Phenological Behaviour of Early Spring Flowering Trees

This chapter reports the phenological trends (reproductive and vegetative events) of some early spring and late winter flowering trees all around the world and especially Europe: Corylus avellana L. (hazel); Quercus robur L. (common oak); Quercus ilex subsp. ballota, (Desf.) Samp. (holm oak); Betula spp. (birch); Salix alba L. (willow); Fraxinus angustifolia Vahl. (ash); and Morus alba L. (white mulberry). They are deciduous and perennial trees growing in different climatic areas of Europe. They have anemophilous pollination liberating huge pollen concentrations to the atmosphere. Aerobiological surveys give us reproductive phenological information of these wind-pollinated species. The phenological response to climate during the last years was analysed, including budburst, leaf unfolding, flowering, fruit ripening, fruit harvesting, leaf colour change, and leaf fall. The response of each taxon to climate was different; most of the revised species and sites presented an advance of the early spring phenophases, especially budburst. On the contrary, some studies detected a delay in autumn vegetative phases, especially leaf fall events. The statistical analyses indicated that phenological advances are a consequence of the increasing temperature trend— minimum temperature being one of the most influential factors. The increase of temperature influenced that leaf unfolding and flowering dates showed a general advance expressed by negative correlations with temperature data, whereas the leaf colour change and leaf- fall presented positive correlations due to the delay of the colder temperatures. The phenological revised results can be considered as reliable and valuable bio-indicators of the impact of the recent climate change in the Northern Hemisphere, and especially Central and Southern Europe.


Phenology
Phenology is derived from the Greek word phaino, meaning 'to show' or 'to appear' . This science studies the recurring biological events as part of the animal and plant life cycles. These events are the phenological stages or phenological phases. Phenology not only studies the timing but also their relationships with weather and climate [1].
Sprouting and flowering of plants in spring and leaves' colour change in the fall are examples of plant phenological events [2]. Phenology has been used as a proxy for climate and weather through all the human history, particularly in relation with agriculture, but only from the last century has emerged as a science in its own right [1]. In last years it is being recognized as an integrative measure of plant responses to the environment changes that can be scaled from a local to a global scale, including climate change. During the last 100 years, the Earth's climate has warmed by approximately 0.6°C. In this last century, two main periods of warming have been detected. The first one was between 1910 and 1945, and the second one from 1976 onward [3]. In this second period, the rate of warming is being doubled than in the first and greater than at any other time during the last 1000 years [3]. The response of the different ecosystems and species is not a global response to a global climate average [4]. To know the regional responses can be more relevant in the context of ecological response to climatic change. In this sense, phenological behaviour data are the more reliable actual bio-indicator of the climate change response. Moreover, sessile life-style characteristic of plants has led them to develop high plasticity phenotypes in order to reach better phenological adaptations to deal with environmental changes [5]. These changes include climate changes that are of critical ecological importance as they affect species competitive ability and net primary productivity. These changes can even prompt ecosystem structure transformations [6]. Therefore, the analysis of trends of spring phenological phases for the past decades could provide important information about changes in climate and the impact on sessile organisms' phenology such us plants and specially trees, with longer lifetimes and shorter capacity of area distribution change.
This study presents a review of recent studies on both vegetative and reproductive field phenological development of different tree species characterized by their foliation or flowering during early spring. The phenological response of different tree species in the North Hemisphere was reviewed: hazel (Corylus avellana L.), alder (Alnus glutinosa (L.) Gaertn), willow (Salix alba L.), birch (Betula pendula L.), holm oak (Quercus ilex subsp. ballota, (Desf.) Samp.) in South Europe and common oak (Quercus robur L.) in Central Europe, ash (Fraxinus angustifolia Vahl.), and white mulberry (Morus alba L.) [7]. All of them are anemophilous species producing high quantities of pollen grains spread to the atmosphere provoking allergy to the sensitized population [8]. Their huge quantities of pollen grains are also a phenological bio-indicator detected through aerobiological studies [9], also revised for the present review. Their phenological behaviour during last 40 years and the impact of the climate change on it were analysed. Particularly remarkable is the fact that the revised species are important for aerobiology and allergy studies, and therefore the changes experimented on their phenology have a special interest. This review offers valuable information due to the scarce number of researches studying field phenological data including those from the last quarter of the twentieth century.

Climate change
Climate change due to human activities has been witnessed for at least the last 100 years and is projected to continue for centuries to come. Climate change involves the whole climate system, including not only our atmosphere but also our hydrosphere, cryosphere, land surface, and biosphere [10].
Greenhouse gases and atmospheric concentrations have exponentially increased since the start of the Industrial Era (1750). Moreover, from this time the CO 2 concentrations have increased by 41% mostly due to the global use of oil fuel [3]. The latest measures of the year 2013 of the National Oceanic and Atmospheric Administration reveal that global annual mean atmospheric CO 2 concentration was 395.22 parts per million (ppm) [11], an increase of over 100 ppm from the pre-Industrial Era. Figure 1 shows that the increase in atmospheric CO2 concentration since 1750 has not been linear, being higher in the last 60 years [11].
This increase in the atmospheric concentration of greenhouse gases such as CO 2 has led to warm the climate. Between 1880 and 2012, the Earth's average surface temperature warmed by 0.85°C [3]. Most of this warming occurred after 1951 [12]; the warming of the Earth's surface varies over space, the land surfaces tending to warm more than the oceans; and some parts of the Earth's surface temperatures have increased the double than other places. Changes in precipitation have also been observed. Since 1901, precipitation has increased over the mid-latitude land areas of the Northern Hemisphere, especially in intensity, with more frequent heavy rain episodes [12].
By the end of this century (2081-2100), global mean surface temperatures are projected to increase from 0.3°C to 4.8°C depending on the sites. The mean warming over land will be larger than over the ocean, and the Arctic region will warm more rapidly than the global mean [3]. With regard to precipitation, it is projected to increase by the end of this century [13]. However, there will be substantial spatial variation in precipitation changes, with some regions experiencing increases, some decreases, and some no change at all [13]. All these factors and the actual impact on phenology of early spring trees will be reviewed in the present chapter.

General phenological behaviour of all studied tree taxa
The revised species were selected because of their flowering time in early spring or late winter and because of their strong presence and distribution in Europe. They are anemophilous, deciduous, and perennial trees growing in different climatic areas of Europe: hazel (Corylus avellana L.) in Central and South Europe, oak (holm oak (Quercus ilex subsp. ballota, (Desf.) Samp.)) in Southern Europe, common oak (Quercus robur L.) in Central Europe, birch (Betula spp.) in Central and North Europe, willow (Salix alba L.) in Central and South Europe, ash (Fraxinus angustifolia Vahl.) in South Europe, and white mulberry (Morus alba L.) in South Europe [14]. All of them are endemic European species expect for white mulberry [7]. Most of the revised species belong to the Fagales order, divided into the Betulaceae, Salicaceae, and Fagaceae families [14]. On the other hand, Fraxinus genus is in the Oleaceae family of the Lamiales order, and Morus in the Moraceae family of the Rosales order.
Fagales order comprises three families: Betulaceae, including the genera Betula (birch), Alnus (alder), and Corylus (hazel); Fagaceae, including the genera Quercus (oak) and Fagus (beech); and Salicaceace including the genus Salix (willow) [14]. These wind-pollinated trees have catkins, which dangle from the branch so that pollen is easily shaken loose in the wind. Interestingly, catkins in deciduous species emerge before the leaves, allowing the pollen to travel further away from the parent without the obstruction of foliage [15].
Birch is the major pollen allergen-producing tree in Northern Europe, although there are high levels of allergenic cross-reactivity between the representative plants of the genera of the order Fagales [16].
As it has been already mentioned, all the revised species are foliating or flowering in early spring in Europe and North America; nevertheless, there are some specific characteristics for each one.
Hazel and alder are the first (December-April) to blossom and to shed pollen in the outdoor air in Europe, followed by birch. This fact joint to an allergenic crossreactivity between hazel and alder provokes that pollen from these species can act as a primer of allergic sensitization to Betulaceae pollen allergens. Consequently, clinical symptoms become more marked during the birch pollen season [17,18]. In the central Alpine regions, the highest concentrations of Alnus pollen are found at the end of May and in early June [17].
In the case of Betula, the budburst occurs at March-April depending on the latitude and altitude. In South and Western Europe, the main flowering period usually starts at the end of March, whereas in Central and Eastern Europe, it occurs at early April. In northern areas the flowering season starts from late April to late May depending on the latitude [8]. Pollen values peak 1-3 weeks after the start of the season, so they are recorded in April in South Europe and in May in Northern Europe. Far shorter or longer periods, with yearly alternating low and high pollen production, have been observed in various European regions [17].
On the other hand, the onset of the oak season in spring, shortly before the beech pollen season, which is usually quite mild, can prolong the season in western, central, and eastern Europe [8]. One important characteristic of the oak pollen is the fact that it includes many species. In South Europe perennial species such as holm oak, kermes oak, and cork oak flower through all the spring from March to June [19]. In Central Europe, the pedunculate oak and the sessile oak usually flower in April-May [8].
Mulberry plants are normally dioecious, but they can also be monoecious on different branches of the same plant. The pendulous pistillate (female) and staminate (male) catkins are arranged on spikes and appear in April and May [20].
All the studied species have their main flowering season on early spring; nevertheless the different phenological phases vary among species, sites, and years depending on the bioclimatic characteristics and fluctuations [8].

Allergenicity
Birch, followed by alder and hazel, has the greatest allergenic potency in this group of allergenic trees. In Central Europe, these tree pollens are the second most common cause of allergic conditions after grass pollen. In the case of birch, the major allergen is Bet v1, and the percentage of subjects with a positivity skin prick test to birch allergens ranges from 5% in the Netherlands to 54% in Zurich (Switzerland)  [17,21]. In recent years, the popularity of Betula as an ornamental plant loved by architects has caused a significant increase in allergic sensitization to this allergen [22,23]. In a large study of cross-sensitization between allergenic plants in adult patients with asthma or rhinitis, it was found that sensitization to birch pollen allergens was frequently associated with other allergens, that it induced mostly nasal symptoms, and that respiratory symptoms started at about 30 years of age [14].
Pollen from the common alder, major pollen allergen Aln g 1, is an important cause of pollen allergy. This pollen has similar physicochemical properties than the pollen of birch, hazel, hornbeam, and oak. The joint presence of these pollen grains in the atmosphere makes difficult to separate out their individual effects [24].
Hazel is well distributed in Europe, and it typically has a flowering occurring from winter to early spring. The major allergen is Cor a 1, cross reactive with Bet v1 [25]. In the case of Corylus pollen, a recent study performed in Poland revealed that ~11% of allergy patients had positive skin reactions to Corylus pollen allergens, and most of these (94.4%) reacted to pollen allergens from other members of the Betulaceae family-alder or birch [26].
Beech trees are related to oaks. These trees are considered as low allergenic [27]. The European beech sheds much more pollen than the American species, but both have been reported to have minor allergenic importance. Despite the large amounts of pollen grains detected in the European atmosphere, Quercus pollen, which is a stenopalynous pollen type for all the genera, does not provoke actual allergy problems [8].
Although willows elicit strong allergic responses from individuals in allergy tests, willows tend to be pollinated more by insects than by wind and therefore present fewer people with the allergenic challenge than other tree types [28]. In fact, the impact of the increase in Salix atmospheric pollen upon asthma admissions is insignificant [29,30].
Mulberry pollen grains cause allergenic symptoms such as rhinitis, conjunctivitis, and asthma [31,32]. A study from Tucson, Arizona, USA, concluded that it is an important allergen for children raised in a semiarid environment [33]. In other climate areas, Mulberry tree pollen has been revealed as an important aeroallergen. This is the case of the tropical area of Caracas, Venezuela [34], the Mediterranean area [35,36], and the Atlantic temperate climate of Argentina [37].
The most important allergenic species revised here, birch, alder, and hazel, have their main pollen emission time mostly in early spring although the exact time depends on the response of these trees to climate [8].

Effects of climate changes on phenology of all tree taxa
Different phenological studies are showing a clear link between anthropogenic climate change, warming winter and spring temperatures, and changes in phenology, especially earlier flowering times and late leaf fall in autumn [8,10,17,18,21]. This occurs in a wide variety of tree species including the early spring species that are analysed here ( Table 1).
There is considerable variation in these studies that reflects the time examined and regional differences in temperature, etc.; however, for all tree species examined, flowering is now occurring, on average, approximately 2 weeks earlier than it did relative to the mid-twentieth-century temperature average [38][39][40][41].
Some studies have shown the impact of climate change on phenology and pollen and therefore on aeroallergens and allergic diseases describing the influence on the amount, distribution, allergenicity, and pollen season of pollen grains [8,10,17,18,21]. A global comparative study of the International Phenological Gardens in Europe (covering 69-42°N to 10°W-27°E) of current data compared and early 1960s phenological data indicated the advance of spring events, such as flowering (+6 days), whereas autumn phenophases have been delayed by 4.8 days [42].
Speaking about early spring species, in the case of Corylus avellana, an earlier flowering onset was observed at 80% of the studied localities of the Iberian Peninsula, earlier fruit ripening at all sampling sites, and earlier fruit harvesting at 75% of them [43]. Salix alba presented a trend towards earlier budburst and earlier leaf unfolding at 67% of the studied Iberian localities. In the case of autumn phases, delay in leaf fall at all sampling sites [40]. Holm oak is suffering a strong advance in the flowering start, as it was previously indicated in the Iberian Peninsula [41]. Northern species such as birch, poplar, or willow are also showing the impact of climate change on phenology [38,39].
As it was demonstrated by [41,43] among others, the relationship between the phenological observations and weather is so clear for tree species and especially for early spring species. The statistical analyses show that in the 55% of the studied localities of the Iberian Peninsula, the temperature is influencing these trees' phenology. In 58% of the sites affected by temperature, the correlation between phenology and minimum temperatures was negative, which is provoking an advance in phenology. The mean temperature results showed negative correlation in 54% of the sites, although different behaviour was observed depending on species and phenophases.
On average, the length of the growing season in Europe increased by 10-11 days during the last 30 years. Trends in pollen amount over the latter decades of the 1900s increased according to local rises in temperature [8,[44][45][46]. The increased CO 2 concentration can be affecting pollen production as it has been demonstrated in experimental conditions [47,48]. Regarding the pollen season length, it is also extending especially in late spring and summer flowering species [49]. Moreover, temperature is influencing towards stronger allergenicity in tree pollen [17,50].
An earlier pollen season starts, and peak is being more pronounced in early spring flowering species [43]. Due to this earlier onset, the seasons are more often interrupted by adverse weather conditions in late winter/early spring [51].
Finally, changes in climate appear to have altered the spatial distribution of pollens. New patterns of atmospheric circulation over Europe might increase the number of long-distance transport episodes of allergenic pollen, increasing the risk of new sensitizations among the allergic population [52]. On the other hand, the temperature increases, and the changes in rainfall regime are provoking the geographical spread of some vegetal species to new areas. In the future the effect of the expected rate of warming (0.5°C per decade) could increase this geographical migration although the effect on pollen distribution is expected to be less pronounced than the effect of changes on land as well as international transport of plant species [53].

Conclusions
The review made about the recent response of the phenology of different species of anemophilous trees to climate change reveals that, apart from the field phenology data, aerobiological pollen data are a valuable tool to obtain reproductive phenological information of wind-pollinated species.
The response to climate of each studied taxon was different; most of the revised species and sites presented an advance of the early spring phenophases, especially budburst. The statistical analyses of the revised studies indicate that phenological advances are a consequence of the increasing temperature trend-minimum temperature being one of the most influential factors. The increase of temperature influenced that leaf unfolding and flowering dates showed a general advance expressed by negative correlations with temperature data, whereas the leaf colour change and leaf-fall presented positive correlations due to the delay of the colder temperatures.
On the contrary, some studies detected a delay in the autumn vegetative phases, especially on leaf-fall events. Both, leaf colour change and leaf-fall events showed positive correlations with temperature due to the delay of the colder temperatures.
The phenological revised results can be considered as reliable and valuable bioindicators of the impact of the recent climate change in the Northern Hemisphere and especially in the Central and Southern Europe.