Thematic network CONSIDER (EVK2-CT-2002-20012)
Second periodic report (deliverable 22, DoW)
”Fragmented habitats and soil biodiversity”
University of Lund, Sweden (April 17-20 2004)
Introduction
CONSIDER deals with the most important anthropogenic activities that pose a threat
towards, or are being implemented to mitigate loss in, soil biodiversity. Threats are
habitat fragmentation and destruction and global climate change, whereas mitigation
activities include land abandonment and environmentally-friendly agriculture.
CONSIDER addresses these four topics, initially at each their workshop. To further
strengthen the focus of discussions, CONSIDER will perform, during the course of its
workshops, assessments or experiments at existing field experiments of relevance to
the theme of the workshop.
The impact of environmental friendly agriculture was the topic of workshop 2
of CONSIDER, held in Lund (Sweden) April 17-20 2004.
Habitat fragmentation is known to be one of the major threats to aboveground
terrestrial biodiversity (1, 3). Reduction of the size of natural areas and natural
landscape elements is known to lead to the extinction of local populations and poor
connections of habitat fragments constrains re-colonisation of the local patches from
the metapopulation. Isolated fragments are also known to have reduced trophic
complexity, which may lead to the reduced natural suppression to pest insects (4). It
has been argued that processes at local scales can be understood only when
considering the species pool in the whole landscape (5). The theory of the ecological
consequences of habitat fragmentation has been developed predominantly for
aboveground organisms, such as birds (6), butterflies (2) and other insects and plants
(4).- However, there is no evidence of how soil biodiversity will respond to habitat
fragmentation. Twelve guests were invited with expertise in the field of habitat
fragmentation.
During the workshop we invited researchers working with landscape ecology,
and on above and below ground interactions. The workshop consisted of two parts,
first a PhD course (one day) for students within the network, that included talks on
theoretical issues of fragmentation and presentation of research projects. On the
second day workshop, all other participants arrived and talks were presented on issues
of fragmentation from both below and above ground communities. We discussed
recent findings of landscape ecologists, which have been focused exclusively above
ground, on the stability of populations and trophic interactions in relation to habitat
size, habitat configuration and fragmentation models. Participants of the thematic
network contributed by providing data on dispersal of soil organisms, and by
discussing functional roles, as well as functional redundancy, in soil communities.
The topics were arranged into the themes (i) linkages between diversity in
vegetation and diversity in soil (ii) evidence for the relationship between soil organic
matter and soil biodiversity, (iii) interactions between heterogeneous inputs and the
stability versus variability of populations in time and space, and (iv) multitrophic
interactions at the living plant. Most emphasis was placed on theme (iii) and (iv) at
this workshop.
(i) Linkages between diversity in vegetation and diversity in soil.
The existing literature on linkages of above- and belowground diversity was
discussed in relation to landscapes with man-made reductions/restrictions in
populated areas. The main question dealt with was: What is the relationship
between fragmentation of plant cover and soil biodiversity?
(ii) Relationship between soil organic matter and soil biodiversity
Driving forces for food-web complexity in detrital systems were discussed. Of
particular interest at this workshop was the relative importance of bottom-up vs.
top-down forces for regulating soil biodiversity. This is because the larger or
more widely separated organisms expected to exert top-down control can be
assumed to be the ones first to be affected by habitat fragmentation. The major
question dealt with at the workshop was: Relation between soil organic matter
and soil biodiversity at various scales vs. habitat structure and disturbance?
(iii) Interactions between heterogeneous inputs and stability/variability of populations
in time and space
The input of nutrient cycling versus pulses of organic resources was discussed to
find the status of current knowledge and practices. The variability of organic
input and the knowledge status was summarized, aiming at integrating practices
with current knowledge. The main questions dealt with at this workshop were:
(a) Will corridors of higher plant diversity/elevated soil organic matter have a
role for soil biodiversity? (b) What is the effect of scaling of a fragmentation on
interactions between soil organisms as dependent on their size? (c) What is the
impact of fragmentation on the ability of the organisms to disperse?
(iv) multitrophic interactions at the living plant
The possible interaction strengths between above- and belowground herbivores
and microorganisms based on the literature was discussed. A spatial and
temporal component had to be added to deal with habitat fragmentation. The
questions dealt with at the workshop can be formuilated in three themes: (a)
How does separation of herbivores and plant specific soil organisms affect soil
biodiversity? (b) Can habitats be so small or remote that soil organisms needed
for plant growth are not available?, and (c) At which (reduced) habitat size will
belowground plant specific biota be impoverished?
1
Hanski, I. (ed.) (1988) Ecological significance of spatial and temporal variability Annales Zoologici
Fennici (Special Issue)
2
Hanski I. (1999) Habitat connectivity, habitat continuity, and metapopulations in dynamic landscapes.
Oikos 87, 209-219
3
Hanski, I. and Gilpin, M. (eds.) (1997) Metapopulation Biology: Ecology, Genetics and Evolution
Academic Press, San Diego
4
Kruess, A. and Tscharntke, T. (1994) Habitat fragmentation, species loss, and biological control.
Science 264, 1581-1584
5
Lawton JH (2000) Excellence in Ecology Series: Community Ecology in a Changing World (ed O
inne). Ecology Institute, Germany, 227pps.
6
Verboom J, Foppen R, Chardon P, Opdam P, Luttikhuizen P (2001) Introducing the key patch
approach for habitat networks with persistent populations: an example for marshland birds. Biological
conservation 100: 89-201
Schedule of the workshop
Saturday 17 April, 15.00 Start of PhD course
Sunday 18 April, 9.00 - 16.00 PhD course
Sunday 18 April, 16.00 start of workshop (all other participants arrived)
Tuesday 20 April 13.00 end of workshop.
Talks presented during the workshop were:
Tadashi Fukami (Lincoln, New Zealand) Community assembly, habitat
fragmentation, and species diversity"
Michael Bonkowski (Darmstadt, Germany) Soil hot spot ecology
Andrew Gonzalez (Montreal Canada), Population and community dynamics in
fragmented landscapes: insights from model systems"
Jens Dauber (Giessen Germany), Response of soil fauna communities to spatiotemporal patterns of land use.
Katja Schneider (Darmstadt, Germany), No effect of habitat fragmentation on
microarthropods in soil
Heikki Setälä (Helsinki, Finland) Are soil decomposer communities sensitive to
habitat fragmentation?
Saskya van Nouhoys ( Cornell, USA)Dispersal and habitat structure in
communities of butterflies, their host plants and parasitoids
Jochen Krauss (Göttingen Germany) Effects of habitat fragmentation and landscape
context on butterflies.
Erik Öckinger (Lund Sweden), Landscape composition affects butterfly diversity
independent of habitat quality.”
Lisa Bjørnlund, Mette Vestergaard Madsen (Copenhagen Denmark) Functional
diversity of rhizosphere bacteria in barley was affected by aphids and soil
nutrients.
Henrik Smith (Lund Sweden) Utilisation of unevenly distributed resources - the
starling in the agricultural landscap
Maj Rundlöf, (Lund Sweden) Effect of organic farming on biodiversity differs
depending on landscape context.
Michelle Fountain (Reading UK)Biodiversity of soil fauna and the importance of
identification to species level.
Joanna Staley (Reading UK) Changes in summer rainfall affect plant and
phytophagous insect abundance at a calcareous grassland site.
Nancy Johnson (Lund Sweden) Arbuscular mycorrhizas in landscapes
Janne Bengtsson (Uppsala Sweden)/summary and end of workshop
Abstracts of talks at workshop 2.
Response of soil fauna communities to spatio-temporal patterns of land use
Jens Dauber (Department of Animal Ecology, Justus-Liebig-University, HeinrichBuff-Ring 26-32, D-35392 Giessen, Germany, e-mail: jens.dauber@allzool.bio.unigiessen.de).
Understanding the response of individual populations and species to landscape change
is one of the major challenges to conservation ecology in cultivated landscapes.
Increased knowledge of temporal changes in species composition and diversity
following land-use change should enhance sustainable conservation efforts.
Biodiversity is strongly influenced by current land use, but also by land-use dynamics
and history, i.e. biodiversity depends not only on current spatial patterns of land use,
but also on temporal patterns created by the historical development of the landscape.
Conversion of extensive arable lands into grasslands is a relatively new but more and
more common practice in Europe. The area covered by managed grassland
continuously increases especially in low-intensity farming systems, and particularly in
regions where conditions are unfavourable for arable farming (‘marginal landscapes’).
The outcomes of successional processes induced by land-use change on biodiversity
at all resolution levels is not sufficiently studied. The sequential conversion of arable
land into grassland impacts communities via changes in colonisation patterns,
maturation of populations or the probability of local extinction.
The studies on the response of soil fauna communities to spatio-temporal patterns of
land use were carried out in the Lahn-Dill-Bergland (Central Hesse, Germany).
Cultivation, especially crop production, is not sufficiently profitable in this marginal
region. Hence, the present visual landscape character has changed fundamentally over
the last sixty years. In many places, extensive areas of grasslands managed by sheep
grazing and annual mowing replaced the traditional small parcelled crop production
and crop-grassland rotation. The increase of managed grassland has created a complex
spatio-temporal pattern of grassland sites of different age. The focus of the studies
was on the response of species richness and community composition of different soil
organisms (ground beetles, ants, oribatid mites) to (i) grassland age and successional
processes and (ii) the spatio-temporal pattern of the landscape matrix. We followed
two approaches, (i) comparison of grassland sites of different age in landscapes of
unique land-use history, and (ii) comparison of grassland sites of the same age in
landscapes of different land-use history. The simultaneous availability of grassland
sites of different age allowed us to apply ‘space-for-time substitution’ as a surrogate
for long-term studies.
No effect of habitat fragmentation on microarthropods in soil
Katja Schneider, Stefan Scheu, Mark Maraun (Technische Universität Darmstadt,
Institut für Zoologie, Schnittspahnstrasse 3, 64287 Darmstadt, Germany).
Habitat fragmentation is considered to be the major threat to biological diversity. In
this study we investigated the effect of habitat fragmentation on the soil
microarthropod community (Oribatida, Mesostigmata, Collembola). In a mixed oak
(Quercus robur)-hornbeam (Carpinus betulus) forest the soil system was fragmented
for 17 months using small closed microcosms ( 6cm) while the control site
remained untreated. We tested the following five hypotheses: (1) the abundance of
large species is more likely to decline than that of small species, as large species have
greater fluctuations in their population densities than small ones; (2) the adundance of
rare species of soil microarthropods will also decline faster than that of abundant
species, because rare species are more likely to became extinct by stochastic
processes; (3) the abundance of species at higher trophic levels (e.g. predators
compared to saprophagous species) is expected to decline due to the fact that they are
subjected to more intense population fluctuations than species at lower trophic levels.
If the later hypothesis is true another hypothesis arises: (4) species that are top-down
controlled (e.g. collembolans) profit from reduced predator densities whereas species
that have few enemies (e.g. oribatid mites) are little affected. Surprisingly, densities of
most soil microarthropod taxa (Oribatida, Mesostigmata, Collembola) were not
affected by habitat fragmentation over a period of 17 months. The density of the
oribatid mite species did not decline significantly in the habitat fragments and
therefore large species are not more likely to decline than small species. Furthermore,
the habitat fragmentation did not alter species richness and rare species are not more
likely to decline than common species. Also the structure of the oribatid mite and the
collembola community was not influenced by habitat fragmentation. We suggest that
due to the small body size and limited dispersal ability of microarthropods they
inhabit isolated microhabitats and therefore are insensitive in respect to
fragmentation. This contrasts above-ground communities, where the isolation of the
habitat is often correlated with decreasing diversity and abundance.
Are soil decomposer communities sensitive to habitat fragmentation?
Heikki Setälä (University of Helsinki, Finland heikki.setala@helsinki.fi).
Soil decomposer communities were applied as a tool to investigate the effects of
habitat fragmentation and corridors on the community assembly. The diverse soil
community was expected to offer plenty of material to search for specific
characteristics, which might render a given organism vulnerable to fragmentation. The
set-up of experiments consisted of habitat (humus) patches, embedded in mineral soil
representing an uninhabitable (or non-preferred) matrix for the decomposers. The
patches were either disconnected or connected to each other with humus corridors. In
some experiments, also the effect of size of the patch-corridor system was studied.
The experiments run for 2 to 3 years.
The results indicate that habitat fragmentation is not likely to induce immediate
extinctions of soil decomposer populations, which appear to be well adapted to living
within a restricted habitat patch. Nevertheless, some predatory mite and rare
collembolan species were negatively affected by restricted habitat size. Due to the
virtual lack of negative effects of fragmentation, also the presence of corridors
appeared to be superfluous. The results suggest that not all communities are
necessarily unanimously negatively affected by restricted habitat size. For such
fragmentation-insensitive communities, also the presence of habitat corridors may be
indifferent. The negative responses of rare and predatory microarthropods to habitat
fragmentation parallels with observations from the above ground milieu.
Effects of habitat fragmentation and landscape context on butterflies
Jochen Krauss (Institute of Environmental Sciences, University of Zürich,
Winterthurerstrasse 190, 8057 Zürich, Switzerland, E-mail:
jkrauss@uwinst.unizh.ch).
Calcareous grasslands are characterized by a high diversity of plants and insects. They
are known as the most species rich habitat for butterflies in Central Europe.
Nevertheless calcareous grasslands are highly fragmented and surrounded by
intensive arable land use.
The effects of habitat area, isolation, quality and the landscape context around
the study sites were tested for butterflies. Butterfly species numbers and population
densities increased with increasing habitat area, but not with increasing habitat
connectivity. Species numbers also increased with increasing landscape diversity.
Habitat specialized butterflies were more affected by habitat area; generalists were
more affected by the surrounding landscape context. Habitat quality was correlated
with habitat area and not independently testable.
Butterflies were studied on the same study sites four years earlier. Between the
two study years local species immigration rates increased, while extinction rates
decreased with increasing habitat area. With decreasing area habitat specialists
became extinct faster than habitat generalists. Habitat isolation again had no
significant impact. Rates of extinction (38 % for habitat specialists vs. 20 % for
generalists) were higher, and rates of immigration (11 % vs. 30 %) were lower for
specialists than for generalists.
On a single species approach population density was shown to be highly
dependent on larval food plant availability, which depends on habitat area, while
isolation again had a minor input. In conclusion habitat area is the most important
factor for species richness, population density, immigration and extinction of
butterflies.
How aphid attack and soil fertility intreract on root associaned biota.
Mette Vestergård, Lisa Bjørnlund, Søren Christensen (Copenhagen Univ., Biological
Inst. Dept. Terrestrial Ecology, Universitetsparken 15, DK-2100 Copenhagen,
Denmark).
We present the first report on aphid effects on rhizosphere organisms as influenced by
soil nutrient status and plant development. Barley plants grown in pots subjected to
low (0), poorly balanced (N) or balanced (NP) fertilisation were sampled in the early
growth phase (day 25), one week before and one week after ear emergence. Aphids
were added 16 days before samplings. In a separate experiment belowground
respiration was measured on N and NP fertilised plant-soil systems with aphid
treatments comparable to the first experiment. Aphids reduced numbers of
rhizosphere bacteria and fungal feeding nematodes one week before ear emergence.
Before ear emergence, aphids reduced belowground respiration in NP treatments.
These findings strongly indicate that aphids reduced allocation of photoassimilates to
roots and deposition of root exudates in the growth phase of the plant. Contrary, one
week after ear emergence numbers of bacteria, fungal feeding nematodes and
protozoa were higher in rhizospheres of plants subject to aphids probably because
aphids enhanced root mortality and root decomposition.
Protozoa and bacterial feeding nematodes were stimulated at different experimental
conditions with nematodes being the dominant bacterial grazers at N fertilisation and
protozoa in NP before ear emergence.
Fragmented habitats – how may these affect insect-mycorrhizal interactions?
Alan Gange (School of Biological Sciences, Royal Holloway, University of London).
There is now good evidence that the presence of arbuscular mycorrhizal fungi in plant
roots can alter the growth and reproduction of foliar-feeding insects. However, a
feature of this literature is that virtually all the experiments have taken place in
laboratory conditions. We need to scale these up to ask what effects AM fungi have
on insect communities. However, the fragmentation of mycorrhizas in field
populations is relatively unknown and could be a major barrier to such studies. In this
talk I will outline the problems that need to be addressed and suggest some ideas for
collaborative experiments that may provide a way forward.
Questions raised by policy makers and end users:
To make the concept “Habitat Fragmentation” operational for policy makers we
believe that it needs to be enriched and expanded from its simpleminded roots in
conservation biology, which is based on a simplified view of classical island
biogeography and metapopulation theory. In homogenous landscapes with intense
human land use, fragmentation of the main habitat component may be positive for
species, diversity, and ecosystem services. Fragmentation of other landscape elements
with a lower proportion in the landscape will, on the other hand, most likely be
negative for biodiversity. In real food webs, effects of fragmentation will vary
according to the scales of dynamics of organisms at different trophic levels,
precluding general statements on how fragmentation affects predators compared to
plants or herbivores (microbivores). A more thorough consideration of indirect effects
of fragmentation, and the processes involved in such chains of interactions, will lead
to a better understanding of the effects of fragmentation induced by human activities.
In soil communities such indirect effects are hypothesised to dominated over the
direct effects of habitat loss and isolation on soil organisms.
In summary, we discussed recent findings of landscape ecologists, and attempted to
compare the differences and similarities of below ground systems with above ground.
We tried to identify the most important issues brought up during the workshop, this is
now present in the paper below.
The input from the workshop has been included in a publication:
Hedlund K, Griffiths BS, Christensen S, Scheu S, Setälä H, Tscharntke T, Verhoef
H. (2004) Soil food web interactions in fragmented landscapes. Basic and Applied
Ecology 5, 495-503.