Download The role of herbivores in mediating responses of tundra ecosystems

The role of herbivores in mediating
responses of tundra ecosystems to
climate change
Elina Kaarlejärvi
Department of Ecology and Environmental Science
Umeå 2014
Copyright © Elina Kaarlejärvi
This work is protected by the Swedish Copyright Legislation (Act 1960:729)
ISBN: 978-91-7459-782-0
Cover: Reindeer grazing in the mountains, photo by E.K.
Elektronisk version tillgänglig på http://umu.diva-portal.org/
Printed by: Print & Media
Umeå, Sweden 2014
To Aune and Alli,
who took me to the mountains
i
Table of contents
Table of contents
ii
List of papers
iii
Author contributions
iv
Abstract
v
Introduction
1
Tundra plant communities in a warming climate
1
Tundra herbivores in a warming climate
2
Plant-herbivore interactions in warming tundra
3
How to study the interaction of climate warming and herbivory in tundra?
4
Objectives of the thesis
7
Methods
8
Results and discussion
13
How do tundra plant communities respond to increased temperature?
13
Are warming-induced vegetation changes reversible and can herbivores
influence the reversibility?
14
Biotic interactions affecting species ranges in a changing climate
14
Concluding remarks
15
Acknowledgements
16
References
16
Acknowledgements
22
ii
List of papers
This thesis is a summary of the following four studies, which will be referred
to by their roman numerals.
I.
Kaarlejärvi, E., Baxter, R., Hofgaard, A., Hytteborn, H.,
Khitun, O., Molau, U., Sjögersten, S., Wookey, P., Olofsson, J.
2012. Effects of Warming on Shrub Abundance and Chemistry
Drive Ecosystem-Level Changes in a Forest–Tundra Ecotone.
Ecosystems 15: 1219-1233.
II.
Kaarlejärvi, E., Eskelinen, A., Olofsson, J. 2013. Herbivory
prevents positive responses of lowland plants to warmer and
more fertile conditions at high altitudes.
Functional Ecology 27: 1244–1253.
III.
Kaarlejärvi, E. and Olofsson J. 2013. Concurrent biotic
interactions influence plant performance at their altitudinal
distribution margins.
Accepted for publication in Oikos.
IV.
Kaarlejärvi, E., Hoset, K. and Olofsson J. 2013. Short-term
herbivory overweighs effects of long-term warming on plant
community.
Manuscript.
Papers I, II and III are reproduced with the kind permission from the
respective publishers.
iii
Author contributions
Paper I
EK analyzed the data and wrote the paper with contributions from most of
the co-authors. EK and OK performed the vegetation analyses. EK and JO
planned the study and prepared samples for chemical analyses. RB, AH, HH,
UM, SS, PW, and JO designed, established, and maintained the field
experiment.
Paper II
EK and AE designed the field experiment and collected the data. EK
analyzed the data and wrote the first version of the manuscript, and all
authors contributed with text and discussions to the manuscript.
Paper III
EK and JO designed the experiment. EK carried out field work, collected and
analyzed data and wrote the first version of the manuscript. JO supervised
the data analysis and contributed to writing.
Paper IV
The warming experiment was started by DART-project in 1998. E.K. and
J.O. planned this study and carried out the fieldwork. K.H conducted the
small rodent trapping. E.K. analyzed the data with the help of J.O. and wrote
the first version of the manuscript that all co-authors edited and commented
on.
Authors:
EK: Elina Kaarlejärvi, JO: Johan Olofsson, AE: Anu Eskelinen, AH: Annika
Hofgaard, HH: Håkan Hytteborn, KH: Katrine Hoset, OK: Olga Khitun, PW:
Philip Wookie, RB: Robert Baxter, SS: Sofie Sjögersten, UM: Ulf Molau
iv
Abstract
Arctic areas are warming more rapidly than other parts of the world.
Increasing temperatures are predicted to result in shrubification, higher
productivity, declining species diversity and new species invasions to the
tundra. Changes in species diversity and plant community composition are
likely to alter ecosystem functions with potential consequences for human
population also at lower latitudes. Thus, in order to better predict the effects
of the rapid arctic warming, we need knowledge on how plant communities
respond to a warmer climate. Here, I investigate the effects of climate
warming on tundra plant communities and focus on the role of mammalian
herbivores in mediating these responses. I examined the role of herbivores
by incorporating herbivore manipulations to short- and long-term warming
experiments as well as along altitudinal gradients. I measured how
individual plants and plant communities respond to warming with and
without herbivores.
Results of my PhD Thesis illustrate several ways how herbivores modify the
responses of plants to warming. I found that herbivores (reindeer, hare,
voles, lemmings) may prevent lowland forbs from invading open tundra.
Herbivores might also protect small tundra forbs from being outcompeted by
taller and denser vegetation under climate warming. Thus, different
herbivore pressures may lead to differing plant abundances and distribution
shifts in different areas. Furthermore, my results show that high herbivore
pressure can reverse the effects of long-term climate warming very rapidly,
even in one year. This finding suggests that well-planned targeted reindeer
grazing episodes could potentially be used as a conservation tool to keep
selected tundra habitats open. Sudden cessation of grazing may initiate rapid
changes in plant community, especially if it coincides with warm
temperatures. Taken together, I show that herbivores counteract the effects
of climate warming by slowing down or preventing warming-induced
vegetation changes in tundra. Therefore, it is important to consider
mammalian herbivores when predicting tundra plant community responses
to changing climate.
v
Introduction
Arctic tundra ecosystems are currently encountering more rapid warming
than lower latitudes (ACIA, 2005; Serreze & Barry, 2011). In general,
diversity within and among plant communities is a prerequisite for
maintenance of ecosystem functioning (Isbell et al., 2011). Tundra
ecosystems are relatively species-poor in terms of vascular plants, which is a
factor that might make them
especially vulnerable in the face of
environmental changes such as climate warming (Post, 2013a). Any potential
alterations in community composition and diversity caused by climate
warming are thus likely to modify ecosystem functions, for example carbon
balance, productivity or nutrient cycles, and may have noteworthy
implications also far beyond the tundra itself. Therefore, realistic predictions
of how plant communities respond to a changing climate form a core of
better understanding of climate change implications for ecosystem
functioning. In this thesis I investigate the effects of climate warming on
tundra plant communities and focus on the role of mammalian herbivores
affecting these responses.
Tundra plant communities in a warming climate
Temperature increase can significantly influence plant individuals, species
and communities in the tundra. A growing body of evidence from plot-scale
tundra experiments to circumpolar observations suggests that increasing
temperatures are linked to higher plant biomass (Walker et al., 2006; Jia et
al., 2009; Forbes et al., 2010; Elmendorf et al., 2012a, 2012b) and
shrubification of tundra (Tape et al., 2006; Myers-Smith et al., 2011).
Experimental warming typically reduces diversity (Walker et al., 2006;
Elmendorf et al., 2012a; Post, 2013b). Tundra plant communities may
change also as a consequence of warming-induced invasions of plants from
lower altitudes and latitudes to tundra. Indeed, recent meta-analyses report
species range shifts to higher latitudes (Chen et al., 2011) and altitudes
(Lenoir et al., 2008; Chen et al., 2011; Gottfried et al., 2012) and link these
shifts to increased temperatures during recent decades.
At the level of plant species, divergent growth responses of different species
to climate warming can modify plant-plant interactions within communities
(e.g. Dormann et al., 2004; Klanderud, 2005; Grau et al., 2012). Also
advanced phenology and a shorter flowering season of several tundra plant
species, associated with increasing summer temperatures and earlier
1
snowmelt (Høye et al., 2013), may result in alterations in intraspecies
demography and plant-plant interactions (Miller-Rushing et al., 2010).
Warmer temperatures and increasing growing season length have been
reported to affect also chemistry of tundra plant species by changing
concentrations of nutrients and defense compounds (Hansen et al., 2005;
Nybakken et al., 2011; Väisänen et al., 2013). However, it remains unknown
how climate warming will influence nutrient concentrations at the level of
plant communities. This is an essential question, since herbivore populations
are dependent on nutrient-rich forage (Sterner & Elser, 2002) and changes
in vegetation’s nutrient concentrations may thus exert cascading effects on
above- and belowground food webs (Schmitz, 2008).
Tundra herbivores in a warming climate
Changing climate will undoubtly affect also tundra herbivore populations.
This can happen either directly by altered fitness of individuals, or indirectly
via altered forage availability, which is dependent on the population density.
As these extrinsic and intrinsic factors take place at the same time, it is not
straight forward to tell apart the direct effects of altered abiotic conditions
and indirect density dependent effects (Tyler, 2010).
Tyler et al. (2008) found that warm winters with melting snow were
associated with more rapidly increasing reindeer numbers, if the population
was already in a growing phase. However, another study links warm and
moist weather (high positive Arctic Oscillation) to reduction of a reindeer
population (Aanes et al., 2002). Recent observational and theorethical
studies suggest that climate can at least partly synchronize the fluctuations
of lemming populations (Krebs et al., 2002; Morris et al., 2012). Especially
rain-on-snow events and the following hard ice crust on the snow can cause
synchronical fluctuations of vertebrate herbivores (sibling voles and
reindeer) (Hansen et al., 2013), or lead to population decline or dampening
lemming cycles (Kausrud et al., 2008). These dampening cycles in turn affect
the higher trophic level by reducing predators' reproductive success and
population densities (Gilg et al., 2009).
Advanced plant phenology, in parallel with advanced nutrient peak and
earlier seasonal decline of nutrients (Doiron et al., 2013), may lead to trophic
mismatch if species at different trophic levels respond at different paces to
climate change (Miller-Rushing et al., 2010), with potentially severe
2
consequences for the whole food web. Kerby and Post (2013) recently
reported such a mismatch in Greenland, where earlier green-up of vegetation
was associated with decline in reproduction of caribou populations.
Plant-herbivore interactions in warming tundra
Since plants are an interlinked part of the ecosystems, it is crucial to consider
their interactions with the other levels of organization for more realistic
predictions of plant species responses to climate change (Gilman et al., 2010;
Post, 2013a). This thesis concentrates on plant-herbivore interactions,
because herbivory is one of the key drivers shaping plant community
dynamics, particularly in low productive tundra ecosystems (e.g. Oksanen et
al., 1981; Aunapuu et al., 2008; van der Wal & Hessen, 2009; Olofsson et al.,
2013). Furthermore, emerging lines of evidence suggest that herbivores play
an important role when aiming to better understand the responses of tundra
plant communities to a warming climate (e.g. Post & Pedersen, 2008;
Hofgaard et al., 2010; Aune et al., 2011; Sjögersten et al., 2012; Post, 2013b).
In addition to herbivory, tundra plant communities can be shaped also by
other lateral interactions, for example by symbiosis with root mychorrhizal
fungi (Read, 1991) and parasitism (Olofsson et al., 2013).
In tundra ecosystems, both densities of herbivores (Olofsson et al., 2009;
Post et al., 2009) and climatic conditions (Gulev et al., 2013) oscillate from
interannual to decadal time scales. The tension hypothesis of biotic response
to climate change predicts that weakening of climatic forcing may strengthen
the importance of exploitative interactions, and, vice versa, climate warming
may have greater influence on plant community composition during periods
of weak exploitation when herbivore populations are low (Post, 2013a). This
hypothesis calls for attention to variability in both climate and exploitative
interactions. A few studies have investigated the impacts of long-term
interannual fluctuations of herbivore populations in relation to vegetation
dynamics (Oksanen & Ericson, 1987; Tømmervik et al., 2004; Olofsson et
al., 2012, 2013), whereas observational studies linking climate change to
vegetation dynamics have typically focused either on long-term climate
trends instead of variability (e.g. Tape et al., 2006; Jia et al., 2009; Frost &
Epstein, 2013), or on sudden extreme events (Bokhorst et al., 2011).
Therefore, it remains unknown how reversible climate-induced vegetation
changes are, as well as whether the importance of herbivores varies
depending on the climatic conditions, as predicted by the tension hypothesis.
3
In addition to community dynamics, biotic interactions may be important
determinants of species’ distributions, as suggested by several theoretical
studies (MacArthur, 1972; Sexton et al., 2009; Lenoir et al., 2010;
Boulangeat et al., 2012). As tundra areas are warming rapidly, there is an
urgent need for knowledge on the role of biotic interactions in affecting
species ranges, but so far empirical evidence is scarce (Sexton et al., 2009;
Wisz et al., 2013). Generally, the upper altitudinal limit of species is typically
controlled by abiotic conditions (Connell, 1961; Brown et al., 1996), whereas
the lower altitudinal distribution limit of species is often controlled by
competitive exclusion (MacArthur, 1972; Lenoir et al., 2010). Warminginduced increases in productivity (Walker et al., 2006) and upward
migration of lowland species may lead to intensified competition, which
could result in an upward shift of the lower distribution margins of native
tundra species and thus threaten their existence. As herbivores are known to
alter plant-plant interactions (Louda et al., 1990; Eskelinen, 2008), they
could potentially reduce the intensity of competition. Thus, for better
predictions of responses of species distributions to climate change, we need
knowledge of both plant-plant and plant-herbivore interactions in tundra
plant communities.
How to study the interaction of climate warming and herbivory in
tundra?
Historical data
Climate has been changing numerous times in the past. The most recent
rapid warming took place approximately 11,000-12,000 years before
present, in the end of the Pleistocene era (Post, 2013a). Did megaherbivores
play a role in the large scale vegetation shifts during this PleistoceneHolocene transition? Comparing the abundances of spores of dung fungi
habiting megafaunal dung and vegetation pollen records, paleoecologists
have been able to illustrate that after a decline in dung fungi, there were
detectable changes in pollen record (reviewed by Gill, 2013). This implies
that not only a warming climate altered vegetation, but also concurrent loss
of megaherbivores caused detectable changes in pollen record (Gill, 2013).
Paleoecological records thus suggest that herbivores could interact with the
effects of climate warming, but fossil and pollen recods do not reveal the
strengths of megaherbivores and climate change as drivers of those regime
shifts.
4
Another source to explore past plant growth is dendrochronology. By
measuring radial growth of birch stems that had grown preceding nine years
in different sheep grazing pressures, Speed et al. (2011) were able to show
that sheep browsing had a stronger effect on the radial growth than changes
in temperature during a 50 years’ period before the grazing experiment.
Modeling
Modeling offers a possibility to test theoretically the interaction of herbivory
and climate change on vegetation dynamics. Using an arctic vegetation
model that incorporates the reindeer diet (via nitrogen concentration and
forage preference) to vegetation dynamics, Yu et al. (2011) showed that both
grazing and climate control the plant community composition and can have
simultaneous but opposite influences on plant abundances.
Experimental approach
Experiments allow interference on causality and therefore can be used for
investigating the mechanisms behind the observed or modeled dynamics.
For a meaningful interpretation, experimental manipulations should be as
natural as possible and manipulate strictly only one factor at time without
confounding factors. Experimental manipulations are well-suited for
studying relatively short-term responses (from a few years to decadal time
scales) of individuals and communities, but are often too short-lasting,
small-scale or loaded with cumulating confounding factors. Experimental
warming manipulates only plants, but does not simulate effects of warming
on mammalian herbivore populations.
So far only few studies have employed an experimental approach for
investigating the interaction of warming and grazing on tundra plants (Table
1). With one exception, all studies have used the same warming method,
passive open top chambers (OTC), but they differ in their choices for grazer
manipulation. Here, especially the interaction term restricts the choice of
applicable methods, since the methods should allow simultaneously both
natural herbivory and natural temperature increase. The cone shape of the
OTCs is likely to block the large mammalian herbivores from grazing evenly
inside the chamber.
Herbivore pressure can be manipulated by two methods: Exclosures are used
to protect certain plots by “fencing out” herbivores that have free access to
grazed control plots. Enclosures, on the other hand, are fences or cages,
5
which “fence in” herbivores, so that they cannot access ungrazed control
plots. This method can be used for studying effects of predetermined
densities of herbivores. The densities of herbivores as well as well as the
temporal application of enclosures have to be realistic in order to achieve
meaningfully interpretable results.
However, in case of wild migratory animals, it is difficult to define “natural”
grazing pressure, timing and duration of grazing, as wild animal grazing
varies spatially and temporally within and among years. The same problem
concerns clipping as a method to simulate grazing. When simulating grazing
by clipping, it is possible to determine the damage intensity. However, it is
challenging to design clipping so that it captures diverse feeding habits of
different herbivores, variations in herbivore density between years and
differences in herbivores’ selectivity due to variation in plant quality between
years, locations or treatments.
In contrast, exclosures allow natural grazing on control plots. However, as
grazing pressure on grazed control plots varies within and between years
depending on the phase of herbivore population dynamics, the effect of
exclosure treatment appears stronger when control plots are heavily grazed,
and weaker during a herbivore population low. Therefore, when using
exclosures as herbivore manipulation method, it is crucial to consider the
herbivore densities and the timing of the grazing, especially if herbivores are
migratory. Furthermore, long-term studies are often needed in order to
capture the variation in population densities.
Table 1. Summary of studies and respective experimental manipulations
investigating the interaction of warming and grazing on plants in tundra.
Location
First
publication
Klein et al.
(2004)
Warming
Grazing
Interaction
OTC
Clipping nested
within grazing
history
Clipping inside the OTCs
Greenland,
Danmark
Post &
Pedersen
(2008)
OTC
Ungulate
exclosure
Natural muskox and
reindeer grazing inside
the OTCs
Spitsbergen,
Norway
Sjögersten
et al. (2008)
OTC
Short-term geese
enclosure
OTC removal during
short-term grazing
Kilpisjärvi,
Finland
Rinnan et al.
(2009)
OTC
Clipping
Clipping inside the OTCs
Tibetan
Plateau
Luo et al.
(2010)
Infrared
heater
Short-term sheep
enclosure
Different timing of
grazing and warming
Tibetan
Plateau,
China
6
Descriptive approach
Altitudinal gradients can be used for studying long-term effects of warmer
climate on plant communities (Dunne et al., 2004), since temperature
increases linearly towards lower altitudes (Körner, 2007). Plant individuals,
populations and communities within a relatively short distance along an
altitudinal gradient have had centuries of time to adapt to local
temperatures. Such long-term climatic difference altering several community
components and ecosystem functions in a large scale is impossible to achieve
with small scale, short-term experiments. Altitudinal gradients can thus offer
a possibility to study long-term community and ecosystem level effects of
climate warming. However, as other climatic factors (e.g. radiation, Körner,
2007) and land use (e.g. herbivores, Speed et al., 2013) can co-vary with
altitude, changes in plant communities along an altitudinal gradient are
never purely temperature-driven, and this should be considered when
interpreting results from gradient studies.
Objectives of the thesis
The overall objective of this thesis is to examine the role of mammalian
herbivores influencing the responses of tundra plant individuals and
communities to temperature increase.
I focus on the following research questions:
1. How do tundra plant communities respond to climate warming in
terms of species abundances and chemical composition?
2. Are warming-induced vegetation changes reversible and can
herbivores influence the reversibility?
3. What are the relative strengths of abiotic factors, plant-plant
interactions and plant-herbivore interactions influencing species
ranges?
7
Methods
As perennial tundra vegetation responds slowly to changes in abiotic
conditions and the first community level responses to experimental warming
are typically recorded 3-4 years after the start of the warming treatment
(Walker et al., 2006), community level responses of experimental warming
can hardly be achieved during a PhD thesis project (ca. 4.5 years in Sweden).
To overcome this apparent mismatch, I used a combination of different
methods: I established a new short-term experiment (paper I), used a
descriptive altitudinal gradient study (paper III) and utilized existing longterm experiments (papers I, IV), to explore both short- and long-term
responses of tundra plant individuals, species and community composition
to increased temperatures and herbiovory.
Study sites
The studies were carried out in four locations in the Fennoscandian
Mountains (Fig. 1). Characteristics of each location are described in detail in
the respective papers.
Figure 1. Map of Fennoscandia showing the locations of the four studies. Paper I:
Dovrefjell, Abisko, Joatka; Paper II: Kilpisjärvi; Paper III: Abisko; Paper IV: Joatka.
8
Temperature manipulations
Experimental warming in each study location was carried out using passive
hexagonal Open Top Chambers (OTC), which are 40 cm high and have a
maximum basal diameter of 146 cm (Fig. 2). The OTCs in our study sites
increased summer time surface air temperatures by 1-2°C (papers I and II),
which is very moderate warming compared to the predictions for the
northern areas (above 60°N) by the end of 21st century (ACIA, 2005). OTCs
are the best passive warming method suitable for open remote habitats
(Aronson & McNulty, 2009), even though they have several drawbacks,
which are discussed in papers I and II.
Paper II examines the short-term effects of warming on plant individuals
and tundra vegetation biomass, whereas papers I and IV study the effects of
longer-term (11 years) warming on tundra plant community composition
using OTCs.
In paper III, the climate manipulation was implemented by establishing
study sites in similar kind of topographical positions at two different
altitudes (ca 600 and 900 m a.s.l.), which differed in their mean summer air
temperatures by 2.1°C. This altitudinal difference and corresponding
microclimatic difference have shaped plant communities along the gradient
for centuries, and consequently, plant community composition varied
between low and high altitude study sites (paper III). This setup allowed me
to study how plant individuals respond to different sets of neighboring
plants, which had had centuries to adapt to local climatic conditions of the
two altitudes. As many abiotic factors co-vary with altitude, this is not solely
a temperature gradient, and therefore results are discussed with caution.
Herbivore manipulations
To study the effects of mammalian herbivores on vegetation, I manipulated
herbivore pressure with exclosures, which excluded either all mammalian
herbivores (papers II and IV), or only large herbivores, i.e. reindeer and hare
(paper III). Exclosures preventing grazing by all mammalian herbivores were
dug into the soil at 10-30 cm depth in order to prevent rodents reaching the
plots from belowground (Fig. 2). Reindeer (Rangifer tarandus L. tarandus),
voles (Myodes spp., Microtus spp.) and lemmings (Lemmus lemmus L.) are
the most abundant herbivores in Abisko, Kilpisjärvi and Joatka. The first
paper did not include herbivore manipulation.
9
Figure 2. Left: Open top chambers (OTC) and mammalian herbivore exclosures in
Kilpisjärvi (paper II). Right: vegetation after 11 years of warming in Joatka, Abisko
and Dovrefjell (paper I).
Interaction of temperature and herbivore manipulations
Papers II and III investigated the interaction of temperature increase and
herbivory. Using different methods, these two papers examined the effects of
this interaction on different aspects of vegetation. In paper II, the interaction
was implemented in a full-factorial design. The interaction of warming and
grazing was achieved by removing all warming chambers from around the
study plots in the middle of the summer for the period when reindeer graze
in the study area (ca 1 month). This way the unfenced plots, both warmed
and unwarmed, experienced similar reindeer grazing. This setup allowed me
to compare the effects of short-term warming and grazer exclosures on
biomasses of transplanted plant individuals and the whole tundra plant
community.
In paper III, the interaction was achieved using large mammalian exclosures
at both low and high altitude sites. Here, I tested how large herbivores and
neighboring vegetation (plant-plant interactions) affect the growth and
reproduction of transplanted individuals in colder and warmer climate.
10
In paper IV, I focused on the reversibility of warming-induced vegetation
changes and investigated the role of herbivores affecting this reversibility. In
order to study this, I removed OTCs after 11 years of warming. To test if
herbivores influence the reversibility, all mammalian herbivores were
excluded from some of the previously warmed plots, while others were left as
open controls.
Manipulation of plant-plant interaction
In order to study the importance of plant-plant interactions on the growth of
plant individuals at different altitudes, I transplanted plants in the middle of
undisturbed native vegetation and on experimental plots where all
aboveground biomass was removed (paper III). This neighborhood
manipulation was nested within large herbivore exclosure treatment at two
altitudes.
Manipulation of soil nutrient availability
In paper II, soil nutrient availability was manipulated by a fertilization
treatment in a full-factorial design with warming and herbivore exclusion.
Fast-dissolving NPK fertilizer was applied on the fertilized plots twice per
growing season (mid-June and end of July) resulting in an addition of 9.6g
N, 5.4g P and 13.2g K m-2 annually. This dose is much higher than predicted
increases due to warming-induced acceleration of decomposition (Keuper et
al., 2012), but it simulates the differences between fertile and infertile
microhabitats.
Transplants
Two of the studies used plant individuals as study organisms (papers II and
III). Seeds of the transplant species were collected in the respective study
areas and grown to seedlings in greenhouses. I transplanted these young
seedlings to study plots in the beginning of the growing season, and their
growth and reproduction was followed for two growing seasons. In paper II,
species were tall forbs from low altitudes (Epilobium angustifolium, Silene
dioica, Solidago virgaurea), which were transplanted above their current
optimum altitude to open tundra. In paper III, I used three tall forbs
commonly occurring at low altitudes (Angelica archangelica, Rumex
lapponum, Solidago virgaurea) and three small forbs with their current
main distribution at high altitudes (Sibbaldia procumbens, Gnaphalium
11
supinum, Potentilla cranzii). I transplanted these species to both high and
low altitude sites along altitudinal gradients.
Recordings of responses of plant individuals and communities
I used the point-intercept method (Jonasson, 1988) for nondestructive
measures of plant community composition (papers I, II, IV). The method
was modified for the specific needs and plot sizes of different studies and
detailed numbers of pins used in each study are reported in the method
sections of each respective paper.
To estimate the growth of transplant individuals, I measured their vegetative
aboveground biomass and reproductive success by weighting the
reproductive biomass (paper II) or by recording the presence/absence of
reproductive organs (paper II).
To investigate the effect of warming on dwarf-shrubs’ nutrient and defense
compound concentrations, leaves of 5-10 shoot tips of four shrub species
were collected from warmed and control plots in August after eight years of
experimental warming (OTC, paper I). Samples were analyzed for carbon
(C), nitrogen (N) and phosphorus (P), condensed tannins and total
phenolics. Species-specific concentrations were used for obtaining dwarfshrub community level nutrient and defense compound concentrations by
calculating shrub abundance-weighted concentrations for each study plot.
Data analysis
For statistical data analysis I used mostly traditional analysis of variance
with and without repeated factor, and Linear Mixed Effect Models (LME).
Both methods allow incorporation of a random variable, which was needed
for taking into account the hierarchical structure of the data sets in papers I,
III and IV. For analyzing binomial response variables originating from
hierarchical experimental design, I used generalized linear mixed models
(GLMM) with binomial distributions and logit link functions (paper III). I
used R statistical software (R development core team, 2013) for all analyses
and package nlme in R for LMEs (Pinheiro et al., 2013) and package lme4 for
GLMM analysis (Bates et al. 2012).
12
Results and discussion
How do tundra plant communities respond to increased
temperature?
In all four papers of this thesis I examined plant community responses to
enhanced temperature or to more benign microclimate in general (paper
III). Tundra plant communities responded slowly to experimentally
increased temperatures, and even fast growing grass-dominated vegetation
needed more than two years of warming to show responses (paper III). This
finding is in line with a meta-analysis of warming experiments reporting
slow responses of tundra vegetation (Walker et al., 2006). However, eleven
years of experimental warming was long enough period to cause vast
increases in the abundance of dwarf-shrubs (papers I, IV). Moreover, I found
that the biomass increase was higher towards south (Fig. 2) and was
probably depended on soil moisture, which also increased towards south.
These results are consistent with a recent meta-analysis of tundra warming
experiments, reporting stronger community responses to warming at moist
sites (Elmendorf et al., 2012a).
Experimental warming did not have large impacts on species’ nutrient
concentrations. Nutrient composition of dwarf-shrub species remained
mainly unchanged after eight years of experimental warming, only Betula
nana showed decreasing nutrient concentrations in warmed plots (paper I).
On the contrary, there were large interspecies differences in nutrient
concentrations. In the paper I, I show that altered species composition as a
response to warmer temperature causes greater effects to community level
nutrient concentrations than do direct warming-induced changes at species
level. Similarly, different species compositions in forest and tundra habitats
in a forest-tundra ecotone translated into large differences in communitylevel nutrient concentrations between these habitats (paper I). These
changes in food quality could potentially influence herbivore populations.
Moreover, since nutrient concentration of living plants correlates with
concentrations in plant litter, (Soudzilovskaia et al., 2007), these changes
may influence nutrient cycling and carbon storage in the soil (Cornelissen et
al., 2007).
13
Are warming-induced vegetation changes reversible and can
herbivores influence the reversibility?
Using consecutive warming and herbivore exclosure treatments (paper IV), I
was able to show two interesting aspects of how both climate and herbivores
control plant community composition. First, a single herbivore outbreak
overrode the effects of 11 years of warming surprisingly rapidly, only in one
year. This vole and lemming peak affected all plant species, including heavily
defended Empetrum hermaphroditum, to such degree that their abundances
declined to levels lower than those recorded at the start of the warming
experiment. These results demonstrate, for the first time, that herbivores can
reverse warming-induced vegetation changes.
Second, in the plots, which were protected from voles and lemmings, plant
abundance continued to increase still after the end of experimental warming,
resulting in ca. 160% higher plant abundance in herbivore exclosures than in
grazed plots. This finding suggests that a warm period can have pronounced
and persistent effects on vegetation in the absence of disturbances even
during a subsequent colder period. Herbivores might thus have an especially
pronounced influence on plant community dynamics in colder
years/periods, when harsh abiotic conditions do not support compensatory
growth after a grazing event. This finding is in agreement with a tension
hypothesis of biotic response to climate change, predicting that weakening of
climatic forcing may strengthen the importance of exploitative interactions
(Post, 2013a).
Biotic interactions affecting species ranges in a changing climate
Papers II and III disentangled how biotic (plant-plant and plant-herbivore)
interactions influence performance of individual plants outside their current
optimum altitudinal distribution in a changing climate. Results of both of
these studies indicate that climate warming may indeed trigger lowland forbs
to migrate to higher altitudes, since individual transplants survived and grew
above their current optimum altitudes. This finding is in agreement with
observations of upward shifts of lowland plant individuals above their
optimum altitude (e.g. Walther et al., 2005; Kullman, 2010). Furthermore,
both of these papers showed that large mammalian grazers reduced the
growth of tall forbs (papers II, III), and that lowland forbs benefited from
warming and nutrient-rich soils at high altitudes only in the absence of
mammalian herbivores (paper II). These results provide experimental
evidence that mammalian herbivores may regulate the upper altitudinal
14
limits of lowland forbs and could thus counteract the anticipated warminginduced distribution shifts, in line with conclusions of observational studies
by Speed et al. along an altitudinal gradient (2012, 2013).
By transplanting high-altitude forbs below their current optimum altitude
(paper III), I found indication that competition may set the lower altitudinal
limits of some small tundra forbs. This finding, though only for one species,
suggests that competition may play a role in determining species’ lower
distribution margins. Thus, increased competition in response to climate
warming may thus potentially cause upward shifts of the lower distribution
margins of some high-altitude forbs. However, the finding that large
mammalian grazers enhanced the flowering of small forbs proposes that
high-altitude tundra forbs benefit from the presence of grazers, which reduce
competition and thus enhance the growth and reproduction of high-altitude
forbs. These results corroborate some previous observations that grazing by
large herbivores can favor the abundance and richness of small-statured
arctic and alpine species (Oksanen & Olofsson, 2005; Evju et al., 2010).
Concluding remarks
In this thesis I describe several ways how herbivores affect responses of
tundra plant communities to climate change. My key findings can be
summarized in following two points:
First, herbivores can reverse the effects of long-term climate warming, i.e.
increased biomass, as rapidly as in one year. In my study, a vole and
lemming peak caused this reversal, but similar impact could be caused, for
example, by locally or temporally high reindeer density. This result suggests
that well-planned and targeted reindeer grazing episodes could potentially
be used as a conservation tool to preserve selected tundra habitats open.
Second, I found that large herbivores (reindeer and hare) may prevent
lowland forbs from invading to open tundra. This finding implies that
different herbivore pressures in different areas may lead to distinct plant
abundances and distribution shifts. Furthermore, my results indicate that
since large mammalian grazers may slow down vegetation changes, a
moderate grazing pressure could protect small tundra forbs from being
outcompeted by taller plants under climate warming. A suden cessation of
reindeer grazing, for example as a consequence of anthropogenic
15
disturbance on key pastures (CAFF, 2013), may thus initiate rapid changes in
plant communities, especially if it coincides with warm temperatures.
Taken together, I show that herbivores can prevent expansions of plant
individuals to open tundra and revert warming-induced changes in local
plant communities. It is thus important to consider mammalian herbivores
when predicting tundra plant community responses to changing climate.
However, it should be kept in mind that my results are based on responses of
individual plants and plant communities in small-scale plots. The capacity of
herbivores to mitigate changes in vegetation in land-scape scale may be
weaker, because the strength of herbivory varies in space and time. Thus,
there is a clear need to up-scale these plot-level findings. This could be
addressed, for example, using space-borne observational data on large-scale
vegetation changes in relation to fluctuations in both climate and herbivore
populations.
Acknowledgements
Many thanks to Anu Eskelinen, Johan Olofsson, Tim Horstkotte and Pieter
Deleu for helpful comments on this thesis summary. This research was
funded by grants from JC Kempe Memorial Fund, Gunnar och Ruth
Björkmans fond för norrländsk botanisk forskning, Societas pro Fauna et
Flora Fennica and the Abisko Scientific Research Station, Norrbotten,
Sweden to E. Kaarlejärvi and from the Nordic Centre of Excellence – Tundra
(ENV4-CT97-0586), the Swedish Research Council for Environment,
Agricultural Sciences and Spatial Planning (2006-1539 and 2012-230),
Stiftelsen Oscar och Lili Lamms minne and Göran Gustafssons Stiftelse för
Natur och Miljö i Lappland to J. Olofsson.
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21
Acknowledgements
There were two reasons why I applied for this PhD position in Umeå: I wanted to
learn how to do experimental science, and Sweden felt like such a safe and wellorganised place (compared to Siberia). Thank you, Johan, for your rather free way of
educating. Sometimes I was frustrated, because you rarely gave simple practical
answers to my questions. But it was a good method to teach a student to think herself
and make decisions independently. Even though I like field work as the best part of
this work, you have taught me how cool it is to connect pieces of data to a larger
context during writing. Thanks for this lesson, I have learned much more than just to
carry out experiments in well-organized conditions!
Anu, I was lucky that you agreed to become my collaborator for Kilpisjärvi
experiment. It was great that you became my second supervisor, I have learned a lot
from you! Thank you for all your practical advice and punctuality, and for your
always supportive attitude. And thanks for the countless hours of discussions, not
only about science. Also thanks to Jon, my third supervisor. Your comments were
helpful; I should have asked them much more often!
I want to thank all the co-authors of these four papers, your comments on the
manuscripts have taught me important things about academic writing, but also about
the meaning of science in general.
Suvi, Sini and Nunnu, where would I be without you? Surely not here! I have been so
luc y to have the world’s best assistants to share the joys and pains during weeks and
months of field work. Your patience and perseverance have been invaluable. Even in
the worst weathers you kept working with dedication and great punctuality. Also
thanks to Jonas, Esa, Niklas, Aino, Maria, Ahti, Roland and Pieter for your
appreciated help and good company in the field.
Sonja, I’m glad that we happened to meet at EMG - it would be a big pity not to know
you! So many good laughters, chats, teas, travels, conferences, dinners, walks, visits,
phone calls and Highly Serious work discussions we have shared. And Tim, it was
good luck that you started your PhD project at the same time in a new place. And that
also you needed to get out from the city in the weekends. Thank you for all the work
discussions, lunch breaks and especially for your always nice and peaceful company
outside the working hours in the forests, mires and mountains.
Otilia, thanks for letting me dig spring soil in your garden plot – and enjoy self-grown
vegetables later in summer. And for trainings and tea breaks. Hélène and Mikaela,
thank you for sharing an office and your tips for managing a common supervisor.
Hélène, it was always nice to hear from you when the distance between our office
desks became very long. Thank you for all your help with various field work issues
and for the skiing trips!
Adela, without your endless positive and curious attitude even in the weirdest
(research?) circumstances and your contagious Russophilia, I would have become a
reindeer herder after the first tundra summer. You convinced me to learn bryophytes,
to play with R, to study Russian and to work again in tundra. So I got seriously
addicted, more and more interested in research, and ended up here instead…
22
Kilpisjärvi Biological Station has always offered perfectly tidy accommodation and
lab facilities during field work periods. Thanks to the stuff of the station, and
especially to Oula for his help in the field. Also Jotka Fjellstue, Abisko Scientific
Research Station and Kongsvoll Biological Station deserve thanks for warm
accommodations.
Sari and Maria, you are running a cool experiment, and it has been an honour to be
trusted to carry out vegetation sampling on your plots. It has been very interesting to
work with you, since you know so much about things which are linked to vegetation,
but require specific skills to be thoroughly studied, like soil processes, phenolics and
CO2 fluxes. Thank you for this great possilibity to learn, and I hope to continue
collaboration in future!
In Umeå, thanks Mats for interesting lectures and excursions to the world of
bryophytes. It was nice to teach with you. And thanks Ingrid, Jolina, Ann-Sofie,
Mattias! Thanks to you, EMG is really a well-organized place even for a worker who
was most of the time far away but still needed help with administration. You have
been so helpful with all paper bureaucracy. Kathrin and Daniela, you made me feel at
home when visiting Umeå. Thank you for your hospitability! Also thanks to all old
and new colleagues at EMG who made time in Umeå nice and memorable. I’m happy
to have met you!
Lidwina and Patrick thousand thanks for your generous hospitability, delicious food
(and desserts!) and baby-sitting help during the very last weeks of writing! Next time
when we meet, there will be much more time for walks, talks and bike-rides…
Kiitos Kilpisjärven poromiehille, Juha Tornensikselle ja Nils-Matti Vasaralle
ystävällisistä vastauksista, kun olen vuosittain kyselly porojen liikkeistä. Teidän
antamat tietonne ovat olleet tarpeen, jotta olemme osanneet poistaa
lämmityskammiot porojen tieltä juuri oikeaan aikaan. Toivottavasti yhteistyö jatkuu
tulevinakin vuosina!
Kiitos Hannelelle ja Tapiolle loistavasta työhuoneesta, missä on voinut häiriöttä
keskittyä työhön — tai katsella kattojen yli merelle.
Kiitos Veeralle, Nooralle, Suville, Nunnulle, Anulle ja Kerttulille olemassaolosta ja
kaikesta jaetusta, te olette tärkeitä. Kiitos Allille ja Aunelle, jotka veivät minut
tunturiin, opettivat kukkien nimet ja miten tunturissa selvitään. Ja herkuttivat
marjarahkoilla retkipäivien päätteeksi. Isälle kiitos retkistä soille, metsiin ja hangille.
Ja kiinnostuksesta kaikenmaailman työprojektejakin kohtaan sekä erityisesti niiden
järkevyyden kyseenalaistamisesta. Äidille kiitos tuesta, kuuntelemisesta ja
vauvanhoitoavusta Kilpisjärvellä.
Mun Pieterke, thank you for your healthy irony in moments when I was taking my
work unnecessary seriously. Thanks for letting me go to the mountains, while normal
people spend warm summer days together. And thank you for the several months of
baby-sitting, while I just enjoyed silence with a cup of tea and a laptop. Dikke-dikke
kus!
Ja minun pikkupikku-Emil!
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