MAST BEHAVIOUR IN EUROPEAN FOREST TREE SPECIES: TRIGGERS, INHIBITORS, AND RESOURCE DYNAMICS MECHANISMS

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Diss. ETH Nr. 27275

MAST BEHAVIOUR IN EUROPEAN FOREST TREE SPECIES: TRIGGERS, INHIBITORS, AND RESOURCE

DYNAMICS MECHANISMS

A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH

(Dr. sc. ETH Zurich)

presented by ANITA NUSSBAUMER

M.Sc. in Geography, University of Zurich born on 5^th October 1976

citizen of Erlenbach (ZH)

accepted on the recommendation of Prof. Dr. Andreas Rigling, examiner Prof. Dr. Harald Bugmann, co-examiner

Prof. Dr. Arthur Gessler, co-examiner Prof. Dr. Giorgio Vacchiano, co-examiner

Dr. Peter Waldner, co-examiner

2020

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Table of contents

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Summary

Synchronisation of seed production is the reproductive strategy of many long-lived plant species. Years with high seed production, so called mast years, impact various ecological and economical areas. It e.g. provides additional nutrition for wildlife populations and livestock, can increase infection pressure of zoonoses, and affects timber production.

Furthermore, mast years are likely to lead to changes in resource allocation to vegetative and generative tissues. For many species, mast years can be triggered by weather conditions in the years before and during the mast year. In the light of the current climate change, spatial and temporal mast patterns are, therefore, likely to change. Hence, improving the knowledge on this phenomenon is crucial for future forest ecosystem research, forest management and forest modelling.

This Ph.D. project investigates several aspects of mast behaviour, i.e. biotic and abiotic triggers and inhibitors for mast years, and changes in resource allocation to vegetative and generative tissues in relation to mast years. The results are assigned to the common proximate mast hypotheses. This Ph.D. study concentrates on the most abundant forest tree species in Europe: Scots pine (Pinus sylvestris L., hereafter pine), Norway spruce (Picea abies [L.] Karst., hereafter spruce), European beech (Fagus sylvatica L., hereafter beech), and sessile and pedunculate oak (Quercus petraea [Matt.] Liebl. and Quercus robur L., hereafter oak). Parameters of the crown condition survey, the fresh leaf survey, the stem growth survey, and the litterfall survey of the International Co-operative Programme on Assessment and Monitoring of Air Pollution Effects on Forests (ICP Forests), together with two additional datasets from Croatia and Switzerland, were assessed to address the questions raised in three chapters.

In the first chapter, weather conditions controlling mast occurrence (weather cues) are investigated for pine, spruce, beech, and oak. Additionally, fruiting intensity in the years before the focal years are analysed as a potential inhibitor of mast years. For pine, weather cues triggering mast years were inconsistent between European regions. For spruce and beech, the most important weather cues leading to mast years were a cool summer two years before mast years, and a warm and dry summer in the year before mast years. The impact of precipitation two summers before mast years differed between the species. For spruce, summers two years before mast years were dry while for beech, they were wet. Additionally, for beech a warm spring in the mast year was important, most likely to provide ideal

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Summary

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conditions for successful pollination. For both spruce and beech, these weather cues were spatially consistent throughout Europe. For oak, the only spatially consistent weather cue was a warm spring in the mast year whereas weather conditions in the two years before mast years differed between the regions. In pine, fruiting intensity was high in both of the two years before a mast year. Additionally, interannual differences in fruiting intensity was lower than in the other species. These findings suggest that pine might not be a masting species sensu stricto. All other species had high fruiting intensity two years before a mast year. Fruiting intensity one year before mast years was not a strong influencing factor in beech and the oak species while in spruce, fruiting intensity in the year before mast years was regionally significantly lower.

In the second chapter, an inhibiting effect of weather conditions is investigated for beech.

It is assumed that this species is a flowering masting species, i.e. strong flowering in spring is very likely followed by successful fruit development. During the extremely hot and dry West and Middle European summer of 2018, beechnuts were scarce in two of three ICP Forests Level II beech stands in Switzerland, despite successful pollination in spring.

Investigation of the long-term data of these two stands from the last 15-19 years showed that similar events occurred in the past. Comparing weather conditions during beechnut ripening revealed that in years with high beech pollen loads in spring but scarce fruits in autumn, summer temperatures were 1.5°C higher and precipitation sums were 45% lower than in the most successful mast years. These extreme weather conditions hence act as an environmental veto for fruit production. Climate models for the next few decades project an increase not only in temperatures but also in summers with extreme heatwaves and drought events. Therefore, the natural regeneration potential of beech is likely to be compromised in the future.

In the third chapter, changes in resource allocation between vegetative and generative tissues in relation to mast years are investigated for beech and oak, and underlying resource dynamics are discussed. Furthermore, changes in leaf nutrient concentrations with increasing fruit production are analysed. Beech showed enhanced vegetative growth in the two years before mast years and a reduction of vegetative growth in mast years. These changes are indication for the resource storage hypothesis with the mechanism resource accumulation before mast years, and for the resource switching hypothesis in mast years which states that during mast years, resources are allocated to generative rather than to vegetative tissues. In the two years after mast years, vegetative growth showed no significant changes. Oak showed enhanced stem growth in the year before a mast year

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Summary

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(resource accumulation), and reduced stem growth in the two years after mast years (resource depletion) which are both mechanisms of the resource storage hypothesis. During mast years, vegetative growth did not change. In beech, but not in oak, leaf nitrogen and phosphorus concentrations were enhanced during mast years, although this effect was mostly site-specific. Mass of 100 leaves was reduced in both species. Beech in the warmer two regions and oak in the whole of Europe did not show a reduction of leaf biomass production during mast years. In the cool temperate region, however, leaf biomass production in beech was reduced which suggests that in this region, beech is not able to compensate for smaller leaves during mast years. High summer precipitation sums in the current year and low summer temperatures in the previous year enhanced stem growth in beech and oak. For beech, also high precipitation sums at the end of the dormancy period, and for oak, high temperatures at the beginning of the vegetation period led to increased stem growth. Beech may be compromised in vegetative growth under future climate conditions as, according to current climate models, precipitation sums will most likely decrease in summer. At the same time, high beechnut production reduces stem growth and may act as a stress factor. Oak, on the other hand, does not show difficulties to simultaneously invest resources in generative and vegetative growth.

Overall, this Ph.D. thesis provides in-depth knowledge for a better understanding of underlying processes and mechanisms in relation to mast behaviour in the five most abundant forest tree species in Europe. It may support future forest planning and management under the aspect of natural regeneration and the potential to adjust to future climates in Europe. Furthermore, the gained knowledge can contribute to the improvement of forest and ecosystem models.

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Zusammenfassung

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Zusammenfassung

Die Synchronisierung der Samenproduktion ist für viele langlebige Pflanzenarten eine erfolgreiche Fortpflanzungsstrategie. Jahre mit starker Samenproduktion, so genannte Mastjahre, wirken sich auf verschiedene ökologische und ökonomische Bereiche aus.

Mastjahre bieten z.B. zusätzliche Nahrung für Wildtierpopulationen und Nutztiere, können den Infektionsdruck von Zoonosen erhöhen und haben einen Einfluss auf die Holzproduktion. Darüber hinaus können Mastjahre zu Veränderungen der Ressourcenallo- kation zwischen vegetativen und generativen Geweben führen. Bei vielen Arten werden Mastjahre durch Wetterbedingungen in den Jahren vor und während des Mastjahres ausge- löst. Es kann davon ausgegangen werden, dass sich räumliche und zeitliche Mastmuster angesichts des aktuellen Klimawandels verändern werden. Daher ist ein besseres Verständ- nis dieses Phänomens von entscheidender Bedeutung für künftige Waldökosystemfor- schung, Waldbewirtschaftung sowie Waldmodellierung.

In dieser Arbeit werden verschiedene Aspekte des Mastverhaltens untersucht, namentlich biotische und abiotische Auslöser und Inhibitoren für Mastjahre sowie Veränderungen der Ressourcenallokation in vegetativen und generativen Geweben in Bezug auf Mastjahre. Die Ergebnisse werden den gängigen proximalen Masthypothesen zugeordnet. Die vorliegende Dissertation konzentriert sich auf die in Europa am häufigsten vorkommenden Waldbaum- arten Waldföhre (Pinus sylvestris L., im Folgenden Föhre), Fichte (Picea abies [L.] Karst), Rotbuche (Fagus sylvatica L., im Folgenden Buche) und Stiel- und Traubeneiche (Quercus petraea [Matt.] Liebl. und Quercus robur L., im Folgenden Eiche). Die Parameter der Kronenzustands-, der Frischblatt-, der Stammwachstums- und der Streufallerhebung des International Co-operative Programme on Assessment and Monitoring of Air Pollution Effects on Forests (ICP Forests) wurden zusammen mit zwei zusätzlichen Datensätzen aus Kroatien und der Schweiz ausgewertet, um die in drei Kapiteln gestellten Fragen zu beantworten.

Im ersten Kapitel wird für Föhre, Fichte, Buche und Eiche getestet, welche Wetterbedin- gungen Auslöser für Mastjahre sind. Zusätzlich werden die Fruktifikationsintensitäten in den Jahren vor den betrachteten Jahren als potentiell verhindernder Faktor für Mastjahre analysiert. Bei Föhre waren die Wetterbedingungen, die Mastjahre auslösten, in den ver- schiedenen europäischen Regionen uneinheitlich. Bei Fichte und Buche waren die wichtigsten Wetterbedingungen, die zu Mastjahren führten, ein kühler Sommer zwei Jahre

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Zusammenfassung

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vor einem Mastjahr und ein warmer und trockener Sommer im Jahr vor einem Mastjahr.

Die Niederschlagsbedingungen zwei Sommer vor einem Mastjahr waren unterschiedlich:

Bei Fichte waren diese trocken, bei Buche waren sie feucht. Zusätzlich war für Buche ein warmer Frühling im Mastjahr wichtig, was höchstwahrscheinlich ideale Bedingung für eine erfolgreiche Bestäubung schafft. Sowohl bei Fichte als auch bei Buche waren diese Mast- jahr auslösenden Wetterbedingungen räumlich konsistent. Bei Eiche war die einzige räum- lich konsistente Wetterbedingung ein warmer Frühling im Mastjahr. Die Wetterbedingun- gen in den beiden Jahren vor einem Mastjahr unterschieden sich hingegen zwischen den Regionen. Föhre zeigte in beiden Jahren vor dem Mastjahr hohe Fruktifikationsintensitäten.

Zusätzlich waren die jährlichen Unterschiede der Fruktifikationsintensitäten geringer als bei den anderen Arten. Diese Ergebnisse deuten darauf hin, dass Föhre kein Mastverhalten im engeren Sinne zeigt. Alle anderen Arten wiesen zwei Jahre vor einem Mastjahr hohe Fruktifikationsintensitäten auf. Bei Buche und Eiche hatten diese ein Jahr vor dem Mastjahr keinen starken Einfluss, während sie bei Fichte im Jahr vor dem Mastjahr regional deutlich niedriger waren.

Im zweiten Kapitel wird ein Wetterphänomen untersucht, das eine erfolgreiche Buchenmast verhindert. Buche wird als flowering masting species angesehen, das heisst, es ist sehr wahr- scheinlich, dass auf eine starke Blüte im Frühling eine erfolgreiche Fruktifikation folgt.

Während des extrem heissen und trockenen west- und mitteleuropäischen Sommers 2018 entwickelten sich auf zwei von drei ICP Forests Level II-Buchenflächen in der Schweiz trotz erfolgreicher Bestäubung im Frühling kaum Bucheckern. Eine Untersuchung der Langzeitdaten dieser beiden Bestände aus den letzten 15-19 Jahren zeigte, dass in der Ver- gangenheit ähnliche Ereignisse stattgefunden haben. Der Vergleich der Witterungsverhält- nisse während der Bucheckernentwicklung ergab, dass in Jahren mit hoher Buchenpollen- konzentration im Frühling, aber wenigen Früchten im Herbst, die Sommertemperaturen um 1,5°C höher und die Sommerniederschläge um 45% tiefer lagen als in den erfolgreichsten Mastjahren. Diese extremen Wetterbedingungen wirken somit als ‘Umweltveto’ für die Bucheckernproduktion. Klimamodelle für die nächsten Jahrzehnte gehen nicht nur von einem Anstieg der Temperaturen aus, sondern auch von einer Zunahme von Sommern mit extremen Hitzewellen und Dürreereignissen. Daher dürfte das Potenzial zur natürlichen Verjüngung von Buche in Zukunft abnehmen.

Im dritten Kapitel werden die Verschiebungen der Ressourcenallokation zwischen vegetativen und generativen Geweben in Bezug auf Mastjahre für Buche und Eiche untersucht. Zusätzlich werden die zugrunde liegenden Ressourcendynamikmechanismen

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Zusammenfassung

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diskutiert. Darüber hinaus werden Blattnährstoffkonzentrationen in Abhängigkeit von zunehmender Fruchtproduktion analysiert. Die Buche zeigte in den zwei Jahren vor den Mastjahren ein verstärktes vegetatives Wachstum und eine Verringerung des vegetativen Wachstums in den Mastjahren. Diese Veränderungen sind ein Indiz für die resource storage hypothesis mit dem Mechanismus Ressourcenakkumulation vor Mastjahren und für die resource switching hypothesis während Mastjahren, die besagt, dass in Mastjahren Ressour- cen eher in generatives als in vegetatives Gewebe investiert werden. In den zwei Jahren nach Mastjahren zeigten sich keine signifikanten Änderungen beim vegetativen Wachstum.

Bei Eiche war das Stammwachstum im Jahr vor einem Mastjahr verstärkt (Ressourcenakku- mulation) und nach Mastjahren reduziert (Ressourcenerschöpfung), beides Mechanismen der resource storage hypothesis. Während der Mastjahre zeigte das vegetative Wachstum hingegen keine Veränderung. In Mastjahren waren bei Buche, aber nicht bei Eiche, die Stickstoff- und Phosphorkonzentrationen der Blätter erhöht, wobei dieser Effekt meist standortspezifisch war. Die Masse von 100 Blättern war bei beiden Arten reduziert.

Während der Mastjahre zeigten Buche in den beiden wärmeren Regionen und Eiche in ganz Europa keine Reduktion der Blattbiomasseproduktion. In der kühleren gemäßigten Region hingegen war die Blattbiomasseproduktion bei Buche reduziert, was darauf hindeutet, dass Buche in dieser Region nicht in der Lage ist, kleinere Blätter während der Mastjahre mit der Produktion von mehr Blättern zu kompensieren. Erhöhte Sommerniederschläge förderten das Stammwachstum von Buche und Eiche. Zusätzlich führten bei Buche hohe Niederschlä- ge am Ende der Dormanz zu erhöhtem Stammwachstum, während bei Eiche erhöhte Tem- peraturen zu Beginn der Wachstumsperiode von Vorteil waren. Das vegetative Wachstum von Buche könnte unter zukünftigen Klimabedingungen beeinträchtigt werden, da nach den aktuellen Klimamodellen die Sommerniederschläge höchstwahrscheinlich abnehmen werden. Gleichzeitig reduziert eine hohe Buchecker-produktion das Stammwachstum und kann als Stressfaktor wirken. Eiche hingegen zeigt keine Schwierigkeiten, Ressourcen gleichzeitig in generatives und vegetatives Wachstum zu investieren.

Insgesamt bietet diese Doktorarbeit vertiefte Erkenntnisse über das Mastverhalten der fünf häufigsten Waldbaumarten in Europa. Dies kann helfen zugrundeliegende Prozesse und Mechanismen besser zu verstehen. Sie kann die künftige Planung und Bewirtschaftung der Wälder unter dem Aspekt der natürlichen Verjüngung und des Potenzials zur Anpassung an zukünftige Klimabedingungen in Europa unterstützen. Ausserdem können die hier gewonnenen Erkenntnisse zur Verbesserung von Wald- und Ökosystemmodellen beisteuern.

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General introduction

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General introduction

Historical significance of the mast phenomenon

Years with mass seed and fruit production, so called mast years, are a widespread reproduction strategy of many long-lived plant species (Nilsson and Wastljung 1987; Kelly 1994; Herrera et al. 1998; Koenig and Knops 2000; Kelly and Sork 2002; Kelly et al. 2013;

Vacchiano et al. 2018). The term ‘mast’ derives from the German expression

‘Schweinemast’ which translates as ‘fattening up pigs’ (Waller 1993). In Europe, especially oak mast years were important for swine herders as in those years, forests provided additional nutrition for livestock. As a consequence, historical sources such as account books which range back to the medieval times can be used to reconstruct long-term mast data (Szabó 2015). Other, more recent sources, derive from forest administration data, harvest estimations, forest inventories, or from seed sellers (Szabó 2015; Nussbaumer et al.

2016; T. Ebinger, per comment). The forest dieback of the 1980s in parts of Europe, the so called ‘Waldsterben’, brought attention to the importance of ecological knowledge on many aspects of vegetative and generative growth of the main forest tree species in Europe.

Therefore, forest scientists began to systematically investigate various traits in forest ecosystems which are coordinated e.g. in the International Co-operative Programme on Assessment and Monitoring of Air Pollution Effects on Forests (ICP Forests; UNECE ICP Forests 2016). In the late 1990s it became obvious that the worst-case scenarios of widespread deforestation in Middle Europe did not occur and the interest in mast behaviour of forest tree species decreased. However, in the last few years, the importance of understanding the mechanisms, triggers, and the underlying resource dynamics mechanisms of mast behaviour became evident in the face of the current climate change. Mast behaviour is controlled by environmental and internal factors. Therefore, environmental changes due to climate change may very likely alter spatial and temporal mast patterns.

The ICP Forests network

The 1980s forest dieback in Middle Europe (‘Waldsterben’) was caused i.a. by heavy air pollution. This led to the establishment of the ICP Forests in 1985 by the Convention on Long-range Transboundary Air Pollution (CLRTAP) under the United Nations Economic Commission for Europe (Seidling et al. 2017). Today, 40 European countries, along with the USA and Canada, are involved in the ICP Forests. Two network systems are established:

Level I comprises of extensively monitored plots on a systematic 16x16 km² grid. Level II

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consists of intensively monitored plots in representative forest ecosystems of each country.

On Level I plots, surveys are periodically performed, while on Level II plots, parameters are measured continuously or at short intervals. In this Ph.D. thesis, the parameter ‘fruiting intensity’ from the crown condition survey of Level I and Level II plots, estimated each summer, and fruit biomass from the litterfall, continuously collected in littertraps on Level II plots, were used as a proxy for fruit production (Eichhorn et al. 2016; Ukonmaanaho et al. 2016). Data from other sources used in this Ph.D. project were collected in a comparable way (Braun et al. 2013; Anić et al. 2018).

Ultimate and proximate hypotheses for mast behaviour

Mast behaviour is based on individual annual variability in seed production and synchrony between individuals (Herrera et al. 1998; Koenig et al. 2003). Two groups of hypotheses are commonly discussed to explain mast behaviour: ultimate hypotheses explain the evolutionary advantages of mast years, while proximate hypotheses concentrate on the mechanisms which lead to mast years (Kelly 1994; Pearse et al. 2016).

Ultimate hypotheses include the predator satiation hypothesis, the pollination efficiency hypothesis (and the pollen coupling hypothesis), and the environmental prediction hypothesis (Pearse et al. 2016). These hypotheses assume that synchrony of seed production between individual trees is advantageous for tree populations by reducing the costs for seed production. Therefore, they all include economy of scale effects (Pearse et al. 2016).

The predator satiation hypothesis assumes that in a mast year enough seeds will survive due to supersaturation of predators (Janzen 1971; Kelly 1994; Vander Wall 2010; Pearse et al. 2016). Furthermore, fruit dispersion is enhanced as scatter-hoarding seed dispersers are attracted when fruit density is higher (Janzen et al. 1971; Gurnell 1983; Kelly 1994; Kon et al. 2005; Vander Wall 2010; Pearse et al. 2016). The pollination efficiency hypothesis states that in years with synchronised flowering, pollination success is higher than in years when only few trees bear blossoms (Kelly 1994; Crone and Rapp 2014; Pearse et al. 2016). A subsequent hypothesis of the pollination efficiency hypothesis is the pollen coupling hypothesis which states that synchrony of phenology between individual trees, such as bud break and flowering, will lead to pollen coupling (Bogdziewicz et al. 2017). The environmental prediction hypothesis concerns serotinous species whose seed production is triggered by wildfires or which produce serotinous fruits which only release seeds after wildfires (Kelly 1994; Pearse et al. 2016). This leads to a higher survival rate especially for herbaceous species which are dependent on high light transmission of forest canopies.

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The most commonly discussed proximate hypotheses are the resource budget hypothesis (also known as resource budget model) which includes the resource storage hypothesis with the underlying mechanisms “resource accumulation” and “resource depletion”, the resource switching hypothesis, and the resource matching hypothesis (Janzen 1971; Kelly 1994;

Kelly and Sork 2002; Monks and Kelly 2006; Hacket-Pain et al. 2015; Pearse et al. 2016;

Bogdziewicz et al. 2020a). According to the resource storage hypothesis, a mast year only occurs after at least one year with no or low seed production in which resources will be accumulated and stored (resource accumulation / resource storage) until a certain threshold is reached (Isagi et al. 1997; Satake and Iwasa 2000; Masaka and Maguchi 2001; Monks and Kelly 2006; Crone and Rapp 2014; Han et al. 2014; Abe et al. 2016; Pearse et al. 2016;

Pesendorfer et al. 2016; Venner et al. 2016; Bogdziewicz et al. 2018; 2020a).

Synchronisation of seed production between individual trees occurs due to an additional factor such as pollination efficiency or weather cues (Rees et al. 2002; Pearse et al. 2016).

Due to the reproductive effort during the mast year resource depletion will likely occur in the year(s) after the mast year (Janzen 1971; Hacket-Pain et al. 2015; Pearse et al. 2016).

The resource switching hypothesis assumes that trees have a relatively constant annual resource budget of which a variable fraction is allocated to generative growth. Therefore, vegetative growth is likely to be reduced during a mast year (Kelly 1994; Pearse et al. 2016;

Bogdziewicz et al. 2020a). The resource matching hypothesis states that favourable environmental conditions will lead to enhanced resource availability, which then triggers fruit and seed production (Kelly and Sork 2002; Monks and Kelly 2006; Pearse et al. 2016).

Hence, generative as well as vegetative growth will be enhanced in mast years (Kelly 1994;

Pearse et al. 2016).

Masting strategies

Pearse et al. (2016) found indication for two differing masting strategies in long-lived species. Flowering masting species require preparation of flower buds in the previous year as they do not produce flowers every year. Thus, they are dependent on weather cues in the years before a mast year to induce the process of flower bud production. In contrast, fruit maturation masting species produce flowers every year and are solely dependent on advantageous weather conditions in the flowering season to synchronise pollination.

Geburek et al. (2012) found that forest tree species also differ in pollen production strategies which can be linked to the masting strategies described by Pearse et al. (2016). Geburek et al. (2012) found that in some species the amount of produced pollen shows fluctuations between years while in other species, pollen production was abundant every year.

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Furthermore, the latter species exceeded by far the amount of produced pollen of the species with fluctuating pollen production. Due to these findings Geburek et al. (2012) defined two pollen producing types: masting pollen producers and non-masting pollen producers.

Masting pollen producers flower only in some years and are very likely to succeed in subsequent fruit production, while non-masting pollen producers bloom every year and are mostly dependent on favourable weather conditions during flowering for successful pollination. Only then they will produce fruits. Hence, in some species flower production occurs only in some years, and investment into flower production is lower (flowering masting species / masting pollen producer; Geburek et al. 2012; Pearse et al. 2016). For other species, annual flower production occurs but is not necessarily followed by fruit production (fruit maturation masting species / non-masting pollen producers; Geburek et al. 2012; Pearse et al. 2016).

Triggers and inhibitors for mast years

Important triggers for fruit production in forest tree species often include specific weather conditions, so called weather cues. These traits have been investigated for a multitude of species (Sork et al. 1993; Smaill et al. 2011; Kelly et al. 2013; Kasprzyk et al. 2014; Koenig and Knops 2014; Holland and James 2015; Moreira et al. 2015; Bisi et al. 2016; Monks et al. 2016; Bogdziewicz et al. 2017; Lebourgeois et al. 2018). In recent studies, distinct weather cues as triggers for mast years could be found for Norway spruce, European beech, and sessile and pedunculate oak. Scots pine, however, did not show consistent weather cues inducing mass seeding on a larger spatial scale (Bisi et al. 2016). Earlier studies showed that in Scots pine, the temporal fluctuation in fruit production is smaller than in other species (Wauters et al. 2001; 2004; Bisi et al. 2016). In Norway spruce and European beech, the main weather cues leading to mast years are a cool summer, followed by a warm and dry summer, which is then followed by a mast year (Piovesan and Adams 2001; Selås et al.

2002; Solberg et al. 2004; Drobyshev et al. 2010, 2014; Müller-Haubold et al. 2013; 2015;

Hacket-Pain et al. 2015; Bisi et al. 2016; Bogdziewicz et al. 2017; Vacchiano et al. 2017;

Lebourgeois et al. 2018). This distinct weather pattern in the two years before a mast year for Norway spruce and European beech is in accordance with the ΔT hypothesis of Kelly et al. (2013) which states that the difference in summer temperatures in the two years before the mast year is the main explanatory weather cue for mast years, the first summer being cooler than the second. For oak species, weather conditions in the years before a mast year showed no spatially consistent weather cues to induce masting (Sork et al. 1993; Pérez- Ramos et al. 2010; Fernández-Martínez et al. 2012; 2016; Kasprzyk et al. 2014; Wesolowski

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et al. 2015). For oak species, warm conditions during the pollination period is the only consistent weather driver for mast years (Bogdziewicz et al. 2017; Lebourgeois et al. 2018).

Weather conditions can also act as an inhibiting factor, preventing successful pollination or ripening of the fruits. Typical negative weather conditions include frost events, prolonged rain periods, or hail storms during the pollination period (Stephenson 1981; Selås et al.

2002; Bogdziewicz et al. 2018). Another important inhibiting factor for fruit development (after successful pollination) are pest events. In those cases, trees stop further development of fruits and lose the damaged fruits (Williamson 1966; Stephenson 1981).

Impacts of mast years

The additional food source provided during mast years in large fruit species is not only advantageous for livestock. In Europe, wildlife populations are typically affected by mast years of Fagus sylvatica L. and Quercus species. In wild boar (Sus scrofa L.) populations, the number of piglets is enhanced in the year following oak mast years (Wohlgemuth et al.

2016; Touzot et al. 2020). A similar increase in offsprings in the year after a mast year has been described by Gurnell (1983) for grey squirrels (Sciurus carolinensis J. F. GMEL.).

Analysis of the stomach content of red deer (Cervus elaphus L.) showed that in mast years, significantly less crop was consummated than in other years, leading to less severe crop losses (Picard et al. 1991). To save resources, the roost building species of bramblings (Fringilla montifringilla L.) which breeds i.a. in Northern Europe winters in the northernmost areas where food supply is sufficient. Jenni (1987) found that this behaviour is dependent on beech mast years in Middle Europe.

Historically, acorns and beechnuts were an important additional food source for humans during years of famine (Bolle 1891). However, mast years can also have negative effects on humans. They can lead to enhanced infection pressure of several zoonoses which are transmitted via invertebrate and vertebrate vectors (Vapalahti et al. 2003; Ostfeld 2012).

Hanta viruses which can cause haemorrhagic fever are transmitted via animal faeces (Vapalahti et al. 2003). In their wake, mast years generally lead to an increase of the vector populations for these viruses, typically small rodents, and the infection pressure is higher after mast years. Lyme borreliosis is transmitted by ticks which themselves are dependent on mice and deer populations. Randolph (1998) states that in the USA, researchers detected clear transmission pathways between the deer tick (Ixodes scapularis SAY), the white-footed mouse (Peromyscus leucopus RAF.) and the white-tailed deer (Odocoileus virginianus W.

ZIMM.) for Borrelia burgdorferi sensu lato which triggers Lyme borreliosis. Brugger et al.

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(2018) found that in South Germany, high fructification levels in European beech lead to an increase in infection pressure of tick-borne encephalitis and Lyme borreliosis, transmitted by the castor bean tick (Ixodes ricinus L.), two years after beech mast years.

High fruit production can also change resource allocation between generative and vegetative growth. In European beech stem growth is known to be reduced during mast years which has been shown for various European regions (France: Lebourgeois et al. 2018; Germany:

Eichhorn et al. 2008; South Sweden: Drobyshev et al. 2010). In oak species, however, stem growth increased during mast years in France (Lebourgeois et al. 2018) while in the Russian Volga region, Askeyev et al. (2005) found that stem growth was not only enhanced during the mast year but also in the subsequent year. Furthermore, mast years can change allocation dynamics of carbon (C), nitrogen (N), and phosphorus (P) which was investigated in recent studies. In deciduous European tree species, stored C is primarily invested into leaf production, and C allocated to fruits is currently synthesised (Hoch et al. 2013; Ichie et al.

2013; Han and Kabeya 2017). A reduction of leaf N during mast years was found for deciduous species (Han et al. 2011; Müller-Haubold et al. 2015), and in F. crenata, leaf and branch N concentration was still reduced in the year after the mast year (Han et al. 2014).

Jonard et al. (2009) suggested that leaf N and P may be reduced during mast years in European beech and oak species. Abe et al. (2016) and Yasumura et al. (2006) showed that fruit production in European beech requires huge amounts of N but Yasumura et al. (2006) did not find a reduction in leaf N during mast years. Fernández-Martínez et al. (2017) showed that leaf P concentrations in deciduous species across Europe correlated positively with fruit production. These results suggest that, in accordance with the resource accumulation / resource storage mechanism of the resource budget hypothesis, N and P availability may be a main trigger for mast years.

Impact of climate change on mast behaviour

Mast frequency in all investigated deciduous species increased in the last few decades (European beech: Bogdziewicz et al. 2020b; sessile and pedunculate oak: Caignard et al.

2017; Shibata et al. 2020). According to the latest IPCC reports (IPCC 2013; 2019) extreme weather events, including prolonged summer heat waves and droughts, late frost in spring and heavy rain during winter are very likely to increase. Recent climate models such as Representative Concentration Pathways (RCP 8.5) forecast a temperature rise in all seasons.

Annual precipitation sums might not change, but summer precipitation sums are likely to decrease up to 40%, leading to a higher risk for summer droughts, while winter precipitation

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sums are likely to increase up to 30% (IPCC 2013). As dry summer conditions are unfavourable for stem growth in the investigated deciduous species, stem growth may decrease in the next few decades (Piovesan et al. 2008; Scharnweber et al. 2012; Michelot et al. 2012; Seidling et al. 2012). These climatic changes have the potential to induce stress in formerly well adapted forest tree species and, consequently, in forest ecosystems.

Recently published studies investigating several aspects of the impact of the Swiss 2018 heat wave and prolonged drought on forests show that such events are likely to have severe impacts on future forest management (Rigling et al. 2020; Rohner et al. 2020; Schuldt et al.

2020; Wohlgemuth et al. 2020). Especially European beech and Norway spruce were affected by the 2018 summer heat wave and drought, showing signs of stress such as reduced stem growth, early leaf fall, branch dieback, bark beetle and leaf parasite infestations (Rigling et al. 2020; Rohner et al. 2020; Schuldt et al. 2020; Wohlgemuth et al.

2020) and, in European beech, early fruit abortion (Chapter II). In contrast, oak species do not appear to be negatively affected by high summer temperatures so far (Shibata et al.

2020).

Investigated species

The most abundant tree species in Europe are Scots pine (Pinus sylvestris L.) and Norway spruce (Picea abies (L.) KARST.), European beech (Fagus sylvatica L.), sessile oak (Quercus petraea (MATT.) LIEBL.), and pedunculate oak (Q. robur L.). The natural range of Scots pine stretches from Scotland to Siberia, and from Fennoscandia to the Alpine Arc.

Scots pine relics can also be found in the southern mountainous regions of the Pyrenees, the Massif Central, the Apennines, the Dinar Mountains, the Carpathians, the Pontic Mountains, and the Caucasus (Caudullo et al. 2017; Fig. 1). In Middle Europe, Scots pine has low competitive strength but is tolerant to dry and very moist soil conditions, as well as to nutrient poor soils (Ellenberg 2009; Fig. 2).

The natural range of Norway spruce stretches from the western Alps to the Ural Mountains, and from Fennoscandia to the Balkan Peninsula. Similar to Scots pine, in the South Norway spruce is only present in mountainous regions, namely in the Dinar Mountains, the Carpathians, and the Rhodope Massif at the Bulgarian-Greek border (Schmidt-Vogt 1974;

Caudullo et al. 2017; Fig. 1). It is less tolerant to dry or wet conditions than Scots pine which leads to the absence of Norway spruce in western Europe, Iberia and Great Britain (Lang 1994; Fig. 2).

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Figure 1 Natural ranges of the focal species in Europe according to Caudullo et al. (2017).

European beech is spatially distributed from Brittany and South England to approximately 40° East, and from South Scandinavia to Sicily, with a mountain relic on Crimea. In Iberia, European beech is only native in the Pyrenees (Caudullo et al. 2017; Fig. 1). European beech typically occurs in temperate and maritime climates with moist summers and mild winters, but is not tolerant to continental climates (Bolte et al. 2007; Fig. 2). Furthermore, it is susceptible to spring frosts and droughts (Ellenberg 2009).

Sessile oak occurs from Ireland to the Black Sea, and from South Scandinavia to Italy and the Balkan Peninsula. In the southern regions it mainly grows in mountainous areas, such as the Pyrenees, the Apennines, the Pontic Mountains, and the Caucasus, whereas in the Alps and the Carpathians, temperatures are too low, and in the Pannonian basin, it is too dry for this species (Ellenberg 2009; Caudullo et al. 2017; Figs. 1, 2).

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The natural range of pedunculate oak stretches from Ireland and Portugal to the Ural Mountains, and from South Scandinavia to South Europe. On the Iberian Peninsula, it only occurs at the west coast, but is absent in the heartland and the Mediterranean coast of Spain (Caudullo et al. 2017; Fig. 1). Pedunculate oak is more tolerant to continental climates than sessile oak, hence the occurrence in Eastern Europe. This species is less shade tolerant than European beech. It only dominates regions where European beech is a weak competitor, e.g.

on periodically flooded or nutrient poor soils, and in the northern areas with a high risk of late frost events (Ducousso and Bordacs 2004; Fig. 2).

Figure 2 Ecological niches of the focal species. The range of moisture and acidity affecting the three species in the submontane belt in a temperate sub-oceanic climate in the absence of forest management according to Ellenberg and Klötzli (1972) and ETH Zurich (2002).

Research gap

In the face of the current climate change, understanding the mechanisms behind mast behaviour, the triggers and inhibitors for mast occurrence, the resource dynamics mechanisms leading to mass seeding, and the impact of mast years on forest ecosystems is crucial for system understanding, estimating future trait dynamics and, finally, also for forest management. For a sustainable forest management strategy it is important to know

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which tree species will be able to succeed in future climates in the next few decades. Mast years are partly triggered by weather conditions and, therefore, gaining knowledge about risks for successful pollination and fruit development is crucial for natural regeneration of forests. Furthermore, estimating the survival potential for recent forest tree species can help to decide if changes in species composition are necessary to guarantee forest ecosystem services in future climates, such as climate change mitigation, protection against natural disasters, provision of wildlife habitats or timber and firewood production. Although in the last few years research on mast behaviour became an important field in forest ecosystem science, studies often concentrate on quite limited spatial and temporal data ranges. Only a few studies were performed lately at continental scale. Ascoli et al. (2017) found that mast years in Norway spruce and European beech are triggered by the North Atlantic Oscillation, and Piovesan and Adams (2001) and Vacchiano et al. (2017) showed that weather conditions in the previous two summers induce mast years in European beech. For the other main European forest tree species, studies on mast behaviour at a continental scale are rare.

Especially for species which do not synchronise their flowering over large areas but show more regional patterns, such as oak species and Scots pine (Nussbaumer et al. 2016), harmonised measurements of environmental and arboreal parameters at a continental scale is an important source for better understanding ecological processes which involve mast years. The present thesis aimed to make a substantial contribution to reducing this knowledge gap.

Main objectives

The overall objective of this Ph.D. project was to investigate i) triggers and ii) inhibitors of mast years, iii) changes in vegetative growth and nutrient concentrations before, during and after mast years, iv) changes in nutrient concentrations in mast years, and v) the resource dynamics mechanisms behind mast years in the main European forest tree species. To address these issues, long-term data from various surveys of the European ICP Forests Level I and Level II sites, along with similar sites in Croatia and Switzerland, were analysed.

Specifically, the following research questions were raised and addressed in three chapters:

i) Chapter I

• Which weather conditions are triggers for mast years in the focal species and how spatially consistent are these weather conditions at a continental scale?

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• Do inhibiting environmental or internal factors exist which prevent mast occurrence in the focal species?

iii) Chapter III

• How does vegetative tree growth change when mast years occur?

Which resource dynamics mechanisms are involved in fruit and leaf production, and stem growth of the investigated species?

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Mast triggers in European forest tree species

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Chapter I

Impact of weather cues and resource dynamics on mast occurrence in the main forest tree species in Europe

Published as:

Anita Nussbaumer, Peter Waldner, Vladislav Apuhtin, Fatih Aytar, Sue Benham, Filippo Bussotti, Johannes Eichhorn, Nadine Eickenscheidt, Petr Fabianek, Lutz Falkenried, Stefan Leca, Martti Lindgren, María José Manzano Serrano, Stefan Neagu, Seppo Nevalainen, Jozef Pajtik, Nenad Potočić, Pasi Rautio, Geert Sioen, Vidas Stakėnas, Celal Tașdemir, Iben Margrete Thomsen, Volkmar Timmermann, Liisa Ukonmaanaho, Arne Verstraeten, Sören Wulff, Arthur Gessler. 2018. Impact of weather cues and resource dynamics on mast occurrence in the main forest tree species in Europe. Forest Ecology and Management 429:

336-350. doi: 10.1016/j.foreco.2018.07.011

This peer-reviewed article is reprinted as the final submitted manuscript. It has been modified to fit into the layout of this thesis.

Keywords: Fagus sylvatica, mast fruiting, Picea abies, Pinus sylvestris, Quercus petraea, Quercus robur, resource dynamics, weather cues