![Redundancy Analysis (RDA) of species composition, with envelopes around samples (plots) representing groups of identified plant communities. RDA without site (RDA − s) used for creating ordination diagrams. RDA axis 1 explained 7% of total variance, RDA axis 2 explained 4.8%. The nine plant communities differ in aspects of vegetation structure (a), species composition (b), species richness (species/[4 m2]; c), and the linear constraints identified in RDA − s for explaining species composition differences (d). Constraints were age structure of heather (% of cover; P, Pioneer; B, Building; M, Mature; and D, Degeneration, explaining all together 3.8%), airborne nitrogen deposition (0.8% exp. variance) and humus accumulation (2.4%). For species composition (b), only the 10% of the species fitting best to the RDA ordination and the 70% most abundant species were displayed using the ordiselect()-function in R (Goral and Schellenberg, 2019). Three main gradients shaping heathland species composition were identified: (1) along the first axis: shift of edaphic soil conditions along a successional gradient, with early stages at the left and later ones on the right part of the diagram; (2) along the second axis: structural gradient with open, grass-rich stand in the upper part of the diagram and dominance, but bryophyte-and lichenrich stands at the bottom; (3) climate and airborne nitrogen deposition, with sub Atlantic/subcontinental sites with low nitrogen deposition at the lower left quadrant of the diagram and higher nitrogen loads and Atlanticsubatlantic sites in the upper right quadrant.](https://www.researchgate.net/profile/Jenny-Schellenberg-2/publication/363271558/figure/fig2/AS:11431281098601349@1669024865624/Redundancy-Analysis-RDA-of-species-composition-with-envelopes-around-samples-plots_Q320.jpg)
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Vitality of heather (Calluna vulgaris)
along gradients of climate, structure and
diversity in dry lowland heathland habitats
of Northern Germany
Dissertation for the award of the degree
“Doctor rerum naturalium” (Dr.rer.nat.)
of the Georg-August University Göttingen
within the doctoral program Biology
of the Georg-August-University School of Science
(GAUSS)
doi :10 .53 846/g oed iss -92 85
submitted by
Jenny Schellenberg
from Dresden
Göttingen, 2022
Thesis committee
Prof. Dr. Erwin Bergmeier
Department Vegetation and Phytodiversity Analysis, Albrecht von Haller Institute for Plant
Sciences, University of Göttingen
Prof. Dr. Markus Hauck
Department Applied Vegetation Ecology, University of Freiburg
Members of the Examination Board
Reviewer:
Prof. Dr. Erwin Bergmeier
Department Vegetation and Phytodiversity Analysis, Albrecht von Haller Institute for Plant
Sciences, University of Göttingen
Second Reviewer:
Prof. Dr. Markus Hauck
Department Applied Vegetation Ecology, University of Freiburg
Further members of the Examination Board:
Prof. Dr. Hermann Behling
Department of Palynology and Climate Dynamics, Albrecht von Haller Institute for Plant
Sciences, University of Göttingen
Prof. Dr. Johannes Isselstein
Institute of Grassland Science, University of Göttingen
Prof. Dr. Matthias Waltert
Department of Conservation Biology, University of Göttingen
Prof. Dr. Catrin Westphal
Functional Agrobiodiversity, Department of Crop Sciences, University of Göttingen
Date of the oral examination: 15.02.2022
Calluna vulgaris
Table of contents
Chapter 1: Introduction 1
1.1 A short history of North German heathlands 2
1.2 Calluna vulgaris 4
1.3 Heathland conservation efforts 6
Protection facts and framework 6
Heathland management 7
Threats and pressures 9
Assessing the conservation status 10
1.4 Study areas and Sampling 12
Study areas 12
Sampling 17
1.5 Dry Lowland heathland ecology: Gaps of knowledge to cover 18
Heathland plant species composition and vegetation structures 18
Calluna life cycle as the determinant for heathland dynamics 19
Drought susceptibility of young Calluna plants under changing
climate and high N loads 20
Chapter 2: Heathland plant species composition and vegetation
structures reflect soil-related paths of development and site history
23
2.1 Introduction 25
2.2 Methods 27
Study sites 27
Sampling Design 27
Statistical analysis 30
2.3 Results 32
Main characteristics of North German dry heathland plant
communities 32
Factors shaping species composition and structures 33
Pathways of heathland development 39
Conservation value of heathland plant communities 41
2.4 Discussion 44
Floristic and structural characteristics of dry lowland heathlands 44
Environmental conditions determining heathland vegetation 45
Heathland succession pathways 46
Conclusions and implications for conservation management 47
Chapter 3: The Calluna life cycle concept revisited: implications for
heathland management 51
3.1 Introduction 53
3.2 Methods 56
Study areas and sampling 56
Statistical Analysis 58
3.3 Results 60
Determinants of heather vitality 60
Calluna vitality depends on age and life history 63
3.4 Discussion 67
Determinants for heather vitality and its dependence on age 67
The life cycle concept 69
Conclusions 74
Chapter 4: High nitrogen deposition increases the susceptibility of
Calluna vulgaris recruitment to drought 77
4.1 Introduction 79
4.2 Methods 83
Data sampling 83
Climate 85
N deposition 85
GLMM 85
4.3 Results 87
Climate 87
Response overview 92
Effects of drought on young Calluna plants 92
Responses of seedlings (PS) and resprouted plants (PR) to drought 93
Nitrogen deposition affecting Calluna recruitment under drought 96
4.4 Discussion 98
How does drought during growing season affect young
Calluna plants? 98
Differ resprouted and germinated young plants in their resistance
to drought? 100
Does nitrogen deposition reduce young Calluna plants’ resistance
to drought? 100
Chapter 5: Synthesis 105
5.1 New insights into North German dry lowland heathland ecology 106
Heathland plant community ecology and floristic patterning 106
The Calluna life cycle revisited 108
Calluna recruitment response to drought and high airborne
nitrogen loads 111
5.2 Implications for future dry lowland heathland management 113
The role of management for the provision of high nature
conservation value heathland 113
Managing Calluna demographics under changing climate and
high N depositions 115
Implications for the future nature conservation status assessment
and monitoring 117
References 121
Appendix 137
Electronic Supplementary Material Folders and files on included CD 140
Acknowledgements 142
Academic Curriculum Vitae 143
List of Abbreviations
B Building growth phase
CI95 95% Confidence interval
D Degeneration growth phase
D_2014 Scenario used in Chapter 4, representing the maximum drought conditions in 2014
ESM Electronic Supplementary Material, see Appendix p. 140
GLMM Generalized Linear Mixed Model
HT Habitat type in the Natura 2000 network
K Kotilainen’s Index of Oceanicity
LMM Linear Mixed Model
M Mature growth phase
MaxD_10YEAR Scenario used in Chapter 4, representing the most severe drought conditions in 2011-
2020
N Nitrogen, unless otherwise specified the airborne nitrogen load in kg*ha-1*yr-1
NoD_2014 Scenario used in Chapter 4, representing the minimum drought conditions in 2014
P Pioneer growth phase (Chapter 3); Precipitation sum in the survey period (Chapter 4)
PL Calluna plants from prostrate adventitiously rooted stems (‘layering’)
PS young Calluna recruits germinated from seed
PR Calluna plants resprouted from older ones, mostly from Mature- or Building stage
plants after aboveground biomass disturbance
SD Standard deviation
SPEI Standardized Precipitation and Evapotranspiration Index (Chapter 4)
T Mean air temperature (°C) in the survey period (Chapter 4)
List of Figures
Chapter 1: Introduction
Fig. 1.1 Map of study area locations and the gradients of Climate (Oceanicity, Annual
precipitation and mean Temperature) and N deposition 14
Fig. 1.2 Schematic Sampling Design 17
Chapter 2: Heathland plant species composition and vegetation structures
reflect soil-related paths of development and site history
Fig. 2.1 Map of Study areas 29
Fig. 2.2 NMDS: development stages and main structural differences between floristic groups
in North German lowland heathlands 37
Fig. 2.3 Heathland plant community structures; cover proportions (%) of Calluna vulgaris,
open soil, non-graminoid herbs, graminoids, bryophytes and lichens 38
Fig. 2.4 Succession schemes of German dry lowland heathlands 41
Chapter 3: The Calluna life cycle concept revisited – implications for heathland
management
Fig. 3.1 Calluna habit and plant morphological terms used in this study 56
Fig. 3.2 Age of the individual plant and the stems for plants grown from seed (PS), from
resprouting (PR) and from layering (PL) 63
Fig. 3.3 Calluna plant age at the time of severe disturbance 64
Fig. 3.4 Calluna vitality attributes over the plants’ life span 65
Fig. 3.5 Flower density in PS, PR and PL 66
Fig. 3.6 Calluna life cycle 71
Chapter 4: High nitrogen deposition increases the susceptibility of Calluna
vulgaris recruitment to drought
Fig. 4.1 Photographs of highly vigorous and drought-damaged Calluna seedlings and
resprouted plants 80
Fig. 4.2 Schematic examples for yearly increment and drought damage data sampling 84
Fig. 4.3 10-Year overview for SPEI, mean daily air temperature and precipitation sum during
the survey period in the 19 study areas 89
Fig. 4.4 Study area climate in 2014 91
Fig. 4.5 Overview of response variables 92
Fig. 4.6 Yearly increment and long shoot damage frequency in the three climate scenarios 93
Fig. 4.7 Responses of seedlings and resprouted plants in the three climate scenarios 95
Fig. 4.8 Effects of life history N deposition on yearly increment and long shoot damage
frequency, in the three climate scenarios 97
List of Tables
Chapter 1: Introduction
Table 1.1 Distribution and extent of designated Dry lowland heathland in the EU and
Germany 6
Table 1.2 Study area characteristics: Location, size, protection status, site history and recent
management. 13
Table 1.3 Study area characteristics: Climate conditions and N deposition 16
Chapter 2: Heathland plant species composition and vegetation structures
reflect soil-related paths of development and site history
Table 2.1 Environmental variables and their attributes used to relate species composition to
site history, recent management and soil conditions 28
Table 2.2 Synoptic table of heathland plant communities in the North German Plain 34
Table 2.3 Gross and net effects of environmental factors on species composition 36
Table 2.4 Assessment of potential nature conservation status, based on national criteria,
considering heathland-typical species inventory, structures and threats 43
Chapter 3: The Calluna life cycle concept revisited – implications for heathland
management
Table 3.1 Calluna vitality attributes 57
Table 3.2 Proportion of explained inertia of RDAroot and RDAstem on the vitality parameters 61
Table 3.3 Age-dependent vitality LMM results 62
Table 3.4 Vitality differences between seedlings, resprouting plants and layering plants 67
Chapter 4: High nitrogen deposition increases the susceptibility of Calluna
vulgaris recruitment to drought
Table 4.1 Vitality attributes (responses) and predictors for modelling drought 87
Table 4.2 Explanatory power (R²) of partial and full models 94
Table 4.3 Scenario mean differences 95
Summary
This thesis provides a fundamental overview to North German Dry lowland heathland
vegetation composition, vegetation structures and the determinants for the vitality of the key
species, Calluna vulgaris. It offers new insights into the complex interactions of site history-
related disturbances, edaphic conditions, climate and nitrogen (N) deposition, with
consequences for heathland habitat quality. The main threats protected heathland habitats
are faced with are primarily related to recent management. The purpose of heathland
management is to provide suitable conditions for favourable habitat diversity and structures,
ensuring the long-term maintenance of the ecosystem functionality. Under changing
conditions of climate and pollution, heathland management is challenged with inter- and
counteracting effects of traditional management and recent threats.
Heathlands in the German Northwest are among the most nutrient-poor habitats. In historical
times, heathland faming induced and maintained the nutrient poverty, as well as associated
species and structures, but the invention of artificial fertilizers allowed for the cultivation of
the poor sandy substrates in the early 19th century. As a consequence, the former nitrogen
(N)-limited heathland ecosystems were exposed to inputs of N, either directly with fertilizers,
or indirectly with airborne or fluent deposits. The fast increase in plant-available N within a
century faces the recent heathlands with threats like species composition changes, fertilizing
effects with boosted growth and accelerated ageing as well as reduced drought resistance.
Additionally, there is a trend towards longer and more severe droughts in the study areas, as
well as more imbalanced and generally lower rainfall. As a consequence, the changing climate
and high N depositions are challenging efforts for heathland protection, demanding for an
improved basic knowledge to heathland responses to those threats and the possibility to
compensate for them.
Based upon 352 plots in 19 dry lowland heathlands, data to plant assemblages, soil
conditions as well as Calluna age structures and vitality were collected in the years 2013 and
2014. The analysis focussed on 1) heathland plant community ecology, with a
characterisation of plant composition and its determinants along dynamic heathland
development pathways, 2) Calluna plant life history, with the revision of the Calluna life cycle
as the central criterion for the assessment of age structures and 3) the drought susceptibility
of Calluna recruitment under high N loads, as a determinant for post-disturbance heathland
recovery with potential consequence for long-term heathland maintenance.
The analysis of plant community composition and structures revealed two edaphically
distinct pathways of heathland development; 1) the psammophilous heathland pathway,
which describes heathland development on poor, loose drift sands, representing early stages
in the seral progression of altering soil conditions along long-term successional changes, and
2) the consolidated sand heathland pathway, representing heathland development on more
developed, but still poor sandy soils. Their edaphic conditions are determined by historical
and recent land use, emphasizing the character of young psammophilous heaths occurring in
the North German East as a product of military training activities in the past century and the
older, historical heathlands in the Northwest, with consolidated sand heaths prevailing.
Mosaic heathlands in close contact to pioneer grasslands provided highest diversity in
species and structures, thus confirming the importance of early –stage conditions, providing
host for many threatened species, in particular lichens.
The Calluna life cycle is the key criterion for determining age structures in the terms of
heathland habitat nature conservation status assessments. But the established concept lacks
in some detail to regeneration processes and the habitual diagnostics of regenerating plants,
with consequences for management planning and the estimation of regeneration potentials.
Hence, this study provides an extended life cycle, including the regeneration processes of
post-distubance resprouting and layering Calluna plants. The study provides evidence that
age-related shifts in Calluna vitality are determined by both, the aboveground (regeneration)
age and the total plant age. Thereby, the high-vital life phase is restricted to approx. 15 years,
and resprouting may induce a regrowth to a mature plant again, with another approx. 10
years of high vigour, but there was no evidence for an elongated total life by a resprouting
cycle. The inability to regenerate with a high vigour and to regrow to a Mature-phase plant
again was related to the shift from the primary rooting supply to de-central adventitious
rooting, a process which was shown to be determined by the total plant age and hence
irreversible. As a consequence, the findings of this study do not support the theory of
repetitive cycling in terms of unrestricted highly vigorous resprouting and the constant
layering of procumbent stems as the regeneration of older plants was confirmed as a quite
stable, but often low-productive stage of degeneration.
Young Calluna plants had a high resistance to drought during the growing season, although
growth rates were reduced and tissue damages increased under severe drought conditions.
Thereby, seedlings were rather negatively affected than resprouted plants.
The results presented in this thesis clearly show that droughts under high N depositions are
important post-disturbance heather regeneration determinants. Thereby, the effect of N
deposition depends chiefly on the drought severity; high N loads limit Calluna seedlings
under conditions of extreme drought on the one hand, but favour the growth of seedlings and
resprouted plants under non-drought conditions on the other. Under severe drought,
complete generations of young Calluna seedlings may get lost, especially under high N loads,
and successful Calluna recruitment from seed may only take place in years of favourable
conditions. As a consequence, heath stands that regenerate mainly from seed, e.g. after sod-
cutting, are particularly vulnerable to droughts in their early regeneration stages, especially
under high N load, whereas regeneration from resprouting plants provides a high resistance.
However, the results presented in this study showed that high N loads reduce the competitive
power of young Calluna plants by altering the stomatal sensitivity, with lethal consequences
for seedlings, and a reduced growth for resprouted plants under drought.
With a reduction of competitive strength, not only Calluna cover decreases, but also general
heathland plant species composition changes take place. The results of this thesis support a
high N-load induced reduction of the low-productive species pool from early successional
stages, such as lichens, and an increase of regeneration stages of low diversity. Mosaic stands
with a high potential to harbour high species diversity become grass-dominated heathland
mosaics under high N.
The results to North German dry lowland heathland species composition and their dynamics,
the Calluna life cycle and the drought resistance of Calluna recruitment strengthens the
biological-ecological knowledge required for informed advice on heathland management and
thus provides some implication for the specification of nature conservation assessment
criteria, ensuring an improved assessment of heathland habitat quality and regeneration
potentials. Additionally, the findings of this thesis highlight the need for a sharpened view on
the changes in dry lowland heathland ecosystems and to figure out whether managements
have the potential to counteract some of the recent threats and degeneration processes
induced by natural succession, but altered by changing climate and high N loads. The specific
need for intensive soil disturbances to provide early-stage soil conditions was highlighted in
this study, but it also pointed out that post-disturbance regenerations are prone to droughts.
Hence, the challenge for future management is to weigh between trade-offs and to balance
probabilities of risks and success. Thereby, high-intense, but small-scale disturbances in
varying frequencies and management combinations may provide the highest probability to
improve the resilience of heathland habitats to future climate changes and to ensure a high
species and structural diversity in heathland landscapes for maintaining their functionality.
Zusammenfassung
Heidelebensräume des norddeutschen Tieflands sind aufgrund ihrer kulturhistorischen
Bedeutung, ihrer Einzigartigkeit und ihrer vielfältigen Ökosystemdienstleistungen schützens-
werte Habitate. Sie verfügen über eine Artengemeinschaft die zwar nicht durch
Artenreichtum besticht, aber die sich über die letzten Jahrhunderte an nährstoffarme,
menschenbeeinflusste Offenlandlebensräume angepasst hat. Durch den Verlust solcher
Habitate seit der Mitte des 19. Jahrhunderts, bei denen es durch vielfältige Landnutzungs-
änderungen zur Wiederaufforstung, Umwandlung in Grünländer oder Äcker zum Rückgang
der Lebensraumfläche insgesamt kam, sind die heute verbliebenen Flächen unter
europäischem und nationalem Naturschutzrecht geschützt und die Lebensräume müssen in
ihrer Artengemeinschaft und Vielfältigkeit, die die Strukturen und Funktion bestimmen,
geschützt werden.
Der Erhaltungszustand von trockenen Tieflandsheiden in Mitteleuropa wird überwiegend als
schlecht bewertet, maßgeblich verursacht durch fehlendes oder falsches Management. Hinzu
kommen jedoch Veränderungen im Nährstoffhaushalt und dem Klima, die die Effizienz der
etablierten Maßnahmen einschränken und die generelle Resistenz der Heide gegenüber
ökologischen Stressfaktoren, wie Trockenheit oder Insektenkalamitäten vermindern. Lang-
fristig bedeutet eine verminderte Vitalität der Besenheide (Calluna vulgaris), die als
Schlüsselart maßgeblich zum Aufbau, der Struktur und den Habitatbedingungen der
vorkommenden Heide-Lebensgemeinschaften beiträgt, eine Verschiebung im Konkurrenz-
gefüge, was zur Habitatdegradation, z.B. zur Vergrasung mit Deschampsia flexuosa oder
Molinia caerulea, führt.
Zahlreiche Studien untersuchten bisher die Gründe und Ursachen vom Rückgang der Heide-
Habitatqualität, mit dem Ergebnis, dass nur die Berücksichtigung sehr vieler, komplexer
Zusammenhänge Erklärungsansätze bieten. Die vorliegende Arbeit versucht diese für die
norddeutschen trockenen Tieflandsheiden zu untersuchen und gibt daher zunächst einen
umfassenden Überblick über die Vegetation und ihren ökologischen und strukturellen
Charakteristika. Aus diesen werden die historisch und/oder edaphisch bedingte Vergesell-
schaftungen der Arten sowie Vegetationsstrukturen herausgearbeitet und in ihren
Entwicklungspotentialen bewertet. Da die Habitatqualität maßgeblich von der Vitalität und
vom Lebenszyklus der Calluna vulgaris bestimmt wird, beschäftigt sich ein weiterer
Schwerpunkt dieser Arbeit mit dem Alterungsprozess des Zwergstrauchs. Eine wichtige
Frage hierbei ist, ob dieser unter den in Norddeutschland herrschenden Bedingungen an der
Arealgrenze trockener Tieflandsheiden Unterschiede zu den typischen Atlantischen
Vorkommen aufzeigt, ob Alterungsprozesse beschleunigt oder Regenerationsmechanismen
variieren. Weiterhin wird untersucht inwiefern vegetative Regenerationen, z.B. nach Brand,
den Lebenszyklus beeinflussen. Hierbei ist von besonderem Interesse wie langlebig die
einzelnen Stadien im Lebenszyklus sind, da diese direkt mit bestimmten Ökosystem-
dienstleistungen verknüpft sind und direkt als Bewertungsmaßstab für die Habitatqualität
dienen.
Ein weiterer wichtiger Themenbereich ist die Re-Etablierung neuer Heidevegetation nach
Störung, z.B. nach Mahd oder Brand, die nach aktuellem Kenntnisstand durch klimatische
Veränderungen und die athmogenen Stickstoffdepositionen beeinträchtigt sein könnte. Die
vorliegende Studie untersucht daher wie junge Calluna-Pflanzen auf die in Norddeutschland
vorkommenden Bedingungen von Sommertrockenheit und Stickstoffdepositionen reagieren.
In 19 Heidegebieten, verteilt über das gesamte Norddeutsche Tiefland, wurden in den Jahren
2013 und 2014 auf insgesamt 352 Aufnahmeflächen Artenzusammensetzung und
Vegetationsstruktur sowie detaillierte Parameter zum Habitus, dem Pflanzenalter, dem
Jahreszuwachs sowie Schäden an Trieb- und Blattmaterial an Calluna-Individuen erhoben.
Die daraus erstellten Klassifikationen und Modellierungen berücksichtigen jeweils eine
Vielzahl an ökologischen Einflussfaktoren und ermöglichen eine Analyse des komplexen
Gefüges sowie das Herausarbeiten der wichtigsten bestimmenden Parameter.
Die Analyse der Heidevegetation ergab zwei grundsätzlich unterscheidbare Entwicklungs-
wege, die standörtlich durch Bodencharakteristika und Nutzungsgeschichte bestimmt
werden. Ein Entwicklungsweg kennzeichnet psammophile Heiden auf nur sehr initial
entwickelten Sandböden, oft Flugsanddecken oder Inlanddünen mit extremer Nährstoffarmut,
die in engem Kontakt zum Pioniergrasland des Corynephorion vorkommen. Dement-
sprechend beherbergen sie eine Vielzahl der dort typischen Arten mit der Anpassung an
diese sehr speziellen Lebensbedingungen und stellen die artenreichsten trockenen
Heidelebensräume im Norddeutschen Tiefland dar, maßgeblich durch ihre hohe Zahl an
geschützten Flechten. Diese Artenvielfalt hält sich auch über initiale Heide-Entwicklungs-
stadien hinaus, so dass die vorliegende Untersuchung auch aufzeigt, dass die Arten-
zusammensetzung und –vielfalt nicht vorrangig durch das vorherrschende Heidealter
bestimmt wird, sondern eher durch edaphische und strukturelle Charakteristika.
Der zweite Entwicklungsweg kennzeichnet typische Heidelebensräume in den Gebieten mit
fortgeschrittener Entwicklung der Sandböden, mit Rohhumusauflagen und einer gegenüber
den reinen Sandböden verbesserten Wasserhaltekapazität und Nährstoffverfügbarkeit. Diese
Heiden beherbergen eine Vielzahl der typischen Gefäßpflanzenflora, und sind sehr variabel in
Artenausstattung und struktureller Diversität, sind aber generell recht artenarm. Mosaike
können mit dem typischen (Gefäß-)Pflanzeninventar und guter struktureller Vielfalt
auftreten, allerdings kommen auch Mosaike vor die Vergrasungsprozesse anzeigen und dann
extrem artenarm sind. Calluna-Dominanzbestände auf konsolidierten Sandböden sind oft
gleichaltrig und extrem artenarm. Sie entstehen oft als Regeneration auf Mahd- oder
Brandflächen, bei denen aber Bodenentwicklung und Humusanreicherung fortgeschritten
sind.
Ein Subtyp des zweiten Entwicklungsweges beschreibt die Entwicklung von Heiden auf
basenreicheren Standorten, wo sie in Kontakt mit basophilen Sandtrockenrasen vorkommen
und über ein sehr großes Artenspektrum verfügen können. Diese sind im Vergleich zu den
azidophilen Sandheiden relativ selten oder nur kleinräumig vorhanden.
Obwohl die Artenzusammensetzung also hauptsächlich durch nutzungsgeschichtlich
beeinflusste Bodenmerkmale und lokale Arteninventare bestimmt ist, zeigte sich, dass junge
Entwicklungsstadien eine höhere Artenvielfalt aufweisen als ältere, begründet durch die
hohe Zahl an Arten aus den Gesellschaften der am Mosaik beteiligen Pflanzengesellschaften
und der Armut an tatsächlich eng nur an Heide gebundenen Arten.
In der Störungsdynamik der Tieflandsheiden kommt demnach jungen Entwicklungsstadien
eine besondere Bedeutung zu. Managementmaßnahmen wie Plaggen, Brennen oder Mahd
bestimmen die Intensität und Schnelligkeit der Calluna-Regeneration, und daraus folgend
Bestandesstrukturmerkmale, wie die Dichte an Calluna-Individuen, die Alterszusammen-
setzung der regenerierenden Calluna und die Anteile der weiteren Arten bzw. Lebensformen,
entsprechend der oben skizzierten edaphisch bedingten Entwicklungswege.
Der Lebenszyklus der Besenheide bestimmt dabei diese Dynamik entscheidend, indem z.B.
die Aufwuchsgeschwindigkeit in der ersten Zeit nach der Störung entscheidend für den
Konkurrenzkampf mit Gräsern, v. A. Deschampsia flexuosa und Molinia caerulea, ist. In dieser
Arbeit wird gezeigt, dass der Austrieb aus wurzelhalsnahen, basalen Sprossachsen nach
Störung sehr schnell erfolgt, vorausgesetzt die Pflanzen sind zur Zeit der Störung nicht älter
als 15 Jahre. Dieser Wiederaustrieb ist durch eine hohe Biomasseproduktion und Blüh-
intensität gekennzeichnet, verlängert allerdings die totale Lebenszeit der Pflanze nicht
unbedingt, da diese sekundäre hochvitale Phase kürzer anhält als die typische Aufbauphase
einer aus dem Samen herangewachsenen Pflanze. Die Betrachtung der altersabhängigen
Veränderungen im Habitus der ober- und unterirdischen Biomasse zeigte außerdem, dass
Pflanzen aus Regeneration seltener die End-Wuchshöhe von Pflanzen, die direkt aus Samen
herangewachsen sind, erreichen. Weiterhin zeigte sich dass die Pflanzen aus Wiederaustrieb
zwar nur über wenige Jahre eine höhere Blühintensität aufweisen, aber schneller als direkt
aus Keimlingen aufgewachsene Pflanzen beginnen an niederliegenden Ästen durch
Adventivbewurzelung die Versorgung mit Wasser und Nährstoffen zu dezentralisieren und
auf eine stammweise Versorgung umzustellen. Dieser Prozess beginnt bei Pflanzen die direkt
aus Samen aufwachsen nach ca. 15 Jahren, nach oberirdischem Biomasse-Entzug allerdings
auch schon eher und wird mit dem Wiederaustrieb intensiviert. Diese Umstellung vom
primären Wurzelsystem auf das dezentrale Adventiv-Wurzelsystem geht einher mit einer
allmählichen physiognomischen Wuchsformänderung, bei der schließlich die basalen
Sprossachsenabschnitte fortlaufend neu bewurzeln und nur der diesjährig belaubte
Haupttrieb aufrecht bleibt (‚layering‘). Solche Pflanzen bilden dann dicht belaubte, grüne
Matten und können bei Unkenntnis dieser Regenerationsmechanismen fälschlicherweise als
eine Pflanze in der Aufbauphase gehalten werden. Gegenüber einer solchen sind sie
allerdings altersbedingt in ihrer Regenerationsfähigkeit stark eingeschränkt.
Der Lebenszyklus von Calluna vulgaris in Norddeutschen Tieflandsheiden unterscheidet sich
nicht grundlegend von denen anderer Tieflandheiden im Atlantischen Mitteleuropa, z.B. im
Vereinigten Königreich. Es fanden sich weder Hinweise auf eine Verkürzung der Lebensdauer
noch grundlegende Unterschiede in der Persistenz der einzelnen Wuchsphasen. Es fanden
sich Hinweise dass unter den im Norddeutschen Tiefland herrschenden Klima- und N-
Depositionsbedingungen ein etwas schnellerer Aufwuchs zur Reifephase stattfindet, aber
ohne die Lebenszeit der Pflanze zu verkürzen.
Klimaereignisse, besonders Dürreereignisse während der Vegetationsperiode, werden als
limitierende Faktoren für die Verbreitung trockener Atlantischer Tieflandsheiden vermutet.
In der vorliegenden Arbeit fanden sich jedoch kaum Hinweise auf eine klimatisch begründ-
bare floristische Unterscheidung von Atlantischer und kontinentaler Heidevegetation im
norddeutschen Tiefland, auch wenn die enge Verzahnung von Heide und Silbergrasfluren im
subkontinentalen Osten öfter auftraten. Nur wenige Arten, die zudem auf eher basen-
reicheren Standorten vorkamen, ließen eine gewisse Zunahme an Kontinentalität erahnen,
deren Wirkung aber geringer ist als die deutlich überprägenden edaphischen Unterschiede
und die gebietsspezifischen Nutzungsgeschichten. Auch der Lebenszyklus der Besenheide
scheint nicht sehr von der abnehmenden Ozeanität beeinflusst, aber weitere Studien sind
nötig um hier Gewissheit zu erlangen.
Dürre während der Vegetationsperiode beeinträchtigt die Vitalität von jungen Calluna-
pflanzen; die Jahreszuwachsraten waren geringer und die Blätter zeigten mehr
Trockenschäden. Keimlinge zeigten eine erhöhte Empfindlichkeit gegenüber Trockenheit
wenn die Stickstoffeinträge bei 25kg*ha-1*a-1 lagen, der hier genutzte erhöhte
Depositionswert, so wie dies in vielen nordwestdeutschen Heiden der Fall ist. Im östlichen
Teil des Norddeutschen Tieflandes ist die Stickstoffdeposition geringer (10-12kg*ha-1*a-1),
unter solchen Bedingungen war die Vitalität zwar unter Trockenheit verringert, war aber
zumeist nicht tödlich, selbst unter den modellierten stärksten Dürrebedingungen die
aufgrund des 10-Jahres-Trends (2011-2020) zu erwarten sind. Diese Ergebnisse belegen
dass Calluna generell eine sehr hohe Trockenheitsresistenz hat, auch unter subkontinentalen
Bedingungen, aber dass hohe Stickstoffdepositionen diese bei Keimlingen vermindern kann.
Generell zeigte sich, dass ein hoher Stickstoffeintrag die Konkurrenzfähigkeit von jungen
Calluna-Pflanzen unter Dürre reduziert und daher eine durch Vergrasung bedingte
Habitatdegradation selbst unter moderatem Trockenstress verursachen kann.
Die hier vorliegenden Ergebnisse zeigen auf, dass die Vitalität und die Lebensgeschichte der
Besenheide die Artenzusammensetzung zwar nur marginal direkt beeinflusst, denn dafür
sind die edaphischen Standortfaktoren sowie die gebietsspezifischen Arteninventare und
Managementeinflüsse wichtiger, aber dass die Habitatstruktur und die sich daraus
ergebenden Habitat-Qualitätsmerkmale stark von der altersabhängigen Vitalität determiniert
werden. Außerdem zeigte sich dass die Re-Etablierung von Calluna nach Störungen nicht nur
von der Art des Managements abhängt, sondern auch durch sommerliche Trockenheit und
hohe Stickstoffdeposition beeinträchtigt ist.
Die Arbeit untermauert die naturschutzfachlich hohe Bedeutung von frühen Heide-
Entwicklungsstadien, insbesondere diese mit mosaikartig verzahnten Pioniergrasländern, die
die höchste Arten- und Strukturvielfalt beherbergen. Die Bedeutung der Bereitstellung von
günstigen Bodenbedingungen und die Notwendigkeit der dafür notwendigen Maßnahmen
wurde erneut bestätigt, zugleich aber auch die Empfindlichkeit der jungen Regenerations-
stadien gegenüber ungünstigen Klimabedingungen während der frühen Re-etablierungs-
phase.
Außerdem stellt die Arbeit durch die Erweiterung des klassischen Calluna-Lebenszyklus um
die Regenerationswege und die Beschreibung der altersbedingten, habituellen Unterschiede
zwischen dem ungestörten und dem gestörten Lebenszyklus eine bessere Einschätzung der
Lebenshistorie von Calluna-Pflanzen bereit, so dass Einschätzungen zu Regenerations-
potenzialen und Altersstrukturen im Rahmen der Erhebung von Habitat-Qualitätsmerkmalen
treffender vorgenommen werden können.
1
Chapter 1:
Introduction
Chapter 1: Introduction
2
1.1 A short history of North German heathlands
Dry lowland heathlands dominated by Calluna vulgaris (L.) Hull (hereinafter: Calluna) are
widespread over the oceanic and sub-oceanic regions of Europe, which comprise coastal
areas bordering the North Sea and the English Channel (Gimingham 1972), but also inland
regions of France, the Netherlands, Belgium, Germany, Poland and the Czech Republic.
The typical stratification in Atlantic dry heathlands is characterized by the absence of trees,
due to the influence of man, as in temperate Atlantic or sub-Atlantic lowlands forests always
preceded heath and natural dry heathlands occur as forest understory of Oak, Pine or Birch
woodlands or small-scale clearings on nutrient-poor Pleistocene sandy sediments
(Gimingham 1972; Gimingham 1975; Hüppe 1993a, 1993b). They are dominated by Calluna
vulgaris and other Ericaceae, in Germany moreover Vaccinium myrtillus, V. vitis-idaea, Genista
pilasoa, G. tictoria and G. anglica, accompanied by stress-tolerant hemicryptophytes, pioneer
tree species (e.g. Pinus sylvestris, Betula pendula) as well as cryptogams.
The landscape character of dry lowland heathlands in Mid-Western Europe is a result of the
complex interaction of human impact and natural processes of the past 5000 years, induced
by forest degradation and historical heathland farming, with frequent disturbances resetting
successional processes in soils and vegetation (Gimingham 1975; Gimingham & de Smidt
1983; Webb 1998). This conversion of former forests and woodlands to heathlands has been
subjected in many studies, for heathlands in general (e.g. Gimingham 1972), but also
specifically for German lowland heathlands (e.g. Behre 2008; Graebner & v. Bentheim 1904;
Graebner et al. 1925; Hüppe 1993a, 1993b). During the conversion process, which started
about 3000BC, the former woodland soils became extremely nutrient-poor and acidic, first
induced by the reduction of trees, but later in the 10th century intensified by the periodical
removal of aboveground biomass, humus and topsoil (‘plaggen’; Ellenberg & Leuschner 2010).
Maximum heathland area extent in Germany was reached in the mid 19th century, with a
subsequent rapid decline, predominately due to the invention of chemical fertilisers and the
many fundamental changes in land use associated with it (Ellenberg & Leuschner 2010;
Hooftman & Bullock 2012; Piessens et al. 2005).
The large traditionally farmed open heathlands have been shaping the landscape in the
German Northwest, but they did not occur in the Eastern part of the North German Plains, or
to a much lower extent (Mortensen 1941, Pott 1999). Today, nearly 75% of the recent
heathlands is located there (referring to those designed as dry heathland habitat types in the
Natura 2000 network, Table 1.1, p. 6, with the German East roughly corresponding to the
Continental biogeographic region). The prevalence of open heathland there is a result of
Chapter 1: Introduction
3
intensive military training activities in the past century, with the sites differing to the
traditional heathlands not only in their specific origin, but also in edaphic and climatic
conditions (Schellenberg & Bergmeier 2014).
For instance, their disturbance regime differed in recent historical times, with northwestern
heathlands managed moreover constantly over time, providing a higher habitat continuity
and a lower amplitude of disturbances, whereas the eastern heathlands are exposed to
irregular, but high-intensive biomass and soil disturbances due to military training activities.
The high-frequent fires, during summer, too, in combination with intense mechanical impact,
such as tank driving, are assumed to be the predominant factors for the inland dune-like,
vegetation-free conditions and the high spatial differentiation of development stages, often
created by chance (Ellwanger & Ssymank 2016). After the Russian troop withdrawal in the
early 1990s, the neglection of the former military training sites induced a small-scale mosaic
succession, resulting in a high diversity in Calluna age structures and species, reflecting a
wide range of development stages and associated soil conditions. The positive influence of
military training activities on the nature conservation status of dry lowland heaths has often
been emphasized (e.g. Burkart et al. 2004), but the recent heathland maintenance with
methods of mechanical management is restricted, due to unexploded ordnance (Ellwanger &
Ssymank 2016).
Up to now, there are no studies to the potential differences in heathland species composition
or vegetation structures among heathlands in the German Northwest and Northeast, and little
is known about the role of site history and its complex consequences on species composition
and diversity. Almost all heathland nature conservation assessment schemes and references,
as well as management approaches are moreover based on knowledge derived from studies
conducted in Atlantic, traditional dry lowland heathlands. This thesis aims to figure out
species composition patterns and vegetation structures along the range of climatic and
edaphic conditions in the North German Plains and their relation to historical and recent land
use to identify whether the traditional heathlands of the Northwest are differing to those in
the East (Chapter 2).
Chapter 1: Introduction
4
1.2 Calluna vulgaris
The ericoid sclerophyllous dwarf shrub Calluna vulgaris acts as the key species of dry lowland
heathlands, determining heathland habit and stand structures. Although it has a world-wide
distribution range, covering almost the entire boreal to meridional northern hemisphere, its
role as the dominant species in Atlantic dry lowland heaths is restricted to coastal-near
regions in Northwestern Europe (Floraweb 2013; Gimingham 1972: 10). The distribution
limit of Atlantic dry lowland heathland is determined by oceanic climatic conditions
(Gimingham 1972, Loidi et al. 2010).
The wide distribution of Calluna suggests an ecological profile of a broad tolerance
concerning temperature and moisture conditions, but the morphological characteristics, such
like the woody, dense habit and the small, convolute, sclerophyllous leaves arranged like
scales, with sunken stomata and hairs point to specific adaptions to drought. Consequently,
Calluna has a wide tolerance towards water shortage and a high resistance to drought (e.g.
Albert et al. 2012; Bannister 1964a, b; Gordon et al. 1999, Haugum et al. 2021; Kongstad et al.
2012). However, this drought resistance seems to be limited to moderate drought conditions
under oceanic or sub-oceanic climate conditions, and Calluna rather suffers under longer
droughts like occasionally occurring in subcontinental regions (Marrs & Diemont 2013;
Gimingham 1972; own observations in 2013 and 2018, Chapter 4).
Calluna-dominated heathlands in Germany are located partially within the main distribution
areal for Atlantic dry lowland heaths, especially the German Northwest, but some areas in the
North German East provide moreover subcontinental climate conditions and are therefore on
the distribution rear edge (Fig. 1.1, p. 14; Table 1.2, p. 13; Gimingham 1975: 87). Under such
climate conditions, Calluna dieback events induced by drought or winter frosts occur more
often (Gimingham 1972; Marrs & Diemont 2013; Pott 1995), and especially summer droughts
are assumed to determine the distribution limit (Loidi et al. 2010).
During its life, Calluna growth form and vitality alters, described in the life cycle concept
introduced by Watt (1955) and later refined by Gimingham (1972, 1975). This concept
comprises four life phases, with distinct age-related shifts in the plant’s height and shape,
growth rate, flowering intensity and the proportion of dead shoots (after Gimingham 1972):
1. Pioneer phase (germination – approx. 10 years)
2. Building phase (up to approx. 15 years)
3. Mature phase (up to 25 years) and
4. Degeneration phase up to plant death with approx. 30 years
Chapter 1: Introduction
5
Since its introduction, this life cycle is established as a key criterion for determining age
structures in heathlands, providing an easy and fast estimation of heather plant age. It allows
for the detection of degeneration processes indicating the need for mechanical biomass
disturbances that prevent over-ageing.
However, this theoretical concept is basing on the idea of an undisturbed Calluna life and
therefore does not reflect heathlands under conservation management, with occasional fires,
mowing or sod-cutting. The probability that a Calluna plant in a dry lowland heath in
Germany is faced with one or several of such disturbances at least once in its lifetime is very
high. Although this restriction for the application of the life cycle concept have been discussed
and descriptions of post-disturbance growth stages are existent (e.g. Gimingham 1988), there
is still a poor knowledge whether the growth phases detection may validly represent Calluna
age and regeneration capacities. Additionally, potential alterations of this cycle, induced by
unfavourable climate conditions or high airborne nitrogen (N) loads, are assumed (e.g.
Berdowski & Siepel 1988), but evidence is still sparse.
The knowledge to Calluna drought resistance, drought adaption potentials and their effects
on plant demographics at their distribution margin is still poorly understood. This study aims
to contribute to a broader understanding of the Calluna life cycle and potential alterations of
growth, vigour and regeneration potential under gradients of climate and N deposition.
Calluna’s age-specific vigour and growth are analysed along the gradient from oceanic
conditions (Coastal areas of Lower Saxony, Schleswig-Holstein and Hamburg), to sub-oceanic
(Mecklenburg-Western Pomerania, northern parts of Lower Saxony and Saxony-Anhalt as
well as North-West Brandenburg) and even subcontinental conditions in the south-eastern
parts of Saxony Anhalt, Saxony and Brandenburg. Thereby, a special focus is on post-
disturbance regeneration mechanisms (Chapter 3), as well as their drought resistance
(Chapter 4).
Chapter 1: Introduction
6
1.3 Heathland conservation efforts
Protection facts and framework
Dry lowland heathlands play a crucial role in the traditional European landscape, providing
many ecosystems services, hosting a large number of threatened species and representing a
cultural heritage (e.g. Fagúndez 2013; Gimingham 1975; Wessel et al. 2004).
The heathland biotopes considered in this study are protected by European and National law
(Natura 2000 Habitats Directive 92/43/EEC; §30 BNatSchG). They are assigned as Habitat
type F4.2 in the EUNIS habitat classification and as either European Dry heaths (HT 4030;
Habitats directive Annex I: 4030, EIONET 2021a) or Dry sand heaths with Calluna and Genista
(HT 2310; Habitats directive Annex I: 2310; EC 2013, EIONET 2021b) in the Natura 2000
network. On the national scale, they are referred to as Heaths on sandy soils (40.03, Finck et
al. 2017).
There is an unsharp distinction between the HT 4030 and HT 2310, based almost only on the
geological substrate and weak floristic support (c.f. EC 2013; Olmeda et al. 2020). As an
inconsequential result, according to the latest report to the nature conservation status of HT
2310, its distribution ends abruptly on the German frontier, with no more occurrences in the
adjacent Poland (c.f. map in EIONET 2021b). Of course, it is unlikely that they do not occur in
Poland, and much more likely that they are designated as HT 4030 there, due to EU member
state-specific HT assessment criteria. The imprecise distinction between the HT 4030 and HT
2310 led to the decision to include sites either assigned as HT 4030 or HT 2310 in this study,
representing dry lowland heathlands on sandy soils.
Table 1.1 Distribution and extent of designated Dry lowland heathland in the EU and Germany (km² and
proportion). Calculated for HT 4030 and HT 2310, in the EU and in Germany, for Atlantic (ATL) and Continental (C)
biogeographical regions, as well as pooled. Calculated after data from EIONET (2021a, 2021b), for the report
period 2013-2018.
HT 4030
European Dry heath
HT 2310
Sand dunes with Calluna and Genista
EU
1 019 710
51 019
Germany
178 205 (17.5%)
32 569 (64.0%)
ATL
C
ATL
C
EU
590 453
429 257
33 923
17 096
Germany
39 678 (6.7%)
138 527 (32%)
15 623 (46.1%)
16 946 (99.1%)
HT 4030 European Dry heath + HT 2310 Sand dunes with Calluna and Genista
ATL
C
EU
624 376
446 353
Germany
55 301 (8.9%)
155 473 (34.8%)
Chapter 1: Introduction
7
Dry heath is listed as ‘vulnerable’ in the Red List of European habitats (Janssen et al. 2016).
On the national scale, degenerated heaths (biotope code 40.03.03) are ‘not threatened’, but
those of high vitality and structure are ‘critically endangered’ (40.03.01; Finck et al. 2017).
The responsibility of Germany to contribute to the European dry lowland heathland
maintenance is very high, as Germany hosts a considerable share of the total European dry
lowland heathland, in particular in the Continental biogeographical region (Table 1.1).
Germany has the highest number of designated 4030 sites (>400), although with a relatively
low size per site (Olmeda et al. 2020).
Many of the dry heathlands, both on dunes or not, have been assessed as being in an
unfavourable to bad nature conservation status, with a deteriorating future trend. The
reasons are abandonment of traditional management, insufficient or wrong management,
airborne nitrogen deposition, loss of specific habitat structure, fragmentation and invasive
non-native species (BfN 2019, Ellwanger et al. 2020, Olmeda et al. 2020, EIONET 2021a,
2021b)
Heathland management
Heathland management purpose changed from historic to recent times. Up to the 19th century,
heathlands have been primarily used as pastures, and traditional farming practices allowed
for the cultivation of the poor, sandy land (Ellenberg & Leuschner 2010, Gimingham 1975).
The aims of traditional heathland farming were to provide a sufficient fodder quality for the
robust livestock breeds and to cultivate the poor sandy soils. This was achieved by
transferring the limiting nutrient (N) from the heathland to the cereal fields by periodically
removing heathland aboveground biomass and topsoil, using it as bedding for the livestock,
and then bringing it to the cereal fields to enrich the poor soils with nutrients and humus. The
re-establishment of heathland vegetation ensured fodder for the livestock, but the quality
decreased with Calluna age. As a consequence, cyclical mowing or burning was applied to
induce vegetative regeneration with a high fodder quality due to highly vigorous resprouting.
Nowadays the main scope of conservation measures is to optimize heathland habitat
structures for maintaining the several ecosystem functions and services. The rejuvenation of
heather is still the driver of vital heathland development, and mechanical disturbances are
still applied with a similar aim than historically; transferring nutrients from the heath. But
today, the scope changed more to providing suitable nutrient-poor conditions to re-establish
typical heathland species assemblages, including the compensation of airborne N depositions.
The objectives of recent dry lowland heathland nature conservation management according
to Olmeda et al. (2020) are
Chapter 1: Introduction
8
1) maintaining or improving the structure and the function of heathlands,
2) providing suitable conditions for the typical species inventory and plant communites, and
3) to ensure a favourable future prospect.
In the North German lowlands, the former traditional heathland sites with a long history of
heathland farming were either converted into non-heath habitats or managed by the
continuation or re-introduction of heather rejuvenation-inducing biomass disturbances for
nature conservation purposes. Thereby, the used techniques are adopted from traditional
heathland farming and comprise grazing, mechanical biomass and soil disturbances (sod
cutting, ‘plaggen’), as well as prescribed burning.
Mechanical managements differ widely in their intensity and extend to remove biomass and
topsoil, mowing with the lowest, and a deep sod cutting (‘plaggen’) with the highest intensity.
They attempt to restore suitable soil conditions for heathlands, thereby the effectiveness is
dependent on the management type and the airborne nitrogen loads to compensate for
(Jones et al. 2017; Walmsley & Härdtle 2021).
Traditional grazing in the North German lowlands is with herded robust sheep breeds, but
recently, fenced grazing regimes are common as traditional shepherding is hardly
economically beneficial today and is applied primarily for nature conservation and touristic
purposes. There is a wide variety in used breeds, grazing intervals and stock densities (Table
1.2 p. 13). Grazing with other animals, such like robust cattle and horse breeds as year-round
extensive pastures or small-scale goat grazing is less frequent. Not perceived adequately, and
therefore likely underestimated in their potential positive value for heathland management,
browsing activities by free ranging deer (red deer, fallow deer, roar deer) contribute to
heathland dynamics wherever those animals occur in sufficient densities (Tschöpe et al. 2004,
2011; own observations).
Without a doubt, grazing is an important tool for heathland conservation management, but its
advantages, disadvantages and effectiveness must be assessed on a regional, site-specific
scale (e.g. Bakker et al. 1983; Bullock & Pakeman 1997; Brunk et al. 2004; Bunzel-Drüke et al.
2008; Fagúndez 2013; García et al. 2013; Gimingham 1972, 1994; Kirkpatrick & de Blust
2013; Newton et al. 2009; Vandvik et al. 2005).
A high number of studies addressed impact, efficiency, (dis)advantages, as well as
possibilities and restrictions of the different heathland managements (e.g. Anders et al. 2004;
Ellwanger & Ssymank 2016; Fagúndez 2013; Gimingham 1972, 1994; Olmeda et al. 2020;
Walmsley & Härdtle 2021; Walmsley et al. 2021; Webb 1998), but despite some general
findings, results and conclusions differ widely across regions and management types, even
within one management type, due to the complex study area-specific situation determining
Chapter 1: Introduction
9
the success or failure. Therefore, this study aims to find general determinants for Calluna
vitality and heathland diversity rather than comparing different management types.
Threats and pressures
The main reasons for Atlantic dry lowland heathland habitat quality and distribution decline
in the recent history were related to land use changes (Fagúndez 2013; Fagúndez & Izco
2016). The decrease of the economic value of traditional pastoralism and the introduction of
chemical fertilizers in the mid 19th century introduced a large-scale heathland distribution
decline (Ellenberg & Leuschner 2010; Fagúndez 2013; Gimingham 1972). As a consequence,
many heathlands were abandoned, afforested, converted into agricultural fields, or were used
for housing, mineral working and others (Olmeda et al. 2020). The establishment of nature
reserves and the (re-)introduction of heathland management for nature conservation
purposes prevented further habitat losses, but cannot compensate for habitat quality decline,
which is the major threat today.
Heathland habitat quality depends on whether the recent management is sufficient in
providing favourable Calluna rejuvenation and age structures, typical species compositions,
edaphic conditions and habitat connections, for enabling heathland ecosystem services and
functions. The management methods applied in the past and up to now are usually based on
the local site-specific conditions and opportunities given. Despite the fact that sometimes
frequency or intensity was too low to prevent for tree invasion or Calluna degradation, the
overall problem may not be that there is a general uncertainty about the efficiency of the
methods applied. The problem is that recent conditions of changing climate and high airborne
nitrogen (N) deposition is assumed to cause inter- and counteracting effects on heathland
dynamics, with a yet unclear future prospective (Diemont et al. 2013; Fagúndez 2013).
High N loads are known to be threats to nutrient-poor ecosystems, altering species
composition (e.g. Diemont et al. 2013) and ecosystem functioning (e.g. Bähring et al. 2017). In
the 1980s, the sensitivity of heathland ecosystems to high airborne N loads was detected,
with the observation that heathland became grasslands under high N deposition (Heil &
Diemont 1983). Later on, several studies detected the fertilizing effects of high N loads (e.g.
Bähring et al. 2017) and vitality reduction (e.g. Krupa 2003), particularly in interaction with
climatic and edaphic conditions (e.g. Gordon et al. 1999; Calvo-Fernández et al. 2018; Meyer-
Grünefeldt et al. 2015, 2016). High N deposition shifts the N-limited heathlands to
phosphorus limitation, causing competitive advantages for species that can use low soil
phosphorus more efficiently than Calluna, such like Molinia caerulea or Deschampsia flexuosa
(Falk et al. 2010; Härdtle et al. 2006; Grimoldi et al. 2005; Roem et al. 2002). These findings
Chapter 1: Introduction
10
highlighted the need for disentangling counter- and interacting impacts of high N deposition,
managements and disturbance-induced Calluna population dynamics.
The critical loads for airborne N in dry heathlands are ranging within 10-20kg/ha*y (Bobbink &
Hettelingh 2011), but many regions in Europe are above that level (Diemont et al. 2013;
Erisman et al. 2015; Waldner et al. 2014), including the German Northwest (Table 1.3, p. 16).
As a consequence, removing N from heathland ecosystems to compensate for the airborne
loads is one of the most important challenges in today’s heathland management (Jones et al.
2017; Härdtle et al. 2006, 2009; Vogels et al. 2020; Walmsley & Härdtle 2021; Walmsley
2021).
European heathlands are affected by the changing climate. In the past years, severe droughts
during vegetation period induced large Calluna dieback events in dry lowland heathlands
(Marrs & Diemont 2013; own observations during the survey period 2013 and in 2018). Such
droughts will occur more often in future (e.g. IPCC 2021; Schönwiese & Janoschitz 2008,
Wagner et al. 2013) and may challenge Calluna and its high adaption potential. Recent studies
showed that drought resistance is negatively affected by high atmospheric N loads (e.g.
Meyer-Grünefeldt et al. 2015, 2016), thus increasing the complexity of ecological stressors
and their interactions Calluna is faced with.
Other threats and pressures, such like invasive species or disturbances destroying typical
habitat structures are moreover local threats, but may not contribute to the overall trend of
declining habitat quality.
Assessing the conservation status
Several criteria are used for assessing the recent status of habitat quality and the
effectiveness of nature conservation efforts, comprising parameters of habitat distribution,
structure and threats. The assessment schemes are varying among the EU member states,
causing difficulties in the comparability and the validity of overall European nature
conservation strategy efficiency assessments. Additionally, favourable reference values,
acting as target conditions, are not well defined (Olmeda et al. 2020).
In Germany, the first assessment scheme was defined in 2007, later revised for two times
(2010, 2017). Heathlands with a high nature conservation value have a complete ‘typical’
species composition, complete ‘typical’ structures (Calluna growth phases, open soil) and no
recent pressures or potential future threats, such like grass dominances, invasive species or
signs of succession (BfN & BLAK 2017, assessment scheme: Appendix: Table A-1, p. 138).
Chapter 1: Introduction
11
Hereby, ‘typical’ refers to an expert rating rather than clearly defined and assessable criteria
in the national assessment schemes (BfN & BLAK 2017). To improve the regional-specific
assessment concerning the ‘typical’ plant inventory, the German Federal states provide
modified lists (e.g. for Brandenburg: LfU Brandenburg 2014a, 2014b).
The assessment scheme provides some uncertainty in the determination of typical plant
assemblages, Calluna age and their associated growth phases. According to the assessment
scheme from BfN & BLAK (2017) growth phases are determined focusing on the successional
context, assessed together with habitual characteristics of the prevailing Calluna growth form.
Thereby, specific early-stage (pioneer) species compositions and later stage (degeneration)
species assemblages, adapted from Gimingham (1972) and van der Ende (1993), were used
to substantiate the growth stage assessment.
Several problems coincide with this. First, this approach is strongly depending on the spatial
scale the habitats are mapped. In the optimum, heathlands are mosaics, comprising small-
scale heathland patches of different ages, and are mapped together as one habitat, resulting
in a high diversity of age structures. Mechanically managed heathlands are often patchy as
well, but on a larger scale, with clear distinct patches of e.g. burnt or mowed sites and sharp
borders to adjacent heathland habitats. The criteria for either combining or separating such
heathland patches as one or several habitat(s) are rather imprecise, differ between the
federal states and depend on the expert’s decision, maybe pre-specified by the mapping
customer. As a result, the validity of the assessments in the diversity of age structures and
species composition depends chiefly on the mapping scale.
Second, this approach assumes that the complex edaphic changes in succession, e.g. raw
humus accumulation and podsolization, are reflected by the species composition and the
Calluna age. During my field work, I got the impression of species composition reflecting
edaphic conditions rather than the aboveground age of Calluna, which seems not to give any
informative value for the successional edaphic processes but was moreover determined by
the management. Hence, one aim of this study is to analyse the interactions of species
composition and edaphic conditions, and setting the findings into a context of successional
heathland development on the plant community scale (Chapter 2).
Additionally, the current methodology of age structure assessment via growth phases lacks in
the informative value concerning regeneration processes and the safe detection of
regeneration growth phases, with yet unknown consequences for the assessment of Calluna
vitality regeneration capacities and reproductive potential. Therefore, this study aims to
refine and revise the established life cycle concept to provide a new basis for criteria
adjustment, refinement and improvement (Chapter 3).
Chapter 1: Introduction
12
1.4 Study areas and Sampling
Study areas
The study region comprises the North German Plains, including the federal states of Lower
Saxony, including coastal and inland sites in Schleswig-Holstein, Hamburg, Mecklenburg-
Western Pomerania, Saxony-Anhalt, Brandenburg and Saxony (Fig. 1.1 p. 14; Fig. 2.1 p. 29).
Study areas were selected on the basis of meeting several criteria:
Dry lowland heathland area, protected either as Natura2000 site or National Natural
Heritage with protected heathland biotopes.
Representing heathland variability in size, site history and recent managements.
Reflecting the range of abiotic environmental conditions for heathlands in the North
German plains (soils, climate, airborne nitrogen deposition).
Hosting heathland habitats of different stages, ages and vitality.
Aim of the study design was to represent the variability of North German heathland habitats,
for analyzing general characteristics, the commons and differences, but also the interplay of
the complex environmental conditions under field conditions.
Some of the study areas have already been subject of studies on regional heathland plant
communities and heathland ecology (e.g. Preising et al. 2012; Pott 1999; Schubert 1973), but
a general study to North German dry lowland heathland communities, both the Northwestern
and Northeastern part, has never been conducted so far, probably due to historical reasons.
Hence, this study provides the first overview to North German Plain lowland heathland plant
communities, as well as the vitality of its key species Calluna vulgaris along the gradients of
climate, soils and management provided by the study region.
The 19 heathlands considered in this study are protected habitats within the framework of
the Natura 2000 Habitats Directive (17 sites), and/or natural heritage sites with protected
dry lowland heathland habitats (10 sites, Table 1.2). From small heathland patches of less
than 100 ha, such like the Süderlügumer Binnendünen near the Danish frontier or the former
airfield Vietmannsdorfer Heide north of Berlin in Brandenburg, study areas range in size up
to more than 20,000 ha (Lüneburger Heide and the NATO military training area Bergen, both
Lower Saxony, Table 1.2).
Chapter 1: Introduction
13
Table 1.2 Study area characteristics: Location, size, protection status, site history and recent management.
Nr in map .
Fig. 1.1
size [ha]
Natural
Heritage
Natura
2000 site
Study area
Meters
above
sea level
Area
Heathland
area 4)
Federal state
Site history and recent management
Plots
sampled
1
Tinner Dose
21
19480
360
Lower Saxony
military training with high-frequent fires, intense mowing
no
yes
11
2
Cuxhavener Küstenheiden
10
1279
360
Lower Saxony
former military training area (until 2003), n ow year-round extensive
grazing with cattle/horses or sheep grazing (fenced), sometimes mowing,
scrub clearing on pastures
yes
yes
10
3
Süderlügumer
Binnendünen
16
303
<100
Schleswig-
Holstein
old inland dune area, sheep and goat grazing (fenced)
no
yes
5
4
Fischbeker Heide
11
773
155
Hamburg
traditional heathland area; sheep grazing (herded), mechanical
measurements (sod cutting, mowing)
no
yes
11
5
NATO training area
Bergen-Hohne
70
28702
3100
Lower Saxony
military training area with high-frequent fires and mechanical disturbances
due to tanks and other military vehicles; mowing and scrub clearing
no
yes
60
6
Lüneburger Heide
92
23286
4700
Lower Saxony
traditional heathland area; party former military training, sheep grazed
(herded), mechanical measurements (sod cutting, burning, mowing), scrub
clearing
no
yes
91
7
Nemitzer Heide
26
1061
360
Lower Saxony
accidental fire in 1971; sheep grazing (herded), sod cutti ng, mowing 5)
no
yes
11
8
Leussower Heide
40
6205
1000
Mecklenburg-
Western
Pomerania
former military training (until 2013); no management since then
yes
yes 3)
15
9
Marienfliess
72
1082
150
Mecklenburg-
Western
Pomerania 1)
former military training area (until 1991); sheep grazing (fenced) and
burning
yes
yes
10
10
Kyritz-Ruppiner Heide
75
12871
1000 2)
Brandenburg
former military training area (until 1991); burning, mowing, high deer
browsing activity
yes
yes 3)
20
11
Oranienbaumer Heide
75
3331
350
Saxony-Anhalt
former military training area (until 1991); year-roun d extensive grazing
with horses/cattle, scrub clearing, mowing
yes
yes
10
12
Rüthnicker Heide
45
3957
120
Brandenburg
former military training area (until 1991); mowing
yes
-
10
13a
/b
Kleine Schorfheide /
Vietmannsdorfer Heide
60/
55
3620/
1675
1000/
<100
Brandenburg
former military training area/ airfield (until 1991); sheep grazing (fenced)
and mowing
no
yes
20
14
Glücksburger Heide
85
2812
550
Saxony-Anhalt
former military training area (until 1991); mowing, sheep grazing (fenced,
started after survey)
yes
yes
14
15
Bundeswehr training area
Jägerbrück
20
8813
1000
Mecklenburg-
Western
Pomerania
active military training with high-frequent fires and mechanical soil
disturbances due to driving activities
no
yes
20
16
Prösa
118
3732
200
Brandenburg
former military training area (until 1991); mowing, sheep grazing (herded)
yes
yes
12
17
Zschornoer Wald
110
2148
200
Brandenburg
former military training area (until 1991); burning, mo wing
yes
no
12
18
Daubaner Wald
140
3531
225
Saxony
former military training area (until 1991); mowing, sheep grazing (herded)
yes
yes
10
1) only partly sampled in Mecklenburg-Western Pomerania. 2) area only partly sampled; only southern part in ownership of Sielmann foundation. 3) in parts. 4) heathland area calculated and rounded, based on
rough digitalisation of identifiable heathland on satellite maps of study areas in QGIS. This rough estimation was used for determination of amount of samples per area. 5) Nemitzer Heide was assigned as
‘traditional heathland site’ in this study, because it was a traditional heathland up to the mid 19th century, then afforested, and then again open heathland due to an accidental burning 1971. This Table was
modified after a table provided in the electronic supplement to Chapter 2.
Chapter 1: Introduction
14
It is difficult to determine which of the study areas can be considered as ‘historical’ heathland,
as the term “heath” is used in varying senses, often with regional differentiations (Ellenberg
& Leuschner 2010, Hüppe 1993a, b; Schellenberg & Bergmeier 2014). However, in this study,
I roughly distinguished between heathlands under active military training (n = 10; e.g. NATO
training area Bergen, Lower Saxony (No. 5 in Fig. 1.1) and the Bundeswehr training area
Jägerbrück, Mecklenburg-Western Pomerania (No. 15 in Fig. 1.1)), those with a traditional
heathland farming history (n = 4; e.g. Lüneburger Heide, Lower Saxony (No. 6 in Fig. 1.1);
Fischbeker Heide, Hamburg (No. 4 in Fig. 1.1)) and those shaped by military training
activities in the past century, but now under nature conservation management (n = 4; former
military training areas, e.g. Kyritz-Ruppiner Heide, Brandenburg (No. 10 in Fig. 1.1),
Glücksburger Heide, Saxony-Anhalt (No. 14 in Fig. 1.1; Table 1.2)).
Fig. 1.1 Map of study area locations and the gradients of Climate (Oceanicity, Annual precipitation and mean
temperature) and N deposition. Arrows indicate in which directions the gradient is increasing, but they are only
roughly corresponding to the values given in Table 1.3 for showing the general patterning. Biogeographic regions
(EEA 2016): Atlantic, grey hatched; Continental, white. For study area names 1-18 see Table 1.2 or Table 1.3.
Administrative boundaries © Bundesamt für Kartographie und Geodäsie, Frankfurt 2011.
Chapter 1: Introduction
15
North German lowland heathlands are exposed to climatic conditions varying from oceanic,
coastal areas in the Northwest, over suboceanic to even subcontinental properties in the East
and Southeast (Table 1.3; Fig. 1.1; Schellenberg & Bergmeier 2014: 113). As a measure of
Oceanicity, the Kotilainen’s Index (K)was used, reported to provide the best correlation of
climatic conditions and biological phenomena (Godske 1944):
K =N∗dt
100Δ
with N = yearly precipitation in mm, dt = number of vernal or autumnal days with mean
temperatures ranging from 0°C – 10°C and Δ = difference between the mean temperature of
the warmest and coldest month. For the calculation of K, daily observations of the reference
period from 1980-2010 was used (DWD 2015; Table 1.3). For the coastal heathlands in
Norway, K ranges roughly from 100 to 300, with some peaks (>400) but also regions with K <
100 (Godske 1944). There were similar ranges in the Scottish upland heaths (Poore &
McVean 1957), but with no values K < 100. In contrast, none of our study areas reached a K >
100 (Table 1.3), they moreover ranged from 40 (Glücksburger Heide and Oranienbaumer
Heide, No. 11 and No. 14 in Fig. 1.1, both in the southern Saxony-Anhalt) to 85 (Süderlügumer
Binnendünen, Schleswig-Holstein, near the coast and the Danish frontier, No. 3 in Fig. 1.1).
Heathlands in the North German Plains stock on acidic Pleistocene sandy sediments of
varying thickness and development stage (Härdtle et al. 1997). The substrates are
determined by the age of the sediments, the site history and the climate. In the German
Northwest, the sandy sediments are older, and under the Atlantic climate, podsolization and
raw humus accumulation rates are higher (Lache 1979, Härdtle 1997). Eastern the river Elbe,
sandy sediments are younger. Although they were stocked with woodland before the military
training activities started, the specific and high-intense disturbances caused by accidental
fires throughout the whole year, tree and scrub clearings as well as tank driving resulted in
an exposition of bare sands, often inland dune-like (e.g. the drifting dune in the Leussower
Heide). In contrast to surrounding sites, the military training areas have never been subject
to fertilizing or soil improvement for agricultural purposes, a factor which favoured erosion
to bare, exposed and extremely nutrient-poor sands (Burkart et al. 2004).
Hence, the sandy soil development stages, with varying raw humus accumulation and
podsolization intensity differ across the regions, with potential influences on the recent
heathland plant composition and heathland dynamics, thus not have been subject for any
studies up to now.
Chapter 1: Introduction
16
Table 1.3 Study area characteristics: Climate conditions, location above sea level and annual N deposition (UBA 2019, basing on the PINETI-3 model for the reference period 2013-2015,
Schaap et al. 2018). Kotilainen’s Index of Oceanicity is calculated after Godske (1944): Kotilainen’s Index of Oceanicity and the climate data are basing on the reference period 1981-2010
(DWD 2015, stations used see Appendix: Table A-2).
m asl
Annual N
deposition
[kg*ha-1*yr-1]
Kotilainen's
Index of
oceanicity
Annual precipitation
[mm]
Days without
precipitation
Mean annual temperature
Annual amplitude of
daily mean temperature
1 - Tinner Dose
21
23
71.4
797
168
10.0
33.1
2 - Cuxhavener Küstenheiden
10
18
79.2
882
171
9.6
30.0
3 - Süderlügumer Binnendünen
16
17
84.6
855
157
8.5
31.2
4 - Fischbeker Heide
11
18
68.7
710
173
9.6
33.7
5 - NATO training area Bergen-Hohne
70
15
56.7
771
173
9.6
35.3
6 - Lüneburger Heide
92
15
68.6
812
171
9.0
34.8
7 - Nemitzer Heide
26
12
45.2
611
187
9.2
35.6
8 - Leussower Heide
40
15
51.6
610
179
9.0
34.6
9 – Marienfliess
72
12
51.7
621
179
8.8
35.3
10 - Kyritz-Ruppiner Heide
75
11
41.4
574
198
9.2
35.4
11 - Oranienbaumer Heide
75
11
40.1
525
194
9.4
37.2
13a - Kleine Schorfheide
60
10
43.1
582
196
8.6
37.2
13b - Vietmannsdorfer Heide
55
10
45.0
624
188
9.0
37.2
14 - Glücksburger Heide
85
11
40.1
525
194
9.4
37.2
15 - Bundeswehr training area Jägerbrück
20
11
45.7
536
190
8.8
35.8
16 - Prösa
118
11
41.9
615
220
9.2
37.6
17 - Zschornoer Wald
110
10
42.5
683
189
9.2
38.8
18 - Daubaner Wald
140
11
45.0
691
182
9.2
39.2
Chapter 1: Introduction
17
Sampling
Depending on the study area size and the diversity in managements a total of 352 plots was
selected, each a 25m² quadrat with a randomly generated GPS coordinate as Southwestern
corner (Fig. 1.2, using QGIS versions 2.1-2.8, 2013-2017). The sampling took place in two
survey periods, with the first survey period focusing on species composition and vegetation
structure (May-August 2013), and the second on Calluna-individual plant vitality attributes
(August-September 2014, field protocols: ESM1_1).
In 2013, the data for the vegetation classification (Chapter 2) was collected, with vegetation
structures and topsoil samples gathered in the 25m² plots and a vegetation relevé conducted
on the 4m² subplots (Fig. 1.2). Two of the 352 plots have been recently sod-cut with an initial
regrowth of only Calluna, and have been therefore excluded from the plant community
analysis in Chapter 2.
In 2014, freshly sod-cut or burnt sites were excluded, as they provided no valuable plant
material for the vitality attribute analysis. Additionally, area or plot accessibility problems
reduced the dataset to 319 plots. The sampled vitality data on individual Calluna plants
within the 25m² plot in 2014 was used for the analysis of age-dependant changes in plant
habit and vigour (Chapter 3) as well as for the analysis of drought susceptibility (Chapter 4).
In the latter, only up to three-year old plants were selected from this dataset, from 259 plots.
N
5m
5m
Fig. 1.2 Schematic Sampling Design for the survey periods 2013 and 2014. The 4m² quadrat was used for the
vegetation relevé, the 25m² quadrat for the collection of structure and vitality data. The lower left corner
(=Southeast corner, shown as grey dot) is the randomized GPS coordinate.
2m
2m
Chapter 1: Introduction
18
1.5 Dry Lowland heathland ecology: Gaps of
knowledge to cover
Heathland plant species composition and vegetation
structures
The present study aims to assess overall commons, patterns and differences in species
diversity and composition of North German dry lowland heathlands. To the best of my
knowledge, such a study has never been conducted in the North German lowlands, neither
with the complexity nor with the spatial extent. The existing studies are often focussing on
phytosociological analyses, often with a limited spatial scope (e.g. Berg 2004; Preising et al.
2012; Schubert 1973, 1974), providing fundamental community descriptions and ecological
profiles of the plant assemblages in the specific regions addressed. They do not allow for a
direct comparison of plant community species composition over the entire North German
plains, due to different analysis methods, publishing times and subjective interpretations of
the different authors.
The interplay of species composition, species diversity and heathland development stage is
still insufficiently understood. The theory of heathland development phases, determined by
the prevailing Calluna growth phase with its associated species (c.f. Gimingham 1972, van der
Ende 1993) is the basis of our heathland dynamics understanding and status assessment, but
its application lacks in some details.
First, this idea was introduced and approved for unmanaged stands in North-East Scotland
(Gimingham 1972). German (and of course many other) dry lowland heathlands are usually
managed, with their development describing a seral change of communities after
disturbances. Thereby, the type and intensity of the disturbance determines the starting
point for the succession, either starting from ‘real’ early-stage conditions (e.g. bare sands
after sod-cutting) or only early Calluna growth phase conditions (e.g. after mowing or
burning). As a consequence, the idea of growth-phase specific plant assemblages may only be
valid for sites with a ‘real’ reset to early-stage edaphic conditions, and an undisturbed Calluna
life cycle. This shows that the assumption of specific heathland plants associated with each
Calluna growth phase may be invalid for frequently managed stands, where the species
composition of sod-cut sites is probably different to those on mowed or burnt sites, although
with the same Calluna growth phase prevailing.
Second, an even-aged, dense stand with prevailing Building-phase plants, e.g. after mowing,
provides other microclimatic conditions for e.g. cryptogams than an open mosaic heath with
Chapter 1: Introduction
19
Calluna in the Building phase, e.g. after burning. Hence, heathland plant community changes
along successional gradients cannot be analysed without considering 1) edaphic conditions
and 2) the vegetation structures. I assume both to play a central role in the species
composition along heathland development paths.
Therefore, an aim of the study presented in Chapter 2 is to improve the understanding of
heathland community dynamics and the role of regional patterning. More specifically, it tries
to identify species and structures that allow for a valid estimation of the successional stage,
reflecting soil and vegetation dynamics as well as restoration potentials.
Additionally, the study asks for the importance of ecological key factors determining the
species composition and the vegetation structure, whether it is the site history or climate
(oceanic vs. subcontinental conditions), and how high airborne N loads alter species
composition and heathland dynamics.
Derived from those findings, the study aims to assess the potential nature conservation value
of the heathland plant communities by using the established criteria for determining nature
conservation status in the mapping of Natura 2000 protected habitat types. Thereby, the
criteria were critically revised and potential specifications to improve their informative value
concerning heathland habitat quality assessment were provided.
Calluna life cycle as the determinant for heathland
dynamics
The established Calluna life cycle concept with its distinct four growth phases is the basis for
determining heathland age structures, one of the key criteria for nature conservation status
assessment. This cycle refers to an undisturbed Calluna life and although regeneration
processes have been mentioned to alter it (‘post-fire regeneration’; Gimingham 1988; Wallen
1980), the recent usage does not distinguish between plants of different life histories.
Calluna has generally a very high potential for vegetative regeneration (e.g. Gimingham &
Mohamed 1970), a trait which allowed for the establishment on sites frequently disturbed by
man. Two mechanisms are typical for the Calluna vegetative regeneration after disturbance,
the resprouting, resulting in vigorous clusters of new shoots from stem bases or axillary
dormant buds, and the layering, where procumbent shoots are rooting adventitiously.
Resprouting is the prevailing vegetative regeneration of younger plants, whereas layering
occurs in older plants. The resprouting capacity is limited to young plants of up to 15 years,
due to the secondary xylem growth reducing the capacity of buds to resprout (Miller & Miles
1970; Mohamed & Gimingham 1970).
The assumption that any heather regeneration may entry a new Calluna-typical life cycle
again, like assumed in the ‘repetitive cycling’ theory, lacks in evidence-based research, as well
Chapter 1: Introduction
20
as the assumption that any regeneration may improve heathland vitality and Calluna is
immortal (Wallen 1980; Webb 1986). Some studies already indicated that older plants have a
restricted regeneration capacity, but there is no study that aims to track the further
development of regenerated plants, their persistence in post-disturbance growth phases,
their longevity and general vigour. In the second chapter of this thesis, vitality attributes that
are known to alter with age have been analysed, considering plants of different age and life
history. I aimed to disentangle effects of the total plant age, the regeneration age, the plant life
history, management, climate, and N deposition. The aim was to detect potential differences
in age-related vitality between the plants grown from seeds (PS), plants resprouting from
buds near stem base (PR) and those growing from rooted stems lying on the ground (PL). The
persistence of PS, PR and PL in the physiognomically determined growth phases was
assessed and compared to find potential differences in their regeneration potential.
Additionally, this study aimed to answer the question whether there is evidence for
‘repetitive cycling’ processes, i.p. whether recurring regeneration cycles produce highly
vigorous plants independent from the total plant age, and whether Calluna plants are
immortal or not.
Furthermore, I asked whether the Calluna life cycle in North German lowland heathlands
shows evidence for any alteration compared to other regions, and whether those may be
explained by high N depositions or the conditions of climate in the marginal distribution
range.
Drought susceptibility of young Calluna plants under
changing climate and high N loads
Although Calluna has a wide tolerance towards water shortage and a high adaption potential
to regional ecological conditions (c.f. 1.2 Calluna vulgaris), field observations show that
extreme droughts, as in 2018, caused lethal damages on both, adult and young Calluna plants
(University Hasselt 2021; own observations). It is hitherto unknown whether these damages
indicate that the physiological drought tolerance limit is simply already reached under those
severe drought conditions, thus supporting the drought limitation of Calluna-dominated dry
lowland heathland distribution (Loidi et al. 2010), or whether the ability to withstand severe
drought is potentially reduced by other, external factors, such like high N depositions or the
frequency of severe droughts, or other ecological stressors. This is of specific interest for
young Calluna plants, as they are rather sensitive to drought than older plants (Meyer-
Grünefeldt et al. 2015). As a consequence, young post-disturbance regeneration phases are
prone to suffer from severe droughts, but are highly important for a successful heathland re-
establishment after management.
Chapter 1: Introduction
21
The fourth chapter of this thesis focusses on the young Calluna plant establishment after
biomass disturbances, such as mechanical managements, and asks for the influences of
drought and N deposition. More specifically, I asked how young Calluna plants react to
drought, referring to the drought conditions of the survey year 2014 and modelled their
response to the most severe drought conditions that occurred in the years 2011-2020.
Furthermore, I aimed to analyse whether seedlings are rather affected by drought than
resprouted plants, as the latter may profit from their already developed rooting systems and
are supplied by stored reserves in the post-disturbance remaining biomass. Additionally, I
analysed how high N depositions potentially altered the young Calluna plant responses to
drought, and whether high N loads increased drought susceptibility, like evident in recently
published studies (Meyer-Grünefeldt et al. 2015, 2016). Thereby, I asked whether the
influence of high N on drought susceptibility may differ between seedlings and resprouting
plants.
Chapter 1: Introduction
22
23
Chapter 2:
Heathland plant species
composition and vegetation
structures reflect soil-related paths
of development and site history
Schellenberg J, Bergmeier E (2020) Heathland plant species composition and vegetation
structures reflect soil-related paths of development and site history. Appl Veg Sci 23: 386–
405. https://doi.org/10.1111/avsc.12489
Chapter 2: Heathland plant species composition and vegetation structures
24
Abstract
Questions: To improve our knowledge on how environmental conditions determine the
development of high-value Calluna vulgaris heathland habitats, we studied the floristic and
structural characteristics of heathland plant communities across North Germany and how
they are influenced by edaphic, climatic and management factors. We ask how heathland
development is related to these factors and what are the implications for conservation
management and restoration.
Location: North German Plain.
Methods: We collected 350 relevés in 18 dry Calluna heathland areas. Plant communities
were classified using Isopam, RDA determined effects of environmental conditions. Potential
pathways of development and the nature conservation status of the communities were
identified on a multifactorial basis.
Results: We found nine floristically and structurally distinct heathland plant communities.
Heathland vegetation showed distinct patterns along Calluna age development stages and
environmental conditions. Soil conditions and related effects of long-term site history and
recent management turned out to be the predominant factors influencing species
composition and diversity, resulting in three potential heathland succession pathways.
Mosaic-like communities with particularly high taxonomic diversity and conservation value
occurred on early-successional inland dunes or as regeneration stage growing on nutrient-
poor sandy soils without humus accumulation.
Conclusions: The study reveals fundamental differences between historically farmed
heathland in the oceanic Northwest and former military training areas mainly in
northeastern Germany with consequences for restoration ecology. Present nature
conservation criteria turned out to be insufficient in predicting habitat quality, as lichens are
frequently disregarded. Our findings highlight the need for intense soil disturbance to
maintain early-stage soil conditions and a diverse Calluna growth phase composition, as
these factors essentially determine species richness in lowland heaths.
Keywords
Calluna vulgaris, heath development, heather, heathland, heathland history, historical
heathland, lowland heath, military training, phytodiversity, succession, vegetation
classification, vegetation dynamics
Chapter 2: Heathland plant species composition and vegetation structures
25
2.1 Introduction
Dry open to semi-open dwarf-shrub heathland dominated by heather, Calluna vulgaris (L.)
Hull (hereinafter: Calluna), occur in the oceanic and suboceanic, cool-temperate parts of
Northwest Europe. They show a wide variety of plant assemblages along edaphic,
geographical and climatic gradients (Berg 2004; Bridgewater 1981; Preising et al. 2012;
Schubert 1973, 1974; Stortelder et al. 1996). With the exception of some coastal and montane
habitats, they are formed and maintained by animal and human influences (Gimingham 1972;
Hüppe 1993b; Webb 1986). In Germany, sheep farming with heathland burning and sod-
cutting was practiced in the oceanic northwestern part of the country (Leuschner & Ellenberg
2017). Further east, grazing and litter raking was practiced, but no sod-cutting or similarly
severe interference took place. The establishment of open heathlands in these northeastern
regions of Germany are chiefly the result of military training activities in the 20th century
(Ellwanger & Ssymank 2016; Schellenberg & Bergmeier 2014).
Within the entire Northwest of Europe merely a fraction of the formerly vast heathland areas
still exist, mainly due to changes in land use (fertilisation and agricultural intensification,
afforestation, abandonment, nitrogen deposition) or other adverse effects. Dry lowland
heathlands considered in this study are protected biotopes in the nature conservation
network of Natura 2000, assignable to the habitat type (HT) 4030 - European dry heaths and
HT 2310 - Dry sand heaths with Calluna and Genista (EC 2013). In Germany, both HT are
widely distributed over the northern lowlands, corresponding to two biogeographical regions
(EEA 2016); the Atlantic region (A) in the North and Northwest and the Continental region (C)
in the East and Southeast. Both HT have larger extensions in the eastern, ‘Continental’, part of
the country (HT 4030 A: 165 km²; C: 325 km²; HT 2310 A: 10 km²; C: 27 km²; BfN 2019). The
recent conservation status especially for HT 2310 has been assessed as being unfavourable
(BfN 2019), and for the EU member states dry heath has been rated as ‘vulnerable’ in the
European Red List of habitats (Janssen et al. 2016). The principal reasons for heathland
habitat quality decline are abandonment of traditional management, insufficient or wrong
management, airborne nitrogen deposition, loss of specific habitat structures and invasive
non-native species (BfN 2019). At present, nature conservation management measures which
attempt to imitate the effects of historical farming practices are in place in most of the
remaining heathland areas.
For an assessment of nature conservation value, including habitat quality and the
effectiveness of conservation efforts, the current conservation status is defined by using
criteria of structural and floristic diversity (BfN 2019). Additionally, potential threats or
Chapter 2: Heathland plant species composition and vegetation structures
26
conditions reducing habitat quality are considered. For structural diversity, Calluna age
structures and composition of heathland-typical life form groups are used. For Calluna age
structure, a categorical model commonly distinguishes four phases for describing patterns in
heathland dynamics: Pioneer, Building, Mature, and Degeneration (Gimingham 1972; Watt
1955). Plant life form group composition is assumed to be instructive for indicating
favourable (e.g. presence of lichens) or unfavourable conditions (e.g. tree invasion or grass
dominances, NLWKN 2012; LfU 2014a, 2014b). In terms of floristic diversity, the heathland-
typical species assemblage is defined for each HT, comprising both, typical, highly-frequent
and rare species.
Using these assessment criteria, we aim to identify heathland plant communities of high
nature conservation value and to derive plant-community-wise threats and development
potentials. To test for habitat quality variation between potential pathways of heathland
development we relate the Calluna growth patterning to species composition and edaphic
conditions. The key processes underlying heathland development are favourable soil
conditions and cyclical regeneration of heather, but a broader approach to disentangle these
relationships in the European subatlantic-subcontinental region using local-scale data does
not exist. However, when attempting to predict the vegetation dynamics and heather
regeneration potential of historically young heathlands in the Northeast German lowland in
particular, questions of transferability and long-term site development may arise.
In this study we provide a basic overview of the entire North German dry lowland heath plant
communities and relate their floristic traits to edaphic, climatic and management conditions.
Based on this, we attempt to disentangle complex developmental processes in heathlands,
thus helping to understand successional pathways and regeneration potentials. Hence, this
study may serve as a basis for conservation management decision-making and predicting
heath development.
Specifically, we attempt to answer the following questions:
(1) What are the floristic and structural characteristics of dry lowland heath plant
communities in Germany?
(2) How do gradients of edaphic conditions, climate, management and/or site history
shape these characteristics?
(3) Do specific environmental conditions result in different pathways of heathland
development?
(4) Which types of heathland vegetation are of particular nature conservation concern
and what conservation management implications can be derived from the results of
this study?
Chapter 2: Heathland plant species composition and vegetation structures
27
2.2 Methods
Study sites
We surveyed dry heathlands of the HT 4030 and HT 2310 throughout North Germany. In the
federal states of Lower Saxony, Schleswig-Holstein, Mecklenburg-Western Pomerania,
Brandenburg, Saxony-Anhalt and Saxony, eighteen study sites were selected located along a
northwestern to southeastern gradient of decreasing oceanicity (Fig. 2.1). Field data were
collected in May to August 2013.
The heathlands were not influenced by groundwater, the mean annual precipitation ranged
from approximately 500 mm in the subcontinental parts of eastern Germany up to 900 mm in
coastal areas in the Northwest (DWD, 2015). Oceanicity (K) was calculated based on daily
weather data from the period 1980-2010 (DWD, 2015; Fig. 2.1), using an algorithm proposed
by Godske (1944).
Airborne nitrogen deposition ranged between 23 kg N ha-1*yr-1 in the Northwest and 10-11
kg N ha-1*yr-1 in the East (UBA 2019, ESM2_1: Table S1-1). All heathlands were on sandy soils,
differing in soil development and depth.
The study sites were either long-term heathlands with a traditional farming history or
military training areas, abandoned or active, with or without recent management, thus
reflecting the most important management types of heathlands in the North German Plain
(study site details: ESM2_1). Multiple management categories, e.g. burning and subsequent
grazing, were each considered separately (see Table 2.1 for a list of all management
categories).
Sampling Design
At each study site randomly chosen plot locations were stratified according to recent
management using QGIS (versions 2.1-2.8, 2013-2017). The total sample comprised 350
quadrates of 5 m × 5 m = 25 m² for measuring structural data and 4 m² (2 m × 2 m) in the
lower left corner for recording floristic and species abundance data (vegetation relevés). The
sample plot size for floristic data was consensual for sampling vascular plants and
cryptogams (Dierschke 1994; Chytrý & Otýpkova 2003). All species of vascular plants and
epigeal bryophytes and lichens were recorded; lichens, if not identified on-site, were
collected for identification using chemical properties. Cover values of each species were
assessed using the 7-level Braun-Blanquet scale (Dierschke 1994; Nomenclature for vascular
plants: Buttler et al. 2018, Bryophytes: Caspari et al. 2018, Lichens: Wirth et al. 2011).
Chapter 2: Heathland plant species composition and vegetation structures
28
Table 2.1 Environmental variables and their attributes used to relate species composition to site history, recent
management and soil conditions.
Variable
Attribute/levels
Characteristics, effects
Site history (past and present land use)
Active military training
Long-term and frequent disturbances of varying spatial scale and intensity,
with or without characteristics of historical farming. Distributed throughout
North Germany.
Former military training
Long-term and frequent disturbances of varying spatial scale and intensity in
the recent past now abandoned and often advanced in succession, without
characteristics of historical farming. Distributed mainly in the eastern part of
the North German Plain.
Historical-farming
heathland
Characterized by long-term historical farming; with or without temporary
military use in the more distant past. Distributed mainly in Northwest
Germany.
Recent management (incidents in the past five years)
Burning
Intensive management: prescribed or accidental; (almost) complete
destruction of aboveground plant material, ash deposition; of varying
intensity.
Intensive
managements
Mowing
Intensive management: plants cut in 5-10cm height, often with soil surface
disturbances and removal of mowed plants and litter.
Sod cutting
Intensive management: removal of humus and uppermost mineral soil,
together with aboveground plant parts, only a few rootstocks may survive;
of highest intensity.
none
No intense management such as burning, mowing or sod cutting in the past
five years; former incidents likely especially in active military training areas
and historical-farming heathlands.
Deer grazing
Browsing mainly by red deer and fallow deer, not enclosed, y ear-round; of
varying impact on phytomass and soil
Horse and cattle grazing
Grazing mainly non-intensive by Konik horses and Heck cattle in spacious
enclosures, year-round; of varying but overall moderate impact on
phytomass and soil, with small-scale disturbance
Grazing
no grazing
No grazing impact become known or observed but non-intensive deer
grazing cannot be ruled out
sheep enclosure
Intense sheep grazing over periods of varying length and with variable
sheep density in temporarily fenced sites; overall high-intensity browsing
and trampling
sheep herded
Traditional sheep herding, not enclosed; high spatial heterogeneity in
browsing and trampling.
sheep pen
Daily concentration of herded sheep and trails; very high browsing and
trampling intensity.
Edaphic conditions
Humus layer
layer thickness [cm]
thickness of accumulated undecomposed or partly decomposed humus
above, not permeated in the mineral topsoil.
Soil organic matter
rich (1) / poor (0)
Organic matter content of upper 10 cm topsoil assessed visually as rich (1)
or poor (0, comparable to pure sand)
Soil texture
Loamy sand (1) / pure
sand (0)
Sands with marked fraction of clay or silt, often humus-rich, or pure sands.
Airborne nitrogen
deposition
kg/ha-1*a-1
Data from UBA (2019)
Climatic conditions
Oceanicity
Kotilainen´s Index for
Oceanicity
Calculated after Godske (1944).
Calluna age structures
%
Cover of plants in the 4 growth phases P – Pioneer, B – Building, M-Mature
and D-Degeneration
Chapter 2: Heathland plant species composition and vegetation structures
29
Fig. 2.1 Study areas 1-18 (black dots) in
northern Germany, in the legend with full
names, sample size (n) and oceanicity K -
Kotilainen's Index of Oceanicity (Godske
1944). Biogeographic regions (EEA 2016):
Atlantic, grey hatched; Continental, white.
Slightly different K values within study
area 13 refer to ‘Kleine Schorfheide’ and
‘Vietmannsdorfer Heide’, 8 km away. For
details on study areas see ESM2_1.
Administrative boundaries © Bundesamt
für Kartographie und Geodäsie, Frankfurt
2011.
Study area
n
K
1
Tinner Dose
11
71.4
2
Cuxhavener Küstenheiden
10
79.2
3
Süderlügumer Binnendünen
5
84.6
4
Fischbeker Heide
11
68.7
5
NATO training area Bergen-Hohne
60
56.7
6
Lüneburger Heide
89
68.6
7
Nemitzer Heide
11
45.2
8
Leussower Heide
15
51.6
9
Marienfließ
10
51.7
10
Kyritz-Ruppiner Heide
20
41.4
11
Oranienbaumer Heide
10
39.9
12
Rüthnicker Heide
10
40.9
13
a) Kleine Schorfheide /
b) Vietmannsdorfer Heide
20
43.1/
45.0
14
Glücksburger Heide
14
40.1
15
Bundeswehr training area Jägerbrück
20
45.7
16
Prösa
12
41.9
17
Zschornoer Wald
12
42.5
18
Daubaner Wald
10
45.0
Chapter 2: Heathland plant species composition and vegetation structures
30
Structural diversity was measured as the cover of six life-form groups (trees, heather,
graminoids, non-graminoid herbs, bryophytes, lichens) as well as bare sand per 25 m² plot.
The tree cover was assessed on a 100 m radius around the plot’s initial GPS coordinate in
order to assess the structural context of the plot.
Age structures of heather were evaluated by noting the life history stage covers of Calluna,
with designing plants to one of the four growth phases (Watt 1955; Gimingham 1972):
(1) Pioneer phase is defined as the timespan between germination and switching from
monopodial to sympodial growth of the heather plant,
(2) Building phase comprises the ageing of the plant up to maximum size and vitality,
(3) Mature phase is the optimal to slightly degenerating status with continuing growth, but
ageing in the central plant parts, stems beginning to prostrate and start adventitious (cauline)
rooting, until in the
(4) Degeneration phase only adventitiously rooted stems are still alive, the plant is generally
of decreasing vitality and eventually dies.
For the designation of a plant to one of these four growth phases, we used visual attributes
such as growth form (monopodial or sympodial growth), habit (proportion of (sub)erect
branches and adventitious roots, total plant height and width) as well as vitality (flowering
intensity, leafless branches).
Humus layer thickness and soil texture were determined by finger test and by visual
inspection at 3-4 random points per 25 m² plot.
Statistical analysis
For classification, Braun-Blanquet species cover values were translated to cover percentages
(r = 0.01%, + = 0.5%, 1 = 3%, 2 = 15%, 3 = 37.5%, 4 = 62.5%, 5 = 87.5%) and the latter
arcsine transformed. Rare species in the dataset (fewer than 3 occurrences) were excluded
prior to classification to reduce noise.
Among several classification methods tested (Kmeans, TWINSPAN, PAM), the results of a
non-hierarchical Isopam were the most clearly interpretable (Schmidtlein et al. 2010). In our
empirical classification approach, floristic-based results of 6- to 9-group non-hierarchical
Isopam were compared in terms of their validity in representing structural differences
between plant communities. Partial Isopam was performed to test further group separation
to improve floristic and/or structural distinctness.
For validation on floristic level, silhouette plots (Rousseeuw 1987) were used for numerical
clustering goodness measurement. Fidelity and differential taxa were used to interpret the
compositional pattern in synoptic tables. Differential taxa were calculated by implementing
the algorithm of Tsiripidis et al. (2009) to a function into R (package ‘goeveg’, Goral &
Chapter 2: Heathland plant species composition and vegetation structures
31
Schellenberg 2019). The fidelity measure phi (Φ) after Sokal & Rohlf (1995) was
implemented in ‘goeveg’ to calculate species fidelity per cluster.
For validation of significant structural differences between Isopam clusters, cover of Calluna,
life form groups and open soil were compared cluster-wise using non-parametric multiple
Mann-Whitney U tests with Bonferroni correction for different sample sizes.
Redundancy Analysis (RDA) was used to determine effects of site history, recent
management, climate, Calluna age structure and edaphic conditions on plant composition. To
this effect, a subset of only diagnostic species with a minimum percentage frequency of 20%
in the synoptic table and without Calluna was used. The final model for best explaining
environmental influences on species composition was selected by ‘ordistep’ function, starting
from null model with multiple forward/backward selections (Oksanen et al. 2019). Tested
numerical constraints were scaled with the scale()-function in R in advance of RDA model
selection. The final model was checked for variance inflation to detect collinearity of included
predictors. Significant influences of the final model predictors were tested with a post-hoc
ANOVA with 999 permutations.
Gross and net effects of environmental variables were calculated by using partial RDA (pRDA).
Gross effects were assessed by setting up models for each single predictor, without
considering any covariables. For detecting net effects, a single predictor was tested with all
other final model predictors included as covariables to partial out their effects.
As the study sites as such had a considerable influence on species composition, likely to
suppress measureable effects of history, climate and other site-related factors, two final
models were set up; one with site as conditional term (RDA+s), the other without it (RDA-s).
Site-specific pseudoreplication effects bias was judged by quantifying remaining area-specific
parts of explained variance in net area model, where all predictors of the final model were
used as covariables.
For assessing plant species richness, species alpha-diversity (total species richness per 4 m²
plot) was calculated. Threatened species occurrences per life form group were counted based
on the most recent national red lists (vascular plants: Metzing et al. 2018; bryophytes:
Caspari et al. 2018; lichens: Wirth et al. 2011; ESM2_4: Table S4-1 includes a list of all red list
species).
For the purpose of rating the plant communities with respect to their nature conservation
value, they were assessed in their heathland-typical species composition as well as their
typical structures and threats, according to the criteria for nature conservation assessment of
European dry heaths (HT 4030) and Dry sand heaths (HT 2310) (NLWKN 2012; LfU 2014a,
2014b). The criteria given in the national mapping instructions were extrapolated for
application at the community scale (see definition of modified criteria ESM2_4: Table S4-2).
Chapter 2: Heathland plant species composition and vegetation structures
32
Following the mapping instructions, the rating categories range between A – favourable, B –
unfavourable and C – unfavourable-bad.
Statistical analyses and plots were performed in statistical software R (R Core Team,
www.rproject.org Version 3.4.1). We used the packages ‘isopam’ (Schmidtlein 2014) for
Isopam clustering, ‘cluster’ (Maechler et al. 2018) for calculating silhouette widths, ‘goeveg’
(Goral & Schellenberg 2019) for creating synoptic Tables, calculating diagnostic species and
fidelity Φ, and ‘vegan’ (Oksanen et al. 2019) for calculating RDA, pRDA and ordination plots.
2.3 Results
Main characteristics of North German dry heathland plant
communities
The classification revealed nine floristically and structurally distinct heathland plant
communities (Table 2.2, Fig. 2.2). The identified communities belong to the Genisto pilosae-
Callunetum Braun 1915 (syn. Genisto anglicae-Callunetum Tüxen 1937), represented by
communities 1-6 and 8-9, and the Euphorbio cyparissiae-Callunetum vulgaris Schubert 1960,
approached by community 7. The main floristic differences are roughly related to vascular-
plant richness (units 1,4,7), lichen richness (units 2,4,5) or generally species poverty (3,6,8,9).
For phytosociological and floristic detail, complete synoptic tables and fidelity values see
ESM2_2.
The nine communities were grouped into three heathland development stages, according to
their dominant Calluna growth phase:
1) early-stage regeneration, from Pioneer to early Mature stage (3 communities);
2) Late Building up to Mature stage (4 communities); and
3) Late Mature up to Degeneration stage (2 communities).
Additionally, the communities showed distinct patterning in two types of Calluna cover
characteristics (stand mosaic structure vs. Calluna dominance). Generally, mosaic
communities (1, 4, 6, 7, 9) showed lower Calluna cover, but high cover of vascular non-ericoid
plants, whereas Calluna dominance stands (2, 3, 5, 8) have simple stand structure with dense
Calluna canopy and an understory of cryptogam mats (Fig. 2.3). Hence, vascular plant
diversity was clearly related to mosaic structure (communities 1, 4, 7), whereas lichen
diversity was potentially high in Calluna dominance stands as well (community 5, Fig. 2.3,
ESM2_4: Fig. S4-1).
Chapter 2: Heathland plant species composition and vegetation structures
33
Factors shaping species composition and structures
The RDA revealed that species composition was explained best by humus layer thickness and
cover of mature heather, irrespective of whether site effects have been included (RDA+s) or
not (RDA-s), Table 2.3). These two factors, along with related environmental conditions, span
two of the three main gradients shaping compositional patterns in the ordination diagram
(Fig. 2.2).
The first gradient describes the shift of edaphic soil conditions along a successional gradient,
expressed by decreasing bare sand and increasing humus layer thickness along the first axis
(Fig. 2.2a). Floristic diversity, as well as cover of herbs and lichens was related to open stands
of early successional stage (Fig. 2.2c), more specifically in communities with early-
successional edaphic conditions rather than in communities with early-stage regeneration of
heather (Fig. 2.2d).
The second gradient was characterized by a change of structural components along the
second axis, explaining 4.8% of variance. Open, grass-rich stands differ clearly from those
dominated by Calluna, reflecting the structural attributes of Calluna cover characteristics
reported above.
Calluna age structure explained 3.5% (RDA+s) or 3.8% (RDA-s) of diagnostic species
composition, with the major share explained by cover of mature heather plants (Table 2.3). It
was only marginally reduced when including site effects, thus validating its general effect on
heathland species composition.
Calluna age structures and their changes along the gradient could be related to recent and
historical management, because disturbances directly affect heather growth. Recent
management explained 7.1% of total species composition variance (RDA-s), with highest
explanation power of grazing regimes (2.8%, p ≤ 0.01), while intensive management (2.1%, p
≤ 0.001) and site history (1.1%, p ≤ 0.001) showed weaker explanatory power.
Cryptogam-rich regeneration (community 2) often occurred after burning, whereas the
vascular-plant rich or species-poor regeneration stages (communities 1 and 3) developed
more frequently after mowing (ESM2_3). The high vascular plant diversity of community 7
was strongly related to horse- and cattle-grazing, the other plant assemblages showed a
rather weak pattern concerning grazing regimes (ESM2_3).
Chapter 2: Heathland plant species composition and vegetation structures
34
Table 2.2 Synoptic table of heathland plant communities in the North German Plain. Species with a minimum
frequency of 20% and a diagnostic character in one of the identified plant groups are listed. Frequencies
highlighted in grey refer to positively differentiating species. Frequency values ≥ 25% are in bold type. Asterisks
are indicating diagnostic fidelity values (Φ > 0.3). Life form groups: s – shrubs and dwarf shrubs, h – non-
graminoid herbs, g – graminoids, m – bryophytes, l – lichens, t – trees. Silhouette width s(i) is a measure of Isopam
clustering validity, with values ranging from 0 (low structure) to 1 (optimum clustering structure). Not included
species of high frequency, but low diagnostic value: Calluna vulgaris, Carex pilulifera, Deschampsia flexuosa, Rumex
acetosella, Hypnum cupressiforme, Pinus sylvestris, Brachythecium rutabulum. A table of all species and fidelity
values is presented in ESM2_2. Table continues on the next page.
I Early-stage regeneration
heathland
II Late Building and Mature stage
III Late Mature
and
Degeneration
stage
1
2
3
4
5
6
7
8
9
association
Genisto pilosae-Callunetum typicum,
vascular plant-rich regeneration stage
Genisto pilosae-Callunetum
cladonietosum, cryptogam-ric h
regeneration stage
Genisto pilosae-Callunetum typicum,
species-poor regeneration stage
Genisto pilosae-Callunetum
cladonietosum, Corynephorus variant,
cryptogram-rich open sand grass-
heathland
Genisto pilosae-Callunetum
cladonietosum, Mature-stage cryptogam-
rich open sand heathland
Genisto pilosae-Callunetum
danthonietosum,
consolidated dry sand heath
Euphorbio cyparissiae-Callu-netum
vulgaris, subcontinenttal dry grass-
heathland on base-containing ground
Genisto pilosae-Callunetum typicum,
moss-rich degeneration stage
Genisto pilosae-Callunetum typicum,
Deschampsia flexuosa- and moss-rich
degeneration stage
Sample
size
41
21
32
40
53
23
8
55
77
s(i)
0.02
0.03
0.05
0.07
0.08
0.06
0.14
0.11
0.11
Life
form
group
I Early stage regeneration
heathland
Placynthiella
oligotropha
l
7
38*
9
5
13
0
0
2
1
Betula pendula
t
7
24
12
2
4
9
12
15
4
Molinia caerulea
g
37
52
34
0
6
22
0
16
23
Cladonia pyxidata
l
32
48
22
35
55
22
12
5
5
Cladonia macilenta ssp.
macilenta
l
10
29
9
22
21
0
0
4
3
Campylopus introflexus
m
12
38
16
0
21
0
0
5
8
Ceratodon purpureus
m
41
86*
3
30
17
17
25
7
4
Placynthiella icmalea
l
41
62
34
28
30
13
0
0
0
Cephaloziella divaricata
m
32
57
41
60
74*
0
25
9
5
Cladonia coccifera
l
27
14
22
68*
45
4
0
5
4
Corynephorus canescens
g
24
0
0
58*
4
35
12
0
1
Festuca filiformis
g
29
38
3
5
4
52
0
9
8
Hypochaeris radicata
h
32
5
0
25
2
70*
12
2
4
Nardus stricta
g
20
0
6
2
4
22
0
9
17
Hieracium pilosella
h
41
19
0
32
8
91*
75
5
1
Agrostis capillaris
g
59
5
3
35
9
74*
75
9
14
Agrostis vinealis
g
29
5
0
22
4
22
62
4
9
Polytrichum piliferum
m
71
43
31
98*
57
70
12
7
3
II Mature-stage
Open sand grassland group
Spergula morisonii
h
12
0
0
50*
9
4
0
5
1
Cladonia furcata
l
7
0
0
28
19
13
0
5
5
Trapeliopsis granulosa
l
5
19
6
28*
6
0
0
0
0
Cetraria aculeata
l
0
5
0
25*
9
0
0
0
1
Cladonia pleurota
l
2
0
3
20
11
0
0
0
0
Cladonia uncialis
l
5
0
0
20
11
4
0
4
4
Cladonia subulata et rei
l
39
52
19
92*
87*
39
25
18
12
Cladonia ramulosa
l
20
10
6
48
49*
0
0
4
5
Cladonia cervicornis s.l.
l
5
10
9
35
28
0
0
2
3
Cladonia gracilis
l
2
5
3
30
28
0
0
2
3
Pohlia nutans
m
5
29
19
32
45*
4
12
7
4
Cladonia fimbriata
l
10
24
9
35
64*
17
38
24
16
Cladonia portentosa
l
2
14
3
12
32
0
0
11
9
Cladonia coniocraea
l
2
5
3
10
23
0
0
11
3
Dicranum polysetum
m
2
0
3
8
23
0
0
11
9
Continued on next page
Chapter 2: Heathland plant species composition and vegetation structures
35
Table continued from previous page
I Early-stage regeneration
heathland
II Late Building and Mature stage
III Late Mature
and
Degeneration
stage
1
2
3
4
5
6
7
8
9
association
Genisto pilosae-Callunetum typicum,
vascular plant-rich regeneration stage
Genisto pilosae-Callunetum
cladonietosum, cryptogam-rich
regeneration stage
Genisto pilosae-Callunetum typicum,
species-poor regeneration stage
Genisto pilosae-Callunetum
cladonietosum, Corynephorus variant,
cryptogram-rich open sand grass-
heathland
Genisto pilosae-Callunetum
cladonietosum, Mature-stage
cryptogam-rich open sand heathland
Genisto pilosae-Callunetum
danthonietosum, consolidated dry
sand heath
Euphorbio cyparissiae-Callunetum
vulgaris, subcontinental dry grass-
heathland on base-containing ground
Genisto pilosae-Callunetum typicum,
moss-rich degeneration stage
Genisto pilosae-Callunetum typicum,
Deschampsia flexuosa- and moss-rich
degeneration stage
Sample
size
41
21
32
40
53
23
8
55
77
s(i)
0.02
0.03
0.05
0.07
0.08
0.06
0.14
0.11
0.11
Life
form
group
Dense grass-heathland
plant group
Carex arenaria
g
12
0
6
15
4
22
12
4
3
Festuca ovina
g
15
0
3
42
17
30
62
9
17
Hypericum perforatum
h
12
10
0
8
2
35
75*
4
1
Danthonia decumbens
g
2
5
0
8
0
13
88*
5
1
Genista tinctoria
s
0
0
0
0
0
0
62*
0
0
Luzula campestris
g
5
0
3
5
6
30
50
9
9
Potentilla argentea
h
0
0
0
0
0
4
50*
0
0
Koeleria macrantha
g
4
0
0
0
0
0
38*
0
0
Polygala vulgaris
h
0
0
0
0
0
0
38*
0
0
Campanula rotundifolia
h
0
0
0
0
0
0
25*
0
0
Thymus serpyllum
s
0
0
0
2
0
0
25*
0
0
Subcontinental grass-
heathlands on base-
containing sands
Calamagrostis epigejos
h
17
0
0
10
6
0
100*
11
10
Galium verum
h
0
0
0
0
0
0
50*
0
0
Helichrysum arenarium
h
2
0
0
0
0
4
50*
0
0
Leucanthemum
ircutianum
h
0
0
0
0
0
0
50*
0
0
Plantago lanceolata
h
2
5
0
0
0
13
50*
0
1
Euphorbia cyparissias
h
0
0
0
0
0
4
38*
0
1
Viola riviniana
h
0
0
0
0
0
0
38*
0
3
Achillea millefolium
h
2
0
0
0
0
9
25
2
0
Anthoxanthum
odoratum
g
0
0
0
0
2
4
25
0
3
Centaurea jacea
h
0
0
0
0
0
4
25*
0
0
Centaurium erythraea
h
0
0
0
0
0
0
25*
0
0
Dianthus deltoides
h
2
0
0
0
0
0
25*
0
0
Disturbed sites
Populus tremula
t
2
0
3
2
4
0
38
5
4
Tanacetum vulgare
h
0
0
0
0
0
9
38*
0
0
Taraxacum sec.
Ruderalia
h
0
0
0
0
0
0
25*
2
0
III Mature and late
mature-stage plants
Hypnum jutlandicum
m
22
10
25
60
89
17
12
93*
73
Dicranum scoparium
m
15
19
12
35
55
0
0
29
57
Pleurozium schreberi
m
2
0
6
22
51
4
0
51
71*
Galium saxatile
h
15
0
0
0
2
13
0
4
32*
Chapter 2: Heathland plant species composition and vegetation structures
36
Table 2.3 Gross and net effects of environmental factors on species composition (% of explained variance). Gross effects given for all tested constraints, but net effects only calculated for
those included in the final model. Final models given for the version with including site effects, were site was included as covariable (conditional term and for the model version without
considering site effects (RDA without site). Net effects were calculated using one predictor of the final model and the others as covariables. Asterisks show effect significances in the net
model (*** p<0.001).
Chapter 2: Heathland plant species composition and vegetation structures
37
Fig. 2.2 Redundancy Analysis (RDA) of species composition, with envelopes around samples (plots) representing
groups of identified plant communities. RDA without site (RDA − s) used for creating ordination diagrams. RDA
axis 1 explained 7% of total variance, RDA axis 2 explained 4.8%. The nine plant communities differ in aspects of
vegetation structure (a), species composition (b), species richness (species/[4 m2]; c), and the linear constraints
identified in RDA − s for explaining species composition differences (d). Constraints were age structure of heather
(% of cover; P, Pioneer; B, Building; M, Mature; and D, Degeneration, explaining all together 3.8%), airborne
nitrogen deposition (0.8% exp. variance) and humus accumulation (2.4%). For species composition (b), only the
10% of the species fitting best to the RDA ordination and the 70% most abundant species were displayed using
the ordiselect()-function in R (Goral and Schellenberg, 2019). Three main gradients shaping heathland species
composition were identified: (1) along the first axis: shift of edaphic soil conditions along a successional gradient,
with early stages at the left and later ones on the right part of the diagram; (2) along the second axis: structural
gradient with open, grass-rich stand in the upper part of the diagram and dominance, but bryophyte- and lichen-
rich stands at the bottom; (3) climate and airborne nitrogen deposition, with sub Atlantic/subcontinental sites
with low nitrogen deposition at the lower left quadrant of the diagram and higher nitrogen loads and Atlantic-
subatlantic sites in the upper right quadrant.
Chapter 2: Heathland plant species composition and vegetation structures
38
Fig. 2.3 Heathland plant community cover proportions (%) of a) Calluna vulgaris, b) open soil, c) non-graminoid herbs, d)
graminoids, e) bryophytes and f) lichens. 1-3 Early-stage regeneration heathlands; 4-7 Late Building to Mature stages; 8-9 Late
Mature and Degeneration stages. For names of plant communities 1-9 see Table 2.2. Single letters at the boxplot top are
indicating significant group differences (<0.05).
The third gradient is encoded in the strongly coupled factors of climate, nitrogen deposition
and site history. Former military training areas included in our study are distributed in the
subatlantic-subcontinental eastern and southeastern part of the German Lowland, showing
rather low oceanicity, with lower airborne nitrogen loads (Fig. 2.2d, ESM2_1: Table S1-1,
ESM2_3). Communities there provide potentially higher lichen cover and diversity, the
cryptogam-rich bare sand grass-heathland (community 4) is strongly restricted to those
conditions.
In contrast, the grass-rich communities 1 and 9 are old traditional heathlands or active
military training sites of the Atlantic biogeographic region, exposed to higher nitrogen loads.
Site effects caused a strong patterning, overlaying effects of management, climate and
edaphic conditions (cf. explanatory power of predictors RDA+s vs. RDA-s, Table 2.3).
Management effect was strongly reduced by including site effects in the model as covariates
(1.6% in RDA+s vs. 7.1% in RDA-s, Table 2.3). A weaker reduction was found for climatic and
edaphic conditions (3.7% in RDA+s vs. 5.3% in RDA-s). This indicates site-specific
management and climate inseparable from general site effects and may involve
pseudocorrelation issues. To reduce this uncertainty, we calculated the remaining net
explained variance by area when the explanatory power of final model constraints was
factored out. We interpreted this as the component of site effects not explainable by the
factors included in the model but by pseudocorrelation. With 12.7% of explained net variance
Chapter 2: Heathland plant species composition and vegetation structures
39
in RDA+s and 8.2% in RDA-s, effects of site-specific species pools and composition appeared
to be strong.
Pathways of heathland development
The interplay of the RDA gradients interpretation of the conditions shaping community-
specific plant assemblages allowed for an identification of two edaphically driven
successional pathways, each with specific plant communities involved and characteristic
plant species turnover (Fig. 2.4):
(1) Psammophilous heathland pathway: Initial Corynephorion pioneer grassland is
invaded by Calluna, forming an open sand grassland-heathland mosaic (community 4).
With increasing heather cover and soil development, two-layered stands of tall
Mature-phase dominant heather plants with regrowth in the understory and a highly
diverse cryptogam layer develops (community 5, cryptogam-rich bare sand heath).
Cryptogam synusial assemblages show clear successional turnover, with an early-
stage species group indicating exposed sand dune conditions (e.g. Cladonia furcata,
Trapeliopsis granulosa, Cetraria aculeata), followed by assemblages of humus- (or
wood-)dwelling lichens demanding relatively high humidity, such as Cladonia
fimbriata, C. coniocraea and C. portentosa. Intense management leads to cryptogam-
rich regeneration stages (community 2). With lack of management, they develop
towards moss-rich degeneration stage (community 8) or to moss-rich heath-
woodlands.
This pathway is linked to very poor sandy soils and to former military training areas,
where frequency and intensity of soil disturbances used to be very high in the past,
but are now absent for at least 5 years. Due to the fact that military training sites
occurred mainly in the eastern part of Germany, this pathway is also linked to rather
low oceanicity.
Under conditions of high airborne nitrogen deposition, a cryptogam-poor
regeneration stage (community 3) or grass- and moss-rich degeneration stages
(community 9) may occur.
Chapter 2: Heathland plant species composition and vegetation structures
40
Chapter 2: Heathland plant species composition and vegetation structures
41
<< Fig. 2.4 Succession schemes of German dry lowland heathlands, (a) Psammophilous heathland pathway (ht
2310 – Dry sand heaths with Calluna and Genista) and (b) Consolidated heathland pathway (ht 4030 - European
dry heath). Potential pathways in heathland succession were determined by edaphic conditions and related site
history and climate. Numbers of units refer to plant communities in Table 2.2. Potential development under high
airborne nitrogen load (approx. >15kg N/ha-1*a-1) is shaded in grey.
(2) Consolidated sand pathway: This heathland succession pathway was found on acidic,
more or less nutrient-poor sands which are more fine-grained, humus-rich and
consolidated than in the preceding pathway. The typical form, involving communities
1, 3, 6 and 9, results in fairly species-poor heathlands of varying structure, but often
with Calluna dominance; regeneration stages of the Genisto-Callunetum typicum
(community 3) generally had less than 10 species per 4 m². Further succession leads
to species-poor variants of the Genisto-Callunetum danthonietosum with high Calluna
cover (community 6), but also directly towards a moss-rich degeneration stage
(community 9), without a species-rich mature stage. Although generally poor in
species, the communities along this successional pathway represent heathlands with
a typical vascular plant composition but rather low structural diversity.
A base-rich subtype in Young Drift landscapes in subcontinental eastern Germany is
characteristic of slightly more favourable sandy soils with considerable humus and
base content where heaths rich in vascular plants and generally low cryptogam
diversity develop. Within stands containing a mosaic structure, suitable management
often leads to species-rich regeneration stages with high structural diversity
(community 1). Mature stages with these conditions were restricted to only one site
in our study (community 7, Oranienbaumer Heide), where the Euphorbio cyparissiae-
Callunetum vulgaris represents a local grass-heathland mosaic.
High nitrogen deposition rates may favour grass-rich subtypes, thus explaining grass-
dominated species-poor regeneration (community 3) or degeneration stages
(community 9).
Conservation value of heathland plant communities
The nature conservation status of plant communities varied widely, ranging from a quite
good (A-B) to an unfavourable status (B-C, Table 2.4). Specifically, when applying heathland-
typical structures as criterion mosaic communities (1, 2, 4) provided a higher potential value
for favourable conservation status than dominance stands (communities 3 and 5).
Degeneration stages, if prevailing, generally had low potential for favourable structural
conditions.
In terms of the second criterion of ‘heathland-typical species composition’, vascular-plant-
rich mosaic communities of early regeneration to mature stage qualified for grade A.
Chapter 2: Heathland plant species composition and vegetation structures
42
Although generally rich in threatened lichen taxa, cryptogam-rich communities often
achieved only a grade B due to the fact that these communities were often deficient in
vascular plant composition.
We found 191 species in total, with 57 of them nationally red-listed. The majority of red-
listed species were lichens or non-graminoid herbs (see ESM2_4 for more details). The
majority of red-list bryophytes and vascular plants were category V, corresponding
approximately to IUCN category ‘Near Threatened’, whereas most of the lichens were listed
as ‘Vulnerable’, ‘Endangered’ or even ‘Critically Endangered’.
Applying the third conservation value criterion, ‘threats such as unfavourable grass
dominances, tree or neophytes/ruderals invasions’, generally resulted in low quality
assessment, but some communities appeared to be more vulnerable than others. The
regeneration stage rich in vascular plants (community 1) was found to be subjected to a high
risk of grass encroachment by Molinia caerulea or Deschampsia flexuosa. However, mature
stages were assessed as being subjected to only low to moderate risk of grass prevalence. The
vascular-plant rich and structurally diverse Euphorbio-Callunetum (community 7) often
suffered from invasion by grasses (Calamagrostis epigejos) and ruderal plants. Neophytes
were found regardless of specific patterning. Campylopus introflexus, an invasive acrocarpous
moss, Erigeron canadensis, a summer-annual or biennial herb, and Prunus serotina, a rapidly
regenerating shrub or small tree, were the most frequent and locally abundant neophytes. On
degeneration-stage plots, neophytes were usually absent. Ruderal plants occurred only on
base-rich sands in the Euphorbio-Callunetum (community 7, ESM2_2: Table S2-1).
Taken together, three communities were rated to be of high nature conservation value; the
mosaic heaths of the Genisto-Callunetum typicum, including its species-rich regeneration
stage (communities 1 and 6) and the Corynephorus variant of the Genisto-Callunetum
cladonietosum (community 4).
Chapter 2: Heathland plant species composition and vegetation structures
43
Table 2.4 Assessment of potential nature conservation status, based on national criteria, considering heathland-typical species inventory, structures and threats (according to mapping
instructions for the monitoring of Natura 2000 habitat types 2310/4030 (NLWKN 2012, LfU 2014a & 2014b). Highest values are highlighted in bold. Nature conservation status: A –
Favourable, B – Unfavourable - inadequate, C – Unfavourable - bad.
Early-stage regeneration
Late Building to Mature heathland
Late Mature to
Degeneration stage
1
2
3
4
5
6
7
8
9
habitat-typical
structures
typical relief
high
high /
moderate
moderate
high
moderate
high /
moderate
high
low
low
open sand [%]
high
high
moderate
high
high
high
high
moderate
low
beneficial Calluna age structures
high
high
moderate
high
high /
moderate
high /
moderate
moderate
low
moderate
typical structures grade
A
A
B
A
B
A-B
A-B
C
B-C
heathland-typical species composition
vascular plants
mean frequency of typical vascular plants [4m²]
ht 2310
5.1
2.4
2.2
4.4
2.2
6.2
6.8
2.6
3.6
ht 4030
5.6
3
2.8
4.9
2.5
6.4
6.6
3
4.3
mean frequency of red list vascular plant species/4m²
0.5
0.2
0.3
0.7
0.2
0.6
3.9
0.3
0.3
vascular plant interim grade
A
B
B
A
B
A
A
B
A-B
cryptogams
mean frequency of typical mosses
1.2
1.0
1.0
2.2
2.8
1.0
0.5
2.1
2.2
mean frequency of typical lichens
2.1
3.1
1.5
5.7
4.9
1.0
0.4
0.6
0.6
endangered cryptogam species [per community]
13
11
12
21
24
5
1
11
16
mean occurence of endangered cryptogam species/4m²
0.7
1.1
0.7
3.1
2.9
0.3
0.1
0.5
0.5
cryptogams interim grade
B
B
B
A-B
A-B
B-C
B-C
B-C
B-C
total red list species
total endangered species
24
15
16
28
29
12
12
19
25
mean occurence of endangered species/4m²
1.2
1.3
0.9
3.8
3.2
0.9
4.0
0.8
0.9
species composition grade
A
B
B
A
A-B
A
A
B
A-B
threats
potential risk of unfavourable dominating grasses (<30%
cover)
high
low
low
low
low
moderate
moderate
low
high
neophyte/ruderal occurences
low
moderate
moderate
low
moderate
moderate
high
low
low
tree invasion
low
moderate
moderate
moderate
high
low
high
high
high
threats grade
A-B
B
B
A-B
B
A-B
B-C
B
B-C
Total nature conservation
status potential (total rating)
A-B
B
B
A-B
B
A-B
B
B-C
B-C
Chapter 2: Heathland plant species composition and vegetation structures
44
2.4 Discussion
Floristic and structural characteristics of dry lowland
heathlands
Our analysis of heathland plant communities, their structures and species composition as
well as their relationship to climate, soil and management provided valuable insights into the
complex conditions governing the ecology and appearance of heathlands in northern
Germany. The important role of the dwarf shrub Calluna vulgaris as the key species of
Northwest European dry lowland heath could be verified. Calluna determines stand structure
and developmental stages by growth phase composition and plant canopy cover.
Furthermore, we show that considering Calluna age structures and the life form group
composition improves the floristic-based classification in terms of ecological information
value considerably. In this study, we linked its versatile growth habit directly to patterns of
species diversity and composition.
The total cover of Calluna determines the stand character as rather dense Calluna dominance
heath or a more open grass-heather mosaic. This confirms the general concept of heathland
formations described by Gimingham (1972). Mosaic stands can be ‘typically’ three-layered
with Calluna canopy, herbaceous plant layer (incl. graminoids) and cryptogam layer
(Leuschner & Ellenberg 2017). We showed that such a typical heathland structure does not
coincide with high species diversity nor with high conservation value and presence of red-
listed taxa. The mosaic-type dry grass-heathland on base-rich sands (community 7) lacks a
cryptogam layer, but shows high vascular plant diversity. In contrast, the lichen-rich open
Calluna-dominated heath (community 4) is structurally simple but includes many red-list
lichen species.
The dominant Calluna growth phase determines the heathland development stage, along with
characteristic species turnover and shift of soil conditions. It is noteworthy that the pattern
formation (dominance, mosaic) is not strongly related to heathland development stages.
Richness patterns of vascular plants and lichens are directly determined by edaphic
conditions and Calluna density and age, resulting in distinct lichen-rich, vascular-plant-rich or
generally species-poor assemblages. Generally, we found heathland-typical vascular plant
diversity to decrease towards the East and Southeast, where more grassland species
contribute to the general heathland plant composition, supporting findings of Schubert
(1973).
Chapter 2: Heathland plant species composition and vegetation structures
45
Environmental conditions determining heathland
vegetation
The drivers of heathland biodiversity are known to be complex and characterized by several,
interacting factors (Fagúndez 2013). We showed that additive effects of Calluna age
structures and site history, recent management, edaphic and climatic factors are shaping
heathland vegetation patterns and stand structures, and their interaction may further
strengthen these effects. The two identified soil-related pathways of heathland development
confirmed that floristic patterns may be explained primarily by soil conditions (De Graaf et al.
2009) and by stand-internal structural features.
During heathland succession the proportions of organic matter and clay in the sands enhance
nutrient and water supply, favouring vascular plants (De Graaf et al. 2009; Heil & Diemont
1983; Mitchell et al. 2000, Sevink & de Waal 2010). In our study, this process, involving
consolidated, somewhat more nutrient-rich sandy soils, was found to result in higher
vascular plant cover and diversity. The edaphic tipping point between the lichen-rich and the
vascular-plant-rich pathway appears to depend on soil texture and the amount of nutrient
and water supply. Additionally, differences in herb and lichen diversity between heathlands
were found to be determined by grazing and nitrogen deposition. Whereas the absence of
sheep grazing does not adversely affect lichen diversity and cover (nor is it necessarily
favourable for lichens), heathland grazing with horse and cattle inhibits high cryptogam
diversity, either directly through trampling and nutrient enrichment or indirectly in that
cattle and horse pastures are inherently more nutrient-rich.
Management affects heathland plant assemblages; either directly by shaping Calluna growth
or indirectly by site-history effects forming soil conditions. Heathlands, both on former
military training and historically farmed areas, depend on intense disturbance but they differ
considerably in the continuity and amplitude of anthropogenic impacts. On long-term farmed
heathlands, regularly though not pervasively disturbed, originated a fairly stable vegetation
with low-amplitude successional cycle. In contrast, military training areas are characterized
by irregular high-amplitude disturbances. The military training regime with frequent fires
and intense mechanical disturbance leads to sparsely vegetated areas or to locally bare drift
sand flats. These dune-like areas provide habitat conditions with poor water supply, towards
the East enhanced by subcontinental droughts and low relative humidity during the
vegetation period. After abandonment, which generally took place in the 1990s, natural
succession took over, resulting in small-scale habitat variation with diverse structure and
species composition (Ellwanger & Ssymank 2016).
Chapter 2: Heathland plant species composition and vegetation structures
46
Direct effects of climate appear to be of minor importance, probably influencing individual
plants, but not (yet) entire assemblages. We found no evidence for the occurrence of more
drought-tolerant taxa in subcontinental than in oceanic heathlands – except for lichens, which
showed a tendency to higher diversity and cover values in suboceanic-subcontinental regions,
no doubt supported by favourable edaphic (early-stage inland dune) conditions and lower
airborne nitrogen deposits.
Heathland succession pathways
We found that species composition differed across edaphic conditions rather than along
heathland development stages, supporting the scheme of two distinct heathland successional
pathways:
(1) The psammophilous heathland pathway, often with pronouncedly lichen-rich
communities, on dune-like habitats of bare acidic drift sands show floristic
relations to Corynephorion canescentis pioneer grasslands on sand dunes,
persistent only with continued micro-scale erosion or other frequent and
adequate disturbance events (Schubert 1974). Contrary to some reports, e.g.
Lache (1976), there was no interim stage with dominating Festuca spp. in the
subcontinental East of northern Germany. On a few occasions were Agrostis
grasslands or a direct encroachment to dense heathland or pine woodland
observed. The latter development has been reported to be typical for succession
on sand drift areas (Ketner-Oostra et al. 2010; Sevink & de Waal 2010). This
pathway is related to the HT 2310 (EC 2013), especially in the eastern German
lowlands typical for many former military training sites.
(2a) The consolidated sand heath succession pathway occurs as two subtypes. One
subtype represents the typically species-poor variant of the HT 4030 on dry Old
Drift sands. The heath structure as even-aged Calluna dominance stands may be
related to fast vegetative regeneration, favoured by mowing and burning. These
stands have a rather rudimentary, but relatively stable species composition. To
provide suitable habitats for vascular plants, nutrient-poor conditions of the
consolidated sands should be maintained, although this is difficult in areas of
high loads of airborne nitrogen such as in northwestern Germany.
(2b) The subtype of the consolidated dry heath pathway on base-rich sands includes
heaths rich in vascular plants with generally low cryptogam diversity. Not
uncommon in Young Drift landscapes in eastern Germany, this pathway
culminates in a subcontinental form of HT 4030 and also encompasses mosaics
with xeric base-rich sand grasslands (HT 6120).
Chapter 2: Heathland plant species composition and vegetation structures
47
Conclusions and implications for conservation
management
Heathland habitats are of high nature conservation value if they contain many heathland-
typical species and structures. Three of our identified communities met these criteria,
whereas the other six suffered mainly from unfavourable structures and/or imminent threats,
rather than incomplete species composition. As adverse impacts are mainly related to
insufficient or failed management, the bleak future perspective for HT 2310 and 4030 (BfN
2019) indicates that knowledge on how to efficiently and successfully manage such systems
is urgently needed in order to improve the long-term stability and restoration of heathlands.
The findings of the present study provide several implications relevant for heathland
conservation management:
(1) Our study showed that species richness patterns and occurrences of rare species are
related to soil conditions and long-term site history. Communities with the highest diversity
of (rare) species were those of early successional stage, with high bare-sand proportions and
without notable humus accumulation. Hence, maintaining or restoring heathland successfully
requires suitable soil conditions, in particular nutrient-poor early-stage sandy soils for
European dry heaths (HT 4030; De Graaf et al. 2009) or even bare dune-like conditions for
inland sand dune heathlands (HT 2310; Ketner-Oostra et al. 2010).
Our study suggests that heaths where humus accumulated and has not been removed may
provide Calluna age structural diversity after disturbance, but they are often of low floristic
diversity. In practice, sufficiently profound soil disturbance may sometimes be problematic
due to management obstacles, e.g. unexploded ordnance on active and former military
training sites (Ellwanger & Ssymank 2016; Goldammer et al. 2016).
(2) Among the differences in species composition explained by edaphic conditions, there is
only relatively little species turnover or structural change from the pioneer through to the
mature stage. This indicates a species pool already existent at early Calluna regeneration
stages. Hence, the floristic regeneration potential is predetermined during early heathland
development stages. With heathland ageing and degeneration structural diversity decreases.
However, there is also a continuous and substantial loss of species diversity. Older
development stages provide only a reduced restoration or regeneration potential.
Maintaining typical heathland of high nature conservation value in the long term means the
provision of refugia for rare heathland-typical species in Building and Mature-phase
dominated stages, so as to migrate to adjacent, currently intensively managed heathland sites.
Hence, in areas where intense management possibilities are restricted (e.g. former military
Chapter 2: Heathland plant species composition and vegetation structures
48
training areas) the focus should be to preserve the local species pools rather than
maintaining typical structures in order to prevent a gradual depletion of species diversity.
(3) Mosaic heaths provide higher floristic and structural diversity compared to dominance
stands. Therefore, management should target restoring mosaic-structured open heathlands.
Locally intensive management practices such as sod-cutting or military training may favour
such structures. In contrast, mowing tends to promote even-aged dense dominance stands.
(4) Heaths in former military training areas in the subcontinental eastern part of northern
Germany differ in species diversity and heath development pathway from historically farmed
heathlands in the northwestern part of the country. A high proportion of the former are
moreover psammophilous heaths (Sevink & de Waal 2010), generally poorer in heathland-
typical vascular plants but richer in cryptogams, floristically similar to inland drift sand
vegetation or to steppe-like heathland (c.f. Ketner-Oostra 2010; Schubert 1974). Therefore,
site-specific management schemes should be developed that respect different local species
pools and heathland successional pathways.
(5) The Calluna growth phases and life cycle concept (Gimingham 1972) need to be critically
re-assessed, taking into account (multiple) regeneration cycles and age-dependant vitality of
heather. Calluna growth phases should be considered at three different scales: (1) individual
plant life history scale, (2) mid-term heathland development, reflected by the dominant
heather growth phase in the stand (stand scale), and (3) the mid- to long-term site-history
scale, where edaphic conditions change in the course of heathland succession. Heather life
history often determines stand stage, but not necessarily site history stage as well.
Disturbances, e.g. burning, may cause a reset of early-phase Calluna plants by regeneration,
but not necessarily a reset to early-stage soil conditions. Additionally, age-dependant
resprouting capacities are likely to determine post-disturbance stand habit. Hence, the
growth-phase derived mid- and long-term development potential requires further research.
Furthermore, successful rejuvenation of heather is known to be influenced by the
predominant type (generative reproduction or vegetative regeneration), management and
favourable (micro-)climatic conditions (Henning et al. 2017; Miller & Miles 1970; Mitchell et
al. 1998). Applicability of the established Calluna life cycle concept throughout its range may
also be constrained by high airborne nitrogen loads and subcontinental weather events
affecting adversely Calluna plant vitality and heathland health (Fagúndez 2013, Meyer-
Grünefeldt et al. 2015).
Chapter 2: Heathland plant species composition and vegetation structures
49
(6) High floristic diversity is not necessarily linked to high structural diversity. This reveals
interpretation deficits of vegetation maps focussed on vascular plant composition and
contradicts the common belief that only highly structured heaths can provide high species
diversity, which is true for vascular plants, but not for lichens. Therefore, structural diversity
is an important proxy for habitat quality but should not be overinterpreted with regards to its
ability to predict floristic diversity or rare species occurrences.
(7) The lists of species considered heathland-typical (NLWKN 2012; LfU 2014a, 2014b) need
adjustment. Species instructive for conservation status and heathland development stage
need to be diagnostic for specific favourable or unfavourable habitat conditions. We showed
that determining factors are mainly soil conditions; hence species related to specific soils are
of particular informative value. In our study, lichens turned out to be diagnostic for both
favourable soil conditions and species richness. In contrast, many ‘typical’ vascular plants
being almost always present, even in species-poor communities, were indicators for more
consolidated sands, and they were less informative concerning floristic diversity.
We found that cryptogam synusial patterns turned out to be most instructive for heathland
development stages. In contrast to studies where lichen-richness is considered to be
characteristic of young pioneer or old degeneration stages (e.g. Gimingham 1972), the
present study establishes that vital lichen stands of remarkable diversity, as typical
communities of the psammophilous heath development pathway (Ketner-Oostra et al. 2010),
may also occur in heath stages dominated by Building and Mature phase heather. Typical
synusial changes along succession gradients as suggested by Coppins & Shimwell (1971) and
Daniels et al. (1993) can be confirmed for the most part, although our findings suggest
variation in floristic detail. Hence, general patterning of cryptogam assemblages are highly
indicative for assessing heathland development stages. This highlights the need for valuing
both lichens, mosses and vascular plants in their contribution to ‘typical’ heathland species
assemblage.
Chapter 2: Heathland plant species composition and vegetation structures
50
Electronic Supplementary Material
ESM2_1: Additional information to study sites and community distribution.
ESM2_2: Floristic and phytosociological remarks. Text and Synoptic Tables.
ESM2_3: Additional results. Figures for Calluna growth phase composition, site history,
climate, edaphic conditions, grazing regimes and intense managements in
heathland plant communities.
ESM2_4: Nature conservation status additional information. Tables of rare species and nature
conservation status assessment criteria applied.
ESM2_5: R source codes and original data Tables.
51
Chapter 3:
The Calluna life cycle concept
revisited: implications for heathland
management
Schellenberg J, Bergmeier E (2021) The Calluna life cycle concept revisited: implications for
heathland management. Biodiv Cons https://doi.org/10.1007/s10531-021-02325-1
Chapter 3: The Calluna life cycle concept revisited
52
Abstract
Heather, Calluna vulgaris, is a key species of European dry heath and central determinant of
its conservation status. The established Calluna life cycle concept describes four phases –
pioneer, building, mature, and degeneration – distinguishable by growth and vitality
characteristics of undisturbed plants grown from seeds. However, little is known about the
life cycle and ageing of plants subjected to severe disturbance, although measures to this
effect (burning, mowing) are common in heathland management. We studied the vitality of
over 400 heather plants by examining multiple morphological (plant height, long shoot and
inflorescence lengths, flowering activity), anatomical (growth rings) and environmental
(management, nitrogen deposition, climate) attributes. We found Calluna vitality to be mainly
determined by the aboveground stem age, and that severe disturbances promote vigorous
vegetative regeneration. Ageing-related shifts in the habit and vitality of plants resprouting
from stem-base buds is similar to that of seed-based plants, but the former revealed higher
vitality when young, at the cost of a shorter life span. In contrast, plants originating from
decumbent stems resemble building-stage plants but apparently lack the capacity to re-enter
a cycle including stages other than degeneration-type. As a consequence, we supplemented
the established heather life cycle concept with a post-disturbance regeneration cycle of plants
derived from resprouting. We conclude that management of dry lowland heathlands should
include rotational small-scale severe disturbance to support both seed germination and
seedling establishment as well as vegetative regeneration chiefly of young heather plants
capable of resprouting from buds near rootstock.
Keywords
Calluna vulgaris, degeneration, disturbance, growth phase, heathland conservation, heather
vitality, life cycle, plant age.
Chapter 3: The Calluna life cycle concept revisited
53
3.1 Introduction
Calluna vulgaris (L.) Hull (henceforth referred to as Calluna or heather) is the dominant
species of European dry heath and inland dune heath (European Union Habitats Directive
Annex 1 habitat types 4030 and 2310, EC 2013). It is an evergreen small shrub of rarely more
than 60 cm, multiple-stemmed and much-branched with numerous axillary short shoots and
erect long shoots terminating in long raceme-like inflorescences. It is of hemispherical shape
when young and mature, and with age develops decumbent or horizontal stems rooting by
adventitious buds when in ground contact (Gimingham 1972).
The vast majority of lowland dry heath in Northwest Europe is anthropogenic, semi-natural
and disturbance-driven, forming an often century- if not millennia-old landscape (Behre 2008;
Ellenberg and Leuschner 2010). As such, it is an important cultural heritage and protected
habitat for biodiversity (Chatters 2021). Throughout the last century dry heathlands have
been suffering serious habitat loss, mainly due to land use change and succession coupled
with ageing of heather, and degradation resulting from nitrogen deposition and perhaps also
climate change (Ellenberg and Leuschner 2010; Fagundez 2013). The ongoing loss of
heathland habitat in temperate Europe requires vitality monitoring of heather to assess
habitat quality, guide management planning, and estimate heath restoration and
regeneration potential. Most widely used in this context is the life cycle concept of heather
conceived by Watt (1955) and refined by Gimingham (1972; 1975). This concept defines
development phases centred on age-related attributes such as plant height and shape, growth,
flowering intensity and the proportion of dead shoots. It involves the pioneer (in British
upland heathlands plants aged up to 10 years), building (to 15 years), mature (to 25 years)
and degeneration phases (plants aged to 30–40 years; Gimingham 1975, Webb 1986). The
early stages of development up until the young mature phase are the ones with highest
biomass production and flowering intensity, whereas late mature and degenerating heather
is characterized by a decrease in flowering intensity and an increase in bare, non-flowering
shoots, especially on stems in the plant centre, and a shift from erect or ascending stems to
decumbent growth. Variations in growth form with dense compact prostrate stems with
short internodes have been reported to be caused by stress, such as exposure to wind at high
altitudes or heavy grazing pressure (Gimingham 1975).
In former times, heathland farmers aimed to maintain or improve fodder quality for their
livestock by burning and cutting, thereby enhancing rejuvenation (García et al. 2013;
Gimingham 1972; Webb 1998). Then as now, Calluna ageing and heath succession make it
mandatory to periodically reset heather to retain habitat functions and biodiversity. To this
Chapter 3: The Calluna life cycle concept revisited
54
effect, severe measures such as burning, cutting or sod cutting are carried out periodically,
e.g., every 10-20 years for burning and 20-30 years for sod cutting (pers. comm. by heathland
managers in North-German lowland heaths; Härdtle et al. 2009). Additionally, scrub and tree
management may become necessary in order to retard or prevent succession (Marrs and
Diemont 2013). Grazing is another important management factor as it delays the senescence
of heather plants and enhances seed germination by moderate soil surface disturbance
through trampling (Henning et al. 2017; Kirkpatrick and de Blust 2013).
Successful heathland recovery after severe disturbance depends on both seed germination
followed by seedling establishment and the vegetative regeneration of plants that survived
the disturbance. The rate of sexual reproduction success and asexual regeneration depends
on climate (Velle and Vandvik 2014), management type and plant age (Mohamed and
Gimingham 1970). In a subcontinental lowland heath, the amount of seed production and
germination was similar to more oceanic sites, but seedling establishment was very low
(Henning et al. 2017; Ibe et al. 2020). Favourable microclimatic conditions, such as sufficient
water supply and humidity are critical for successful seedling establishment (Gimingham
1972; Henning et al. 2017). These findings indicate that the role of seed production and
vegetative regeneration of heather varies along climatic gradients of oceanicity.
The conditions of cyclical regeneration in heathlands have been much discussed (Gimingham
1988; Marrs and Diemont 2013), particularly whether Calluna rejuvenation requires periodic
disturbances or not. According to Watt (1955), undisturbed late mature or degeneration-
stage heath can enter ‘repetitive cycling’ whereby Calluna plants rejuvenate vegetatively in
gaps. This was affirmed by Wallen (1980) who reported repetitive regeneration cycles in
long-term stable heathlands without severe disturbances, and by Webb (1986) who assumed
potential immortality of Calluna. Gimingham (1988) concluded that repeated vegetative
regeneration occurs as long as succession through trees or grasses is prevented. The
hypothesis of repetitive rejuvenation would presume constant vitality of the individual plants,
with ageing affecting aboveground biomass only. This repetitive cycling hypothesis was,
however, not addressed in more than a theoretical way up to now, probably because it is hard
to identify individual plants’ life histories by other than long-term or genetic studies.
Nevertheless, our study attempts to challenge the hypothesis and aims to provide evidence
for either vegetative regeneration capacities being constrained by plant age, or for unlimited
vegetative regrowth and thus potential immortality of individual plants.
Apart from the hitherto poorly known conditions of cyclical rejuvenation in Calluna, the role
of heather regeneration in heathland dynamics is as yet insufficiently understood. In general,
the plant has two strategies of vegetative regeneration, (1) resprouting from dormant buds
Chapter 3: The Calluna life cycle concept revisited
55
near stem base in a short timespan after biomass loss through disturbance, and (2) layering,
where older decumbent stems form dense mats by adventitious rooting, often around centres
of senescent Calluna plants (Gimingham 1972). Although mentioned repeatedly (e.g., Marrs
and Diemont 2013; Mohamed and Gimingham 1970), the role of the regeneration strategies
in the plant’s life history and in the cyclical dynamics of Calluna has not yet been covered in
depth. Moreover, existing criteria for determining Calluna growth phases do not distinguish
between plants grown from seeds, stem-base buds or from layering plants. Hence, potential
age-dependent vitality reduction cannot easily be assessed in the field, unless by keen experts.
In this study, we aim to formulate more readily accessible criteria for determining heather
plant age and growth phase.
Heather plant age at the time of disturbance (Mohamed and Gimingham 1970) and post-
disturbance Calluna regeneration capacity have often been studied, post-fire (Grau-Andrés et
al. 2019; Velle and Vandvik 2014) as well as after cutting and grazing (Henning et al. 2017).
Nevertheless, the processes and traits associated with ageing of regenerating plants remain
unclear. Little is known about how heather plants with different life histories, whether grown
from seeds, derived from resprouting or from layering, differ in ageing and life span. Further,
it is not known whether vitality attributes, such as flowering intensity and yearly increment,
differ among plants of the same age but with different life histories. A complex set of
environmental conditions may counter- or interact with age-dependent and life history
effects, interrelationships that are insufficiently understood yet: (1) management; (2) climate,
e.g. vitality-reducing droughts, and (3) nitrogen deposition (e.g. Meyer-Grünefeldt et al. 2015).
The overall aim of our study is to revise and refine the established Calluna growth phase and
life cycle concept (Gimingham 1975) so as to improve the validity of vitality-based heath
conservation status assessments and to strengthen the biological-ecological knowledge
required for informed advice on heathland management. Therefore we studied vitality
attributes in plants of different age and investigated (1) which parameters influence heather
vitality most: plant age, life history, management, climate, or nitrogen deposition; and (2)
how vitality attributes change with age. Specifically, we address the question whether there
are (3) differences in age-related vitality between plants grown from seeds (PS), plants
resprouting from buds near stem base (PR) and those growing from rooted stems lying on
the ground (PL).
Chapter 3: The Calluna life cycle concept revisited
56
3.2 Methods
Study areas and sampling
We examined a total of 445 Calluna plants in 319 plots of 25 m², randomly placed by QGIS
coordinate generation in 19 study areas across the North German lowlands (for location and
details see ESM3_1: Fig. 1, Tables 1 and 2; see also Schellenberg and Bergmeier 2020). Up to 8
representative plants were collected on each plot, two of each development phase (ESM3_1:
Table 3). Plants in pioneer phase were disregarded, as they usually had no or few flowers and
their measured parameters turned out to be not comparable to those of older plants.
For age determination, growth ring samples were taken from the rootstock just below the soil
surface (analysed to reveal the plant age) and in stems at heights of 10–15 cm (stem age). The
stem pieces of 3–6 cm length were examined by counting the growth rings on a fresh-cut
diameter surface using a binocular microscope (20–50×). In some cases, where rings were
hard to identify, cut surfaces were sprayed thinly with white interior paint. After cleaning,
white pigment particles remaining in the xylem cell lumina enabled better visibility of the
rings. All complete circular rings were counted as growth rings, incomplete ones were
assumed to be stress-induced, e.g. by drought during the growth period (Webb 1986). Counts
on very young Calluna plants showed that in the first two years no growth rings are
developed, so the approximate age of the plant was assessed to constitute its rootstock
growth ring number plus 2, and the stem age plus 3, respectively.
Fig. 3.1 Calluna habit and plant morphological terms used in this study. The yearly
increment (a+b) of a long shoot is made up of the length of the inflorescence (a) and the
length of the non-flowering part with foliate short shoots (b)
Chapter 3: The Calluna life cycle concept revisited
57
To understand the life history and development phases, we examined the plants’ habit,
adventitious rooting, and considered known management events to assess whether or not the
plant had suffered severe disturbance-induced damage so far. By comparing the growth ring
numbers of the rootstock and the stems we determined whether the aboveground plant
directly grew from seed (PS) or developed by vegetative regeneration through resprouting
from stem bases (PR) or from prostrate adventitiously rooted stems, whether or not still
connected to the original plant (PL). As it turned out that in many plants the original
rootstock was lacking or rotten to such a degree that growth rings were no longer identifiable,
two datasets were created, one containing all plants with complete growth ring counts
including rootstock used for total plant age analysis (n = 218, dataroot), and another
containing all plants, used for stem age analysis (n = 445, datastem). Despite smaller sample
size in dataroot, both datasets showed similar patterns of growth ring numbers across
development phases (ESM3_2: Fig. 2).
The trait data collected for age-dependent vitality analysis were associated either with
flowering (flower density, proportion of long shoots with inflorescences, flowers per plant,
length of inflorescence) or with vegetative growth (proportion of bare long shoots, yearly
increment) (Table 3.1).
Table 3.1 Calluna vitality attributes.
Vitality attribute
Description
Unit
Numbers of plants
examined
In dataroot / datastem
Flower density
Mean number of flowers per cm
inflorescence
count
218 / 421
Flowering long shoots
Proportion of long shoots with
inflorescences
%
218 / 445
Flowers per plant
Estimate of flowers per plant
number
218 / 445
Length of inflorescence
Mean length of inflorescence per plant (Fig.
3.1: a)
cm
218 / 445
Bare long shoots
Proportion of dead terminal long shoot tips
%
212 / 426
Relative yearly increment
Yearly increment (long shoots) as
proportion of total plant height
%
206 / 414
Total yearly increment
Annual growth: Total length of this year’s
long shoot (Fig. 3.1: a+b)
cm
218 / 445
Plant height
Maximum plant height
cm
207 / 415
Chapter 3: The Calluna life cycle concept revisited
58
The study areas are situated along a climate gradient from oceanic conditions in the
Northwest (annual precipitation about 880 mm) to subcontinental in the Southeast (annual
precipitation about 520 mm, ESM3_1: Table 2). Soils were sandy or sandy-loamy, the topsoils
more or less enriched by decomposed organic matter.
Information on management necessary for the determination of the plant life history was
gathered by questionnaires returned from site managers as well as through personal
observations during fieldwork (August-September 2014). The two management categories
used in this study can be classified as intensive, comprising measures severely affecting
aboveground plant biomass in the five years preceding fieldwork, in particular sod cutting,
low-cutting (mowing at 5-10 cm height) and burning (both accidental and prescribed), and
the less intensive grazing. Grazing regimes included reported and observed grazing and
browsing (ESM3_2: Fig. 7, Fig. 8).
Airborne nitrogen rates were extracted from the interactive map service to airborne nitrogen
deposition in Germany (UBA 2019; ESM3_1: Table 2), ranging from 10 kg/ha*y up to 23 kg/ha*y.
Oceanicity was calculated using the algorithm of Godske (1944), see ESM3_1: Table 2.
Statistical Analysis
All analyses were carried out and visualized in R (Rproject.org, Version 4.0.0). In an initial
analysis, we inspected the data for patterns that may disturb age-related effects or may cause
bias due to unbalanced sampling. An overview of the initial analysis results is given in
ESM3_2. For flower density, a correction for the sampling date turned out to be necessary (ρ
= 0.36). Therefore, we set up a simple linear model (lm() function) with the flower density as
the response and the sampling date as the predictor and then corrected for the sampling date
effect by centering the residuals around the predicted model mean.
To detect the main determinants for Calluna vitality, referring to research question (1), we
used a subset of dataroot (n = 206) with all vitality attributes as response variables and
checked the gradient length with a Detrended Correspondence Analysis (DCA, package
‘vegan’, Oksanen et al. 2019). The length of the first DCA axis was 1.82 SD, suggesting a linear
multivariate model approach (Lepš and Šmilauer 2003). Hence, Redundancy Analysis (RDA,
package ‘vegan’) with an automatic model selection (ordistep function, package ‘vegan’) was
used to detect the main factors determining Calluna vitality, out of growth ring numbers, life
history, management, oceanicity, and nitrogen deposition (RDAall). Then, we set up three RDA
with different groups of predictors: (1) RDAenv included only severe management, grazing
Chapter 3: The Calluna life cycle concept revisited
59
and nitrogen deposition as predictors to identify their effects without considering any age-
related effects; (2) RDAroot and RDAstem with rootstock or stem age and life history as
responses, respectively, and grazing, severe management as well as area as conditional terms
to quantify explanatory power of growth ring numbers and life history; (3) RDAarea, where we
used study area as fixed term to assess area-related effects on vitality that are not detected by
age and life history, set here as conditional terms (= remaining spatial autocorrelation). In all
RDA, post-hoc test for variance inflation (Zuur et al. 2009) was performed to prevent
collinearity effects.
For the analysis of age-related effects on the specific eight vitality parameters (research
questions (2) and (3)), we used linear mixed models (LMM, lmer-function of package ‘lme4’,
Bates et al. 2015; for model diagnostics: ‘lmertest’, Kuznetsova et al. 2017; ‘multcomp’,
Hothorn 2008), with each vitality parameter as a dependent variable and growth ring counts
of rootstock (dataroot) and of stems (datastem) as predictors. If necessary, response variable
was square-root transformed to account for better linear model assumptions. Model selection
was conducted with a start model containing only the vitality response depending on the
growth ring count and study area as random term to account for spatial autocorrelation. If
the initial analysis revealed significant difference(s) in the vitality response variable between
severe management or grazing categories, we included it in the model setup as random term
in order to partial out its effect, as we aimed to focus on age-related effects only. We did not
include oceanicity and nitrogen deposition, as both variables were study-area specific
(ESM3_2: Fig. 2 & Fig. 3). We then checked whether there is a linear or a unimodal (2nd order
polynomial) response of the vitality parameter to growth ring number, with visually checking
their relation in a scatter plot and comparing the resulting models. Additionally, we tested
whether the inclusion of the Calluna life history (PS, PR or PL) improved the model
significantly. To detect improvement, we compared the models using AIC-statistics and post-
model ANOVA of residuals. Plausibility checks of predictions and of the functional
relationship between vitality and age prevented probable overfitting and influenced the
selection of the final model. Final model diagnostics included a visual check of residuals
according to Zuur et al. (2009). Partial R² of growth rings, life history, management and
grazing – as far as included – were calculated by using the ‘r2beta()’-function (package
‘r2glmm’, Jaeger 2017).
For modelling age-related differences in vitality and revising the life cycle concept,
addressing our research questions (2) and (3), we used a dataset with all combinations of
category levels and values of terms included in the single vitality parameter models and then
calculated predictions with the 95% confidence interval using predictInterval-function
Chapter 3: The Calluna life cycle concept revisited
60
(package ‘merTools’, Knowles and Frederick 2020). We extrapolated the prediction range for
up to 60 years for modelling ageing processes over the entire hypothetical Calluna life span.
Age of plants at date of disturbance was calculated by subtracting the branch age from total
plant age. Results from modelling and observations of the author in the field were used for
illustrating the life cycles for PS and PR, manually drawn using the Sketchbook software
(Version 8.7.1 2019, https://sketchbook.com/).
3.3 Results
Determinants of heather vitality
RDAall revealed the strongest constraining effect of stem age and life history, which together
explained about 26% of total inertia (Table 3.2). In contrast, RDAenv with nitrogen deposition,
severe management and grazing as fixed terms explained together only 5.6% in constrained
terms, with grazing explaining the majority of it (ESM3_3). In this model, nitrogen was
included as it explained vitality better than the highly collinear factor oceanicity (ρ = 0.92).
Study area explained about 9–10% of total inertia (RDAarea), with the effects of age and life
history considered as conditional terms (ESM3_3). Hence, this variance explained by area is
the spatial autocorrelation effect in vitality not explained by age, but probably study area-
specific differences in managements, nitrogen and oceanicity (ESM3_2: Fig. 1, Fig. 3, Fig. 5).
The clear, significant influence of age on Calluna vitality in RDAroot and RDAstem explained
about 13–23% of total variation, whereby the explanatory power of rootstock age was lower
than that of stem age (Table 3.2). RDAstem revealed a significant influence of life history and
branch age on Calluna vitality (p ≤ 0.01, Table 3.2). In contrast, life history did not contribute
significantly in explaining vitality constrained to total plant age (RDAroot), indicating that life
history-related vitality is somewhat masked when focusing on total plant age. However,
relating the single attributes to age revealed some clear differences in age-dependent vitality
between PS, PR and PL, for both total plant age and branch age (Table 3.3: partial R² for lh –
life history; Fig. 3.4).
In both RDA age models as well as in RDAenv, management during the past five years and
nitrogen deposition contributed together only about 6% to explained total inertia, indicating
that age explained vitality rather than recent management activities and nitrogen loads
(Table 3.2). In LMM vitality attribute models, there was a broad confidence interval which
reflects the variability of original data, explained by random terms or remaining unexplained.
As study area was set to random, this random variance can be partly interpreted as area-
Chapter 3: The Calluna life cycle concept revisited
61
specific effects of oceanicity and/or nitrogen deposition (ESM3_2: Fig. 1, Fig. 3, Fig. 5). If
grazing and/or severe management were included as random terms, they, too, explain parts
of the variability (effect sizes: Table 3.3, ESM3_2: Fig. 5, Fig. 6, Fig. 7, Fig. 8). However, severe
management had hardly any explanatory power if included, and grazing had only marginal
effects on the relative yearly increment (Table 3.2, Table 3.3). Nonetheless, we detected some
relevant effects of climate, nitrogen deposition and management in the initial analysis by
applying simple group mean comparisons visualized as boxplots (ESM3_2). Total yearly
increment was positively correlated to nitrogen deposition (ρ = 0.28 for both dataroot and
datastem), as well as the relative yearly increment (ρ = 0.27 for dataroot, not evident in datastem)
and the inflorescence length (ρ = 0.22 in dataroot, ρ = 0.23 in datastem). Relations to oceanicity
showed a similar pattern, due to the high correlation between oceanicity and nitrogen
deposition as a sampling effect, but at a weaker level (ESM3_2: Fig 3, Fig. 5). We found a
remarkable inverse correlation of rootstock age with nitrogen deposition (ρ ≤ -0.35),
indicating that Calluna plants in areas with higher airborne nitrogen loads have a shorter life
span, or the rootstock dies early (ESM3_2: Fig. 2a,d,g).
Table 3.2 Proportion of explained inertia of RDAroot and RDAstem on the vitality parameters presented in Table 3.1.
Rootstock age or stem age (growth rings) as well as plant life history were included as constraining terms, grazing,
severe management and nitrogen deposition were included as conditional terms. Asterisks indicate significance of
parameters, from a post-hoc ANOVA of residuals with 999 permutations (*** p ≤ 0.001, ** p ≤ 0.01, * p ≤ 0.05, n.s. =
not significant).
Growth rings
Plant life history
(primary/secondary)
Constrained
terms
Grazing + Management +
Nitrogen deposition
Unexplained
RDAroot
0.13***
0.02n.s.
0.15
0.06
0.79
RDAstem
0.23***
0.03*
0.26
0.06
0.69
Chapter 3: The Calluna life cycle concept revisited
62
Table 3.3 Age-dependent vitality results from LMM for each of the vitality attributes and their response transformation ( . = no transformation, sqrt = square-root transformation), fixed
terms included (lh - life history (seed-grown (PS), resprouted (PR) or layering plant material (PL)) as additive term (lh) or as interaction to growth ring count (*lh), total model R², partial
R² for the included fixed terms and relative explained variance for random terms (total variance = 1). Severe management and grazing were only included if there was a significant
detection of category level differences in the initial analysis, see Online Resources 2 for details. R² value of model is for marginal effects, partial R² values are given for each of the fixed
term. All R² values are highlighted in bold when R²/partial R² > 0.10 and with grey font colour when R²/ partial R² < 0.05. For fixed terms, t-test based p-values from model summary
were included as asterisks (*** p ≤ 0.001, ** p ≤ 0.01, * p ≤ 0.05, n.s. not significant). In the case of non-linear relation of response and growth ring count, the R² and p-values are given for
the linear term (1st order polynomial) as well as the quadratic term (2nd order polynomial).
Model
Partial R² for fixed terms
Random terms
(relative explained variance,
total variance = 1)
Response
transfor-
mation
Fixed terms
(random terms)
R²
Growth rings
Life history
Interaction terms
Study
area
Severe
management
Grazing
a) Growth rings of rootstock
Flower density
.
lh (area)
0.04
.
0.04**
.
< 0.01
.
.
Proportion of flowering long
shoots
.
lh (area)
0.18
0.12***
0.10***
.
< 0.01
.
.
Flowers/plant
sqrt
(area)
0.18
1st: 0.14***/2nd: 0.05**
.
.
0.02
.
.
Length of inflorescence
sqrt
lh (area) (man)
0.06
0.05**
0.02*
.
0.07
< 0.01
.
Proportion bare long shoot
tips
sqrt
*lh (area)
0.58
0.53***
<0.01n.s.
lh:RA 0.09***
< 0.01
.
.
Relative yearly increment
sqrt
lh (area) (man) (grazing)
0.34
1st: 0.31***/2nd: 0.05***
0.09***
.
0.05
< 0.01
0.08
Total yearly increment
sqrt
lh (area) (man) (grazing)
0.12
0.11***
0.04**
.
0.11
< 0.01
0.02
Plant height
sqrt
*lh (area)
0.43
1st: 0.39***/2nd: <0.01n.s.
0.11***
lh:RA 1st: 0.09***/2nd: <0.01n.s.
< 0.01
.
.
b) Growth rings of stems (10-15cm of plant height)
Flower density
.
*lh (area)
0.10
0.07***
0.06***
lh:AAA 0.03***
0.03
.
.
Proportion of flowering long
shoots
.
lh (area)
0.17
1st: 0.05***/2nd: 0.05***
0.08***
.
0.05
.
.
Flowers/plant
sqrt
lh (area)
0.31
1st: 0.28***/2nd:0.03***
0.02**
.
0.03
.
.
Length of inflorescence
sqrt
*lh (area) (man)
0.13
1st: 0.07***/2nd: 0.03***
0.03***
lh:AAA 1st: 0.02**/2nd: <0.01n.s.
0.09
0.03
.
Proportion bare long shoot
tips
sqrt
lh (area) (man)
0.21
0.12***
0.09***
.
0.03
0.01
.
Relative yearly increment
sqrt
(area) (man) (grazing)
0.36
1st: 0.36***/2nd: 0.02**
.
.
0.11
< 0.01
0.04
Total yearly increment
sqrt
*lh (area) (man) (grazing)
0.08
0.03***
0.07***
lh:AAA 0.02**
0.15
< 0.01
< 0.01
Plant height
sqrt
(area)
0.53
1st: 0.52***/2nd: 0.04***
.
.
0.02
.
.
Chapter 3: The Calluna life cycle concept revisited
63
Burning supported vitality in the short-term, with growth rates (length of inflorescences,
total and relative yearly increment) significantly higher on burned sites compared to mowed
sites or those without any such severe management (ESM3_2: Fig. 5, 6). In contrast to
mowing, burning effectively reduced the amount of bare long shoot tips. Grazing affected the
annual increment, the length of inflorescences and therefore, albeit only slightly, total growth
rate (ESM3_2: Fig 7, Fig. 8).
The strength and specificity of age-dependent vitality effects in the LMMs varied between
attributes, lower R² values indicated weaker relationships between the original data and
model predictions, resulting in only marginal effects of age on the total yearly increment (R²
≤ 0.11, Table 3.3), the length of inflorescence (R² ≤ 0.13), on flowering long shoots (%, R² ≤
0.18) and on flower density (R² ≤ 0.10). In contrast, clear age-related effects were found for
the total number of flowers per plant, the relative yearly increment and plant height, which
responded specifically to branch age (R² = 0.31, R² = 0.36, R² = 0.53, respectively). The
strongest response to total plant age was found for the proportion of bare long shoot tips (R²
= 0.58).
Calluna vitality depends on age and life history
The oldest plant examined was 26 years old (i.e., with 24 growth rings counted), but the
majority of the rootstocks (dataroot) were younger than 17 years (with 15 growth rings). PS
rootstocks showed the widest age range, PR the narrowest; the majority of PR with still
existent rootstock were only 9–14 years old (Fig. 3.2a, b).
Fig. 3.2 Age of the individual plant (a, b) and the stems (c, d), for plants grown from seed (PS), from resprouting
(PR) and from layering (PL).
Chapter 3: The Calluna life cycle concept revisited
64
After severe biomass disturbance, resprouting from rootstock-near stem bases was
associated with adventitious rooting of the stems, followed by degeneration of the rootstock.
Layering started when plants were between 7 and 15 years old, but the total age of PL was
not accessible as the original rootstock was often already rotten in degenerating plants or not
identifiable due to the intertwining of decumbent stems of several plants. In general, we
found Calluna stems older than 10 years were uncommon (Fig. 3.2c, d), in particular in plants
originating from re-sprouting (PR). Erect PS stems rarely reached an age of more than 20
years. PR regenerated from plants that were largely 5-15 years old at the time of disturbance
(Fig. 3.3).
Fig. 3.3 Calluna plant age at the time of severe disturbance
(which commonly prompts resprouting). Calculated as the
frequency of the difference between total plant age (measured
on rootstock) and stem age of resprouted plants (n = 43)
The age of plants derived from stems lying on the ground (PL) depended on their distance to
the original plant’s centre. If adventitiously rooted close to it, old stems were ascending and
lying on the ground only at their bases, therefore PL were relatively old. If prostrate stems
rooted adventitiously along their length, PL were younger. The majority of the plants derived
from layering stock were younger than 9 years old, indicating that they originated from stems
of fully prostrate habit rather than from older ascending stems.
Chapter 3: The Calluna life cycle concept revisited
65
Fig. 3.4 Calluna vitality attributes over the plants’ life span, (a, b) for plants grown from seed (PS), (c, d) for plants
derived from re-sprouting near stem bases (PR), and (e, f) for plants derived from prostrate, adventitiously rooted
old branches (PL). Solid lines and coloured areas mark the original data range; dashed lines are extrapolated mean
predictions. Translucent coloured areas show 95% confidence intervals around predicted means. The predictions
shown here are based on the single vitality parameter LMMs for rootstock age (a-b) and branch age (c-f, Table 3.3).
The black vertical line indicates the hypothetical plant death when either bare long shoot tip proportion becomes
100%, or yearly increment is 0 cm
All vitality parameters –except flower density– showed a response to age (growth rings,
Table 3.3, Fig. 3.4, Fig. 3.5). PS yearly increment showed a linear decrease with age, the same
pattern was observed for the proportion of flowering long shoots. Plant height and the
proportion of bare long shoot tips increased strongly with plant age. Attributes associated
with flowering showed a unimodal response to plant age, with the longest inflorescences
observed in plants of 10-15 years, but a maximum of flowers per plant found in plants of 17-
22 years. The model predicted death of PS at a mean of about 30 years, when all long shoot
tips of the plant become bare (Fig. 3.4a, b). Branches of PS still flowering after 20 years had a
reduced growth rate and flowering. These old stems, lying on the ground but connected to the
PS plant centre, counted as PS.
Chapter 3: The Calluna life cycle concept revisited
66
Fig. 3.5 Flower density differed significantly between PS (blue), PR (red)
and PL (green). Although there was no linear response to age detected in
LMM, younger plants (<10 years) tend to have a lower flower density than
older ones. Original data points were shown as grey points. Sample size (n)
is given above the boxes. Letters above the boxes indicate significant
differences between PS, PR and PL based on a post-hoc Tukey multiple
comparisons of means test. (*** p ≤ 0.001, ** p ≤ 0.01, * p ≤ 0.05, n.s. = not
significant)
PR showed similar responses to age in plant height, relative yearly increment, but with a shift
to younger plant age, resulting in a predicted plant death after no more than 18 years (Fig.
3.4c-d). In contrast to PS, plants derived from resprouting exhibited a higher proportion,
density and length of inflorescences, as well as a greater number of flowers per plant of the
same aboveground age. The relative yearly increment was higher and the proportion of bare
long shoot tips significantly lower (Table 3.4). The number of flowers increased strongly and
linearly with age, at a much higher level than PS and PL, but parts of this prediction may be
biased due to very rich-flowering post-fire plants, observed especially in sites of high
nitrogen deposition (Fig. 3.4d). The mean prediction for total yearly increment showed a
peak in the first 10 years of growth after disturbance, but PR stopped growing at an age of
approx. 18 years, an age where the other vitality attributes do not show distinct signs of
senescence (Fig. 3.4c, d). This indicates an abrupt death of PR after an accelerated life cycle,
or a shift towards layering, which starts earlier in PR than in PS, which was observed at about
5–10 years after resprouting. These findings suggest a persistence time of PR to be restricted
to a maximum age of approx. 18 years (c.f. Fig. 3.2b).
PL vitality responses to age were similar to those of PR in terms of plant height and
proportions of flowering and bare long shoots, but more similar to those of PS in terms of the
total number of flowers, total yearly increment and inflorescence length. PL had significantly
higher relative and total yearly increments than PS, but a significantly lower proportion of
bare long shoot tips, though with high plant longevity (predicted to die after about 38 years),
Chapter 3: The Calluna life cycle concept revisited
67
even if at low level of vitality (Fig. 3.4e, f). The inflorescence length and the total number of
flowers per plant was significantly lower in PL compared or PR (Table 3.4).
Table 3.4 Vitality differences between life history categories: PS = plants grown from seed, PR = plants resprouted
from stem base, PL = plants growing from prostrate stems adventitiously rooting, for dataroot (lefthand columns)
and datastem (righthand columns). Mean estimated differences and their significances between the groups from
post-ANOVA Tukey HSD test ( . = life history not included in model, n.s. = difference was not significant, *** p ≤
0.001, ** p ≤ 0.01, * p ≤ 0.05). Significant differences are highlighted in bold font.
PS - PL
PR - PL
PR - PS
PS - PL
PR - PL
PR - PS
Flower density
-1.21n.s.
-0.09n.s.
1.12n.s.
-0.96**
1.37n.s.
2.33*
Proportion flowering long shoots
-11.57*
5.77n.s.
17.34***
-14.39***
8.63n.s.
23.02***
Flowers/plant
.
.
.
84*
1602***
2417***
Length of inflorescence [cm]
-0.03n.s.
0.04n.s.
0.14*
-0.06**
0.13**
0.36***
Bare long shoot tips
-1.95n.s.
-1.63n.s.
0.01n.s.
2.71***
-0.09n.s.
-3.77***
Relative early increment
-0.73*
0.42n.s.
2.26***
-0.03n.s.
0.28n.s.
0.48*
Total yearly increment
-0.11n.s.
0.04n.s.
0.29**
-0.15***
0.00n.s.
0.19n.s.
Plant height
0.43*
0.12n.s.
0.95**
.
.
.
The flower density (flowers per cm inflorescence) was significantly higher in PR and PL
compared to PS. There was no influence of rootstock age on inflorescence density, and only a
marginal influence of branch age, hence flower density is determined by life history or other
influences rather than by age (Fig. 3.5, model details: Table 3.3). However, splitting PS, PR
and PL in two data subsets, one containing all growth ring numbers <10, the other all
observations with >10 growth rings, reveals a clear tendency towards higher flower densities
with higher age, especially for PS (Fig. 3.5).
3.4 Discussion
Determinants for heather vitality and its dependence on
age
Calluna vitality is influenced by plant age and life history rather than by the type of
management. Visual attributes of Calluna vitality are determined by stem age rather than by
rootstock age, indicating that aboveground regeneration compensates for total plant age-
related vitality loss. Further, our results revealed that PR show even higher vitality than PS,
but only in early phases of development after disturbance up to a stem age of about 15 years.
In comparison to young PS of the same age, PR may benefit from a fully developed root
system, which allows for better water and nutrient supply (Meyer-Grünefeldt et al. 2015).
Chapter 3: The Calluna life cycle concept revisited
68
With Calluna stem age identified as the major determinant for plant vitality, successful
heathland management depends on whether the measures support sufficient aboveground
regeneration of heather plants. According to our results, burning and mowing, and in case of
surviving belowground plant material also sod cutting, induce resprouting from buds at
rootstock or stem base level, thus fostering Calluna vitality in the subsequent regeneration.
Additionally, we found a positive short-term effect of burning on the yearly increment,
possibly due to improved nutrient supply after fire (Mohamed et al. 2007, Green et al. 2013).
In contrast to severe management measures, grazing does not seem to trigger vegetative
regeneration from the plant base, although resprouting is common in terminal branches.
Grazing influenced inflorescence length and yearly increment, both highly variable between
study areas, indicating that these vitality attributes were also affected by area-specific factors
such as climate or nitrogen deposition. Our results show a clear decline in Calluna vitality
after 10–15 years, irrespective of grazing activities, indicating that grazing alone is
insufficient to ensure longer-term Calluna vitality (Kirkpatrick and de Blust 2013). On the
other hand, frequent grazing may promote layering even in pre-degenerate plants, leading to
dense mats formed by shoots with short internodes and low proportions of flowering long
shoots (own observations; Gimingham 1975).
Regeneration ability of heather after severe disturbance is known to decline with age, due to
reduced regeneration capacities by buds at stem bases and branches in older plants (Hobbs
et al. 1984; Mohamed and Gimingham 1970). Hence, severe management measures may
induce vigorous regeneration, but only in plants disturbed at an age of younger than 15 years
(Mohamed and Gimingham 1970), a fact supported by our findings. Older plants may
regenerate only by building new leading long shoots from decumbent stems. Further, we
found evidence for an aboveground biomass turnover rate of about 15–20 years, with high
vitality restricted to the first 15 years. These findings suggest either cyclical, highly vigorous
regeneration after disturbance or generally stable vitality conditions by constant
regeneration via rooting of stems lying on the ground, albeit at a lower level of vitality.
The role of climate (oceanicity) and nitrogen deposition for Calluna vitality remains
somewhat unclear, since the age structure of heath stands differs between study areas for
historical reasons, blurring possible effects of oceanicity and nitrogen load. Several study
areas with a subcontinental climate are abandoned military training sites under ongoing
succession, in contrast to oceanic, mostly continuously managed historical heathland farming
sites. Nevertheless, vitality of heather is likely to differ in oceanic and subcontinental climates,
as periods of drought or insect calamities causing heather dieback to occur more commonly
in subcontinental than in Atlantic heathlands (Marrs and Diemont 2013). We found evidence
for this in the potentially high rate of bare long shoot tips, suggesting reduced vitality at
young ages in PS. This indicates that PS might be more susceptible to unfavourable growth
Chapter 3: The Calluna life cycle concept revisited
69
conditions than PR and PL, which showed in general a lower number of bare long shoots per
plant. Seedling establishment under subcontinental climate is also hampered (Henning et al.
2017). We found evidence that layering is common in lowland heathlands, and that they may
stabilize heathlands suffering from dieback and low seedling establishment.
The yearly increment lengths found in our study (about 10 cm up to the sampling date) are
comparable to values found in Atlantic upland heathlands such as in Northeast Scotland,
where 11 cm/year have been documented (Mohamed and Gimingham 1970). We found that
growth rates in PS declined soon after seedling establishment, whereas PR peaked in growth
rate at about 5-7 years after resprouting. Other studies reported similar values (e.g. Webb
1986, p. 93).
Growth rates were influenced by nitrogen deposition rather than by oceanicity. In our initial
analysis, we detected fertilizing effects by nitrogen deposition, in particular increasing total
growth rate and longer inflorescences. Additionally, we found symptoms of accelerated
ageing and a shorter life span of heather plants under high nitrogen loads, findings supported
by several authors (Berdowski and Siepel 1988; Calvo-Fernández et al. 2018; Diemont et al.
2013; Meyer-Grünefeldt et al. 2015), although our results may also be influenced by site-
specific management, heather age structure and oceanicity. Additionally, the effects of
nitrogen loads on the growth of Calluna may further be complicated by other soil
characteristics and water supply (Diemont et al. 2013).
The life cycle concept
A vital finding of our study is the age-dependent loss of Calluna vitality cannot be interpreted
without considering the plant’s life history. Our study revealed life history-related differences
in the longevity, vitality and persistence of Calluna plants. To illustrate our findings, we
supplement the primary (undisturbed) life cycle of a plant that germinated from seed with a
secondary life cycle (‘regeneration cycle’) for plants regenerating after severe disturbance
(Fig. 3.6).
In approximation, the life cycle of a Calluna plant grown from seed and without severe
disturbance comprises three parts, (1) the pioneer and building phase, comprising 10–15
years, when the plant grows to maximum size at high vitality, (2) the mature phase, lasting a
further 10–15 years, with plants retaining their vitality or at least their height, and (3) the
degeneration phase characterized by a constant loss of vitality, biomass production and plant
size, again comprising 10–15 years. We distinguish typical mature from late mature plants,
the latter being characterized by the beginning of distal stem layering often followed by the
death of rootstock and opening of the plant centre (own observations). This shift in habit,
which takes place at an age of 12–20 years, may be used to assess the regeneration capacity,
Chapter 3: The Calluna life cycle concept revisited
70
as is can be interpreted as the maximum age for high resprouting capacity in case of severe
disturbance. While the shift from late mature to degeneration stage by definition of habitual
characteristics remains somewhat unclear in the Calluna life cycle concept established by
Gimingham (1972), we define the end of the late mature stage when the plant’s nutrient and
water supply shifted from the primary root system (near stem base) to adventitious roots.
The persistence of plants at degeneration stage remains unclear, as many of the examined
plants derived from adventitiously rooted lying stems were disconnected from the original
rootstocks. Nevertheless, from what we found, layering may occur for 5–15 years, resulting in
a total life span of 30–45 years (Fig. 3.6), which is similar to the life span of Calluna reported
for British upland heaths (Gimingham 1972, Webb 1986). Our models revealed that the first
plants die after 20 years, occasionally even earlier. This pre-mature ageing in PS may be
caused by unfavourable external factors such as periods of drought (Marrs and Diemont
2013).
After severe disturbance by high-impact management such as sod-cutting, mowing or
burning surviving heather plants may regenerate asexually from buds just below ground,
near stem bases or at decumbent or procumbent stems (Mohamed and Gimingham 1970;
‘post-fire-phases’, Webb 1986). In contrast, moderate grazing supports resprouting from
buds on the ends of browsed long shoots or last year’s short shoots (Mohamed and
Gimingham 1970). We found that severe aboveground biomass loss of up to 15-year-old
Calluna plants may trigger a secondary life cycle with high-vitality (Fig. 3.6), as opposed to
less intensive biomass disturbances, such as grazing. In our study, the majority of plants that
resprouted from buds at soil surface or just belowground derived from plants of 10 years at
the time of disturbance, usually an age of high vitality, where the plant is at the end of the
building or in an early mature stage. Post-disturbance resprouting prompts a fast regrowth to
early mature-stage plants within 10–15 years, under exceptionally favourable conditions on
burnt sites already after 3–4 years (own observations). Such vigorous resprouting after fire is
supported by a higher nutrient supply due to ash deposition, but also to the fast post-fire
recovery of microbial communities, i.e. ericoid mycorrhizal fungi (Green et al. 2013). The
latter allows for a very efficient nutrient uptake under the conditions of high acidification and
aluminium toxicity (Shaw & Read 1989), hence providing a competitive advantage for Calluna
(Vogels et al. 2020).
Chapter 3: The Calluna life cycle concept revisited
71
Fig. 3.6 Calluna life cycle, with the undisturbed growth of plants growing from seeds (PS, upper line), and below after severe biomass disturbance, indicated by arrows. Young plants in
the mature stage resprout vigorously, as long as plants are sustained through functioning rootstock and stem base. Later, regeneration leads to dense, but not persistent mature-stage
plants of a maximum height of 50-60cm. Growth phases: P – pioneer, B – building, M – mature, LM – late mature, D – degeneration. Age spans given indicate the approximate plant age or
the age of regenerating plants after disturbance with x = age of plant at disturbance time
Chapter 3: The Calluna life cycle concept revisited
72
In general, PR turned out to be more vigorous than PS of the same age. Compared to PS, PR
was less susceptible to external stress factors, such as drought, as shown by lower rates of
bare long shoot tips which are beneficial, particularly in climates where periods of drought
occur more frequently. Nutrients available due to ash deposition may be used more
effectively by an extant root system. We observed intensified adventitious rooting after fire,
which also favours nutrient uptake. As another consequence, intensified rooting leads to a
shift in plant nutrient supply via rootstock to stem base roots, probably resulting in PS
rootstock decay and layering to occur earlier in PR of the same aboveground biomass age (Fig.
3.6). While both PS and PR are highly vital up to 10–15 years, PR then show a strong decline
in vitality, and a shift from the majority of stems in the plants’ centres towards more
adventitiously rooting stems. We showed that the turnover time of resprouted plants is about
10–15 years and found no evidence of stems with longer persistence. Layering processes
become dominant in plants about 15–20 years of age after disturbance, with vitality similar
to seed-based plants with decumbent stems. In contrast to the life cycle of undisturbed plants,
resprouted plants perform an accelerated regeneration cycle, reaching building, mature, late
mature and degeneration stages earlier than PS of the same aboveground age. The plant habit
of PR can imitate the PS-typical hemispherical growth in the first years after resprouting, but
the stems are usually generated by multiple resprouting buds near the rootstock, which is
why the habit of PR is often denser. Plants at the end of the building stage began layering,
flatten or become diffuse in shape, especially in dense regeneration stands as earlier as 10–15
years after disturbance. The reduction of yearly increment and the layering limits the plant
height to max. 50–60 cm, even at mature stage. Hence, the mature stage of a regeneration
cycle lacks high-growing distinct Calluna bushes, and is characterized by dense, rather flat
cushions. We found no signs of the total life span of resprouted Calluna being extended, but
resprouting prolongs the plant’s high-vitality life phase.
We showed that layering plants in both the primary and the regeneration cycle are part of the
degeneration stage of Calluna, with low vitality, as far as flowering traits are concerned, and
the inability to achieve ‘repetitive cycling’, i.e. to become a mature plant again. Moreover, we
could show that layering can be a quite stable and resilient growth form of degenerating
Calluna plants. Unlike Gimingham (1975), who described stems lying on the ground as a
characteristic of the degeneration phase persisting about 5–8 years or as a specific
modification of wind-exposed plants, e.g., at high altitudes, or under high grazing pressure,
we found this phase to persist for a third or more of the Calluna life cycle, i.e. for at least 15
years. Wallen (1980) found lying stems from regeneration not older than 13 years but, under
the impression that heather had existed much longer in that site, he concluded there must be
also older plants lying on the ground. In fact, our results confirmed the age determination by
Chapter 3: The Calluna life cycle concept revisited
73
Wallen (1980), though not his assumption, as the vast majority of our layering stems were
indeed younger than 15 years. Wallen (1980) reported that a valid determination of the
growth phase and age of plants was impossible, a fact we confirmed in our study, as total
plant ages were often not determinable due to rotten rootstocks.
Due to their low height, the dense growth as well as the high proportion of non-flowering
long shoots, these plants regenerating from decumbent stock resemble, and may easily be
mistaken for, “building phase” plants. As a result, one may fail to recognize them as what they
actually are: plants originating from degenerating plants. Nonetheless, our results show that
plants consisting of stems lying on the ground are often older than 15 years. A false
designation of such plants as “building phase” may result in an overestimation of
regeneration capacities after severe disturbance, as we found regeneration ability being
clearly age-related and strongly declining after 10–15 years, confirming Miller and Miles
(1970) as well as Mohamed and Gimingham (1970). Our results suggest that high-vital
regeneration capacity is confined to dormant buds near rootstock which produce new leading
shoots, whereas with the beginning of layering of PS and PR plants, the central rootstock
vanishes, and its role is partly taken over by adventitiously rooting stems. We found no older
decumbent stems regenerating through high-vital resprouting, but instead mat-shaped
regeneration unable to regrow to mature-plant shape.
As a result we also found no evidence of ‘repetitive cycling’, i.e., several consecutive
resprouting cycles, although further studies appear necessary. Layering plants may persist
several decades, a stage interpreted by us as prolonged degeneration phase rather than a full
cycle. We did not observe regrowth from seeds produced during layering stages, but such
rejuvenation may well occur under suitable conditions. In fact, long-term persistence of
heathlands without management, as suggested by Marrs and Diemont (2013), would require
this kind of regeneration cycle. Those authors described two scenarios of heathland
maintenance without management – one driven by endogenous factors controlling dynamics
involving generative and vegetative regeneration in an undisturbed habitat, and one with
exogenous control by stressors such as frost or drought causing dieback. Both scenarios
require specific site conditions to promote seed production, seed germination and seedling
establishment. Although recent studies tried to figure out the determinants, (e.g. Henning et
al. 2017), our knowledge on the regeneration potential of heathlands is still sketchy,
especially under suboceanic-subcontinental climate conditions. Without management, the
existence of long-term open heathland requires sufficient impact by natural disturbance as
well as fairly low competitive pressure by late-successional species (Marrs and Diemont
2013). It may be assumed, as a consequence, that long-term successful maintenance of open
lowland dry heathlands by natural dynamics rather than by management would depend
chiefly on chance.
Chapter 3: The Calluna life cycle concept revisited
74
Conclusions
The primary Calluna life cycle as established by Watt (1955) and Gimingham (1972) based on
the conditions of Atlantic upland heath was confirmed in our study, with minor deviations
and an apparently higher mortality rate of pre-mature plants under subcontinental climate
conditions, as in the Northeast German lowlands. Our novel findings concern chiefly the
regeneration cycle, including an accelerated vigorous regrowth of Calluna after severe
disturbance. Only plants of 10-15 years at the time of disturbance are capable of such a full
additional cycle, given that the microclimate is favourable (Marrs and Diemont 2013).
We showed that Calluna plants that regenerated from stems lying on the ground may form
stable degeneration stages persisting up to 25 years but are unable to perform a regeneration
cycle including the building and mature phase. Especially in older stands, the history of such
patches of degeneration heath may not be detectable anymore and may thus be
misinterpreted as building-stage plants, due to their dense foliose habit. Such erroneous
assessment may lead to an overestimation of the plants’ regeneration capacities and
consequently to Calluna recovery failure after severe management. In fact, our findings
suggest reconsideration of the established criteria used for distinguishing building and
degeneration-phase plants or plant patches, which are mainly based on visual attributes such
as height and the proportion of bare branches indicating ageing.
As a consequence, for the management of dry lowland heathlands under suboceanic-
subcontinental climate conditions, our findings suggest:
1) Severe management should be applied primarily on heath consisting of young plants with
high resprouting capacity and subsequently quick vegetation recovery. A delayed Calluna
recovery may enhance a shift in vegetation composition towards a higher proportion of
grasses (Grau-Andrés et al. 2018, Marrs and Diemont 2013). This may be of particular
importance under a subcontinental climate, where heather recovery is determined by
vegetative regrowth rather than by rejuvenation from seeds, as seedling establishment
needs favourable microsites, which are rare under subcontinental conditions (Henning et
al. 2017). Additionally, the nutrient-poor heathland habitat in much of Northeast
Germany, often dune-like with dry sandy soils limited in water and nutrient supply,
favours plants with high resilience to drought, hence vegetative regeneration with extant
root system and mycorrhizal fungi unimpaired by severe biomass loss as is the case after
high-intensity fire (Green et al. 2013).
2) Plants of different ages react differently to disturbances. Our findings suggest that Calluna
regeneration after severe disturbance is diverse in terms of survival and regeneration
Chapter 3: The Calluna life cycle concept revisited
75
capacity of plants. In consequence, such disturbances do not necessarily promote even-
aged uniform heath, but may well support uneven-aged structures with fast regrowth of
young resprouting plants to mature stage, accompanied by some older plants, consisting
mainly of decumbent stems, providing shelter for seedlings. At 10–15 years after
disturbance, plants that regenerated from younger resprouting and from older plants
with decumbent stems begin to degenerate, but by then, young plants from seeds should
be established. Hence, the type and severity of the management determines the age
structure in subsequent heathland, with mowing and burning enabling the survival of
Calluna rootstocks and sufficiently promoting regeneration. Grazing additionally
contributes positively to species diversity and community structure (Kirkpatrick & de
Blust 2013, Henning et al. 2017) by prolonging high-vital phases in the Calluna life cycle.
Sod-cutting, on the other hand, is less advisable for subcontinental heathlands, as the
total removal of aboveground biomass in combination with hampered seedling
establishment (Henning et. al. 2017) may lead to recovery failure. Moreover, the need to
restore suitable trophic conditions by sod-cutting is less pronounced in the northeast
German heathlands where humus accumulation and nutrient input are lower than in the
Northwest (Lüttschwager and Ewald 2012).
3) Small-scale management that includes sites being subject to short-term rotation (e.g., 10-
15 years) and others allowing longer successional development is beneficial for the
heathland ecosystem as a whole. Heathland management focussing only on optimum
Calluna vitality may disregard species adapted to later successional stages. For long-term
stability of heathlands, heather rejuvenation from seeds is needed, requiring further
investigations on seed germination and seedling establishment especially in
subcontinental heathlands. An urgent question to be solved is whether and to what extent
seedling establishment takes place in the period between disturbances, with resprouted
plants providing favourable microsite conditions and sufficient shelter for a new Calluna
generation to establish.
Chapter 3: The Calluna life cycle concept revisited
76
Electronic Supplementary Material
ESM3_1: Study areas. This PDF contains supplementary material to all sites, including
information to study area location, management, climate, nitrogen deposition and sampling
statistics.
ESM3_2: Initial analysis. This PDF contains a brief graphical overview of initial analysis
results concerning dataset-inherent correlations and associations, as well as ecological
patterns and dependencies. Additionally, they provide further information on the effects of
management, nitrogen deposition and oceanicity on the vitality of Calluna plants not
addressed in the present article.
ESM3_3: Analysis documentation. The zip-folder contains the html documentation of the
statistical analysis performed in R.
77
Chapter 4:
High nitrogen deposition increases
the susceptibility of Calluna vulgaris
recruitment to drought
Chapter 4: High nitrogen deposition increases the susceptibility to drought
78
Abstract
Dry lowland Calluna vulgaris heathlands, once widespread in Northwest Europe but declining
since the 19th century, is reliant upon disturbance such as burning, mowing or sod-cutting to
remain open. Two factors may compromise the success of post-disturbance heather
recruitment; droughts and high airborne nitrogen (N) loads. I asked to what extent young
Calluna plants suffer from drought, whether there is a difference in drought resistance
between seedlings and resprouted plants, and if high N deposition reduces the drought
resistance. I sampled 683 young heather plants in 19 North German dry lowland heathland
areas and analysed how the annual growth, the frequency of damaged leading long shoots
and the severity of damage were influenced by the drought severity, mean temperatures and
precipitation during the growing season, using negative binomial mixed-effects models.
Results were shown for three scenarios of varying intensity of drought, two nitrogen
deposition scenarios, separately for seedlings and resprouted plants.
Droughts reduced young Calluna plant growth rate and increased tissue damages. Drought
resistance was higher in resprouted plants than in seedlings. High N loads increased growth
rates and mortality rates as well as the frequency of tissue damages under drought, but
rather in seedlings than in resprouted plants. The interaction effect of high N deposition and
drought caused a growth stimulation and consequently unfavourable shoot:root ratios in
Calluna seedlings, inducing a critical water balance exacerbated by the restricted ability of
Calluna seedlings to regulate stomata conductivity. In contrast, resprouted plants ceased
growth under high N and drought, avoiding critical water losses and damages. The drought
tolerance strategy of seedlings may provide competitive advantages under moderate drought
conditions, but generally, the results rather support a decrease of competitive power under
drought and high N, thus hampering post-disturbance Calluna recruitment.
Keywords
Calluna, drought, heathland, nitrogen load, regeneration, vitality
Chapter 4: High nitrogen deposition increases the susceptibility to drought
79
4.1 Introduction
Dry lowland heathlands of the North German Plain, dominated by Calluna vulgaris, are
declining since more than a century as a result of land use changes and consequential habitat
destruction, fragmentation and abandonment. What has remained is often threatened by a
lack of appropriate management and in addition, by climate- and pollution-driven degrada-
tion (EEA 2019a; EEA 2019b; Fagundez et al. 2013; Olmeda et al. 2020). Hereby, the yet
unknown threats of the changing climate, in particular the effects of more frequent and more
severe drought during growing season, as well as their interaction with other threats and
pressures, such like airborne nitrogen deposition (henceforth N deposition), are not well
understood yet.
Calluna vulgaris (L.) Hull (henceforth referred to as Calluna) is an evergreen ericoid dwarf
shrub and the dominant species of Atlantic dry lowland heathlands in Northwest Europe.
Those heathland habitats are distributed in regions with oceanic climate, “lacking
temperature extremes, whether high or low, but with abundant and well-distributed rainfall
and the maintenance of a generally high humidity” Gimingham (1972: 11). They occur mostly
on sandy soils with low water holding capacity where Calluna is rooting chiefly in the topsoil.
Studies showed that Calluna generally has a wide tolerance towards water shortage (e.g.
Albert et al. 2012; Bannister 1964a, b; Gordon et al. 1999, Kongstad et al. 2012), a high
potential for recovery from former droughts (Backhaus et al. 2014; Gordon et al. 1999;
Kongstad et al. 2012; Walter et al. 2016) and a high morpho-physiological plasticity to
ecological stressors (Bartoli et al. 2013; Ibe et al. 2020; Petrova et al. 2017). Morphological
adaptions to drought include the small ericoid leaves, revolute at margins, with the abaxial
side reduced to a narrow groove containing sunken stomata and hairs (Gimingham 1972).
However, in oceanic-suboceanic regions, where Calluna populations are adapted to a
balanced and even water supply during the growing season (Loidi et al. 2010), climate
changes provide new challenges for the species’ adaption potential. In most parts, the North
German Plain is relatively dry, representing the eastern margin of Atlantic lowland heathland
vegetation (c.f. Gimingham 1972; Loidi et al. 2010; Meyer-Grünefeldt et al. 2016). Recent
studies found evidence for provenance-specific drought resistance in Calluna (Meyer-
Grünefeldt et al. 2016, Ibe et al. 2020), suggesting a higher drought resistance in marginal
populations, but with reduced precipitation in summer and rising temperatures with heat
spells during the growing season, the climatic conditions in the region will exacerbate
(Alcamo et al. 2007; IPCC 2021; May et al. 2016; Schönwiese & Janoschitz 2008; Spinoni et al.
2015; Wagner et al. 2013).
Chapter 4: High nitrogen deposition increases the susceptibility to drought
80
Fig. 4.1 Highly vigorous (left) and drought-damaged (right) Calluna seedlings (a) and
resprouted plants (b). During the early summer drought period in 2013, many young Calluna
plants showed remarkable drought damages at early flowering time in July, whereas the older
plants surrounding remained moreover unaffected (c).
Chapter 4: High nitrogen deposition increases the susceptibility to drought
81
In Atlantic regions, drought-induced tissue damages occur mainly after cold spells in winter
(‘frosting’, ‘winter browning’, Beijerinck 1940), with the sensitivity towards climatic stressors
enhanced by drought in the previous growing season (Gordon et al. 1999). Under continental
climate, severe tissue damages are moreover induced by droughts during the growing season
(Bannister 1964a; Gimingham 1972; Marrs & Diemont 2013; Peñuelas et al. 2004). This
became obvious in the North German Plain during the drought years 2013 and 2018, with
extensive diebacks of (mostly but not only) young Calluna plants (Fig. 4.1).
Calluna heathlands are ecosystems in landscapes associated with pastoral economies. Being
“naturally in a continuous state of change” (Chatters 2021), heathlands require disturbance-
driven dynamics for their maintenance. Management such as burning, mowing or sod cutting
induce heather regeneration, which comprises vegetative regrowth from buds at stem bases
and branches (resprouting plants, PR), as well as the establishment of plants germinated
from seeds (PS). Young Calluna plants are more strongly affected by drought than old ones
(Britton et al. 2001; Ibe et al. 2020; Kongstad et al. 2012; Meyer-Grünefeldt et al. 2015), due
to their high shoot:root ratio and a limited rooting system (Weiner 2004). Hence, the Calluna
pioneer stage in the plant’s life-cycle, comprising young plants up to six years, is particularly
sensitive to summer droughts (Meyer-Grünefeldt et al. 2015) and substantial damages of
Calluna regeneration during the early stage may hamper the recovery of heathlands after
disturbances, leading to reduced Calluna but increased grass cover (Britton et al. 2003; Marrs
& Diemont 2013). Up to now, there is no study that examined whether resprouted plants are
less susceptible to summer droughts than seedlings, although that is assumable due to a very
low shoot:root ratio in the early post-disturbance recovery stage, and the developed Mature-
stage rooting system, providing a better water supply.
Apart from the purpose to stimulate heather regeneration, mechanical managements and
burning are applied to restore suitable soil conditions to compensate for nutrient and humus
accumulation as a result of natural succession processes. Additionally, in the past decades,
the need for restoring nutrient balances in the heathland soils, altered by atmospheric N
depositions, became important, challenging the heathland management to weigh between the
management-type induced trade-offs (Walmsley et al. 2021). High airborne N loads play a
major role in dry lowland heathland habitat degradation, the critical loads for dry lowland
heathland has been assessed at 10-20 kg/h-1*y-1 (Bobbink & Hettelingh 2011). In the study
areas, airborne N loads range from 10-23kg*ha-1*yr-1 (UBA 2017, PINETI-3 model data for the
reference period 2013-2015).
Since the 1980s, as first observations indicated species composition changes possibly related
to high airborne N deposition (Heil & Diemont 1983), many studies subjected high N-induced
Chapter 4: High nitrogen deposition increases the susceptibility to drought
82
alterations of heathland ecosystem inventory, function and structure (Aerts et al. 1990;
Bobbink et al. 1998; Bobbink et al. 2010; Carrol et al. 1999; Diemont et al. 2013; Southon et al.
2012; Stevens et al. 2018; Taboada et al. 2018; Walmsley & Härdtle 2021). Some studies
found that high N deposition increased the drought susceptibility and drought damages (e.g.
Gordon et al. 1999; Meyer-Grünefeldt et al. 2015).
Both, climate change and air pollution, have been identified to play a major role in future
heathland species composition, restoration potentials and for the long-term maintenance of
heathland functioning (Gordon et al. 1999; Meyer-Grünefeldt et al. 2015, Carroll et al. 1999;
Power et al. 1998; Saebo et al. 2001; Southon et al. 2012). However, the complex interactions
are insufficiently understood up to now, in particular concerning the determinants for post-
disturbance heathland recovery potentials and the establishment success of young Calluna
plants under recent and projected climate and N deposition conditions. To gain a better
insight, I analysed the responses of seedlings and respouting plants to drought and high N
deposition in 19 North-German heathland areas, and asked:
1) How does drought during the growing season affect young Calluna plants? I hypothesize a
reduction of growth rates and an increase of tissue damages with drought.
2) Is there a difference in drought resistance between seedlings (PS) and resprouted plants
(PR)? I hypothesize PR having a higher drought resistance than PS, due to their extant
mature-stage rooting system and a beneficial shoot:root ratio.
3) Does high N deposition affect the drought resistance of young Calluna plants, and do high
N loads alter the PS and PR responses to drought? I hypothesize high N depositions to reduce
drought resistance and I generally expect an increase of drought-induced tissue damages in
young Calluna plants. Thereby, I expect PS more adversely affected than PR, due to their
hypothesized generally lower drought resistance.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
83
4.2 Methods
Data sampling
Young Calluna plants were collected in August and September 2014 in 19 heathland areas
located in the North German Plain (Fig. 2.1, p. 29; Chapter 1.4 for study area details and
characteristics). On 259 plots (25m²), up to 2 randomly selected plants of each growth phase
were examined. Wood sections from the root crown, the stem bases and the branches in 10-
15cm height were used for growth ring counts. From the total dataset, all plants with up to 3
years of aboveground biomass age were selected.
As a proxy for biomass production, the length of the living leading long shoot yearly
increment in mm was noted [LYI]. Tissue damages comprised entirely or partially dead
leaves on the axillary short shoots or on the leading long shoots. Damages may be due to
unfavourable weather during winter (‘winter browning’ or ‘frosting’, Bannister 1964a, b), or
by summer drought, insect damage or pathogenic fungi. I focused on summer-drought
induced tissue diebacks and therefore distinguished carefully between winter browning
(greyish-brownish in colour), damages due to heather beetle Lochmaea suturalis (orange-
brown, reddish colour), and damages by summer drought (reddish-brown, sometimes dark
green-brown), with only the latter used for the present analysis. Plants obviously damaged by
insects (e.g. Lochmaea suturalis, aphids of Saturnia pavonia) were excluded from this study,
but Lochmaea-induced damage was sometimes hard to distinguish from drought damage.
Reddish-purple and violet colouring of tissues is an adaption to high solar radiation and was
not accounted as drought damage. Other insect calamities or damages caused by pathogenic
fungi could always be detected safely and were not considered.
We distinguished between the extent of a single long shoot damage (PDYI) and the frequency
of living but damaged long shoots in a plant, regardless of severity (PDL). For PDYI, I
measured the damaged part as a proportion of the total active long shoot length, given as a
mean over all living long shoots. For PDL, I estimated the proportion of all active, yet
damaged long shoots of the entire plant (Fig. 4.2).
Chapter 4: High nitrogen deposition increases the susceptibility to drought
84
Fig. 4.2 Schematic examples for yearly increment and drought damage data sampling of a 3-year-old Calluna plant
in August, with a drought in early summer (a) or recently before sampling in late summer (b). The mean annual
increment (LYI) of the leading long shoots (1-7) was 15cm, the mean extent of long shoot damage (PDYI) was
calculated as the proportion of the mean damaged long shoot part length (3cm) from the mean total annual
increment (15cm) = 20% in the left plant (a) and 4cm of 15cm = 26.7% in the right plant (b). The frequency of
damaged long shoots was 100% (7/7) in (a) and 6/7 (c. 85%) in (b).
The life history of the Calluna plants was assessed from plot history information (e.g. recent
burning, mowing or sod cutting), the plant habit and the growth ring counts. I distinguished
plants from seeds (PS, n = 476) and one- to three-year-old resprouted plants (PR, n = 207).
Most plants were in the first year (total dataset: 83%, PS: 86%, PR: 75%). PR originated
predominately from mature plants up to 21 years old, but 95% were younger than 14 years
at the date of disturbance. As it turned out that the total plant age had a considerable effect on
LYI (ρ = 0.73) and PDL (ρ = 0.59), those effects have been corrected by setting up simple
linear models with logarithmized LYI and PDL as the responses and the total plant age as the
predictor and then corrected for the age effect by centering the residuals around the
predicted model mean. In pretests, I analysed differences of the responses concerning grazing
and intense managements by using Kruskal multiple comparisons of means tests, and I
detected no differences between the grazing regimes, but significant, marginal differences in
all vitality attributes between sites mowed or burnt to those sod cut. These differences
turned out to be coupled with the regeneration type, with mowed or burnt sites favouring PR
and sod cut sites inducing regeneration with PS. Hence, the potential effects of intensive
managements, although not directly included in the final full models are considered by
including the life history. All analyses and figures were performed and created with R
statistical software (R.project.org, Version 4.1.1).
Chapter 4: High nitrogen deposition increases the susceptibility to drought
85
Climate
The study areas represent a climate gradient from oceanic conditions in the Northwest
(>800mm annual precipitation, mean annual temperature up to 10°C, Kotilainen’s Index of
Oceanicity up to 85) to subcontinental conditions in the East (500-600mm annual
precipitation, mean annual temperature 9°C, Kotilainen’s Index of Oceanicity lower than 50,
Fig. 1.1, p. 14; Table 1.3 p. 16). Observations of mean temperature (T) and precipitation sums
(P) over the period 1st of May – 31st of August (hereafter: survey period) were gathered for
the years 2011-2020 (DWD 2021). This decade was characterized by a fluctuation between
years of severe drought and those of quite wet conditions, with a wide range of rainfall
distribution patterns, representing the drought conditions Calluna plants are recently faced
with in the North German Plain. From those daily observations, I calculated the Standardized
Precipitation and Evapotranspiration Index (SPEI), a widely used measure for drought
severity (Vicente-Serrano et al. 2010, calculation with R package “SPEI” Beguería & Vicente-
Serrano 2017). This index uses the climatic balance (P - Potential evapotranspiration (PET,
calculated with the Thornthwaite equation with T)) to identify periods with drought,
resulting in a negative SPEI then. SPEI was calculated on a time scale of seven days, implying
that the SPEI was calculated as an accumulative effect of a seven-day-period to account for
the distribution of drought and non-drought periods.
N deposition
Annual airborne N deposition ranged from 10kg*ha-1*yr-1 to 23kg*ha-1*yr-1, roughly
corresponding to the macroclimate gradient, increasing in the direction from East Germany
to the Northwest (Fig. 1.1, p. 14; Table 1.3, p. 16; UBA 2019, based on the PINETI-3 model for
the reference period 2013-2015; Schaap et al. 2018).
GLMM
To analyse effects of the climate, N deposition and life history on the response variables I
used negative binomial mixed models, as the tested Poisson-GLMM for LYI was overdispersed,
and residual diagnostics indicated rather the usage of the Negative Binomial than the
Binomial approaches for PDYI and PDL (‘glmmTMB’ package: Brooks et al. 2017; residual
diagnostics Chambers & Hastie 1992, visual residual diagnostics with package DHARMa:
Hartig 2021). All numerical fixed terms were rescaled to values ranging between 0-1 prior to
modelling for enhancing comparability between non-equal ranges and variances in the
original dataset.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
86
I used a nested random term structure (study area/plot) for accounting spatial auto-
correlation and pseudoreplication effects.
For assessing the partial explanatory power of N, life history and their interaction, I
conducted partial models containing only the random term (mnull), only nitrogen deposition
(mnitro), only life history (mlife) as well as the interaction of both (mnitro x life) for each response,
respectively. Unless otherwise specified, the marginal R² values are given in the text for
assessing the model explanatory power using the package “performance” (Lüdecke et al.
2021). For the full models I included all fixed terms, with the additive effects of P, N and SPEI
in interaction with N and life history (PS/PR): response variable ~ (SPEI + T + P) * N * life
history + (1|study area/plot). Model diagnostics included visual residuals diagnostics with
package DHARMa (Hartig 2021) and slight deviations from residual uniformity were
accepted. An R documentation with all diagnostic plots is provided in ESM4_1.
Based upon the models, I calculated predictions over the CI95 range for six scenarios,
reflecting three intensities of drought: 1) NoD_2014, representing conditions without severe
drought, with the wettest and coldest conditions of the survey year growing season; 2)
D_2014 with the driest conditions of the survey year growing season, representing a
moderate drought and 3) MaxD_10YEAR with the driest conditions measured in the 2011-
2020 time period, representing severe drought, under low (10kg*ha-1*a-1) or high N loads
(25kg*ha-1*a-1), respectively (scenario thresholds: Table 4.1). The prediction dataset was set
up from all potential combinations of fixed terms, including the random terms, and due to the
large size of over 500.000 recombinations and computational limits, a subset of randomly
selected 50.000 samples was used for the further analysis and the plotting of results. From
this dataset, the mean differences of LYI, PDYI or PDL between the three scenarios were
calculated and tested for significant differences with a non-parametric Kruskal multiple
comparison of means test (package pgirmess: Giraudoux 2021). Simple two-group mean
comparison significances, e.g. between low and high N-depositions or between the life
histories were calculated with the non-parametric Mann Whitney U-test.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
87
Table 4.1 Vitality attributes (responses) and predictors for modelling drought.
Description
Model term
Range
2014
(2011-2020)
Scenario thresholds
LYI: Growth rate, yearly increment
LYI model response
5-370
PDYI: Proportion of yearly increment
with tissue dieback
PDYI model response
0-40
PDL: Proportion of all living long
shoots with tissue dieback
PDL model response
0-100
P: Precipitation sum: Total
precipitation sum fallen in the survey
period (1st of May – 31st of August)
Fixed effect
214.8 - 385.7
(40.7 - 480.5)
NoD_2014: 386
D_2014: 215
MaxD_10YEAR: 41
T: Mean air temperature in the survey
period (1st of May – 31st of August)
Fixed effect
15.6 - 17.1
(13.6 - 20.2)
NoD_2014: 16
D_2014: 17
MaxD_10YEAR: 20
SPEI: Standardized
Evapotranspiration Index in the
survey period (1st of May – 31st of
August)
Fixed effect
-0.03 - 0.00
(-0.05 - 0.10)
NoD_2014: 0.00
D_2014: -0.03
MaxD_10YEAR: -0.05
N: Airborne N deposition
Fixed effect
10-23kg/ha*y
Low N deposition: 10kg*ha-1 *yr-1
High N deposition:
25 kg*ha-1*yr-1
Calluna plant life history:
regeneration type
Fixed effect
Study area
Random effect
4.3 Results
Climate
The ten-year analysis of SPEI, T and P revealed that there are huge fluctuations between the
years 2011-2020 (Fig. 4.3). Variation among study areas within a year is highest in P, and
quite low in T. Only one study area located near the Danish border had considerably lower
annual mean temperatures than the others (SBD, black line Fig. 4.3b).
The years 2012 and 2017 represent cold and wet conditions during the survey period, with
almost only positive SPEI and high P, whereas 2015 and especially 2018 had severe droughts,
with high T and low P levels. Although the ten years may not represent general climate
changes in the study areas, there is a trend towards higher T (Fig. 4.3b) and lower P (Fig.
4.3c), and a higher fluctuation and amplitude of SPEI (4.3a).
The ranges of SPEI, P and T for the survey year 2014 are given in Table 4.1 and are overall
moderate against the background of the ten-year fluctuations (Fig. 4.3). The SPEI ranged from
no-drought conditions (SPEI = 0) to moderate drought (SPEI = -0.03). T varied between 16°C
and 17°C, and was therefore slightly below the 10-year mean of approx. 17.0°C. The amount
of rainfall during the survey period (P) showed the highest variation between study areas,
ranging from 215-368mm, but the variation did not correspond to oceanicity effects, as the
Chapter 4: High nitrogen deposition increases the susceptibility to drought
88
highest P values were reached in the sites with low and high K (Fig. 4.3c). In contrast, T
showed a clear patterning concerning long-term oceanicity and was higher in the more
continental areas with a low K than in those with high K.
In the growing season 2014, there were two short drought periods in early summer, one at
the end of May and one at the mid of June (Fig. 4.4). From early July to mid-August, a longer
drought occurred, with high T in all study regions, but highly variable P. Some areas had
heavy rainfall events with more than 30mm*day-1, occurring at the beginning (FH, LT), during
(OH, ZW), or at the end of the drought (SBD), and some areas had overall low precipitations
during mid and late summer (KS, VH).
The study area with the wettest and coldest conditions was TD, located in Northwest Lower
Saxony, showing a balanced SPEI of rd. 0.00, at T = 16°C, and P = 336mm. The two study areas
with the driest conditions during the growing season 2014 were in North Brandenburg (RH,
VH), with SPEI = -0.03, T = 16.5°C and P = 231mm.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
89
a)
b)
c)
Fig. 4.3 Standardized Precipitation and Evapotranspiration Index (SPEI, a), mean daily air temperature in °C (T, b)
and precipitation sum in mm (P, c) during survey period (1st of May - 31st of August) in the 19 study areas. Study
area lines are coloured according to their Oceanicity (K, Table 1.3, p. 16), with increasing K from red over orange,
yellow, green to blue and black. For full names of study areas see Table 1.3, p. 16 and for location of study areas
see Fig. 1.1, p. 14. Study areas KS and VH have nearly identical values, due to their close location and are shown as
overlapping lines.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
90
Chapter 4: High nitrogen deposition increases the susceptibility to drought
91
Fig. 4.4 Study area climate in 2014, showing the daily precipitation (P, blue bars), the
mean daily air temperature (T, red line) and the daily SPEI (black lines) during the
survey period 1st of May – 31st of August. Additionally, the survey period mean values for
SPEI, T and P are given. Study areas showed a general pattern of two short droughts in
early summer, at the end of May and in mid June and a longer drought from early July to
mid August.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
92
Response overview
Growth rates ranged from 5 to 370mm and were significantly higher in PR than in PS (2.5mm
mean difference, p ≤ 0.001, Fig. 4.5a). Up to 40% of the increment was damaged, independent
from life history (PDYI, Fig. 4.5b). The frequency of damaged long shoot per plant ranged
from 0% to 100%, with slightly higher values in PR (2.2% mean difference, p ≤ 0.001, Fig.
4.5c). PDYI and PDL were correlated (ρ = 0.59), hence increased tissue damage frequency
often, but not necessarily, went ahead with higher damage severity.
Effects of drought on young Calluna plants
None of the tested climate variables had a single significant effect in one of the models.
Generally, LYI was rather affected by life history and N deposition than by climate (mnitro x life
R²=0.36, full model R² = 0.39), PDYI responded not considerably to any of the tested fixed
term combinations (full model R² = 0.07), and PDL showed strong interaction effects of life
history, N deposition and climate (full model R² = 0.39, Table 4.2).
Fig. 4.5 Overview of response variables used for
modelling, a) growth rate (annual increment in mm,
LYI), b) extent of long shoot damage (PDYI, %) and
the long shoot damage frequency (PDL, %), with
group sample size and Mann-Whitney U test for
significant group differences with *** p ≤ 0.001 and
n.s. not significant.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
93
LYI was significantly higher in NoD_2014 compared to D_2014 (mean difference 19.4mm,
p≤0.001) and MaxD_10YEAR (14.1mm, p≤0.05, Fig. 4.6). From the moderate drought (D_2014)
to severe drought (MaxD_10YEAR), LYI showed a weak positive mean difference (5.3mm, p ≤
0.001), due to some outliers with extraordinary growth rates under MaxD_10YEAR. Unless
considering those outliers, the majority of plants had a very low growth rate under the
conditions of MaxD_10YEAR.
A LYI of 0 did not occur in the original data, as I only sampled plants alive in 2014, but the
model predicted some plants without growth which can be assigned as dead. This mortality
rate is 7.7% for NoD_2014, 24.1% for D_2014 and 41.8% in MaxD_10YEAR.
PDL increased significantly from NoD_2014 to D_2014 (11.8%, p≤0.001) and even more to
MaxD_10YEAR (24.1%, p≤0.001). Under the conditions of MaxD_10YEAR the majority of
plants (52%) had all long shoots affected by tissue damages (Fig. 4.6).
Fig. 4.6 Yearly increment and long shoot damage frequency in the three climate scenarios NoD_2014 representing
the coldest and wettest conditions in 2014, with SPEI = 0, T = 16°C and P = 386mm; D_2014 representing the
driest conditions in 2014, with SPEI = -0.03, T = 17°C and P = 215mm; MaxD_10YEAR representing the driest
conditions in 2011-2020, with SPEI = -0.05, T = 20 and P = 41mm. Stars are indicating means. Significance codes
are based on a Kruskal multiple comparisons of means test and indicate significant differences with p≤0.05.
Sample sizes of groups are given above the boxes in italics.
Responses of seedlings (PS) and resprouted plants (PR) to
drought
Life history explained considerable parts of LYI variance (R² mlife = 0.31), although the
proportions of variance explained by random terms (study area and plot) were quite high,
too (conditional R² mlife = 0.50, Table 4.2). The additional explanatory power of including
climate was relatively low, although the significant interactions of life history with P and with
SPEI (both with p≤0.01) revealed slight differences of growth rates under drought in
seedlings and resprouted plants (Fig. 4.7). But those are mainly due to the generally higher
growth rates in PR compared to PS in the original data, which were even more pronounced in
Chapter 4: High nitrogen deposition increases the susceptibility to drought
94
the models (LYI mm mean differences in original data/mlife/mnitro x life/mLYI: 2.5/10.8/7.7/11.2,
all with p≤0.001). The predicted differences between PR and PS decreased with increasing
drought (Fig. 4.7), mainly due to the generally lower growth rates under MaxD_10YEAR. The
majority of PR (51%) died under the severe drought conditions of MaxD_10YEAR, but the
remaining showed a high variation and the potential to reach growth rates similar to those
under NoD_2014. PS LYI was similar under MaxD_10YEAR, but with more distinct outliers
and a lower mortality rate (34%).
Table 4.2 Explanatory power (R²) of partial and full models. R² values >0.10 were highlighted in bold font.
LYI
PDYI
PDL
R²
Cond. R²
R²
Cond. R²
R²
Cond. R²
Random - only model mnu ll
<0.01
0.28
1)
<0.01
0.25
1)
<0.01
0.19
N deposition model mnit ro
0.03
0.28
1)
<0.01
0.25
1)
<0.01
0.21
Life history model mlife
0.31
0.50
1)
<0.01
0.25
0.13
0.45
1)
Life history and N model mnitro x life
0.36
0.50
1)
<0.01
0.26
0.15
0.47
1)
Full model
0.39
0.52
1)
0.07
0.32
1), 2)
0.39
0.56
1)
1) residual diagnostics: Residuals vs. Predicted value distribution: slight quantile deviations detected, but acceptable. 2) not used for predictions
and plots: explanatory power (R²) was too low
PDL showed a high study area- and plot-specific variation (mnull cond. R² = 0.19). The
explanatory power improved significantly with including the climate effects in the full model
(cond. R² mnitro x life = 0.47, cond. R² mPDL = 0.56, Table 4.2). PDL was higher in PR than in PS in
the original dataset and also in the partial models mlife and mnitro x life (% mean difference
2.2/12.5/5.2, respectively, all with p≤0.001), but in the full model, there was a higher PDL in
PS than in PR (11.9% more, p≤0.001, Table 4.3). The reason is that drought significantly
increased tissue damages in PS and reduced it in PR (Fig. 4.7). There was a very low PDL in PS
under NoD_2014 (p≤0.001), but it increased for 49.6% in the mean from No_D_2014 to
D_2014, and another 18.5% to Max_D_10YEAR, with all long shoots affected in the vast
majority of PS (68%). In contrast, in the same scenario, only a third of PR plants (33.3%) had
all long shoots affected, the remaining showed a very high variability. Due to the extended
prediction range of the climate variables in the scenario MaxD_10YEAR and the higher
proportion of PS affected there, PS PDL was now predicted to be higher than that of PR.
There was no effect of life history on PDYI (Table 4.2), but the correlation between PDYI and
PDL was higher in PR (ρ=0.67) than in PS (ρ=0.46), resulting in a higher probability for a
high-severe suffer with high tissue damage frequency in PR than in PS.
The high variability in predictions showed individual plant-, plot- and area-specific
unexplained variance, which was much higher in PR than in PS and higher in PDL than in LYI.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
95
Table 4.3 Scenario differences in predictions, given as mean differences and their significances (non-parametric
Mann Whitney U-tests for the simple two-group PR-PS and high N load-low N load comparisons, Kruskal multiple
comparison of means for the more complex comparisons). *** p≤0.001
LYI
PDL
Difference PR - PS
PR - PS
11.2***
-11.9***
PR - PS difference under low N deposition
18.6***
14.6***
PR - PS difference under high N deposition
3.9***
-38.2***
N deposition
Increase from low to high-load scenario
21.2***
27.3***
PS: increase from low to high N-load scenario
28.5***
53.9***
PR: increase from low to high N-load scenario
13.9***
1.0***
Drought scenario differences
NoD - D_2014
19.4***
-11.8***
NoD - maxD_10Year
14.1***
-24.1***
D_2014 - maxD_10Year
-5.3***
-12.3***
PS: NoD - D_2014
9.1***
-49.6***
PR: NoD - D_2015
28.9***
24.9***
PS: NoD - maxD_10Year
2.5***
-68.0***
PR: NoD - maxD_10Year
24.9***
20.4***
PS: D_2014 - maxD_10Year
-6.6***
-18.5***
PR: D_2014 - maxD_10Year
-4.1***
-4.5***
Fig. 4.7 Responses of seedlings (PS, blue) and resprouted plants (PR, red) in the three scenarios: NoD_2014
representing the coldest and wettest conditions in 2014, with SPEI = 0, T = 16°C and P = 386mm; D_2014
representing the driest conditions in 2014, with SPEI = -0.03, T = 17°C and P = 215mm; MaxD_10YEAR
representing the driest conditions in 2011-2020, with SPEI = -0.05, T = 20 and P = 41mm. Stars are indicating
means. Significance codes are based on a Kruskal multiple comparisons of means test and indicate significant
differences with p≤0.05. Sample sizes of groups are given above the boxes in italics.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
96
Nitrogen deposition affecting Calluna recruitment under
drought
N had no effect on LYI, PDL or PDYI in the partial models mnitro (R² < 0.05), but revealed a
strong interaction effect with life history for LYI (mnitro x life R² = 0.36), and weaker for PDL, too
(R² = 0.15, Table 4.2). In the full models, high N depositions showed complex effects.
The most pronounced effect is the ‘fertilizing effect’ which generally increased LYI for
21.2mm (p≤0.001) from the low-load (10kg*ha-1*yr-1) to the high-load scenario (25kg*ha-
1*yr-1, Table 4.3). Thereby, this growth boost effect was stronger in PS (+28.5mm, p≤0.001)
than in PR (+13.9mm, p≤0.001), and may explain the outliers in Fig. 4.7. The high N-load-
induced growth boost varied among the drought scenarios. Whereas PS growth stimulation
was more pronounced under drought (D_2014 & MaxD_10YEAR), PR showed it only under
NoD_2014. Under drought, PR growth was reduced under high N, and for the moderate
drought scenario (D_2014), this reduction was significant (high N–low N LYI: -7.5mm,
p≤0.001).
High N loads increased the mortality rate. Under low N, 16% of all PS and 34% of all PR died
under the severe drought scenario (MaxD_10YEAR, Fig. 4.8). In contrast, under high N, a third
of all PS died in each of the scenarios, independent from drought. In PR, 33% of plants died
under MaxD_2014 (+33% in comparison to low-N load), but mortality rate in MaxD_10YEAR
was stable compared to the low N-load. In the end, the mortality rate of seedlings and
resprouted plants under high N load and drought (MaxD_2014 and MaxD_10YEAR) was
similar (33%).
The differences in growth rates between PS and PR were more pronounced under low N
deposition (mean difference -18.6mm, p≤0.001) than under high N load (-3.9mm), due to the
generally higher growth rate of PR under low N but an indifferent and highly variable growth
rate response in the scenarios under high N for both, PS and PR.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
97
Fig. 4.8 Effects of life history (PS: blue bars, PR: red bars) and low (lefthand) or high (righthand) N deposition on
yearly increment and long shoot damage frequency, for the three scenarios: NoD_2014 representing the coldest
and wettest conditions in 2014, with SPEI = 0, T = 16°C and P = 386mm; D_2014 representing the driest conditions
in 2014, with SPEI = -0.03, T = 17°C and P = 215mm; MaxD_10YEAR representing the driest conditions in 2011-
2020, with SPEI = -0.05, T = 20 and P = 41mm. Significance codes are based on a Kruskal multiple comparisons of
means test and indicate significant differences with p≤0.05. Sample sizes of groups are given above the boxes in
italics.
Under high N, growth rates were highly variable. Although the model revealed that growth
rates were significantly reduced from NoD_2014 to MaxD_2014 and MaxD_10YEAR
independent from N load (Table 4.3), high N loads increased the variability in LYI towards
drought, indicating that interacting effects of high N-induced growth boost and drought-
induced growth reduction were determining the individual plant-specific growth. As a
consequence, in PS, drought-induced growth reduction could be compensated and even
superimposed by high N growth boost. Some few PS even reached the highest growth rates
under severe drought conditions and high N. Thereby, LYI showed a slight significant
reduction in the mean from No_D2014 to the other both, but there was no difference between
MaxD_2014 and MaxD_10YEAR. However, although the mortality rate of PS was stable with
34% in all scenarios, the boxplots suggest an increasing proportion of low growth rates with
Chapter 4: High nitrogen deposition increases the susceptibility to drought
98
increasing drought (Fig. 4.8), indicating that the potential for the compensation of drought-
induced growth reduction decreases with drought.
In contrast, the high N-induced growth stimulation in PR was restricted to NoD_2014 and
only some few plants in the drought scenarios, but was less sufficient for compensating the
drought-induced growth reduction.
High N loads increased PDL for 27.3% (p≤0.001, Table 4.3), but much more in PS than in PR
(PS: +53.9%, PR: 1%, both p≤0.001). There was a scenario- and life-history-specific reaction
to drought under the varying N depositions. Under low N, PS showed only marginal tissue
damages, not differing between NoD_2014 and MaxD_2014, and significantly less than the
damages of PR. Under severe drought (MaxD_10YEAR), the damages are predicted to strongly
increase in PS, where those of PR got reduced (Fig. 4.8). With high N, all PS had the maximum
PDL under drought (D_2014 & MaxD_10YEAR), whereas PR tissue damages were only high
under non-drought conditions (NoD_2014). There, two thirds of all plants had tissue damages
on all of their long shoots, but the rate halved under drought (D_2014 and MaxD_10YEAR).
Hence, under high N load, tissue damages in PR occurred rather under non-drought
conditions.
4.4 Discussion
How does drought during growing season affect young
Calluna plants?
In the survey year 2014, two moderate droughts in early summer and a more severe drought
in mid-late-summer (July to the mid of August) occurred. Due to the duration and the severity,
the latter can be held responsible for the drought-induced vitality suffer detected in this
study.
Based on the survey year growing season conditions (1st of May to 31st of August), I modelled
young Calluna plant responses towards three drought scenarios, representing the 1) wettest
and coldest conditions during the survey year growing season, 2) moderate drought
conditions, with the driest conditions measured in the growing season 2014, and the 3) most
severe drought conditions Calluna plants were potentially recently faced with in the North
German Plain.
The results confirm that droughts during the growing season reduce the growth rate and
increase the tissue damage frequency of young Calluna plants considerably, supporting the
hypothesis and the findings of other studies (Albert et al. 2012; Chavez et al. 2002; Gordon et
al. 1999; Southon et al. 2012). Surprisingly, the third vitality attribute, the severity of long
Chapter 4: High nitrogen deposition increases the susceptibility to drought
99
shoot damage, could not be explained by life history, N deposition or climatic conditions
validly in the models as the explanatory power was too weak.
Contrary to the expectations, some young Calluna plants increased their growth rates even
under strong drought conditions, a phenomenon already observed in other studies
(Bannister 1964a, b; Gobin et al. 2015; Ibe et al. 2020). This is due to the very high tolerance
towards water shortage and little or no reaction of stomatal conductivity reduction observed
there, suggesting the maintenance of photosynthesis activity (Bannister 1964b; Gobin et al.
2015). Albert et al. 2012 emphasized that Calluna withstands enduring water shortages with
preserving photosynthesis on a low level, without tissue damages. The results confirm this,
and even under the most severe drought conditions I modelled, many plants were able to
survive. As a consequence, the establishment of young Calluna plants is hampered, but not
generally restricted under drought.
The role of regional drought adaption potentials is a factor that contributes to a better
understanding of drought resistance and its variability across studies and regions.
Provenance-specific drought resistances have been found in several species, e.g. beech (Rose
et al. 2009), and is also reported for Calluna, with a higher drought resistance in
subcontinental plant provenances than in plants from Atlantic heathlands (Ibe et al. 2020;
Meyer-Grünefeldt et al. 2016). Plants from subcontinental provenances showed no growth
reduction under drought, enabling for a competitive advantage and additionally provided
higher sclerenchymatic tissue contents, a morphological adaption for a higher drought
resistance (Ibe et al 2020). Such adaptions to regional drought conditions may explain the
varying stomatal reaction sensitivity to a specific extent, and may contribute to the
explanation of the growth rate variation in the study. On the other hand, the analysis of the
ten-year period shows that between-year fluctuation in drought conditions is very high in the
North German Plains, and higher than those between the most oceanic and continental site.
As a consequence, the probability for droughts is quite high in oceanic sites, too. Whether the
adaption potential is determined by individual plant transgenerational effects (Walter et al.
2016) or by ecotype- or provenance-specific adaption potential, is still unclear. Further
research is needed, in particular to determine the speed and efficiency of drought adaption
mechanisms in Calluna.
Chapter 4: High nitrogen deposition increases the susceptibility to drought
100
Differ resprouted and germinated young plants in their
resistance to drought?
As Calluna regeneration and reproduction potentials are similar throughout the range of the
species (Henning et al. 2015; Mohamed & Gimingham 1970; Schellenberg & Bergmeier 2021),
the plants’ capacity to resprout and to germinate appears to be unrestricted under
subcontinental conditions. However, seedling establishment rates are low and successful
establishment seems to be limited to years of favourable weather conditions (Britton et al.
2003; Gimingham 1972; Henning et al. 2015; Lorenz et al. 2016; own observations). The
study confirmed the hypothesis that seedlings indeed have a lower drought resistance than
young resprouted plants.
The key trait for a plant’s susceptibility to drought is the shoot-root ratio (Weiner 2004). Due
to their limited root range and slower growth, seedlings have a much higher shoot-root ratio
than resprouted plants and consequently should have a lower drought resistance (Meyer-
Grünefeldt 2015). Indeed, I found both, seedlings and resprouted plants, to decline in growth
rate under drought, but in contrast to PR, PS tissue damages increased under drought, with
the consequence that half of the seedlings had all long shoots affected by drought-induced
tissue damages under severe drought. Due to their mature-stage rooting system and a
drought-induced growth cease, PR remained moreover unaffected, even under critical
drought conditions. Hence, the critical drought limits are reached earlier in PS than in PR,
confirming the hypothesis of a higher drought resistance in resprouted plants.
The growth rate measurement in the present study does not account for recovery processes
after droughts. Calluna plants profit from favourable post-drought climate conditions and
compensate for growth reduction during drought (Kongstad et al. 2012). In the 2014 climate
data, droughts are mixed with non-drought periods, and after the early summer droughts,
colder and wetter conditions may have induced a high increment. This may partly explain the
high variation under drought and weakens the explanatory power of the relationship
between growth rate and drought.
Does nitrogen deposition reduce young Calluna plants’
resistance to drought?
High N loads stimulated growth (‘fertilization effect’), resulting in higher aboveground
biomass production, like evident in many other studies (e.g. Bähring et al. 2017; Bobbink et al.
1998; Gordon et al. 1999; Taboada et al. 2018; Uren et al. 1997). Drought resistance of young
Calluna plants was generally reduced under high N, with evidence in increased tissue
Chapter 4: High nitrogen deposition increases the susceptibility to drought
101
damages and mortality, confirming findings of e.g. Gordon et al. 1999 or Meyer-Grünefeldt
2015. Under low N deposition, the general Calluna drought resistance strategy with a high
resistance towards drought stressors renders survival of critical drought possible, even at the
cost of severe, though not lethal, damages. The same drought conditions under high N loads
caused potentially lethal damage, indicating that high N loads generally decreased the
drought resistance of Calluna plants.
There was a complex life history-specific interplay between high N-induced growth boost and
drought-induced growth reduction. Seedlings potentially profited from N-induced growth
boost rather than resprouted plants, compensating for the drought-induced growth rate
reduction, but at the cost of critical tissue damages. Whether the biomass was produced
during the drought or in the non-drought periods between could not be determined in the
study, hence a conclusion to whether seedlings continue growing under drought or are able
to regenerate well after drought remains unclear. However, the larger tissue damages
indicate that critical drought conditions are reached earlier in seedlings than in resprouted
plants.
Although the total mortality rate of seedlings and resprouted plants under high N load and
drought was similar, the resprouted plants that survived often had only marginal tissue
damages, indicating that more plants have been affected less severe. As a consequence, the
hypothesis of seedlings rather affected by high N-induced increased drought susceptibility
than resprouting plants could be confirmed.
The physiological mechanisms behind the interaction of high N depositions and drought are
only partially identified yet. One explanation is the high N-induced growth stimulation which
alters the shoot:root ratio, with negative consequences for the plant water balance (Meyer-
Grünefeldt et al. 2015; Weiner 2004). The increased biomass production induces a higher
water demand (Bannister 1964b, Garnier & Laurent 1994; Terzi et al. 2013), and as long as
root biomass is not increasing as well, the water uptake capacity may be not sufficient under
drought conditions. The results presented here suggest that seedlings indeed seem to be
limited by this effect. Due to the extant rooting system, resprouted plants do not have such
limitation problems.
Additionally, there is evidence that high N loads alter the plant response to drought by
affecting the stomatal sensitivity. Gordon et al. 1999 reported that drought under high N
deposition caused unsustainably high transpiration rates, what they did not observe if only
drought or only N-fertilization was applied in their experiments. Ghashghaie & Saugier (1989)
found that Festuca arundinacea plants grown under low N deposition had a higher stomatal
sensitivity than plants under high N. They concluded that plants under low N had the strategy
Chapter 4: High nitrogen deposition increases the susceptibility to drought
102
to rather avoid critical water deficits with an early stomatal closure, whereas those under
high N tolerated high water deficits and continued transpiration.
The stomatal sensitivity is controlled by abscisic acid (ABA) contents in leaves and roots
(Bresinsky et al. 2008), but there is an insufficient knowledge how N availability affects ABA
concentrations and thus affects the stomatal sensitivity. Both, high and low levels of N are
reported to increase stomatal sensitivity (Ghashghaie & Saugier 1989; Song et al. 2019; Yang
et al. 2012). In a Populus species, high N concentrations increased ABA and drought
resistance (Song et al. 2019); other studies confirmed a positive effect of high N to mitigate
effects of drought (Dulamsuren & Hauck 2021; Yang et al. 2012).
The results presented here show that stomatal sensitivity in Calluna seedlings seem to
decline under high N and drought, supporting the findings of (Ghashghaie & Saugier 1989),
resulting in a poorly restricted photosynthesis activity even under severe drought, with lethal
consequences. Calluna vulgaris is a competitor/stress tolerator (CS) plant, with a very high
tolerance towards water shortage, and its drought resistance strategy is moreover a
tolerance strategy, comprising the maintenance of photosynthesis on a quite high level, even
under drought, for the cost of a high risk for dying. This strategy seems appropriate in terms
of competing with other heathland species, such as Deschampsia flexuosa or Molinia caerulea
(Albert et al. 2012; Britton et al. 2003; Friedrich et al. 2012; Kreyling et al. 2008). The
potential to recolonize recently disturbed sites quickly and to tolerate drought stress within
that time is a crucial determinant for the successful establishment process and the initiation
of early-successional heathland structures. Under high N, this strategy is limited by the
disability of young Calluna seedlings to prevent for exceeding the physiological drought limit.
The role of the high-N induced growth boost may be beneficial on sites with Calluna
dominance and no or only little grass cover, but offers risk for high seedling mortality under
drought, thus contributing to the increased grass dominance of heathlands under high N
loads (Britton et al. 2003; Diemont et al. 2013).
In contrast, resprouted plants ceased growth and suffered less damage under drought and
high N loads, thus showed a completely different drought resistance strategy. They avoid
water stress rather than tolerate it, by persisting unfavourable drought with preserving the
existent biomass, but not increasing it. This confirms findings of Gordon et al. 1999 who
found that Building stage Calluna height, density and increment was reduced under drought
and very high N load (50kg/ha*a). Following the finding of Ghashghaie & Saugier (1989) that
Festuca arundinacea plants limited by N showed the drought stress avoidance strategy and
those grown under high N rather tolerated drought stress; this might indicate that N-
limitation determines the strategy in Calluna plants as well. Seedlings may reach levels of N
saturation and limitation by other photosynthesis source materials earlier than resprouted
plants, as the latter have more reserves in their roots and stem bases, and additionally have a
Chapter 4: High nitrogen deposition increases the susceptibility to drought
103
better supply with their mature rooting system. Hence, as long as N is the limiting nutrient,
the tolerance strategy, at the cost of lethal damage, is prevailing. In terms of the limitation by
other factors, e.g. carbon starvation due to drought-induced stomatal closure over a longer
time (Sevanto et al. 2014), growth ceases or tissue damages occur, like observed for the
resprouted plants in this study, but further studies are needed to prove this.
Another reason for the high tissue damages under non-drought conditions may be
undetected Lochmaea damage. A re-inspection of the dataset revealed that tissue damages
were generally higher in areas where Lochmaea (heather beetle) infestation was detected,
namely in the oceanic German Northwest, with generally higher mean daily precipitation
rates, cooler conditions as well as higher N depositions, factors known to promote Lochmaea
outbreaks (Britton et al. 2001; Melber & Heimbach 1984; Power et al. 1998; Stevens 2018,
Taboada et al. 2016; Webb 1986). Larvae and adult Lochmaea beetles feed on Calluna leaves,
as well as on young stems and bark (Gimingham 1972), and although I removed plants with a
validated Lochmaea damage, I cannot exclude that some tissue damages may be induced by
Lochmaea. It is unclear whether the dataset may be biased towards generally reduced vigour
due to severe past year(s) Lochmaea damages, as I have no information whether the
resprouted plants may originate from Mature plants severely affected by the beetle, and
whether a resprouted plant’s vitality is generally affected by past year(s) heather beetle
attacks, or the extent of reduced vitality as a result of former droughts.
The higher prediction range under high N loads indicated that other factors’ influences on the
Calluna drought reaction increased with N. Positive and negative plant- or area-specific
effects are interacting with climatic and edaphic conditions and cause a more complex
situation. As a consequence, individual plant-specific water uptake efficiency and extent of
the rooting system determines the plant’s performance under drought conditions and high N.
Electronic Supplementary Material
ESM 4.1: Model diagnostics (html-files with Rcodes and outputs)
Chapter 4: High nitrogen deposition increases the susceptibility to drought
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105
Chapter 5:
Synthesis
Chapter 5: Synthesis
106
5.1 New insights into North German dry
lowland heathland ecology
Heathland plant community ecology and floristic
patterning
The present study assessed the commons and differences in species composition and
patterns of structural and species diversity across dry lowland heathland habitats in the
North German Plains. The results revealed that patterns in species composition and
vegetation structures are shaped primarily by the complex interaction of edaphic conditions
and site history, but only weakly by climate. As a consequence, the seven plant communities
identified in Chapter 2 represent stages of heathland development on two edaphically
determined successional pathways: 1) the psammophilous pathway representing succession
on poor drift sands in young heathlands, often with an inland dune-like character and 2) the
consolidated heathland pathway, representing the typical historical heathlands, on somewhat
developed, but still poor sandy soils.
Species inventory was rather determined by edaphic conditions and Calluna density than by
development stage. Although the study showed that there are development-specific species
assemblages, there were only few species showing a strict association with one of the
heathland development stages, e.g. Placynthiella oligotropha for early lichen-rich stages, or
the open sand grassland group for mature stages, as well as Galium saxatile for late Mature or
Degeneration stands.
The results do not support that lichens of the genus Cladonia are generally assigned to be
typical for Late Mature and Degeneration stages (e.g. Gimingham 1972), as they occurred
from Pioneer up to Late Mature stage, as typical, high frequent species in the lichen-rich
psammophilous heathland pathway. The prevailing life form group in early heathland
developments stages are the lichens, due to favourable conditions in the dry, exposed and
nutrient-poor environment of pioneer drift sands. The persistence of lichens during later
succession is determined by the presence of strong competitors, such like Deschampsia
flexuosa or pleurocarpous mosses (Müller et al. 1993), but also suitable soil conditions. Hence,
with persisting soil and interspecific competition conditions, lichen-rich synusia are
persistent over one or even more Calluna lifetimes. Hence, they are rather characteristic for
an edaphically determined heathland pathway than a specific Calluna age-related heathland
development stage.
Chapter 5: Synthesis
107
Additionally, our results show that many of the vascular species assigned to be typical for
heathlands in the matter of nature conservation status assessment (c.f. Chapter 1.3) are
moreover distributed over a wide range of heathland development stages, without a specific
informative value to the habitat quality. Species like Hypochaeris radicata, Hieracium pilosella,
Agrostis spec., Carex pilulifera, Deschampsia flexuosa and Rumex acetosella did occur in almost
all of the communities; hence they provide no further informative character than being a
species occurring in heathlands.
The findings of this study revealed that the informative value of species composition
concerning habitat quality increased considerably with considering also vegetation
structures. Thereby, the formation of either Calluna mosaic or dominance type is determined
by site history, recent management and edaphic conditions, but is not associated with species
diversity or heathland development stage. As a consequence, dominance stands, which are
often built from even-aged Calluna and are therefore often poor in age structures, are not per
se poor in species, too. The results presented in Chapter 2 offered that lichen-rich Building
and Mature dominance stands may lack in Calluna age diversity, but host a large number of
threatened lichens, with a high value for the local species pools.
Calluna mosaic heathland communities are not restricted to early-stage or degeneration
stages only (c.f. Gimingham 1972, van der Ende 1993), but are usually rich in Calluna age
structures, and often in life form group diversity, too. Hence, they potentially harbour a high
species diversity, unless the gaps between Calluna bushes are filled with only one dominant
species, such like Molinia caerulea, Deschampsia flexuosa or Hieracium pilosella.
Heathlands are generally poor in species (Ellenberg & Leuschner 2010) and the results
presented here confirm this in terms of vascular plant diversity. On the other hand, the
results support that cryptogam diversity is high in the psammophilous heathland pathway.
These findings emphasize the need for maintaining and restoring early-successional stages
with the highest potential to harbor not only a high species diversity, but also to host many
threatened species, in particular lichens. This is a finding which is not new and is reported
several times before (e.g. recently Haugum et al. 2021, Webb et al. 2010), but it highlights
again the need for the provision of suitable early-stage habitat conditions, achievable with
high-intense (soil) disturbance (e.g. de Graaf et al. 2009; Walmsley & Härdtle 2021).
The present study confirms that especially the low productive stages of Corynephorus
grassland-heathland mosaics on bare drift sands provide a suitable host for a lot of
threatened species (Müller et al. 1993). Such sites are typical for many former military
training areas in the German East. Although we found only weak support for a floristic-based
Chapter 5: Synthesis
108
distinction of Atlantic and subcontinental heathland plant communities, the extent and the
wide distribution of such Corynephorus grassland-heathland patches on former military
training areas in the suboceanic – subcontinental German East may be not only determined
by the site history, but also by climate. Droughts are potentially more severe there (c.f.
Chapter 4), in particular under inland dune-like conditions, where the specialists of pioneer
grasslands, especially many lichens, favour from the reduced competitive power of many
typical Atlantic heathland species, which are only able to reproduce and establish in years of
favourable climate. Additionally, many processes, such like raw humus accumulation and
podsolization rates are slower under subcontinental conditions, because drought reduces
mineralisation rates and leaching processes (Lache 1976; Härdtle et al. 1997). As a
consequence, the seral progression of sandy grasslands to heathlands and later to woodlands
may be delayed due to marginal conditions for typical Atlantic dry heathland species, with a
resulting longer persistence of grassland-heathland mosaics.
Another reason may be the lower N loads in East Germany than in the northwestern part, as
high N loads inhibit lichen growth, mainly due to the shift of competitive advantages to more
productive species and high N-induced metabolism alterations (Carter et al. 2017; Johansson
et al. 2010; Gutiérrez-Larruga et al. 2020; Hauck 2010; Müller 1993; Van Herk et al. 2003).
The military training created large sand drift areas with prevailing early successional stage
conditions in the past century (Ellwanger & Ssymank 2016), providing favourable conditions
for the establishment of diverse and stable populations and species pools for the lichen-rich
heathland succession stages present today. They are threatened by succession, unless intense
management counteracts.
The Calluna life cycle revisited
The results presented in Chapter 3 provide new insights to age-dependant vitality changes
during the Calluna life cycle. Thereby, the visual attributes such like the flowering intensity or
the proportion of dead, bare leading long shoots as well as annual increments are rather
determined by the aboveground plant age than by the total plant age, but they are not
completely independent from the latter.
Regeneration processes provide the potential for improving the vigour on the short term, but
the term ‘rejuvenation’ may be misleading, as it suggests a re-entry in a highly vigorous
regeneration life phase again, similar to an undisturbed growth. The results presented in this
study clearly show that disturbance indeed increases the vigour, and that a post-disturbance
regeneration by resprouting may produce a similar growth habit than undisturbed plants, but
the highly vigorous time is limited to a shorter timespan than that of undisturbed plants.
Additionally, the capacity to resprout vigorously is restricted to quite young plants up to 15
Chapter 5: Synthesis
109
years, confirming former studies (e.g. Mohamed & Gimingham 1970). Hence, even if there
were mechanisms supporting repetitive cycling from vegetative growth, they may not
produce highly vigorous plants on the long-term.
The reasons for that are determined in habitual shifts induced by plant ageing and
disturbances, more specifically in the reduction of the primary central rooting system to a
decentral branch-wise one. This process goes ahead with general shifts in the capacity to
regrow to mature plants again. In young plants resprouting, the clusters of shoots emerging
are close together and provide the highest post-disturbance vitality. In older plants,
resprouting may still take place, but due to the shift from the primary to the adventitious
rooting system, the stems emerging from the buds will rather form dense regeneration
cushions than distinct bushes. As a consequence, regeneration may proceed up to high total
plant ages, but the total vigour reduces.
Resprouting from young plants with an intact primary rooting system induces increased root
development from the stem bases and therefore initiates adventitious rooting, with a
subsequent death of the primary root. As a consequence, mature plants originating from
resprouting seldom provide an intact rootstock any more. Hence, the present study failed in
determining total plant life spans on the basis of growth ring counts, but the modelling
results suggest a total life span of about 30-45 years, which is in accordance to those reported
from British heaths (Gimingham 1972). Compared to the growth phase persistence there, the
results from the present study suggest a slight acceleration of the time Calluna needed to
grow from of a seedling to the mature plant. This is maybe due to general environmental
conditions varying between British heathlands in the 1970s, where the Calluna life cycle was
originally referred to, and the suboceanic - subcontinental German heathlands today, with
influences of airborne N depositions and climate change. High N depositions are found to
increase the yearly increment (c.f. results in Chapter 3 and 4); hence a faster growth may
explain the accelerated growth to Mature and Degeneration stages. Additionally, high N loads
increased the vigour in resprouted plants on the short term, as it triggers flowering intensity
and biomass production, but could not compensate for the fast decline in vitality after 10-15
years though.
On the other hand, drought and high N inputs reduce the regrowth of resprouting plants
(Chapter 4); hence recovery times are determined by summer drought conditions as well.
Dieback induced by drought occurs more often under subcontinental climate (Marrs &
Diemont 2013), hence the longevity of Calluna plants may be reduced as a consequence of
frequent severe droughts. The results of the study presented in Chapter 3 support this, but
further studies are needed to assess drought-induced demographic changes on the long-term.
Chapter 5: Synthesis
110
However, the analysis provided in this thesis found no evidence that the total life span of
Calluna in the North German Plain heathlands is generally either reduced by faster growth,
drought-induced early dieback or elongated by a vegetative (sub)cycle compared to other
regions. Due to the complexity of the field dataset and probable trade-off effects of
components influencing the Calluna life, further research is needed, specifically long-term
studies on Calluna plant individuals. Consequently, the answer to the question whether high
N loads reduce the highly vigorous life time by accelerated ageing or altered responses to
drought remains unclear. Local site managers reported that, e.g. for the Lüneburg Heath (pers.
comm. D. Mertens, VNP), but to the best of my knowledge there is no study confirming this
scientifically. Additionally, effects of general higher temperatures on the life cycle are not
studied yet, but are not unlikely as growth rates and developments are reported to be slower
under colder climate (Haugum et al. 2021).
Many studies analysed the (potentially) cyclical dynamics in heathland demographics, but up
to now, there is no satisfactory answer to the question whether regeneration processes in
heathlands may have a ‘repetitive cycle’ character or Calluna life is of a seral and limited
character (Gimingham 1972, 1988; Marrs and Diemont 2013; Wallen 1980).
This study provided no evidence for a cyclical vegetative and generative reproduction as part
of the natural long-term dynamics in dry lowland heathlands. The analysis of plant
communities and their soil-related pathways of heathland development clearly show that the
succession pressure from grasses and trees increases with time, thus reducing the
competitive power of Calluna. However, very poor inland-dune-like conditions on drift sand
areas with a military training history show a delayed succession, where cyclical regeneration
and reproduction seems to be feasible for several Calluna generations, but not on the long-
term.
Repetitive cycling without generative reproduction but with several consecutive resprouting
cycles could not be verified in the present study. The first resprouting may regrow to a plant
with a habit similar to a plant grown from seed, but it is unlikely that further subsequent
resprouts will do so, as the results presented in Chapter 3 show that the disturbance-induced
modifications of the root biomass allocations from the primary rooting system to the
decentral adventitious one induces a different plant habit after resprouting, building rather
flat cushions than hemispherical shapes.
Repetitive cycling on a low productive level with layering plants continuously creeping and
rooting, like reported for Swedish and Scottish heathlands (Gimingham 1972, Wallen 1980,
Webb 1986), seems to be the most likely type of any natural cyclical regeneration processes
in heathlands. Such ‘immortal’ stand characteristics are reported for heathlands on peat in
Northeast Scotland, but also for sand dunes in South Sweden (Wallen 1980), but the study
Chapter 5: Synthesis
111
presented in Chapter 3 provides no evidence, neither for the existence nor the absence of
such ‘immortal’ layering processes. Layering is a common process in North-German dry
lowland heathlands, with the potential to form quite stable-state stands, but the results do
not allow for any assessment of persistence times, as the total plant age was no more
detectable. However, concluded from observations of successional old heathland stages, with
prevailing layering plants, Calluna immortality seems unlikely due to the constant reduction
of Calluna biomass with age of layering plants. Although the layering phase represents the
last life phase before plant death, it may provide low-productive, but stable biomass
production and flowering, enabling for the provision of heathland ecosystem functions on a
minimum level, but potentially stabilizing heathlands suffering from diebacks and low
establishment rates (Chapter 3).
Calluna recruitment response to drought and high airborne
nitrogen loads
The immediate effects of droughts on Calluna comprise tissue damage and dieback, but more
complex interactions with plant vitality and long-term effects are not well understood.
Droughts can alter Calluna biomass allocation (Schuerings et al. 2014), may induce earlier
biomass production in the subsequent spring and increase frost susceptibility (Gordon et al.
1999). Droughts can also delay or reduce the flowering period (Jentsch et al. 2009; Nagy et al.
2013). It has been shown that drought affects the Calluna root-associated mycobiome, with as
yet unknown consequences for the plants’ vitality, soil nutrient processes and heathland
productivity (Dahl et al. 2021; Tobermann et al. 2008).
Drought resistance is determined by morphological and physiological traits of plants, as well
as their adaptive potential, which is generally assumed to be quite high in Calluna, due to its
wide distribution and plasticity (e.g. Albert et al. 2012; Backhaus et al. 2014; Bannister 1964a;
Bartoli et al. 2013; Gordon et al. 1999, Ibe et al. 2020; Kongstad et al. 2012; Petrova et al.
2017; Walter et al. 2016). In fact, this study provides evidence that even severe drought
conditions and high N loads revealed to be seldomly lethal for resprouting plants, resulting in
a high potential for a fast and successful recovery after disturbances even under drought
conditions. In contrast, droughts under high N lethally affected most of the seedlings.
The physiological background of the interaction between high N loads and drought sensitivity
is still insufficiently understood. There is evidence that drought resistance is altered under
high N loads by affecting the stomatal sensitivity. A study on Festuca arundinacea
(Ghashghaie & Saugier 1989) revealed that plants under N-limitation reacted earlier with
stomata closure under drought conditions than those under high N supply, a finding
Chapter 5: Synthesis
112
supported by the results presented in this study. The Calluna seedlings showed a drought-
induced growth reduction under low N deposition, but not under high N loads. Stomatal
regulation was probably hardly existent under high N, resulting in severe tissue damage and
a high mortality rate. In contrast, the resprouted plants generally reduced growth, but had
only marginal damage, indicating that they were less affected by the high N-induced stomatal
sensitivity alteration. I assume N limitation to be responsible for that, because the load for N
saturation in seedlings should be lower than that for resprouted plants, as the latter profit
from a higher nutrient reservoir in their biomass compensating for the limitation of other
nutrients. As a consequence, seedlings under N saturation have a high-risk strategy to
tolerate drought, with maintaining photosynthesis and biomass production, thus potentially
increasing their competitive power under moderate drought. In contrast, resprouted plants
show a strategy of avoiding even moderate drought stress by a growth cease, probably
induced by stomatal closure. As a conclusion, N depositions of 25kg*ha-1*yr-1 do not induce N
saturation in Mature Calluna plants (Walmsley & Härdtle 2021) and may increase drought
resistance in resprouting plants under moderate drought, but for the cost of reduced growth
and hence reduced competitive power, thus favouring plants dealing better with drought
under high N loads during the post-disturbance re-establishment phase, such like
Deschampsia flexuosa or Molinia caerulea (Albert et al. 2012; Britton et al. 2003, Diemont et al.
2013; Friedrich et al. 2011). This confirms former findings that re-establishment after
drought-induced Calluna dieback altered the heathland species composition, and Calluna was
substituted by fast-growing and more drought-tolerant grasses dominating, especially under
high N deposition levels (Albert et al. 2012; Britton et al. 2003; Kreyling et al. 2008;
University Hasselt 2021). It is yet unknown whether these changes will be temporary,
providing shelter for the next Calluna generation (Marrs & Diemont 2013), or signalize a
persistent loss of typical Calluna heathland under the conditions of frequent severe drought
and high N loads. Further research is needed to assess potential accumulative effects of
reduced vitality as a consequence of frequent droughts and the recovery potential for Calluna
in years with more favourable climate.
Plants with a high adaption potential and a wide tolerance to water shortage provide a
certain climate change resilience (Bannister 1964a, Richter et al. 2012). Gordon et al. (1999)
and Kongstad et al. (2012) claimed such an adaptation effect after repeated drought,
indicating that drought resistance is adjustable. The high adaption potential and
morphological plasticity of Calluna may be the reason for its wide distribution, with
provenance-specific adaptions to the drought conditions in subcontinental marginal
populations, but the complex interactions of N depositions, drought and provenances are still
poorly understood. A recent study showed that Calluna from subcontinental and suboceanic
Chapter 5: Synthesis
113
provenances showed different reactions to elevated VPD, indicating higher drought
resistance in plants from subcontinental regions (Ibe et al. 2020), whereas other studies
found no or only little effects (Meyer-Grünefeldt 2015; Meyer-Grünefeld, 2016). However,
even if there was higher drought resistance in seedlings of subcontinental ecotypes, this
effect is overlaid by effects of high N- induced higher drought susceptibility (Meyer-
Grünefeldt et al. 2016). Further research is needed to understand the adaption potential of
Calluna under changing climate and whether this natural potential is altered by high N
depositions.
5.2 Implications for future dry lowland
heathland management
The role of management for the provision of high nature
conservation value heathland
The conductance and combination of several managements to ensure the habitat diversity
and functionality is a great challenge in recent heathland management (Olmeda et al. 2020,
Walmsley et al. 2021). The strategies need to be assessed in the context of the complex trade-
offs related to different management targets, for example biodiversity protection, climate
change adaptation, compensation of airborne nitrogen inputs, or the protection of landscape
multifunctionality (Ibe et al. 2020; Walmsley 2021). The results presented in this thesis show
that heathlands are faced with a complex situation of inter- and counteracting factors, thus it
is vital to understand heathland habitat dynamics in their complexity in a changing
environment. That emphasizes the need for a more detailed look on specific responses of
Calluna to the known stressors, and how they may contribute to the overall decline in
heathland habitat quality. Therefore, this study provides a specific view on the interaction of
factors influencing Calluna vitality under field conditions to improve the understanding how
they recently influence heathlands and may determine future heathland dynamics and
structures. This knowledge is necessary to include the consequences of heathland
management in the further planning and conduction of nature conservation measures.
Therefore, the results presented in this thesis provide some new insights into the complex
determinants for heathland species composition and vegetation structures, thus helpful in
understanding the heathland dynamics in North German lowlands differing across regions,
characterized by different site histories, edaphic and climatic conditions, recent
managements and N deposition rates, all affecting the Calluna demographics and vitality.
Chapter 5: Synthesis
114
This study showed that the main determinants for heathland vegetation of high nature
conservation value are 1) the provision of suitable soil conditions, favouring early-
successional stages and structures as well as 2) low N depositions to increase the competitive
power of Calluna and other low-productive, but high-value heathland species, such like
threatened lichens. This study showed that species assemblages of high nature conservation
value need components from structural and edaphic conditions, local species pools and
favourable competition conditions, thus a suitable management has to provide the most
beneficial services to achieve this. Thereby, management can only prepare the starting
conditions for the seral succession, followed by initial developments that already determine
the heathland successional pathways. Post-disturbance regeneration species composition
depends chiefly on the soil conditions and the species pool present in adjacent sites, hence
the site-specific potential for high species diversity is always determined by the surrounding
habitats, a finding which highlights the need for habitat connection and the necessity to
preserve local species pools (Piessens et al. 2004, 2005).
Heathland formation character is the predominant structural trait in dry lowland heathlands,
as it determines either a Calluna-only dominance or a mosaic of dwarf shrubs and other life
form groups. Heathland plant communities of a mosaic character provide a high diversity, but
are prone to grass invasion (Britton et al. 2003). The conversion of heathlands to grasslands,
dominated by Deschampsia flexuosa, Molinia caerulea or others, is among the main reasons
for heathland habitat decline (e.g. Olmeda et al. 2020). Deschampsia flexuosa acts as the
strongest competitor under suboceanic- subcontinental conditions with drought and high N
and on sites with raw humus accumulation (Heil & Diemont, Britton et al. 2003), whereas
under more oceanic conditions and P-limitation, it is moreover Molinia caerulea (Friedrich et
al. 2012). Thereby, the interaction- and counteracting effects of co-occuring Calluna and the
grasses showed that already small shifts in competitive advantages induced a conversion of
heathland into grasslands (Aerts et al. 1990; Britton et al. 2003), indicating that minor
changes may be sufficient to hamper Calluna recruitment during early successional stages
and to favour grasses instead. The results presented in this study provide evidence that high
N loads and drought decrease the competitive power of Calluna and consequently confirm
that the risk of grass dominances increases then.
Whether heathland formation is a heathland mosaic or a dense dominance stand of Calluna, is
determined by several factors, beginning with the management or disturbance type, the
initial post-disturbance soil conditions, and the early post-disturbance development of the
vegetation. This study showed that climatic conditions and nitrogen deposition potentially
alter this early post-disturbance regeneration (Chapter 4).
Chapter 5: Synthesis
115
Managements that induce vegetative regrowth, e.g. mowing and burning, often build
dominance stands, unless they have been very open before. This is due to the dense resprout
from stem bases, with the regenerating plants having a higher cover when reaching the pre-
disturbance growth phase again (Fig. 3.6, p. 71).
Regeneration which is predominately from seed provides a higher probability to form mosaic
stands. With a sufficient supply from the seed bank, the absence of strong competitors and
moderate climate conditions (i.p. no drought), seedling-dominated regenerations sites may
become dominance stands, too, especially on sites with a high fire frequency (e.g. shooting
lanes on military training area Bergen, Lower Saxony, own observations).
Regeneration from seed on bare drift sands is slower than on consolidated sands, due to the
better supply of water and the presence of ericoid mycorrhiza in the latter, especially when
the site was previously already colonised by Calluna (Green et al. 2013; own observations).
Bare drift sands are usually colonised by pioneer grassland species first to stabilize the
mobile sands, with a subsequent slow invasion of Calluna, forming open grassland-heathland
patches. Those successional stages with a small-scale mosaic patch structure provide the
highest potential to harbour a rich pool of threatened species and a very high structural
diversity, but need expensive, intensive management for the provision of suitable initial
development conditions, and low N deposition rates.
Managing Calluna demographics under changing climate
and high N depositions
To ensure suitable soil conditions and early-stage habitat conditions, intensive managements,
such like mowing, burning or sod-cutting are essential, but need a careful weighing between
the provision of landscape structure aspects, such like the removal of trees and providing
bare drift sand landscapes, and the provision of edaphic conditions enabling heathland
vegetation to succeed in the re-establishment phase. For managing heathlands successfully, a
fundamental knowledge to Calluna ageing as well as regeneration and establishment
potentials is needed. Assessments to these potentials are derived from the Calluna life cycle,
with using visual attributes that are informative about the plant age to determine plant and
regeneration age. This thesis contributes to a specified determination of age-related changes
in Calluna habit and vigour, in particular the differences between plants grown directly from
seed or regenerated after biomass disturbance (Chapter 3). Hence, with this improved
knowledge, it is easier to determine and interpret Calluna age structures in the field, and to
estimate regeneration potentials. The findings of the present study sharpen the view on the
distinction of plants grown from seed or regenerated from resprouting, and this allows for
explaining and predicting the persistence of highly vigorous phases. The observations and
Chapter 5: Synthesis
116
results presented in Chapter 4 explain the rapid decline of stands regenerating
predominately from resprouting, which we found not predominately determined in higher N
depositions, but rather the general vitality decline of resprouted plants, due to plant age –
related morphological changes. However, the assessment on the role of high N deposition
affecting the Calluna life cycle needs further research, as the results presented here suggest a
general acceleration of early life stages, independent from the individual plant life history,
probably induced by a faster growth.
Calluna demographics seem to be only marginally influenced by climate; subcontinental
marginal population dynamics are not fundamentally different to those in the main Atlantic
lowland heathland areal. But the results presented here suggest that although Calluna
showed a high resistance towards drought, severe droughts have the potential to reduce
seedling establishment rates and cause considerable damage on mature plants as well,
especially under high N deposition rates. Calluna has a high potential to recover completely
after biomass disturbance, hence also drought-induced growth reductions or diebacks can be
compensated by higher growth rates under favourable post-drought conditions. Especially
resprouted plants may ensure a fast post-disturbance Calluna regeneration and re-
establishment then (Kongstad et al. 2012). But to the best of my knowledge, little is known
whether frequent severe droughts rather affect Calluna vigour and regeneration potentials
negatively on the long-term, or whether adaption may compensate for that.
In our study region, the subcontinental sites are simultaneously those with the lowest N
depositions (10-12kg*ha-1*yr-1) hence the additional high N deposition-induced drought
resistance reduction is not present there, but in study areas with higher N loads, already
moderate droughts may hamper post-disturbance Calluna establishment considerably. As a
consequence, the reduction of Calluna’s competitive power favours grass dominances and
habitat degradation.
Although needed to create suitable soil and nutrient conditions (de Graaf et al. 2009),
vigorous heather regeneration (Chapter 3) and typical habitat structures (Olmeda et al. 2020;
Webb 1998), mechanical management has to be applied with caution in respect to the
drought susceptibility of post-disturbance Calluna establishment and to N loads (Britton et al.
2001). Seedlings need stable conditions of high air humidity and sufficient, moreover even
precipitation (Britton et al. 2003, Gimingham 1972). A nursing shelter, provided by older
plants, is favourable (Henning et al. 2015). High-intense practices, such as sod cutting, create
exposed ground with Calluna plants only sparsely germinating in the first 1-3 years (own
observations). In contrast, practices such like burning or mowing favour young resprouting
plants, showing a fast and vigorous recovery after disturbance. This thesis provides evidence
for a high potential of plants emerging from resprouting to persist even critical drought
Chapter 5: Synthesis
117
periods with reduced growth but without severe damage. In consequence, a post-disturbance
site with plants both grown from resprouting and from seed provides a fast and drought-
resistant Calluna establishment by resprouting plants first, and later favours seedlings to
survive droughts by the provision of nursing effects.
Practical approaches to compensate the climate-change related enhanced susceptibility of
post-disturbance Calluna recruitment may be
1) Heathlands with higher heterogeneity provide a higher resilience towards ecological
stressors and climate change (Haugum et al. 2021). Hence, maximising the spatial
heterogeneity of disturbed and undisturbed sites on a small scale for minimizing the
effects of drought-induced failing Calluna establishment and subsequent grass
dominances.
2) On sites selected for shallow sod-cutting, mowing or burning: Enabling highly
vigorous resprouting by the provision of a sufficient amount of Mature plants with the
capacity to do so (<15 years, vigorous) for a save and fast re-establishment even
under drought conditions. A few years later, they provide a nursing shelter for
seedlings to reduce drought susceptibility during the early post-disturbance stage.
3) Minimize the need for high-intense soil disturbance by retarding successional and
Calluna ageing processes. To compensate for rapid degeneration after disturbances,
grazing is the most efficient method to keep Calluna in a highly vigorous lifetime,
especially after burning or mowing (e.g. Kirkpatrick & de Blust 2013; Gimingham
1975, Olmeda et al. 2020). However, grazing alone is insufficient to induce sufficient
aboveground biomass disturbance and to provide suitable soil conditions on the long-
term (Brunk et al. 2004). Additionally, it may alter Calluna growth on the long-term as
it promotes dense mats with short internodes (Gimingham 1974, 1994; own
observations).
In the end, the results presented in this thesis suggest that site-specific management schemes
should be developed that respect different local species pools, heathland successional
pathways, regeneration potentials, as well as the whole framework of edaphic and climatic
conditions.
Implications for the future nature conservation status
assessment and monitoring
Two of the key actions in the EU Habitat Action Plan are the improvement of knowledge
about the habitat and its importance for biodiversity as well as improving the mapping
Chapter 5: Synthesis
118
instructions (Olmeda et al. 2020). This thesis contributes to these two aims by providing a
fundamental revision of heathland plant community ecology and their dynamics, an
improved validity of vitality-based heath conservation status assessments and thus
strengthens the biological-ecological knowledge required for informed advice on heathland
management. Defining criteria for mapping instructions needs suitable references, but they
can only be defined on a national or even regional scale (Olmeda et al. 2020). The present
study provides an analysis of a wide range of dry heathlands varying along gradients of
climate, diversity and structures, and may act as an overview to the North German Plain
lowland heathland ecology. Hence, it can be used for improving and specifying the criteria for
heathland habitat quality assessments, based on the quality range given from the North
German Plain heathlands. Therefore I suggest:
1) To revise the HT 2310 and HT 4030 definitions, mapping instructions and assessment
schemes. The results presented in this study revealed that the distinction of the HT
4030 and 2310 in the North German Plains could be based on the recent floristic
composition, heath stand structure and soil conditions, culminated in a
psammophilous heathland pathway (HT 2310) and a Consolidated sand pathway (HT
4030). The restriction of the HT 2310 occurrences on ‘dunes’ only, with varying
definitions and without a further unique specification over the EU member states
disregards the ecological constraints shaping this habitat type, which is moreover
determined by poor loose drift sands, but not necessarily to dunes of a specific
dimension. The ecological conditions of initial soil development on loose sands and
the mosaic structure with close contacts to acidic pioneer grasslands are the
determinants for the HT 2310, and therefore the related reference criteria should
focus on floristic and structural aspects, but not on geological substrate only.
Therefore, the lists for the ‘typical species’ inventory should be revised to strengthen
the floristically based distinction between the HT 2310 and HT 4030. Valuable species
should represent the close contact to the pioneer grasslands and should include early-
successional mosses and lichens.
2) To specify and clarify the heathland age structure assessment. First, it has to be
emphasized that the prevailing Calluna growth phase is not necessarily congruent to
the heathland successional stage. Several management cycles with a removal of
aboveground biomass, but no removal of raw humus or upper mineral soil horizon
will keep the aboveground Calluna biomass in an early development stage, but
edaphic conditions comply with an advanced soil development. As a consequence, the
competition conditions for Calluna differ between real early stage soil conditions and
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119
those of advanced conditions, critically determining the re-establishment processes.
As a consequence, the heathland succession stage should be assessed independently
from the Calluna age. Heathland succession stage is determined by the sand type
(loose/consolidated), raw humus, the humus content in the topsoil, as well as tree
cover or the presence of typical early or late-successional species (e.g. lichens and
acrocarpous mosses for early stages, pleurocarpous mosses for late stages).
The Calluna age structures should not only be assessed in the cover of the four growth
phases, but also by an appraisal of the life history composition of the stand. Signs of
any vitality damage, either by insect calamities, drought, or other biomass
disturbances should be noted, as well as an approximate age of the aboveground
biomass, for each of the growth phases. Layering processes should be carefully
distinguished from resprouting processes with a better prospect for highly vigorous
regrowth, thereby, the habitual diagnostic should base on the extent of adventitious
rooting and the shape of the plant patches.
3) As N deposition is an important factor for habitat degradation, it should be included
in the monitoring assessment scheme (like in England, Olmeda et al 2020), and also
should be considered in the management planning and conduction.
Chapter 5: Synthesis
120
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121
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Appendix
Appendix
138
Table A-1 Assessment criteria for the estimation of nature conservation status potential of communities found in the present study. Basing on the criteria defined in the mapping
instructions for the federal states of Lower Saxony (NLWKN 2012) and Brandenburg (LfU 2014a & 2014b). 1) not considered in community-scale estimate of nature conservation status
assessment due to insufficient data. 2) not considered separately. 3) list of heathland-typical plant species differs between federal states; a pooled list of all mentioned specimen in the
above mentioned mapping instructions was used for community potential assessment.
A
favourable
B
unfavourable - inadequate
C
unfavourable - bad
criteria/
subcriteria
habitat
type
Lower Saxony
Brandenburg
criteria for
community
potential
Lower Saxony
Brandenburg
criteria for
community
potential
Lower Saxony
Brandenburg
criteria for
community
potential
habitat-typical
structures
Calluna age structures
4030/2310
all growth stages
present
- all growth phases
present,
Degeneration < 50 %
OR
- Pioneer/Building
phase > 75 % and
Degeneration
< 25%
- all growth phases
present on 25 m²,
Degeneration < 50 %
OR
- Pioneer/Building
phase > 75 % and
Degeneration
< 25%
not all growth
stages present
- three growth
stages present OR
- Degeneration 50 -
75 %
not all growth
stages present at 25
m²
low structural
diversity,
Degeneration
dominant
Degeneration > 75 %
Degeneration > 75 %
at 25 m²
typical relief
4030/2310
present
2)
1)
overall present
2)
1)
only partially
2)
1)
proportion of open
sand [%]
4030
5 - 10
> 10
> 5 / 25 m²
< 5
5 - 10
1 - 5 / 25 m²
no
< 5
0 / 25 m²
2310
5 -25
> 10
> 5 / 25 m²
< 5
5 - 10
1 - 5 / 25 m²
no
< 5
0 / 25 m²
habitat-typical species composition
heathland-typical
species
4030/2310
3)
≥ 6 typical vascular
plant species,
upgrade option
when high diversity
of cryptogams
(without
specification)
Among Calluna, at
least 8 typical
vascular plant
species, if less: > 25
cryptogam species
mean occurence of
≥ 5 typical vascular
plant species/4m²,
optional ≥ 5
cryptogam
species/4m²
3 - 5 typical vascular
plant species,
upgrade option
when high diversity
of cryptogams
(without
specification)
Among Calluna, 2-5
typical
vascular plants, if
less: < 15 cryptogam
species
mean occurence of
2-4 typical vascular
plant species/4m² in
the community,
optional 2-4
cryptogam
species/4m²
1 - 2 typical vascular
plant species,
upgrade option
when high diversity
of cryptogams
(without
specification)
Among Calluna at
least
1 typical vascular
plant species
Among Calluna,
1 typical vascular
plant species, low
cryptogam diversity,
too
Threats
tree invasion
4030/2310
< 10 % tree cover
< 10 % tree cover
< 10 % tree cover/
100 m radius
10 - 25 (35) % tree
cover
10 - 30 % tree cover
10 - 30 % tree
cover/
100 m radius
> 25(35) % tree
cover
30 -75 % tree cover
> 25 % / 100 m
radius
destruction of
habitat-typical
structures 1)
4030/2310
no
< 5 %
1)
small-scale
5 - 10 %
1)
intensive
>10 %
1)
Cover of heathland-
destructive grasses such
like Deschmapsia
flexuosa
4030/2310
< 30 %
< 10 %
< 10 % / 4 m²
30 - 50 %
10 - 30 %
10 - 30 % / 4 m²
> 50 - 90 %
30 - 75 %
> 30 % / 4 m²
ruderals, nitrophytes,
neophytes
4030/2310
< 1 % cover
no
< 1 % cover / 4 m²
< 10 % cover
> 5 % cover
> 5 % cover / 4 m²
> 10 % cover
> 10 % cover
> 10 % / 4 m²
afforestation 1)
4030/2310
2)
no
1)
2)
≤ 5 tree groups
1)
2)
> 5 tree groups
1)
Appendix
139
Table A-2 Weather stations used in the present study for calculating long-term climate conditions (DWD
2015), ten-year-trends (DWD 2019) as well as survey period conditions 2014 (DWD 2019). In some areas,
stations differ due to data availability issues:
Weather stations
1 - Tinner Dose
Lingen
2 - Cuxhavener Küstenheiden
Cuxhaven
3 - Suederluegumer Binnenduenen
Leck
4 - Fischbeker Heide
Hamburg-Neuwiedenthal
5 - NATO trainig area Bergen-Hohne
Celle-Wietzenbruch
6 - Lüneburger Heide
Soltau
7 - Nemitzer Heide
Lüchow
8 - Leussower Heide
Boizenburg (Elbe)
9 - Marienfliess
Marnitz
10 - Kyritz-Ruppiner Heide
Neuruppin
11 - Oranienbaumer Heide
Wittenberg1), Jessnitz2)
13a - Kleine Schorfheide
Zehdenick
13b - Vietmannsdorfer Heide
Zehdenick
14 - Glücksburger Heide
Wittenberg
15 - Bundeswehr training area Jägerbrück
Ückermünde
16 - Prösa
Doberlug-Kirchhain
17 - Zschornoer Wald
Döbern1), Bad Muskau2)
18 - Daubaner Wald
Kubschütz
1) data us ed only for years 1980-2020, 2) data used only for 2011-2020 and survey
period conditions 2014.
Appendix
140
Electronic Supplementary Material
Folders and files on included CD
Chapter 1
ESM1_1: Field protocols
Chapter 2
Article pdf and electronic supplementary material to the article
Schellenberg J, Bergmeier E (2020) Heathland plant species composition and vegetation structures
reflect soil-related paths of development and site history. Applied Vegetation Science 23: 386–405.
https://doi.org/10.1111/avsc.12489
ESM2_1: Additional information to study sites and community distribution. (identical to
Appendix S1 in original article)
ESM2_2: Floristic and phytosociological remarks. Text and Synoptic Tables. (identical to
Appendix S2 in original article)
ESM2_3: Additional results. Figures for Calluna growth phase composition, site history,
climate, edaphic conditions, grazing regimes and intense managements in
heathland plant communities. (identical to Appendix S3 in original article)
ESM2_4: Nature conservation status additional information. Tables of rare species and nature
conservation status assessment criteria applied. (identical to Appendix S4 in original article)
ESM2_5: R source codes and original data Tables. (identical to Appendix S5 in original article)
Chapter 3
Article pdf and electronic supplementary material to the article
Schellenberg J, Bergmeier, E (2021) The Calluna life cycle concept revisited: implications for heathland
management. Biodiv Cons https://doi.org/10.1007/s10531-021-02325-1
ESM3_1: Study areas. This PDF contains supplementary material to all sites, including
information to study area location, management, climate, nitrogen deposition and
sampling statistics. (identical to OR 1 in original article)
ESM3_2: Initial analysis. This PDF contains a brief graphical overview of initial analysis
results concerning dataset-inherent correlations and associations, as well as
ecological patterns and dependencies. Additionally, they provide further
information on the effects of management, nitrogen deposition and oceanicity on
the vitality of Calluna plants not addressed in the present article. (identical to OR 2 in
original article)
Appendix
141
ESM3_3: Analysis documentation. The zip-folder contains the html documentation of the
statistical analysis performed in R. (identical to OR 3 in original article)
Chapter 4
ESM4_1: Model diagnostics (html-files with Rcodes and outputs)
142
Acknowledgements
J.S. thanks all people involved in fieldwork preparation and conductance, granting of
permissions, further in data processing, analysis and manuscript drafting.
J.S. specifically thanks all colleagues, friends and family members for their support during the
past decade, for their financial, mental and always helpful advices, revisions of manuscripts,
babysitting, home-schooling during the Corona pandemic and much more.
Special thanks to
Prof. Erwin Bergmeier and Prof. Markus Hauck for scientific counselling, motivation,
patience and general support
The DBU scholarship program
My dear colleagues for scientific discussion, input, giving helpful comments for
manuscripts, providing cookies and coffee, counting growth rings, language checks, in
particular D. Walmsley, L. Sutcliffe, C. Battmer, V. Öder, F. von Lampe, F. Goedecke, I.
Schmiedel, B. Siegesmund, S. Krutemeier and many others.
My family and friends, in particular: H. Altmann, M. Schellenberg, J. Schellenberg, O. de
Boer, H. Rabah, M. Semmler and many, many others.
Academic CV
143
Academic Curriculum Vitae
Jenny Schellenberg, born on 28th June 1984 in Dresden, Germany
Education
2009–2022 PhD studies, Department Vegetation & Phytodiversity Analysis,
Albrecht-von-Haller-Institute for Plant Sciences, University of
Göttingen. Thesis title: Vitality of heather (Calluna vulgaris) along
gradients of climate, structure and diversity in dry lowland heathland
habitats of Northern Germany.
2012–2015 Doctoral scholarship Deutsche Bundesstiftung Umwelt (DBU) in the
scholarship program „Scientific research on DBU natural heritage
sites“ (translated). Thesis title: Vitality of heather (Calluna vulgaris)
along gradients of climate, structure and diversity in dry lowland
heathland habitats of Northern Germany. Department Vegetation &
Phytodiversity Analysis, Albrecht-von-Haller-Institute for Plant
Sciences, University of Göttingen.
2005–2009 Advanced studies in Biology, Georg – August – University of Göttingen.
Examinations: Botany, Nature conservation and Soil Science. Diploma
thesis (translated): Vegetation dynamics of pioneer Corynephorus
grasslands and Calluna heaths on a former military training area in
Northeast Brandenburg, Germany.
2002–2005 Basic studies in Biology, Christian – Albrechts – University of Kiel.
2002 Abitur, Radebeul, Germany.
Work experience
2009-2022 Teaching assistant and lecturer in vegetation analysis courses,
comprising the conception and implementation of new course parts.
Assistance in field work, excursions, seminars and Computer-based
analysis techniques. Counselling of thesis works, counselling of
statistical analysis problems. Department Vegetation & Phytodiversity
Analysis, Albrecht-von-Haller-Institute for Plant Sciences, University of
Göttingen.
Academic CV
144
2019-2020 Lecturer “statistical methods for plant ecologists”, Conception and
implementation of workshops, specific counselling for BSc and MSc
students.
2016-2017 Freelance work: Project “Free ranging Red deer grazing as a
management tool in heathland ecosystems” (translated). Development,
implementation and evaluation of a questionnaire survey. Sifting
David, Erfurt.
2010 – 2012 Employee as Head of coordination, conception and implementation of
the Natura2000 heathland habitat mapping and monitoring, FFH area
„Colbitz-Letzlinger Heide“. GISCON Braunschweig geo.engineering
GmbH.
2010 Freelance work: Report about the effects of heathland management in
selected areas of the nature „Kleine Schorfheide“, Brandenburg,
Germany.
2010 Freelance work: Cryptogam mapping nature reserve „Forsthaus Prösa“,
Brandenburg, Germany.
2006-2009 Teaching assistant in vegetation analysis courses, comprising field
work, excursions and Computer-based analysis techniques.
Department Vegetation & Phytodiversity Analysis, Albrecht-von-
Haller-Institute for Plant Sciences, University of Göttingen.
2004-2005 Teaching assistant in courses to vegetation sampling and plant
determination. Ecology Centre, University of Kiel.
2003-2004 Student assistant: Laboratory studies, preparation of sampling
material. Institute of Crop Science and Plant breeding, University of
Kiel.
Scientific contributions
Articles in peer-reviewed journals:
2021 Schellenberg J, Bergmeier, E (2021) The Calluna life cycle concept revisited:
implications for heathland management. Biodiv Cons.
https://doi.org/10.1007/s10531-021-02325-1
Öder V, Petritan AM, Schellenberg J, Bergmeier E, Walentowski H (2021)
Patterns and drivers of deadwood quantity and variation in mid-latitude
Academic CV
145
deciduous forests. For Ecol Man 487.
https://doi.org/10.1016/j.foreco.2021.118977
Fried O, Westphal C, Schellenberg J, Grescho V, Kühn I, Van Sinh N, Settele J,
Bergmeier E (2021) Vascular plant species diversity in Southeast Asian rice
ecosystems is determined by climate and soil conditions as well as the
proximity of non-paddy habitats. Agric Ecosys Environ 314:
https://doi.org/10.1016/j.agee.2021.107346
2020 Schellenberg J, Bergmeier E (2020) Heathland plant species composition and
vegetation structures reflect soil-related paths of development and site
history. Appl Veg Sci 23: 386–405. https://doi.org/10.1111/avsc.12489
2019 Pätsch R, Bruchmann I, Schellenberg J, Meisert A, Bergmeier E
(2019) Elytrigia repens co-occurs with glycophytes rather than characteristic
halophytes in low-growing salt meadows on the sou-thern Baltic Sea
coast. Biologia 74: 385–394. https://doi.org/10.2478/s11756-019-00195-1
2014 Schellenberg, J & Bergmeier E (2014). Atlantische und subkontinentale
Heiden in Norddeutschland. Nat Landsch 89(3): 110-117.
Other publications:
2017 Schellenberg J (2017) Vitalität der Besenheide (Calluna vulgaris) in
trockenen Zwergstrauchheiden entlang von Klima-, Struktur- und
Diversitätsgradienten im norddeutschen Tiefland. In: DBU, Schaefer, Schlegel-
Starmann (eds.) Ergebnisse aus dem Stipendienschwerpunkt „Forschung auf
DBU-Naturerbeflächen – Ökologische Dynamik zwischen Offenland und Wald.
Available online: (https://www.dbu.de/OPAC/ep/Ergebnisse-
Stipendienschwerpunkt.pdf
Conference contributions:
2019 Schellenberg J „North-German lowland heathland plant communities and
their potential nature conservation value“. Talk. European Heathland
Workshop 2019. 23.08.2019. Dorset, UK.
2017 Schellenberg J „Rethinking relations between heather plant age, growth
stages and vitality“. Talk. European Heathland Workshop 2017. 21.08.2017.
Nijmegen, Netherlands.
Academic CV
146
Memberships
Floristisch-Soziologische Arbeitsgemeinschaft (FlorSoz)
European Heathland Network
