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D E PA RT M E N T O F G E O S C I E N C E S A N D
N AT U R A L R E S O U RC E M A N A G E M E N T
university of copenhagen
Sebastián Kepfer Rojas
Vegetation dynamics and community
assembly in post-agricultural heathland
D E PA RT M E N T O F G E O S C I E N C E S A N D
N AT U R A L R E S O U RC E M A N A G E M E N T
university of copenhagen
Sebastián Kepfer Rojas
Vegetation dynamics and community
assembly in post-agricultural heathland
Title Vegetation dynamics and community assembly in
post-agricultural heathland
Author Sebastián Kepfer Rojas
Citation Rojas, S.K. (2014): Vegetation dynamics and community
assembly in post-agricultural heathland. IGN PhD Thesis
December 2014. Department of Geosciences and Natural Resource Management, University of Copenhagen,
Frederiksberg. 46 pp
Publisher Department of Geosciences and
Natural Resource Management
University of Copenhagen
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PREFACE
A bit over 3 years ago I embarked at my PhD at the Department of Geosciences and Nature
Resource Management at the University of Copenhagen. This PhD evolved in a different direction
than was originally planned. When I first started, Nørholm heathland was going to be only part of
my dissertation. After participating in fieldwork and some months of working with the historical
dataset, the ecological relevance of this wonderful area became clear. The more I familiarized with
the history of Nørholm, the more interesting ecological questions and patterns arose which
ultimately led me to dedicate my PhD study solely to this site.
Coming from Guatemala, most of my experience in ecology and conservation is in tropical
ecosystems. This has, in many ways shaped the way I perceive and think about nature. Observing
the overwhelming diversity of species that coexist in relatively small areas is difficult not to wonder
how the few requirements organisms have can lead to these immensely complex systems. This
has undoubtedly contributed to my interest for alternative or perhaps, complementary explanations
for the coexistence of species and the structure of ecological communities.
During this PhD I had the opportunity to explore some of these alternatives on a contrastingly
different system: heathlands. The “simplicity” of this ecosystem and the close connection to human
activities challenged my preconceived views on nature and nature conservation. Somewhat
idealistically or maybe just naively, I believe that conservation of nature should aim at removing or
at least reducing the influence of anthropogenic impacts on ecosystems and not necessarily lead
to a predefined state but rather a state shaped by ecological and evolutionary processes.
This raises the question on whether conservation efforts should be allocated at managing areas to
maintain a predefined state or should we leave natural processes take over?
To answer this question, evidence and knowledge on the consequences of these options need to
be gathered. This PhD presents a study of the development of a plant community which has been
without direct human intervention for over a century. Hopefully, this will contribute to answering this
question.
September, 2014
Sebastián Kepfer Rojas
3
ACKNOWLEDGEMENTS
I would like to start by expressing my gratitude to my supervisors Inger Kappel Schmidt and Vivian
Kvist Johannsen for allowing me the opportunity to follow my own research interests and ideas; for
allowing to play with this wonderful data and “travel in time”; and for supporting me not only
academically but also in tough times, thank you for your understanding. The same gratitude
extends to Annemarie Bastrup-Birk, for guidance and support at initial periods of my PhD.
I would like to thank the people at the Section of Forest, Nature and Biomass, especially Torben
Riis-Nielsen for sharing his expertise in heathland ecology and botany; Thomas Nord-Larsen, for
advising and checking up on me; Barbro Haar and Oksana Korsgaard for helping me with all the
administrative issues and simply making work-life simpler; and all my fellow PhD /friends: Lucia,
Johannes S., Ludovika, Yoppi (it was great sharing an office with you), Johannes R., Jonas, Mette,
Nanna, Davide, Carmen, Andy, Petros, Teresa, Michael, Noah, Rikke, Geshere, Claudia, Seid,
Marie, Pia, Mads, Heng, Søren and Anders, thanks for the good times. Johannes R., thanks for
commentaries on my thesis and for the academic, political, social, cultural and what not
discussions. Mette, thanks for helping with the Danish summary.
During this PhD I also had the enriching opportunity to work along with researchers from external
institutes. Special thanks to Kris Verheyen who acted almost as an external supervisor, your
guidance and advice was instrumental for this PhD. Similarly, thanks to Christian Damgaard for
welcoming my visit and introducing me to the world of structural equation modeling.
I am also grateful to Francesco de Bello, Bill Shipley, Hanna Tuomisto, Nicholas Gotelli, Jacob
Weiner and Anne Magurran for their willingness to provide advice and for taking the time to answer
my questions; your help got me back in track.
This work could not have been possible without the visionary work of I.K. Rosenørn-Teilmann, and
C.H. Bornebush from “Forstlige Forsøgsvæsen”, who initiated the conservation action and the
long-term survey at Nørholm Heath more than 100 years ago. In the same lines, former owners
and the current owners, Martha and Karl Nielsen are thanked for welcoming the research.
Further, I thank Allan O. Nielsen, Xhevat Haliti, Jane Kongstad, Geshere Abdisa, Annelies Van der
Craats and Karen Sverrild and many others for contributing in collecting this wonderful data and
Preben Frederiksen for help with the soil analysis.
4
On a more personal level I thank my family in Guatemala (Rodolfo, Eugenia, Walter and José),
infinitas gracias por todo. Min vidunderlige svigerfamilie: Lars, Gitte og Søren. Tak, tusind tak, I har
virkelig gjort det bedre for os.
And last but never least, Pia, thank you for your support, love and for always being concerned
about my happiness. Nikolas and Matias, you were born the day before the second interview for
the PhD position, so it is fair to say that you have accompanied me along the whole way. Although
I have learned a lot about myself during this PhD, nothing compares to what I have learned from
being your Papa, los amo.
5
TABLE OF CONTENTS
PREFACE ..................................................................................................................................................................................3
ACKNOWLEDGEMENTS .......................................................................................................................................................... 4
TABLE OF CONTENTS ............................................................................................................................................................. 6
SUMMARIES ............................................................................................................................................................................. 7
LIST OF PAPERS .................................................................................................................................................................... 12
GENERAL INTRODUCTION.................................................................................................................................................... 13
PAPER 1.
DISTANCE TO SEED SOURCES AND LAND USE HISTORY AFFECT FOREST DEVELOPMENT
OVER A LONG TERM HEATHLAND TO FOREST SUCCESSION ................................................................... ..33
PAPER 2- HINTS FOR ALTERNATIVE STABLE STATES FROM LONG-TERM VEGETATION DYNAMICS
IN AN UNMANAGED HEATHLAND ..................................................................................................................... 53
PAPER 3.
INDIRECT EFFECTS OF LAND USE LEGACIES DETERMINE TREE COLONIZATION PATTERNS
IN ABANDONED HEATHLAND ........................................................................................................................... 71
PAPER 4.
INTERACTIVE EFFECTS OF LAND-USE HISTORY, TREE ENCROACHMENT AND DISTANCE TO
EDGE ON SPECIES RICHNESS OF GROUND VEGETATION IN A SUCCESSIONAL HEATHLAND .............. 92
SUMMARY AND SYNTHESIS ............................................................................................................................................... 119
6
SUMMARIES
ENGLISH SUMMARY
The structure and the assembly of plant communities are a result of historical anthropogenic
activities and natural phenomena.
Understanding and distinguishing between the underlying
mechanisms is a challenging but integral part of ecological studies and conservation planning.
Ecological theory proposes that biotic, abiotic and stochastic factors act as “ecological filters” to
determine the assembly and structure of local communities. The functional strategies of the
species in community play a central role as they interact with these filters to determine the
presence and abundance of species in a community.
This PhD study aims at understanding how biotic, abiotic and stochastic factors interact to
structure a heathland community managed under different traditional land-use practices for
centuries. Agriculture ceased in 1865 whereas low intensity grazing occurred until 1895, when
traditional management was abandoned at the heathland. I explore the general hypothesis that the
strength of biotic factors varies along abiotic gradients (i.e. soil fertility) and with the functional
strategies of functional groups in the community (trees, herbs and dwarf shrubs).
The data used in this work is part of one of the longest spontaneous successional studies of
heathland vegetation, where tree colonization and understory vegetation patterns were measured
in successive vegetation surveys initiated in 1921. This data was complemented with an intensive
survey of the vegetation and ecological factors undertaken between 2009 and 2012.
I found that even after a century after abandonment of agricultural practices, land-use legacies
were still present in the soil and were important determinants of vegetation dynamics and
community assembly. However, the effects of land-use legacies were mostly mediated by the
understory vegetation and differed according to the functional groups. The distance to the edge, a
proxy for the proximity to external seed sources, was arguably the most important factor affecting
different components of the structure of the tree/shrub community, particularly at early stages.
Similarly, the distance to the edge was also an important determinant of understory vegetation
patterns, demonstrating the importance of dispersal in the development of the community.
Furthermore, these results suggest a conceptual framework for the development of this heathland
community. This framework proposes that the effect of the biotic interactions varies along abiotic
gradients (e.g. soil fertility) and interacts with the functional strategies of species to determine the
establishment of colonizing species, species’ performances and diversity patterns in the local
community. This framework has broader implications for understanding the maintenance of
7
biodiversity, the csideoexistence of species and the stability of heathland communities, which can
be helpful when designing conservation and management actions for this threatened habitat.
“Plants are evidently in general, tolerably impartial as
regards soil, if we except certain chemical and physical
extremes (abundance of common salt, of lime, or of
water), so long as they have not competitors"
Eugenius Warming, Oecology of Plants (1909)
8
DANSK RESUMÉ
Sammensætning og struktur af plantesamfund er et resultat af historiske, menneskeskabte aktiviteter
og naturlige fænomener. At kunne forstå og skelne imellem de underliggende mekanismer er en
udfordrende, men integreret del af økologiske studier og naturforvaltning. Den økologiske teori foreslår
at biotiske, abiotiske og stokastiske faktorer fungerer som "økologiske filtre" til at bestemme
sammensætning og struktur i plantesamfund. Arternes funktionelle strategier spiller en central rolle, da
de interagerer med disse filtre og dermed bestemmer tilstedeværelsen og tætheden af arter i et
samfund.
Dette ph.d.-studie har til formål at forstå, hvordan biotiske, abiotiske og stokastiske faktorer interagerer
og former vegetationen på en hede forvaltet under forskellige, traditionelle arealanvendelser i
århundreder, før dyrkningen ophørte i 1865 og græsningen i 1895. Jeg udforsker den generelle
hypotese, at styrken af biotiske faktorer varierer langs abiotiske gradienter (dvs. jordens
næringsindhold) og med de funktionelle strategier i plantesamfundets funktionelle grupper (træer, urter
og dværgbuske).
De data, der anvendes i dette arbejde, er en af de længste spontane successionalstudier af lynghede,
hvor kolonisering af træer og bundvegetationsmønstre er målt i en vegetationsundersøgelse indledt i
1921. Disse data blev suppleret med en intensiv undersøgelse af vegetation og økologiske faktorer
foretaget imellem 2009 og 2012.
Jeg fandt, at selv et århundrede efter opgivelse af landbrugsdrift, var der stadig forskelle i jorden
relateret til tidligere arealanvendelse og at disse forskelle var afgørende for vegetationsdynamik og
sammensætningen af plantesamfundet. Dog var effekten af tidligere arealanvendelse primært
medieret af bundvegetationen og varierede i forhold til de funktionelle grupper. Afstanden til kanten af
heden, en proxy for nærhed til eksterne frøkilder, var uden tvivl den vigtigste faktor, der påvirkede de
forskellige dele af strukturen af træ/busksamfundet, især i de tidlige faser af successionen. Afstanden
til kanten var ligeledes også en afgørende faktor for dynamikken i bundvegetationen, hvilket viser
betydningen af spredning for udviklingen af samfundet.
Disse
resultater
tyder
desuden
på
en
konceptuel
ramme
for
udviklingen
af
dette
dværgbuskhedesamfund. Denne ramme indikerer, at effekten af de biotiske interaktioner varierer langs
abiotiske gradienter (f.eks. jordens frugtbarhed) og med funktionelle strategier af arter, og er
bestemmende for etablering af koloniserende arter, arters ydeevne og mangfoldighed i
plantesamfundet. Denne ramme har stor betydning for forståelsen af bevarelse af biodiversitet,
sameksistens og stabilitet af dværgbuskheder. Det kan være nyttigt, når naturbeskyttelse og
forvaltningsplaner skal designes for denne sårbare naturtype.
9
RESUMEN EN ESPAÑOL
La estructura y ensamblaje de las comunidades vegetales son el resultado de actividades
antropogénicas históricas y fenómenos naturales . Comprender y distinguir entre los mecanismos
subyacentes es una parte difícil pero integral de los estudios ecológicos y planes de conservación.
La teoría ecológica propone que factores bióticos , abióticos y estocásticos actúan como " filtros
ecológicos" para determinar la estructura de ensamblaje y de las comunidades locales. Las
estrategias funcionales de las especies en la comunidad juegan un papel central, ya que
interactúan con estos filtros para determinar la presencia y abundancia de las especies en una
comunidad.
Este estudio de doctorado tiene como objetivo la comprensión de cómo los componentes bióticos,
abióticos y estocásticos interactúan para estructurar una comunidad de brezal manejada bajo
diferentes prácticas tradicionales de uso de la tierra por siglos antes de su abandono en 1865.
Asimismo, se explora la hipótesis general de que la magnitud de los factores bióticos varía a lo
largo de gradientes abióticos (e.g., la fertilidad del suelo) y con las estrategias funcionales de
grupos funcionales en la comunidad (árboles , hierbas y arbustos) .
Los datos utilizados en este trabajo forman parte de uno de los más largos estudios de sucesión
espontánea de vegetación de brezales, donde la colonización de árboles y los patrones de
vegetación del suelo fueron registrados en un estudio iniciado en 1921. Estos datos se
complementaron con un estudio intensivo de la vegetación y factores ecológicos llevado a cabo
entre 2009 y 2012.
Se encontró que incluso después de un siglo del abandono de las prácticas agrícolas, los legados
de la agricultura todavía estaban presentes en el suelo y fueron importantes en la determinación
de la dinámica de la vegetación y el ensamblaje de la comunidad. Sin embargo, los efectos del
legado del uso de la tierra fueron mediados principalmente por la vegetación del suelo y difieren
según los grupos funcionales. La distancia al borde del brezal, un indicador de la proximidad a las
fuentes externas de semillas, fue posiblemente el factor más importante afectando a los diferentes
componentes de la estructura de la comunidad de árboles, sobre todo en las etapas iniciales. Del
mismo modo , la distancia hasta el borde fue un factor determinante de los patrones de vegetación
del suelo, demostrando la importancia de la dispersión en el desarrollo de la comunidad .
Además, estos resultados sugieren un marco conceptual para el desarrollo de ésta comunidad.
Este marco propone que el efecto de las interacciones bióticas varía a lo largo de gradientes
abióticos (por ejemplo, de fertilidad del suelo) e interactúa con las estrategias funcionales de las
10
especies para determinar el establecimiento de especies colonizadoras, el rendimiento de las
especies y los patrones de diversidad en la comunidad local. Este marco tiene implicaciones más
amplias para la comprensión de la conservación de la biodiversidad, la convivencia y la estabilidad
de las comunidades de brezales que pueden ser útiles al momento de diseñar acciones de
conservación y gestión de éste tipo de hábitat.
11
12
GENERAL INTRODUCTION
RAPIDLY CHANGING ECOSYSTEMS ON A HUMAN-DOMINATED PLANET
We live in a human dominated planet with a total population of approximately 7 billion. Meeting the
growing demands of humans has led to more rapid and extensive changes in ecosystems over the
last 50 years than in any comparable period of time in human history (Millenium Ecosystems
Assessment, 2005). These staggering demands affects natural ecosystems and biodiversity
through different interrelated processes (Ellis et al. 2013). Among them, land-use changes, plays a
primary role (Foley et al. 2005; Foley et al. 2011).
Land-use change is considered the major threat to terrestrial and marine ecosystems globally
(Vitousek et al. 1997; Sala et al. 2000) and is strongly linked to economic development (Flinn &
Marks, 2007; Foster et al., 2003; Verheyen et al., 2003). Following the pace of industrialization;
intensification and technification of agricultural practices led to high levels of deforestation in North
America and Europe until the first half of the 20th century (Flinn & Vellend 2005). Hereafter,
following a change to a service economy coupled with human exodus to urban areas, an inversion
of the direction of change occurred in some areas (Verheyen et al. 1999; Flinn & Marks 2007;
Améztegui et al. 2010). Extensive former agricultural areas were abandoned, giving place to
reestablishment of forests.
In Denmark the general trend has been similar, although the magnitude of change has been quite
dramatic. At the onset of the 19th century, forest cover was reduced to a mere 3-4 % (Plum 1989).
Since then, forest cover has slowly increased to the current level of ca. 14 % (Nord Larsen et al.
2013). Although afforestation has been mainly driven by economic incentives, international
agreements on conservation of biodiversity (e.g. Nagoya protocol), have set ambitious goals to halt
and reverse the negative trends. A strategic part of these plans in Europe consists of conservation
and restoration of semi-natural and forest habitat areas considered to be important for biodiversity
(Habitat Directive; Natura2000) and, in the case of Denmark, of further increases in the area
covered by forest (Skov og Natustyrelsen 2002; Petersen et al. 2012).
Due to the intensive and extensive modifications to landscapes and ecosystems by former
agriculture, expansion of current nature reserves or establishment of new ones requires
reclamation of agricultural areas with different agricultural history. An implication is that nature
conservation has to be considered within an agricultural context and that the effects of
environmental legacies of previous agricultural practices have to be understood (Perrings et al.
2006). A necessary first step then is to determine the impact of land-use legacies on the different
components of ecosystems and ecological communities.
13
In a step towards this direction, this thesis makes use of a long-term monitoring dataset
complemented with an intensive survey of current vegetation and ecological properties to examine
the effect of land-use change on the development of the vegetation at Nørhom heathland (RiisNielsen et al. 2005).The long-term data series enables the study of fundamental ecological
processes and provides a solid basis for understanding the current patterns in the vegetation.
Central to this work is to understand the impact and determine the importance of land-use legacies
on the structure, dynamics and assembly of the vegetation community. In this section, I first
describe the ecological foundations and the general conceptual framework that motivated and
support this work. Second, I present the objectives. Third, I briefly introduce the study system,
highlighting the features that make it a model system and unique site to study vegetation
dynamics. Fourth, I summarize the methods used, and finally, I give a short overview on the
papers included in this thesis.
A GENERAL FRAMEWORK FOR DEALING WITH THE COMPLEXITY OF ECOLOGICAL COMMUNITIES
A longstanding and fundamental goal in ecology is to understand the processes that determine the
structure of communities. This has proven to be a difficult task. Attempts to find a general law of
community organization have focused in concepts including: keystone predation (Paine 1966),
niche theory (McArthur and Levins 1967), energy flow (Odum, 1969), regeneration dynamics
(Grubb 1977), resource competition (Tilman 1982), neutrality (Hubbell 2001) and metabolic theory
(Brown 2004). Although these concepts have greatly advanced ecological theory, some limitations
have emerged when these hypotheses have been put to empirical test (Roughgarden 1996,
Lawton 1999).
The lack of a general theory of community organization led to strong criticism of community
ecology as a scientific discipline (Lawton, 1999). An important reason for the failure of developing
a general theory is that community structure is highly contingent (Lawton 1999; Simberloff 2004).
At local scales, the interactions between organisms with each other and with their environment are
so complex and site dependent, that even when ecological studies can decipher them, the results
are not likely to be transferable to other sites, even when environmental and historical conditions
are similar (Lawton 1999). Ecologists advocating in favor of community ecological studies argue
though that lack of generalization should not render abandonment of ecological studies at local
scales; but that it does require a new method of study (Keddy 1992; Simberloff 2004;
Roughgarden 2009, McGill 2006). In this matter, Roughgarden (2009) writes: “the sciences rarely
deliver exceptionless generalizations and scientific effort instead may be directed toward finding an
14
‘‘invariant toolkit’’ of mechanisms that yield a variety of outcomes resulting from different interplays
among the mechanisms in various situations”. In other words, when attempting to explain the
factors that determine the local structures of communities, hypotheses on interrelated and
multifactorial control have to be considered and contingencies have to be taken into account
(Grace, 1999).
Renewed
interest
in
community
assembly
during the last 20 years, has directed much of
its effort in reformulating a framework through
which community structure can be studied
(Belyea & Lancaster 1999; McGill et al. 2006;
Weiher et al. 2011; HilleRisLambers et al.
2012). The idea behind this framework (Fig. 1.1)
is that species from the regional pool need to
pass a series of biotic, abiotic and dispersal
filters to finally become members of the local
communities (Zobel 1992; Belyea & Lancaster
1999).
These filters act in a hierarchical multifaceted
manner to determine the identity, number and
abundance of the different species (Bello et al.
2013). More concretely, at the scale of local
communities, abiotic factors (topography, water
availability, soil fertility) select species from the
species pool with the necessary physiological
adaptations, reducing the species pool to those
that can withstand the local conditions (Grime
2006). At finer scales, biotic interactions will
vary along the local environmental gradients to
FIGURE 1.1. Community assembly framework.
Local communities are subsets of the regional
species pool that pass through biotic and
abiotic filters. Dispersal limitation and chance
influence the ability of species to pass the
filters. Once species establish in the local
communities, feedbacks from species
interactions and species´ effects on the
environment modify the filters. Modified from
HilleRisLambers et al. (2012).
determine which species persist and become
dominant. A necessary requirement is though that the species possess the required functional
adaptations to colonize and establish at a local community (dispersal filters).
The “filtering paradigm” is embedded within traditional ecological theory on community structure
mechanisms. At the core of most of these theories are the differences in life history and functional
traits of species and how they mediate the performance of species in different biotic and abiotic
15
milieus. Basic niche theory predicts a limit to the similarity between coexisting species (Abrams
1983). According to the “competitive exclusion principle” (Grime 1973), ecologically similar species
(i.e. similar life history/functional traits) cannot coexist because the best competitor will always
outcompete the others. However, a certain degree of similarity is also predicted because
“environmental filters” select species with the necessary and thus similar adaptations (particularly
at harsh environments).
The balance between these opposing forces can vary according to environmental gradients and is
largely determined by the functional and life-history traits of species. The importance of these
mechanisms varies depending on local site conditions and on the presence of different functional
groups in the community (McGill et al. 2006). For instance, in nutrient poor environments the
success of perennial species is determined by their ability to conserve rather than capture mineral
resources and species possessing traits for this type of strategy are favored (Grime 1979, Aerts
1999). However, if nutrients become available, species that can capture resources more effectively
can have the advantage thus shifting the balance of competitive strength between these groups
(Aerts and Heil, 1993).
As mentioned above dispersal is another important factor structuring communities (Bullock 2002).
However, a successful colonization depends not only on effective dispersal. Local site conditions
and the availability of open space can determine establishment of colonizers (Ehrlén & Eriksson
2000; Myers & Harms 2011). Similarly to species performances, colonization is determined by the
interplay between local environmental conditions, biotic interactions and life history traits of
colonizers. For example, on a nutrient availability gradient, productivity is usually higher at high
nutrient levels. The more vigorous, established vegetation can then limit colonization of other
species due an increase in its competitive strength (Jurena & Archer 2003; Chauchard et al. 2007).
However, the degree to which establishment of colonizers is limited depends on the life history
traits of colonizing species (Ehrlén & Eriksson 2000).
Colonization/competition trade-offs are
typically invoked as being responsible for the differences in colonization success (Tilman 1993;
Westoby et al. 2002). There is a trade-off between the ability to colonize and the ability to compete
so that the best competitor cannot displace all other species in the area because it is a poor
colonizer. New openings in the vegetation (as caused by disturbances) allow poor competitors to
colonize and persist even in the presence of superior competitors (Tilman 1982).
Clearly, the ideas of the filtering framework are very appealing when studying local community
structure as they provide a flexible framework to identify the mechanisms that operate in different
situations and on when they might be the dominant structuring force (rather than pursuing to find a
single unifying mechanism). When combined with information on the life history strategies of
16
functional groups a more mechanistic and rigorous theory on community structure can arise (Mcgill
2006). By considering how the influence of structuring forces varies across environmental
gradients and how they interact with different functional strategies, it is possible to evaluate the
large range of factors and mechanisms that determine the structure and assembly of communities.
TEMPORAL DYNAMICS
Up to this point, community assembly has been presented as the outcome of the structuring forces
acting upon communities. In the majority of ecological studies, communities are typically studied at
fixed point in time, i.e. when the effects of assembly processes have exerted its influence in the
community; without considering historical processes. This provides a narrow view, as in many
cases the influence of multiple interacting factors can obscure underlying mechanisms (Chase &
Myers 2011). Long-term vegetation studies consisting of repeated measurements of the vegetation
offer a better opportunity to disentangle the effect of interacting mechanisms, to compare the
relative magnitude and importance of their effects, and to determine when and how they change
over time (Bakker et al. 1996; Rees et al. 2001).
Studies of long-term vegetation dynamics have traditionally focused on the concept of vegetation
succession (sensu Cowles 1899), i.e. the orderly replacement of species composition along a
temporal scale (after a disturbance in secondary succession). Similarly, community assembly
refers to the temporal changes in species composition over time, however, community
development is determined by random colonization of species and by the difference in the
likelihood of establishment and persistence of colonizers (Young et al. 2001). There is a subtle but
important difference between the two concepts: Community assembly allows for a more stochastic
view of vegetation change, where historical factors, random colonization and species interactions
determine the outcome and often lead to multiple stable states (Chase 2003).
The debate on whether communities develop in a deterministic or stochastic manner dates back to
the early work of plant ecologists like Clements (1916, 1938) and Gleason (1926, 1927). According
to Clements, succession proceeded through a series of states towards a final stable state
(“climax”) in a more or less predictable way, even when the starting vegetation state was different.
Gleason´s, and later Egler´s (1954) views, differed in that community development was determined
by stochastic dispersal events and that the order of arrival of species could determine different
stable endpoints (multiple stable states). Species arriving first could become dominant and then
inhibit colonization by others species, either because first arrivers pre-empt space and resources
17
or through plant-soil feedbacks. An important point is that, in order to demonstrate the occurrence
of multiple stable states, it is necessary that the initial environmental conditions are identical and
that all species have access to the locality (Connell and Sousa 1983), which is rarely the case in
field studies.
Current views on the importance of stochastic vs deterministic processes affecting the structure of
communities have moved away from considering them as mutually exclusive phenomena and
recognize that both processes may act simultaneously (Gravel et al. 2006; Chase & Myers 2011).
Focus has now moved to discerning the strength of these processes along environmental
gradients, history of assemblage space and time (Chase & Myers 2011). With respect to the latter,
Stokes and Archer (2010) proposed a modification to the filter paradigm to incorporate a change in
the importance of structuring forces, from stochastic in early stages after disturbance, to
deterministic at later phases of development (Weiher and Keddy 1999; McGill et al. 2006). The
rationale for that can be traced back to the seminal work of Gleason (1926), who observed that
immediately after disturbances, colonization is not strongly constrained by abiotic and biotic factors
and thus dispersal limitation is the prominent structuring force. As vegetation develops and the
abiotic conditions are modified, environmental selection and biotic interactions become the driving
force.
Despite the limitations that come along with long-term monitoring programs, the long-term dataset
used in this thesis provides an opportunity to examine whether different structuring forces operate
at different points in time and to draw insights on possible underlying mechanisms and infer on
their relative importance.
HEATHLANDS
Outside the natural occurring areas, the vast majority of the north-west European lowland
heathlands (as the one in this study) are closely linked to anthropogenic activities (Gimingham
1979, Gimingham and Schmidt 1983). It is currently accepted that the origin of this type of
heathland can be traced back to the Neolithic period (ca. 2500 B.C.) when nomadic farmers
cleared shrubs and woodlands to establish cultivation fields (Aerts and Heil 1993). Up until the turn
of the 20th century, heathlands dominated the landscape of many north European countries and
were part of the traditional agricultural system. With the advent of modern agricultural techniques
and artificial fertilization, the extension of heathlands has decreased severely and many of the
remaining heathlands occur in isolated and fragmented areas (Piessens et al. 2005).
18
Heathland communities are often dominated by schlerophyllous vegetation from the Ericaceae
family (ericoid dwarf shrubs). Dominant species typically vary from Calluna vulgaris and Empetrum
nigrum at dry heathlands to Erica tetralix in high moisture sites (Aerts and Heil 1993). Under
natural conditions grasses like Deschampsia flexuosa and Molinia caerulea are also present in
heathland communities. These groups (dwarf shrubs and grasses) present two diametrically
contrasting functional strategies. While, dwarf shrubs possess traits characteristic of a resource
conservation strategy (e.g. slow growth rates, low tissue turnover and thick leaves), grasses are
adapted to a rapid resource acquisition (e.g. faster growth rates, high tissue turnover and thin
leaves).
These contrasting strategies are not only key for the coexistence between these groups, but they
also determine the outcome of their interactions (Aerts & Berendse 1988; Aerts & Peijl 1993).
Hence, any factor that affects the availability of nutrients (e.g. atmospheric nitrogen deposition,
fertilization from agriculture) can disrupt this coexistence mechanism (Aerts and Bobbink 1998;
Mitchell et al. 2000).
Traditional agricultural practices in heathlands involved natural fertilization and tillage resulting in
soils with reduced organic matter and increased nitrogen and phosphorus (Webb 1998; von
Oheimb et al. 2008). Increased nutrient availability can then affect the stability of heathlands and
trigger the transition to a grassland or woodland (Bakker & Berendse 1999).
Post-agricultural heathlands present a model setting to study vegetation dynamics and community
assembly, for many reasons: 1. The harsh environmental conditions present a pervasive abiotic
filter, selecting for species with the necessary adaptations; 2. Land-use legacies and tree
colonization can alter the levels of nutrient availability and light levels, modifying the abiotic filter; 3.
The coexistence and balance of biotic interactions (biotic filter) of common functional groups with
distinctive and almost opposing functional strategies is altered by the modification to abiotic
conditions; and 4. Because of few species and contrasting functional groups, heathlands are
relatively “simple” communities to study ecological processes. Moreover, because of the
vulnerability of heathlands to current land use practices, most of the remaining areas are situated
in nature reserves and depend on some type of management.
Therefore, understanding the
mechanisms involved in structuring heathland communities is necessary as a basis for
conservation, management and restoration of these communities.
19
AIMS OF THE STUDY
This thesis used long-term and current vegetation patterns to identify how biotic, abiotic,
historical and stochastic factors interact to structure a heathland plant community
undergoing natural development. Central to this thesis was to identify whether the importance of
these structuring factors vary in time and with functional strategies of the species in the
community.
The specific aims of this thesis were to:
Ͳ
Evaluate the importance of stochastic vs deterministic factors on vegetation dynamics
(Paper 1, 2 and 4)
Ͳ
Assess the importance of land-use legacies as determinants of community structure (Paper
1, 2, 3 and 4)
Ͳ
Determine the effects of biotic, abiotic and stochastic factors differ according to functional
groups (Paper 2, 3 and 4).
Ͳ
Assess the relative importance of direct and indirect effects of abiotic, biotic and stochastic
factors as determinants of diversity patterns (Paper 1 and 4)
20
MATERIAL AND METHODS
NØRHOLM: A unique heathland
Nørholm (NH) is the subject of this thesis and has formerly been the subject of a series of
ecological studies. Detailed topographic, climatic and geological descriptions of NH can be found
in Hansen (1932), Opperman and Bornebush (1930), Riis-Nielsen et al. (2005). In addition, the
papers in this thesis include descriptions of the site and specific methods relevant to each study.
Instead of making an exhaustive description, in this section I will only outline the most relevant
ecological and historical processes that have influenced the development of the vegetation and
briefly summarize the methods used in this thesis.
NH is a 350 ha heathland in the southwestern part of the Jutland peninsula in Denmark (Fig 1.2A).
As most of the Atlantic European lowland heathlands, Nørholm is strongly linked to human
activities (Webb 1998). Following the introduction of agriculture (~4000 BC), the area covered by
forest in Denmark decreased giving place to heathland vegetation and agricultural fields (Nielsen
et al. 2010). In the Jutland peninsula, heathlands were a main component of the landscape
between 1000 BC- 1900 AD (Riis-Nielsen et al. 2005; Nielsen et al. 2010). During this period, NH
was managed under traditional management practices, consisting of a so called “infield /outfield
system. In this type of system, different areas in a farm were utilized at different levels of intensity.
In NH, the infields were cultivated while the outfields were used for grazing. In winter periods,
grazing animals were kept in stables were their manure was collected and applied in the infields as
natural fertilizer, transferring nutrients to the agricultural fields (Christiansen 1978; Webb 1998).
This type of system had a remarkable influence on the abiotic environment due to the mobilization
of nutrients, alteration to the physical soil structure and removal of vegetation that accompanied
ploughing in the infields. This system was maintained until abandonment of agricultural practices in
1865. Low intensity grazing continued until 1895 when NH was left without any human
management. Nowadays, the effect of land-use legacies is still evident in the soil properties. For
example, phosphorus concentrations are clearly higher in the former infields (Fig 1.2B).
In 1913, the owner of NH initiated actions that led to the protection of the heathland with the
objective of conserving it at its “natural condition” (Hansen 1932). At that time, livestock grazing
was considered one of the main threats to heathland vegetation. To protect the heathland from
grazing, a hedge row of mountain pine (Pinus mugo) was planted along the south and east borders
of the heathland. This event had a tremendous impact on the development of the vegetation. The
21
pine dispersed and established widely into the heathland. In addition, scarce forest remnants
enhanced colonization by other pioneer tree species. Tree colonization occurred in an exponential
way, increasing from about 1200 individuals in 1920´s to ca. 900,000 at present time. Currently,
forest covers ca. 30 % of the heathland (Fig 1.2C and Fig 1.3).
FIGURE 1.2. Map of NH (A) showing the grid used for tree registration and the position of the vegetation
plots for the 2009-2012 survey and permanent vegetation plots. The thick line separates the cultivated area
to the West and the uncultivated to the East. The inlet shows the location of the study site in Denmark.
Predicted total phosphorus content (B) obtained by regression kriging using topographical variables as
predictors (R2 = 0.62). Vegetation height classification map (C) obtained from LiDAR images acquired in
2007.
Although the land-use development and the landscape context of NH are typical of other sites in
Denmark and Europe, there are important aspects that make NH a unique and important site for
conservation and ecological research. First, the land-use history and the development of the
vegetation are very well known. A series of aerial photographs, cartographic and cadaster records
have been used to reconstruct the land-use history to a great detail. In addition, a monitoring
program initiated in 1921 has systematically registered changes in the vegetation using permanent
plots and tree colonization surveys. These surveys have been done in 10 occasions (11 for
permanent plot) at irregular intervals spanning over 90 years. To our knowledge this is one of the
longest spontaneous succession vegetation surveys.
22
Second, NH has not been managed for over 100 years. Long-term studies of spontaneous plant
secondary succession are in general rare, and even more so for heathlands. As mentioned before,
because of the conservation status of heathland in Europe and in Denmark, the majority of the
areas are maintained under some type of management actions (e.g. burning, grazing, sod cutting,
tree removal) aiming at controlling invasion by grasses and trees (Pywell et al. 2011).
Third, in spite of the lack of management, typical heathland vegetation has been remarkably stable
in NH. In other abandoned heathlands, tree and grass colonization is known to occur within few
decades, and usually results on drastic alterations to the vegetation (Hester et al. 1991; Manning
et al. 2004; Ascoli & Bovio 2010). A schematic description of the historical development of the
vegetation is given in Fig. 1.3.
FIGURE 1.3. Schematic development
of vegetation at Nørholm heathland.
Dashed lines are hypothesized
vegetation trends obtained from
vegetation studies in Denmark and in
the area (Odgaard & Rasmussen
2000; Nielsen et al. 2010). Full lines
correspond to measurements
obtained from a long term vegetation
study initiated in 1921 (see methods).
ᬅ = introduction of agriculture;
ᬆ = Cessation of agricultural
practices. Notice that the x-axis is not
scaled.
Vegetation communities are dynamic. Quantifying and trying to predict how communities change
has been a major task in ecological studies. The task is difficult because changes in vegetation
communities occur at a pace that cannot be covered by typical ecological studies. To bypass this
problem, ecologists have relied on chronosequences (i.e. space for time substitutions). Although,
these studies have been insightful and pivotal for successional studies, they have also been
23
criticized mainly because in most cases, the assumptions of the method are not likely to hold for
studies of plant communities and they are rarely tested (Johnson and Miyanishi 2008).
On the contrary, and in spite of some limitations, repeated measurements of vegetation are a
straightforward method to study long-term vegetation development over time (Bakker et al. 1996;
Rees et al. 2001; Chazdon 2008). However, depending on the type of plant community, vegetation
development can take several decades or even centuries and thus repeated measurement studies
are rarely available. In NH, the Royal Veterinary and Agricultural University, initiated a survey in
1921 to study vegetation changes and forest succession (Riis-Nielsen et al. 2005). Changes in
ground vegetation were recorded by means of 17 (later 20) permanent plots, each of 10 X 10 m.
Between 1921 and 2014, 11 vegetation surveys were performed. To study tree colonization,
individual trees were measured and registered using a 400 X 400 m grid of 33 quadrats covering
the heathland entirely (Fig 1.2.A). Between 1921 and 2014, 10 tree surveys were performed (RiisNielsen et al. 2005).
In this thesis, I first used the long-term tree surveys data (Paper 1, for methodological details) and
permanent vegetation plots (Paper 2, for methodological details) coupled to the historical records
to describe the long-term vegetation dynamics. This data was complemented with an intensive
survey (2009-2012) of 140 plots (0.03 ha) used to register trees and shrubs and 12 subplots (0.1
m2) nested in each plot (n = 1680) to register the understory vegetation (Fig. 1.2A). In addition, soil
samples, digital elevation models, full cover vegetation structure maps (LiDAR) were included in
analysis focusing on current patterns of tree seedlings colonization (Paper 3) and diversity of
understory vegetation (Paper 4); and to complement the long-term studies.
24
THESIS OUTLINE
GENERAL INTRODUCTION- Delimits the study and presents the theoretical background that
motivated this work.
PAPER 1- examines and compares the effects of land-use legacies and distance to seed sources
on the long-term development (100+ years) of emergent properties of the tree/shrub community´s
structure: species abundances, richness and composition.
PAPER 2- describes the long-term development (100+ years) of the understory vegetation using
permanent vegetation plots. Change in cover of species and functional groups are used to
determine whether the trajectories in vegetation development are deterministically determined by
agricultural legacies in the soil. The possibility of the presence of multiple stable states is raised.
PAPER 3- compares the patterns of tree and shrub seedling establishment between areas with
different land-use history and between species with different functional strategies to determine how
the importance of biotic interactions varies along a nutrient availability gradient.
PAPER 4- proposes a model of multivariate control of the diversity patterns of the understory
vegetation. Using structural equation models, the interacting effects of land-use legacies and forest
development on three functional groups are assessed.
SUMMARY AND SYNTHESIS- integrates the preceding papers and proposes a synthetic
framework for the development of the vegetation at Nørholm heathland since the abandonment of
traditional agricultural practices.
25
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Young, T.P., Chase, J.M., & Huddleston, R.T. 2001. Community succession and assembly.
Ecological Restoration 19: 5–18.
Zobel M. 1992. Plant species coexistence – the role of historical, evolutionary, and ecological
factors. Oikos 65: 314–320.
32
LIST OF PAPERS
1. Kepfer-Rojas, S., Schmidt, I. K., Ransijn, J., Riis-Nielsen, T., & Verheyen, K. (2014).
Distance to seed sources and land-use history affect forest development over a long-term
heathland
to
forest
succession.
Journal
of
Vegetation
Science,
n/a–n/a.
doi:10.1111/jvs.12203
(published in Journal of Vegetation Science)
2. Ransijn, J., Kepfer-Rojas, S., Schmidt, I. K., Riis-Nielsen, T., & Verheyen, K. (2014). Hints
for alternative stable states from long-term vegetation dynamics in an unmanaged
heathland.
(accepted for publication in Journal of Vegetation Science)
3. Kepfer-Rojas, S., Schmidt, I. K., Johannsen, V.K. & Verheyen, K. Indirect effects of land
use legacies determine tree colonization patterns in abandoned heathland.
(manuscript in preparation)
4. Kepfer-Rojas, S., Schmidt, I.K., Riis-Nielsen, T. & Damgaard, C. Interactive effects of landuse history, tree encroachment and distance to edge on species richness of ground
vegetation in a successional heathland.
(manuscript in preparation)
The Papers are not included in this version of WKe thesis due to copyright.
SUMMARY AND SYNTHESIS
The overall aim of this thesis was to study how historical, biotic, abiotic and stochastic factors
interact to structure plant communities and vegetation dynamics of a heathland undergoing
spontaneous development. More specifically, this thesis integrated long-term and current
information to evaluate the impact of land-use history and the proximity to seed sources on the
development of the overstory and understory vegetation.
Land-use legacies and distance to seed sources respectively played determinant roles affecting
the probabilities of establishment and dispersal after abandonment of agricultural practices. Thus,
differential effects of these factors on the structure of developing communities were identified. To
increase our understanding on how they influenced the dynamics and assemblage of vegetation
communities, this work focused on drawing inferences on the importance of these driving factors,
on the mechanisms underlying them, on whether and how they changed over time and on how
they interacted with life history and functional strategies of species.
In this chapter I first summarize how land-use legacies and proximity to seed sources affected
different properties of the structure of the community. Secondly, a synthetic framework for the
development of the vegetation is proposed; and finally, some perspectives for management and
future research at NH are given.
LAND-USE LEGACIES: DIRECT AND INDIRECT EFFECTS
An important first step to determine the impact of land-use legacies on the development of the
vegetation is to determine what these legacies consist of, and whether they are still present (Flinn
& Vellend 2005). Land-use legacies involve a series of processes that can potentially influence the
development of plant communities. The most obvious effects are the disturbance of the vegetation
and impacts on the soil properties (Flinn & Vellend 2005; Hermy & Verheyen 2007).
Based on the latest survey, it was confirmed that land-use legacies were still evident in the soil
even after more than one century since abandonment of agriculture. However, although nutrient
levels and pH were higher in the formerly cultivated area of the heathland, the effects of traditional
heathland agricultural practices are only moderate when compared to the more intense, modern
agriculture (Von Oheimb et al. 2008; Pywell et al. 2011). Even at this relatively lower intensity, the
impact of land-use was evident in many aspects of the development of the vegetation.
Nevertheless, the effect varied in magnitude and was dependent on the functional groups.
Arguably, the most obvious effect of land-use legacies was observed on the understory vegetation
(Paper 4). Higher nutrient availability directly affected the current species richness patterns.
However, this effect was only important for herbs (grasses and forbs), which responded directly to
increased nutrients by achieving higher cover and species number in the formerly cultivated area.
Importantly, species richness of herbs increased directly with increased availability of nutrients (i.e.
independent of species cover), supporting the notion that a release from an environmental filtering
increases the number of species that can coexist at a local community (Grime 2001, Craine 2009).
This effect was particularly important for forb species which were almost exclusively found in areas
with high nutrient availability, indicating that this particular functional group is limited by nutrient
availability.
On the other hand, land-use legacies did not affect the long-term patterns of species richness and
composition of the tree and shrub communities (Paper 1). However, the rate at which species
colonized was lower at the formerly cultivated areas (Paper 1). Coupled with the patterns of
seedling colonization (Paper 3), it was demonstrated that increased nutrient availability increased
the ability of the established vegetation to suppress colonization of tree species (an indirect effect
of land-use legacies). Higher productivity of faster growing species Deschampsia flexuosa, was
promoted by nutrient availability and consequently limited colonization of pioneer species with a
high dispersal and resource acquisition strategy (Paper 3), highlighting that the importance of biotic
interactions is a function of both environmental conditions and the relationship between functional
strategies of established and colonizing species.
As mentioned above, another important factor is the disturbance of the vegetation that follows
abandonment of agricultural fields (although not exclusively related to land-use legacies). When
the fields are abandoned, space for colonization becomes available. If the duration and intensity of
agriculture have depleted the seed sources, colonization becomes a “race for space” where life
history traits and dispersal limitation can be important determinants of the structure of the
assembling community (Cramer, 2008). This mechanism likely explained the long-term
development of the understory vegetation and the long-term increase in cover of grasses
independent of nutrient availability in the permanent plots (Paper 2).
To conclude, although effects of land-use legacies affected the development to the vegetation
widely, most of the effects were indirectly mediated by the effects of nutrient availability on biotic
interactions and priority effects. Importantly, even when the increase in nutrient availability was
only moderate, sustained changes in the development of the vegetation can occur.
DISTANCE TO SEED SOURCES AND DISPERSAL
Although, grass and tree encroachment are occurring at NH, the patterns observed show some
important deviations to what would be expected under an assumption of strict deterministic control
by soil properties. The long-term development of the tree and shrub community was only indirectly
determined by land-use legacies. Instead the distance to seed sources, a proxy for dispersal
limitation, was the single most important factor determining the abundance and identity of the
colonizing species (Paper 1). Similarly, the distance to the edge was an important determinant of
the distribution, abundance and diversity of the understory vegetation (Paper 4). Furthermore,
despite increased nutrient availability and lack of management, grass and tree encroachment have
been limited to some areas and ericoid species have been able to persist, even in areas with
higher nutrient availability (Paper 4). Likewise, the long-term changes in the composition of the
understory vegetation could not be directly associated to soil properties, but was rather explained
by the history of disturbance of the different plots which allowed colonization of grasses (Paper 2).
Altogether, these results demonstrate that stochastic factors like dispersal and history of
colonization are important factors structuring communities.
SYNTHETIC FRAMEWORK FOR INTERACTING DRIVERS OF VEGETATION DYNAMICS AND
COMMUNITY ASSEMBLY
This thesis demonstrates the wide applicability and flexibility of the filtering paradigm of community
assembly to understand changes in vegetation communities. Integrating the results from the longterm and the current vegetation analyses, a mechanistic conceptual framework of vegetation
dynamics and community assembly is proposed (Fig 6.1 and 6.2). This framework illustrates how
life history/functional traits (fig6.1A), species tolerances to abiotic conditions (fig6.1B) and species’
performances (that determine the outcome of biotic interactions), (Fig.1C) interacted over time to
structure this community.
FIGURE 6. 1. Relationship between functional traits, species tolerances to abiotic conditions and species
performances along resources gradients. The position of the functional groups along resource use and
establishment strategies (A), influence: 1) the tolerances to local abiotic conditions (shaded area) and the
abundances along this gradient (B); and 2) the performance of species along a resource gradient (C).
These factors work in a hierarchical way to determine species membership into local communities
(fig. 6.2). At the top level, the presence of species is constrained by abiotic conditions (fig. 6.1B
and fig 6.2). The nutrient poor and acidic soils in heathlands function as strong environmental
filters, limiting species membership into the local communities to those species with the necessary
functional adaptations. In this sense, the legacy of past agriculture has a direct effect, releasing the
community from this abiotic filter and allowing more species to colonize.
FIGURE 6.2. Synthetic filtering framework of community assembly at Nørholm heathland. Local community
assembly is presented as a function of time (X-axis) and distance to external sources (Y-axis at the bottom
of each panel). The local community assembles from species from the regional species pool (classified as
functional groups) passing through abiotic and biotic filters. Only species adapted to local conditions can
pass the abiotic filter. The effect of biotic interactions changes over time and depends on environmental
conditions and functional group feedbacks. Access to the local community is determined by
colonization/competition tradeoffs, mediated by environmental conditions. Curved arrows represent biotic
interactions and the functional group effect on local conditions. Symbols: as in fig 6.1A.
The effect of the release from the abiotic filter becomes evident first after abandonment of
management, because management actively removes species that otherwise could have
established.
Over the course of community assembly the abiotic filter may change if the colonizing species
modify the abiotic conditions. For instance, colonization by woody species can affect the soil
properties through plant soil feedbacks and by limiting light availability (Mason et al. 2012). These
novel conditions can then limit or facilitate further colonization by species depending on their
tolerances to and performances at the modified nutrient and light regimes (Cramer 2008). This is
exemplified by the decrease in the cover of dwarf shrub species and colonization of shade tolerant
species, (e.g. Deschampsia flexuosa, paper 4) under the developed tree canopy at later phases of
community assembly.
At the next hierarchical level, biotic interactions limit species membership into the local community.
This implies that even when species possess the necessary adaptations, they cannot establish in
the local community because other species outcompete them or simply because all available
space is already occupied by these species. In this sense, the occurrence and persistence of the
species along environmental gradients depends on how species’ performances and the outcome
of biotic interactions are determined by the local environmental conditions (fig 6.1C). Furthermore,
the susceptibility of the colonizing species to the biotic filter depends on the life history strategies
and functional trade-offs of the established and the colonizing species (Fig 6.1B). For instance, at
the poor extreme of the nutrient availability gradient, functional groups with a resource
conservation strategy (e.g. dwarfshrubs) can become dominant and further reduce access to the
nutrient pool, limiting colonization or hindering the performance of fast growing species like
grasses (Aerts & Peijl 1993; Aerts 1999). On the richer part of the nutrient gradient a combination
of rapid colonization and fast growth by grasses can lead to priority effects, preventing colonization
by pioneer trees (Paper 3), and/or suppressing dwarf shrubs (Paper 4).
A requirement for the biotic and abiotic filters to operate is that colonizing species need to have
access to the local community. Thus, the probability of different species colonizing the local
community is incorporated as another element in this framework (represented as the distance from
external sources in fig 6.1). In this sense, areas closer to seed sources are more likely to be
colonized. In situations where colonization is not limited by abiotic and biotic factors, stochastic
colonization can lead to a stochastic community assembly (Myers & Harms 2011). However when
biotic interactions are strong the likelihood of a stochastic community assembly decreases. The
stochastic component of the community assembly is expected to be stronger at initial stages and
to decrease in importance as vegetation develops and deterministic processes like competitive
exclusion and niche differentiation become more important (Stokes & Archer 2010), or because
priority effects become stronger over time in the absence of disturbances (Chase 2003).
Life history traits and trade-offs in functional strategies play a central role in the dynamics of the
vegetation and the assembly of the community. First, life history traits determine whether species
can pass the abiotic filter and access the local community. Second, resource use strategies can
determine the performance of species along environmental or fertility gradients. Third, functional
traits controlling competition/colonization trade-offs can determine whether species can
successfully disperse and establish at local communities. Finally, because of the interaction of
functional strategies with environmental gradients, different outcomes in community assembly can
occur depending on the arrival and performance of species along environmental gradients.
NO MANAGEMENT, BAD MANAGEMENT?
Despite that grass and tree encroachment are occurring, NH differs from other areas in that the
transition to grassland or woodland has occurred at a very slow pace. Even more than a century
without management, open heathland is the dominant vegetation at a significant portion of the
area. The temporal scope of this study allowed evaluating the long-term stability of the vegetation
community facing recognized threats (increased nutrient availability and tree encroachment).
Furthermore, the lack of management presented a unique opportunity to study the development of
the vegetation under natural dynamics.
Some of the findings in NH challenge the paradigmatic view of heathland conservation, i.e. that
management actions are necessary for the maintenance of these communities (Mitchell et al.
2000; Pywell et al. 2011). A factor that was of mayor importance to the colonization of grasses and
trees was the disturbance of the vegetation. Paradoxically, current management actions such as
burning, grazing, sod cutting and mechanical removal of trees necessarily disturb the vegetation
and can create establishment windows for colonizing species. Although these actions seem to be
effective in some cases, they are required to be implemented periodically to maintain the
vegetation at some desired state (Mitchel et al. 2000). This can be problematic not only because it
is costly; but because it necessarily requires the continuous intervention and does not lead to a
“self-sustainable” vegetation community.
However, it is likely that the particular circumstances at this heathland are responsible for some of
the observed patterns. For example, perhaps one of the most important factors explaining the slow
colonization rates of trees is that seed source were scarce and at a considerable distance from the
heathland when agriculture was abandoned. This caused a delay in the arrival of first colonizers,
giving grasses, and to a lesser extent dwarf shrubs, time to establish and to modify the
environment and hinder further colonization (Paper 2 and 4).
Despite these contingencies, the conceptual framework developed here (fig 6.1 and 6.2) indicates
that conservation or management designs should consider at least three factors: 1) the influence of
functional strategies and colonization/competition trade-offs; 2) the importance of abiotic factors as
determinants of plant interactions; and 3) the effect of the established vegetation, particularly in the
absence of disturbances. For instance, because of competition/colonization tradeoffs, fast
colonizers might have an initial advantage over dwarf shrub species in colonizing post agricultural
sites. Thus, if the objective is to restore a dwarf shrub community in areas with high nutrient
contents and depleted seed banks, it might be necessary to assist colonization (e.g. seed/seedling
addition, combined with removal of fast colonizers) at early stages after disturbance until dwarf
shrubs develop and can constrain other species (e.g. shading). On the other hand, in low fertility
soils, dwarf shrubs are able to persist up to a point were low light availability strongly limits them. In
this case, allowing more light through the canopy might be a more effective way than tree removal
to maintain the cover of dwarf shrubs until self-thinning of the canopy occurs.
To sum up, considering how different functional strategies respond to abiotic factors; how they
determine the outcome of biotic interactions; and how these relationships vary along environmental
gradients to influence the development of vegetation can help guiding restoration and conservation
of this threatened ecosystem.
FUTURE RESEARCH AT NØRHOLM HEATHLAND
The long-term dataset collected at NH was the backbone of this thesis, evidencing the invaluable
insights into fundamental ecological questions that can be gained with long-term ecological
studies. Furthermore, the absence of direct human intervention during more than a 100 years
following centuries of traditional agricultural practices, presented a unique opportunity to study how
vegetation communities change under natural conditions. Despite the limitations that come along
with this type of studies, it was shown that thorough documentation of changes in the vegetation
and of relevant ecological factors combined with advanced analytical and statistical tools, offer the
opportunity to study the development of communities under “real-life” conditions and to understand
how historical factors affect this development. On the other hand, it is acknowledged that
experimental studies would be necessary to confirm or test emerging hypotheses on causal
relationships and mechanisms. This presents the conundrum of whether research should continue
under a strict “no-human intervention policy” or whether experimental studies should be
implemented at NH?
The answer is not very simple but it is likely to be, at least partly dependent on the scale and
intensity of the experiments. Small scale experiments that do not involve intensive disturbances to
the vegetation, combined with observational studies can provide answers to some unresolved
questions. For instance, stochastic disturbance events such as climatic anomalies, heather beetle
attacks and herbivory undoubtedly influence the structure and assembly of communities. Regular
monitoring programs could be valuable to assess the impact of these stochastic factors. However,
this will require that 1) ad hoc studies can be implemented when these events occurs; 2) that the
number of the permanent plots is increased; and 3) that monitoring becomes regular and at shorter
time intervals (e.g. 5 years). The information obtained can then be complemented with small scale
field experiments (e.g. disturbances, seed additions and fencing) along the main environmental
gradients at NH to study for example, the relationship between disturbances, dispersal limitation
and abiotic gradients.
Another potential direction would be to conduct more detailed studies on tree colonization patterns.
Although, this work identified the importance of the established vegetation, other factors are likely
to be involved. To mention some: conspecific density dependence, the presence of mycorrhiza
(Collier & Bidartondo 2009), allelopathic effects (Zackrisson & Nilsson 1992) and herbivory. To
study these factors under natural conditions, a first step could be to establish large permanent
plots (e.g. 20 ha) to map all individual stems and seedlings and conduct neighborhood effect
studies. These results can then be complemented with small scale field studies and ex situ
experiments. Understanding how these factors interplay with environmental gradients and
functional strategies of colonizing species can be an exciting research direction.
NH is a unique site to answer fundamental and applied ecological questions and to make
comparative studies. Thus the continuation of monitoring programs and addition of new research
projects will likely contribute fruitfully to our understanding of vegetation dynamics, community
assembly, and many other interesting ecological processes. All in all, this work highlighted the
importance and uniqueness of NH as an interesting area for ecological research and as a
benchmark for monitoring. Hopefully, NH will continue to serve as a source of knowledge and
inspiration for the years to come.
REFERENCES
Aerts, R. 1999. Interspecific competition in natural plant communities: mechanisms, trade-offs and
plant-soil feedbacks. Journal of Experimental Botany 50: 29–37.
Aerts, R., & Peijl, M.J. Van Der. 1993. A simple model to explain the dominance of low productive
perennials in nutient-poor environments. Oikos 66: 144–147.
Chase, J.M. 2003. Community assembly: when should history matter? Oecologia 136: 489–98.
Collier, F. a., & Bidartondo, M.I. 2009. Waiting for fungi: the ectomycorrhizal invasion of lowland
heathlands. Journal of Ecology 97: 950–963.
Craine, J.M. 2009. Resource strategies of wild plants. Princeton University Press, Princeton, USA.
Cramer, V.A., Hobbs, R.J., & Standish, R.J. 2008. What’s new about old fields? Land
abandonment and ecosystem assembly. Trends in ecology & evolution 23: 104–12.
Flinn, K.M., & Vellend, M. 2005. Recovery of forest plant communities in post-agricultural
landscapes. Frontiers in Ecology and the Environment 3: 243–250.
Grime, J.P. 2001. Plant strategies, vegetation processes, and ecosystem properties. John Wiley &
Sons, Chichester, UK.
Hermy M, Verheyen K. 2007. Legacies of the past in the presentǦday forest biodiversity: a review
of past landǦuse effects on forest plant species composition and diversity. Ecological
Research 22, 361Ǧ371.
Mason, N.W.H., Richardson, S.J., Peltzer, D.A., de Bello, F., Wardle, D.A., & Allen, R.B. 2012.
Changes in coexistence mechanisms along a long-term soil chronosequence revealed by
functional trait diversity. Journal of Ecology 100: 678–689.
Mitchell, R.J., Auld, M.H.D., Duc, M.G. Le, & Marrs, R.H. 2000. Ecosystem stability and resilienceௗ:
a review of their relevance for the con- servation management of lowland heaths. 3: 142–
160.
Myers, J. A., & Harms, K.E. 2011. Seed arrival and ecological filters interact to assemble highdiversity plant communities. Ecology 92: 676–86.
Stokes, C.J., & Archer, S.R. 2010. Niche differentiation and neutral theory: an integrated
perspective on shrub assemblages in a parkland savanna. Ecology 91: 1152–62.
Pywell, R.F., Meek, W.R., Webb, N.R., Putwain, P.D., & Bullock, J.M. 2011. Long-term heathland
restoration on former grassland: The results of a 17-year experiment. Biological
Conservation 144: 1602–1609.
Stokes, C.J., & Archer, S.R. 2010. Niche differentiation and neutral theory: an integrated
perspective on shrub assemblages in a parkland savanna. Ecology 91: 1152–62.
Von Oheimb, G., Härdtle, W., Naumann, P.S., Westphal, C., Assmann, T., & Meyer, H. 2008.
Long-term effects of historical heathland farming on soil properties of forest ecosystems.
Forest Ecology and Management 255: 1984–1993.
Zackrisson, O., & Nilsson, M. C. 1992. Allelopathic effects by Empetrum hermaphroditum on seed
germination of two boreal tree species. Canadian Journal of Forest Research-Revue
Canadienne De Recherche Forestiere, 22, 1310–1319.
1
FORMER ISSUES
Maj 2013 August 2013
August 2013
Landskabsbyens æstetik. En undersøgelse af fikmmediet som redskab
til belysning af forstadens omgivelseskarakter
Mads Farsø
ISBN 978-87-7903-614-7
Smallholder tree farming systems for livelihood enchancement and
carbon storage
James Michael Roshetko
ISBN 978-87-7903-629-1
Translating Harbourscape. Site-specific Design Approaches in Contemporary European Harbour Transformation
Lisa Diedrich
ISBN 978-87-7903-626-6
January 2014
Changing heathlands in a changing climate. Climate change effects on
heathland plant communities
Johannes Ransijn
ISBN 978-87-7903-644-4
April 2014
Deriving harmonised forest information in Europe using remote sensing
methods. Potentials and limitations for further applications
Lucia Maria Seebach
ISBN 978-87-7903-651-2
October 2014
Cemeteries: Organisation, management and innovation. Diffusion of maintenance specifications in Danish national church cemetery administrations
Christian Philip Kjøller
ISBN 978-87-7903-673-4
November 2014 Parks, People and Places. Place-based governance in urban green
space maintenance
Julie Frøik Molin
ISBN 978-87-7903-675-8
December 2014 Vegetation dynamics and community assembly in post-agricultural
heathland
Sebastián Kepfer Rojas
ISBN 978-87-7903-671-0
PhD Thesis December 2014
ISBN 978-87-7903-671-0
Sebastián Kepfer Rojas
Vegetation dynamics and community
assembly in post-agricultural heathland
department of geosciences and
natural resource management
university of copenhagen
rolighedsvej 23
dk-1958 Frederiksberg
tlf +45 35 33 15 00
[email protected]
www.ign.ku.dk