forecasting and supporting of decision making are conducted. Answers are sought for the following questions:

• Which biotic or abiotic factors affect the date of the given phenophase?
• What effect the date of phenophase has on the ecological and socio-cultural research:
• How this date can be influenced in order to gain better results?

Phenology is also used by strategy-makers. It can provide a great deal of help in issues like politics, environment, environment protection, nature, human health. NGOs can deal with and utilize phenology in such issues that are not sufficiently paid by the government or industry.

In commerce, phenological data can refer to the quality of food or whether it is fit for human consumption or not. Information related to phenology can help in increasing crop yield and avoiding damages caused by frosts or pests.

Among the databases, bibliographical and meta-databases can be found. Meta-databases show what kinds of phenological systems exist or existed before. Bibliographic databases contain data from botany, ornithology, geography, history, agronomy, forestry, and other environmental and health sciences (Jeanneret 1997).

Some phenological networks have online information systems providing maps, tables and graphs about the changes in nature. EPN (European Phenology Network) contains a huge amount of phenological information.

The importance of phenological processes can be found in many places, not only in climate research. For example, species are active until they have nutrients and water sufficient for their development and this determines the time of the optimal period and phase (van Vliet et al. 2003). In agriculture, forestry and fishery it is important that the life-cycles and vegetation periods of plants and animals are affected by biotic and abiotic factors in their reproduction, which heavily affects their productivity. Human health is also affected by phenological processes, considering e.g. allergy, diseases, epidemics or water quality. Among these, the dates of emergence of the allergenic pollens or the hatching of the mosquitoes causing malaria are of utmost importance. Observations of phenophases can also be important when arranging the flight plans of airplanes and taking into account the flight of migratory birds, or when trying to avoid the dangers posed by leaves fallen on roads. Phenology also has a significant role in tourism via the emergence of colourful autumn leaves, appearance of migratory birds, and inflorescence of flowers.

Plant phenology in some bioclimatic zones

Studies conducted in various climates include mainly the research of leaves in tropical and arid climates (Sanchez-Azofeifa et al. 2003). Here, phenophase depends on the length of the rainy and dry periods. The date of new leaf-bearing and leaf-fall is observed and the Leaf Area Index (LAI) is calculated. The correlation between the pollen production of the flowers and the appearance of birds and bats is also studied.

Different kinds of Mediterranean climates form a transition between the dry tropical and the temperate zone. Volatile amount of annual precipitation, variable length of summer draught periods, intense summer insolation, mild-hot summers and cool-cold winters are characteristic for this zone. Based on the structure of the vegetation, six types of Mediterranean climate types are known. Phenophases are affected by environment, summer drought, fires, unstable structure, various floods and erosion in winter, agriculture, grazing and anthropogenic effects. Studies concentrate mostly on the impacts of temperature and precipitation. When studying the changes in temperature it has been observed that warming was 0.5°C in the last century, a study conducted between 1952 and 2000 stated that leaves of trees on average sprout 16 days earlier and fall 13 days later than in 1952 (Peñuelas et al. 2002). Herbaceous plants flowered 6 days earlier than in 1952 and fruit bearing commenced 9 days earlier in 2002 than in 1974. Migratory butterflies and moths arrived 11 days earlier and migratory birds arrived 15 days earlier than in 1952.

The Great Plains of North America can be divided into tallgrass, shortgrass, mixed-grass prairies and sandhills (Henebry 2003). Phenology is affected by the start, length and intensity of drought, the precipitation surplus, hails, snow, frosts, fires, grazing, pests and air pollution. In current studies, impacts of precipitation, temperature and the flowering of plants are observed (Leopold and Jones 1947). Amongst the multitude of study plants Lepidium densiflorum, Andropogon gerardii and Panicum virgatum can be found as examples.

Among the climates on high latitudes, Arctic Circle is characterized by 6 months of daylight and 6 months of night. In the Northern parts of Norway, daily mean temperatures exceed 5°C less than 100 days in a year. In Scandinavia, the number of snow-free days is less than 120 per year. (Björbekk 1993). Phenology research started in Sweden with Carl von Linné. During his examinations in 1751, he observed the budburst, flowering, fruit-bearing and leaf colouration of plants. In studies conducted later in Western Norway, it was found that among the plants studied Prunus padus required the least heat for budburst and Fraxinus excelsior needed the warmest temperatures. Considering inflorescence, colder weather was also sufficient for Salix capra. As for climate change, it was found that a greater increment can be expected in winter than in summer temperatures and precipitation. In Central Europe, budburst commenced 0.2 day/year earlier from 1960 to the end of the century, while autumn phases emerged 0.15 day/year later, which means a longer vegetation period. In Canada, Populus tremuloides brings the first flowers 0.27 day/year earlier.

Among climates of great elevation above sea level, the climate of the Rocky Mountains has been selected as a base. The higher the elevation, the greater the amount of precipitation is, and the greatest amount can be expected around the peak of the mountain. With increasing elevation, temperature decreases. In the last century, summer precipitation increased by 30-33%, and the annual minimum temperature increased by 0.7-0.9°C. In the case of some trees and bulbous plants, budburst and flowering were delayed by 2-5 days. High mountains are characterized by short vegetation period, cold temperatures and snow cover. The beginning of the vegetation period is mainly determined by the melting of the snow cover. The earlier the melting commences, the earlier the vegetation period begins and the productivity of seeds increases. Among the plants studied, Vaccinium myrtillus and Delphinium species can be found as examples.

References

Chen, Xiaoqiu: Assessing Phenology at the Biome Level, Mark D. Schwartz: Phenology: An Integrative Environmental Science, 285-300

IPCC – Intergovernmental Panel on Climate Change (2007): IPCC Fourth Assessment Report.

Jeanneret, F.: International bibliography of phenology, Institute of Geography,University of Berne, Switzerland, 68 pp., 1997.

Kramer, K., G. M. J. Mohren: Sensitivity of FORGRO to climatic change scenarios: a case study on Betula pubescens, Fagus sylvatica and Quercus robur in the Netherlands, Clim. Change, 34, 231-237, 1996.

Keatley, Marie R. and Tim D. Fletcher: Australia, Mark D. Schwartz: Phenology: An Integrative Environmental Science, 27-44

Leopold, A., E. Jones: A phenological record for Sauk and Dane Counties, Wisconsin, 1935-1945, Ecol. Monographs, 17, 83-122, 1947.

Logan J. A., Régniere J., Powell J. A. (2003): Assessing the impacts of global warming on forest pest dynamics. Frontiers in Ecology and the Environment, 1:130-137.

Meier, Uwe: Phenological Growth Stages, Mark D. Schwartz: Phenology: An Integrative Environmental Science, 269-284

Menzel A.: P. Fabian: Growing season extended in Europe, Nature, 397, 659, 1999.