**4. 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].

**31**

*Phenological Behaviour of Early Spring Flowering Trees DOI: http://dx.doi.org/10.5772/intechopen.88259*

symptoms started at about 30 years of age [14].

Betulaceae family—alder or birch [26].

is insignificant [29, 30].

are analysed here (**Table 1**).

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

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

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

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

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

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

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

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

area [35, 36], and the Atlantic temperate climate of Argentina [37].

**5. Effects of climate changes on phenology of all tree taxa**

did relative to the mid-twentieth-century temperature average [38–41].

depends on the response of these trees to climate [8].

*Phenological Behaviour of Early Spring Flowering Trees DOI: http://dx.doi.org/10.5772/intechopen.88259*

*Plant Communities and Their Environment*

without the obstruction of foliage [15].

of the genera of the order Fagales [16].

specific characteristics for each one.

the end of May and in early June [17].

Rosales order.

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

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

Birch is the major pollen allergen-producing tree in Northern Europe, although there are high levels of allergenic cross-reactivity between the representative plants

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

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

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

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

All the studied species have their main flowering season on early spring; nevertheless the different phenological phases vary among species, sites, and years

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].

production, have been observed in various European regions [17].

(male) catkins are arranged on spikes and appear in April and May [20].

depending on the bioclimatic characteristics and fluctuations [8].

**30**

**4. Allergenicity**

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].

## **5. 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 [38–41].

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


### **Table 1.**

*Statistically significant differences in start date between the start and the end of the time are indicated with \*p < 0.05, \*\*p < 0.01, and \*\*\*p < 0.001.*

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, 44–46]. The increased CO2 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

**33**

**Author details**

Córdoba, España

Herminia García-Mozo

**Acknowledgements**

Development Funds (ERDF).

\*Address all correspondence to: bv2gamoh@uco.es

provided the original work is properly cited.

and especially in the Central and Southern Europe.

Departamento de Botánica, Ecología y Fisiología Vegetal, Universidad de Córdoba,

© 2020 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

Author wishes to thank for their support to the projects FENOMED, REF. CGL2014-54731-R, funded by the Spanish Ministery of Economy and Competitiveness; and CLIMAQUER, REF. 1260464, European Regional

*Phenological Behaviour of Early Spring Flowering Trees DOI: http://dx.doi.org/10.5772/intechopen.88259*

cal information of wind-pollinated species.

plant species [53].

**6. Conclusions**

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

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 phenologi-

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

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].
