Seed mobility and connectivity in changing rural

Seed mobility and connectivity in changing
rural landscapes
Alistair G. Auffret
Department of Physical Geography and Quaternary Geology
Stockholm University
Stockholm 2013
c Alistair G. Auffret
ISSN: 1653-7211
ISBN: 978-91-7447-692-7
Cover: Richard Swan. www.richardswan.com. Back cover portrait: Louise Tränk.
Layout: Summary and Papers IV & V: Alistair Auffret based on LATEX templates by Rickard Petterson.
Published papers typeset by respective publishers, reprinted with permission. Graphics created using
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Printed by Universitetsservice US-AB, 2013.
Doctoral dissertation 2013
Alistair G. Auffret
Department of Physical Geography and Quaternary Geology
Stockholm University
Abstract. The success or failure of many organisms to respond to the challenges of habitat destruction and a warming climate lies in the ability of plant species to disperse between
isolated habitats or to migrate to new ranges. European semi-natural grasslands represent
one of the world’s most species-rich habitats at small scales, but agricultural intensification
during the 20th century has meant that many plant species are left only on small fragments
of former habitat. It is important that these plants can disperse, both for the maintenance
of existing populations, and for the colonisation of target species to restored grasslands.
This thesis investigates the ecological, geographical and historical influences on seed dispersal and connectivity in semi-natural grasslands, and the mobility of plants through time and
space. Seed dispersal by human activity has played a large role in the build-up of plant communities in rural landscapes, but patterns have shifted. Livestock are the most traditional,
and probably the most capable seed dispersal vector in the landscape, but other dispersal
methods may also be effective. Motor vehicles disperse seeds with similar traits to those
dispersed by livestock, while 39% of valuable grasslands in southern Sweden are connected
by the road network. Humans are found to disperse around one-third of available grassland
species, including several protected and red-listed species, indicating that humans may have
been valuable seed dispersers in the past when rural populations were larger. Past activities can also affect seed mobility in time through the seed bank, as seeds of grassland plant
species are shown to remain in the soil even after the grassland had been abandoned. Today however, low seed rain in intensively grazed semi-natural grasslands indicates that seed
production may be a limiting factor in allowing seeds to be dispersed in space through the
landscape.
Keywords: Biodiversity, Conservation, Functional connectivity, Historical ecology, Humanmediated dispersal, Invasive species, Landscape Ecology, Long-distance dispersal, Restoration, Seed bank, Seed dispersal, Seed rain, Structural connectivity.
Recommendations for grassland management.
• Grazing pressure must be appropriate for both seed production and colonisation. Overgrazed semi-natural grassland reduces seed availability for dispersal, while a low grazing
intensity in former arable fields reduces the likelihood of colonisation by target species. A
varied within or between year management timing and intensity might improve seed set
within existing grasslands, while still providing enough management intensity to keep the
landscape open.
• There should be a greater movement of grazing livestock in the landscape. Movement
could be between existing semi-natural grasslands or directed from semi-natural grasslands
towards restoration areas. Movement would be most beneficial to the recipient habitat at
the time of highest seed availability in the middle to late summer.
• Boundaries between semi-natural grassland and adjoining areas for restoration should be
opened up. This is another way to increase livestock movement and the spread of seeds,
while larger pastures should result in a more heterogeneous grazing pattern, improving
prospects for seed production and colonisation from both the seed bank and seed rain.
• Road verges should be managed in order to improve the habitat quality of these linear
habitats which connect many grasslands. The timing and intensity of mowing should allow
sufficient seed production for dispersal by motor vehicles.
• When managing rural landscapes, all major seed dispersal vectors should be considered with
regard to their movement, abundance and relationship to the physical landscape. Combining
the dispersal potential and structural connectivity of a landscape can help identify specific
locations for potential management intervention, which can then be considered according
to importance, feasibility and resource limitations.
• Finally, policy regarding agri-environment schemes must give land managers the required
incentives and flexibility to implement such management strategies, despite the resulting
changes in tree cover, grazing pressure and other metrics which are currently used as
guidelines for subsidy provision.
Sammanfattning. Fröspridning är en betydelsefull process för hur olika organismer
(inte bara växter) kan svara på hoten människor utsätter naturen för, till exempel klimatförändring och habitatdegradering. I Sverige skulle det största hotet mot artrikedom/biodiversitet kunna vara degraderingen och försvinnandet av naturbetesmarker och
slåtterängar i jordbrukslandskapet, vilket har skett under de senaste 150 åren. De tekniska
framstegen och rationaliseringen av jordbruket under denna tidsperiod har lett till att
många ängar förvandlats till åkermark och gamla betesmarker övergetts till skog. De
kvarstående naturbetesmarkerna är små och isolerade men är ändå den artrikaste habitattypen i världen om man räknar i liten skala. Man kan säga att naturbetesmarkerna idag är
överbelastade med biodiversitet, därför krävs det spridning av frön över de stora avstånden
mellan naturbetesmarker och till restaurerade habitat för att skydda och gynna biodiversitet för framtiden. I denna avhandling studerar jag hur människor och deras aktiviteter över
åren har påverkat hur frön rör sig genom jorbrukslandskapet i tid och rum. Fröspridning,
både direkt och indirekt påverkad av människor, har visat sig vara viktig i uppbyggnaden av växtsamhällen, men förändringarna i landskapet har också lett till förändringar i
spridningsmönster. Gräsmarksväxter kan överleva markanvändningsförändringar över tiden
genom att deras frön bevaras i jorden på mark där hävden upphört, även efter det
att växterna själva har försvunnit. Människor har haft stor inflytande över den viktiga
fröspridningen över stora avstånd, och har det än idag. Betesdjur är det mest traditionella
och effektiva sätt för frön att sprida sig och gräsmarksarters frön hittades i avföringen från
får, kor och hästar som betar dagens naturbetesmarker. Något överraskande var att bilar
och traktorer också är ganska bra på att sprida frön. Flera gräsmarksarters frön hittades
i jord som hade fastnat på fordon som kör runt i jorbrukslandskapet, trots att de brukar
identifieras som spridare av invasiva arter. Människor själva kan sprida frön när de rör sig
i artrika gräsmarker och arter som fastnar på kläder är ofta samma sorter som förväntas
fastna i pälsen på djur. Det finns flera sätt för gräsmarksväxterna att sprida sig, men samtidigt verkar det höga betestrycket i dagens naturbetesmarker missgynna fröproduktion hos
de viktiga arterna. Människor och dess spridningsförmåga är oftast betraktade som negativa
för biodiversitet men under detta arbete har det påståendet inte kunnat bekräftas. Istället
måste spridningen via mänsklig påverkan räknas med när man planerar naturvårdsåtgärder
för gräsmarker.
Rekommendationer för Naturvård.
• Betestrycket måste tillåta både fröproduktion och eventuell etablering. Ett för högt
betestryck i kvarstående naturbetesmarker minskar frömängden och ett för lågt tryck minskar förmågan för frön att etablera sig i restaurerade gräsmarker. En mer heterogen skötsel
av gräsmarker i både tid och intensitet skulle kunna öka fröproduktionen i dagens betesmarker samtidigt som det skulle hålla landskapet öppet.
• Betesdjur bör röra sig mer genom landskapet. Ökad rörelse kan vara mellan dagens
naturbetesmarker, eller mer riktad från artrika betesmarker till restaurerade områden.
Fröspridningen gynnas mest om djuren flyttas under sensommaren.
• Gränser mellan närliggande naturbetesmarker och restaureringsobjekt kan öppnas. Det
här är ett annat sätt att öka rörelsen av betesdjur och frön. Större betesmarker skulle göra
betestrycket mer heterogent, och fröproduktion och etableringsmöjligheter kunde därmed
öka.
• Vägkanter bör skötas för att förbättra kvalitetet på dessa habitat som redan ansluter till
många gräsmarker. Slåttertid och intensitet bör anpassas för att främja fröproduktion och
för att öka möjligheter för spridning med motorfordon.
• Vid naturvårdande skötsel av ett område bör samtliga fröspridningssätt övervägas. Deras
möjligheter att bidra till ökad artrikedom varierar med landskapets struktur. På så vis
kan konkreta platser för naturvårdsåtgärder identifieras och prioriteras utifrån viktighet,
genomförbarhet och tillgängliga resurser.
• Till sist måste jordbrukspolitiken bli mer flexibel och ge markägare och
naturvårdshandläggare incitament att implementera dessa strategier, trots att de
kan gå emot de parametrar som avgör jordbruksstödet idag.
Seed mobility and connectivity in changing rural landscapes
Alistair G. Auffret
List of papers ∗
This doctoral dissertation consists of this summary and the following papers, which
are referred to by their Roman numerals in the text.
I Auffret, A.G. 2011. Can seed dispersal by human activity play a useful
role for the conservation of European grasslands? Applied Vegetation
Science 14, 291–303.
II Auffret, A.G. & Cousins, S.A.O. 2011. Past and present management influences the seed bank and seed rain in a rural landscape mosaic. Journal
of Applied Ecology 48, 1278–1285.
III Auffret, A.G. & Cousins, S.A.O. Grassland connectivity by motor vehicles
and grazing livestock. Ecography in press.
∗
IV
Auffret, A.G. & Cousins, S.A.O. Humans as long-distance dispersers of rural
plant communities. PLoS ONE in press.
V
Auffret, A.G., Berg, J. & Cousins, S.A.O. Dispersal geography: a new concept for managing seed dispersal in rural landscapes. Manuscript.
Author contributions.
I
Review written by AGA.
II
Conceived and designed: AGA, SAOC. Performed experiment and analysed data: AGA.
Wrote the paper: AGA, SAOC.
III
Conceived and designed: AGA. Performed experiment and analysed data: AGA. Wrote
the paper: AGA, SAOC.
IV
Conceived and designed: AGA, SAOC. Performed experiment and analysed data: AGA.
Wrote the paper: AGA, SAOC.
V
Conceived and designed: AGA, JB, SAOC. Wrote the paper: AGA, JB, SAOC.
Introduction
Humans and the landscape
Semi-natural grasslands
Across the world, humans and their activities interact with the landscape and the organisms which inhabit it. Unfortunately, the effects of human activity
today are largely negative, and many now believe
that we are in the midst of a human-induced sixth
mass extinction of the world’s organisms (Barnosky
et al., 2011). Habitat destruction by land-use change,
and a climate which is warming due to human activity form the most serious threats to biodiversity
worldwide (Sala, 2000; Baillie et al., 2004). Species
the world over are forced to survive on isolated and
ever-smaller patches of habitat (Fahrig, 2003), while
their climatic range moves rapidly through space
(Thomas et al., 2004). If the world’s organisms are
to successfully respond to the challenges posed by
global change, they must be able to move, or disperse. Dispersal is important both for maintaining
populations at the local or regional scale (Hanski,
1999) and for tracking their climatic range to higher
latitudes or altitudes (Thomas et al., 2004), while
also being responsible for the build up of biodiversity in the first place (Eriksson et al., 2006; Vandvik
and Goldberg, 2006). On the other hand, the ability
to disperse is at the core of another currently much
debated problem, the invasion of alien species into
new regions (Baillie et al., 2004; Wilson et al., 2009),
the increase of which is also linked to the increase of
human activity and movement through time (Hulme,
2009).
It is clearly important to understand the process of dispersal, and how it relates to human activity and the physical environment in which it takes
place. The response of plant species to global change
has implications for other organisms (Berg et al.,
2010), including the limitation of dispersal by insects depending on specific host plants (Menéndez
et al., 2007; Müller et al., 2011). To move between
increasingly isolated habitat patches, or to new areas or regions, plant species must disperse further
than might be expected. The long-distance dispersal of plant species (Nathan, 2006) is therefore an
important process for understanding the ecological
responses to human-induced environmental change
worldwide (Trakhtenbrot et al., 2005). In Europe,
landscapes have been changing through human activity since the advent of agriculture around 8000
years ago (Renfrew, 2000), but the severity of recent
habitat destruction is threatening the plant communities that humans have helped to shape.
European semi-natural grasslands (Box 1) are among
the most species-rich habitats worldwide at small
spatial scales (Wilson et al., 2012). Formed and
maintained by hay-cutting and livestock grazing over
several hundreds to thousands of years, pastures
and meadows are now an important habitat for a
range of plant species (Poschlod and WallisDeVries,
2002; Eriksson, 2013). Today, more than 60 individual plant species can be found in one square metre of
species-rich grassland (Kull and Zobel, 1991; Klimeš
et al., 2001), significantly contributing to the biodiversity of rural landscapes. Two-thirds of Swedish
red-listed vascular plant species rely on rural landscapes for survival, along with 41% of red-listed insects (Gärdenfors, 2010), with semi-natural grasslands acting as important habitats for the pollinating
insects which play a vital role in agricultural landscapes (Öckinger and Smith, 2007). In addition to
the wildlife they support, grasslands are also important for recreation and cultural history, often containing sites of archaeological significance (Ihse and
Lindahl, 2000).
While the build-up of grassland habitats and biodiversity occurred slowly over a long period of time,
it took less than a century to put them under serious threat. Across Europe, the intensification of agriculture during the 20th century reduced the area of
semi-natural grassland habitat dramatically. Investigations comparing historical and present-day maps
in rural landscapes has confirmed huge grassland
declines in countries as diverse as Belgium (98% Adriaens et al., 2006), the Czech Republic (72% Skaloš et al., 2011), Estonia (90% - Saar et al., 2012),
Slovenia (70% - Kaligarič et al., 2006), Sweden (90%
- Cousins, 2009) and the United Kingdom (97% Hooftman and Bullock, 2012). As agricultural land
use became more productive and intensive, surplus
arable land was converted to improved (fertilised)
grassland or planted spruce forest, while a lot of the
less-productive semi-natural grassland pasture was
abandoned to become secondary forest.
This change in land use in the rural landscape
has led to a fragmentation of semi-natural grassland
habitat. Habitat fragmentation not only involves a
reduction in the amount of habitat, but also an increase in isolation and a decrease in quality of remaining habitat patches (Fahrig, 2003). A reduction in habitat is generally associated with a reduction in biodiversity, because larger areas are ex1
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pected to support a higher number of species, and
vice versa (the species-area relationship: Arrhenius,
1921; Drakare et al., 2006). Habitat fragmentation
also involves an increase in the relative amounts of
habitat edges in a landscape, which can affect plant
communities in various ways (Ries et al., 2004). Further to the risks of the fragmentation of these grasslands, indirect effects of agricultural change such as
nitrogen deposition are also causing long-term dam2
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age to grassland communities (Stevens et al., 2011;
Isbell et al., 2013).
Despite these challenges, the observed negative
effects of habitat destruction on biodiversity have
been smaller – or at least slower – than expected, and
many rural landscapes still support the kind biodiversity expected before habitat destruction and fragmentation. By comparing historical and present-day
maps, it has been found that a landscape’s current
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
Table 1. Approximate mean and maximum distances seeds can be dispersed by various vectors.
Dispersal vector
Wind
Ballistic
Water
Ant
Vertebrates
- Attachment
- Digestion
- Seed caching
Humans
Known as
Anemochory
Hydrochory
Myrmecochory
Zoochory
Epizoochory
Endozoochory
Approximate
mean distances
9m
1.4 m
538 m
3.61 m
Anthropochory
Motor vehicles
- Mud
- Airflow
biodiversity is often better explained by the past rural landscape, when managed grasslands were much
larger and better connected (Lindborg and Eriksson, 2004; Gustavsson et al., 2007; Cousins and Vanhoenacker, 2011). This phenomenon is known as the
’extinction debt’ (Tilman et al., 1994), by which it
is implied that extinctions will occur in the future
in order to put the landscape and its diversity back
in equilibrium according to the species-area relationship. Although biodiversity has been slow to respond
to landscape change during the 20th century, shifts in
plant species composition to more persistent species
in fragmented habitats have been detected (Maurer
et al., 2003; Lindborg et al., 2012).
So, even though semi-natural grasslands have become very much fragmented, they are still of great
importance for local biodiversity. However, in order
to maintain and support their high biodiversity and
other values in the long-term and at a large spatial scale, plants must be able to move between fragmented grasslands (Hanski, 1999), and former habitat must be restored to increase the area of habitat
in the landscape to ease the threat of the extinction
debt (Kuussaari et al., 2009). For both these points,
seed dispersal across the landscape is key.
Seed dispersal
In flowering plants, effective dispersal entails the establishment of new individual plants (Schupp et al.,
2010), the culmination of a multi-step process from
seed production through seed transport to seedling
recruitment (Eriksson, 2000). Successful seed dispersal between two points can broadly be determined
by geographical and biological conditions: structural
and functional connectivity. Structural connectivity
can generally be defined as the organisation of habi-
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Wichmann et al (2009),
Pickering el al. (2011)
Taylor et al. (2012)
von der Lippe et al. (2013)
tat features within a landscape, while functional connectivity refers to an organism’s response to the landscape’s structure (Taylor et al., 1993). In plants,
functional connectivity involves the dispersal of seeds
between landscape features with the help of a dispersal syndrome (adaptation) and a dispersal vector
(carrier). The unassisted dispersal of plant species
across a fragmented landscape is very slow (van
Dorp et al., 1997), so in rural landscapes with isolated grasslands, the study of long-distance dispersal
vectors is important. The definition of what constitutes long-distance dispersal is case-specific (Nathan,
2006), and in this thesis it is defined as dispersal between fragmented habitat patches, or at least dispersal which has the potential to cover the necessary
distances.
How do seeds disperse?
Seeds have evolved to disperse in a number of ways
(see Table 1; Box 2). Plant species can disperse long
distances in the wind by having very small seeds,
wings or parachute-like structures, while the explosive or ballistic dispersal of seeds can transport seeds
a few metres away from their parent plant (van der
Pijl, 1972). Seeds can also be dispersed in water, by
being flushed or splashed away from the parent plant,
or dispersed longer distances either floating on, or
submerged in streams and rivers (van der Pijl, 1972).
With the help of animals, plants can disperse their
seeds in a more directed manner (Howe and Smallwood, 1982). Seeds with small, lipid-rich attachments
(elaiosomes) which attract ants are present in many
plant families (Lengyel et al., 2010), allowing seeds
be ’planted’ underground in the ants’ nest, usually
up to a few metres away from the parent plant. Animals which have larger ranges are also able to disperse seeds longer distances, while their habitat preferences can allow seeds to arrive at suitable loca3
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tions (D’hondt et al., 2012; Carlo et al., 2013). Seeds
with hooks, hairs or other appendages can disperse
long distances by attaching to the fur of animals
(Sorensen, 1986), although most plant species probably have the capability of being dispersed in this way
(Couvreur et al., 2004a). Small, hard seeds can resist
digestion to be dispersed in the droppings of animals
(Janzen, 1984; Pakeman et al., 2002), while birds and
rodents store (cache) seeds and subsequently forget
4
about them (Vander Wall et al., 2005). There are
many plant species which have seeds that do not appear to be specially adapted to any mechanisms of
dispersal, but despite this can still be transported
by a range different dispersal vectors (van der Pijl,
1972).
In addition to seeds dispersing in space, many
species also have the capacity to disperse in time by
remaining dormant for a period in the soil in seed
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
banks. This allows the seeds to ’wait’ until suitable
conditions for growth in unpredictable environments
(Thompson and Grime, 1979), and traces of former
plant communities can be detected in the seed bank
for a very long time afterwards (Plue et al., 2008).
Temporal seed dispersal might then be another useful
strategy for plant species in a changing rural landscape, especially regarding the restoration of former
habitats (Kalamees et al., 2012).
It is clear from Table 1 that seeds are able to
travel long distances with their different vectors,
however mean dispersal distances are relatively short
compared to the maximum measured distances.
The use of multiple vectors is possible to increase
dispersal distances, and seeds can also travel long
distances using dispersal vectors to which they
are not necessarily adapted. These non-standard
dispersal events are relatively regular providers of
long-distance dispersal, which themselves have a
disproportionately high importance for plant movement and dynamics (Higgins et al., 2003; Nathan,
2006). Humans are a regular and well reported
non-standard means of long-distance dispersal, and
the potential role of humans in seed dispersal has
been recognised for some time (Woodruffe-Peacock,
1918; Clifford, 1959; Hodkinson and Thompson,
1997). Recently, human-mediated dispersal was
defined as:
“...dispersal directly by humans, on their clothes
or by human-associated vectors, including all means
of human transport, pets and livestock, human equipment and food”
Wichmann et al. (2009)
As humans continue to affect all natural systems
and their organisms, including the full range of seed
dispersal vectors (even by indirectly affecting wind
dispersal through climatic change - Bullock et al.,
2012), the study of how human activity directly and
indirectly affects seed dispersal is of great interest
for biodiversity science worldwide. This is particularly relevant in rural landscapes, where human and
landscape histories are so intertwined.
Connectivity and dispersal in rural
landscapes
Connectivity, and the maintenance and restoration
of existing habitats are important for the conservation of ecological communities under threat (Lindenmayer et al., 2008; Hodgson et al., 2009). As
mentioned earlier, dispersal and connectivity are in-
herently linked. Despite the importance of dispersal, plant communities are generally regarded as being seed or dispersal limited (Primack and Miao,
1992; Ehrlén and Eriksson, 2000; Stein et al., 2008).
Furthermore, when a landscape becomes more fragmented, less connected and dispersal becomes more
important, species find it more difficult to disperse.
This increases dispersal limitation (Ozinga et al.,
2005), eventually leading to dispersal failure and local extinctions (Ozinga et al., 2009), and the slow recovery of target communities after restoration (Öster
et al., 2009; Helsen et al., 2013).
In the case of semi-natural grasslands, structural
connectivity was greatly reduced during the 20th
century, but small and linear landscape elements
such as road verges and field boundaries can still
contain grassland communities (Smart et al., 2002;
Cousins, 2006). Functional connectivity through seed
dispersal is also likely to have reduced over the same
period. In the past, dispersal from the local to international scale was provided through the movement of
grazing livestock, which are now largely confined to
small pastures for the whole grazing season (Bruun
and Fritzbøger, 2002). Dispersal was also provided by
other agricultural practices, such as hay-making and
fertilising with manure, and most of the historical
landscape was connected by these different dispersal
processes (Poschlod and Bonn, 1998). As these traditional vectors have disappeared from the landscape,
the dispersal of seeds between fragmented grasslands
is more unlikely (Diacon-Bolli et al., in press), and
the colonisation of grassland plants to different types
of restored areas is also found to be limited by a lack
of dispersal (Walker et al., 2004; Bossuyt and Honnay, 2008).
Despite the apparent threats to dispersal in grasslands, seeds arriving from different spatial scales, as
well as those emerging from the seed bank are important contributors to local diversity when gaps
in the vegetation become available (Pakeman and
Small, 2005; Vandvik and Goldberg, 2006). In terms
of potential restoration, seed banks also contain significant reserves of diversity in abandoned pastures
(Plue and Cousins, 2013). Although dispersal (especially long-distance) is clearly important for conservation (Trakhtenbrot et al., 2005), it is generally not
directly considered in conservation planning (McConkey et al., 2012). In rural landscapes, where for
centuries human activity has shaped plant communities and had both direct and indirect effects on dispersal and connectivity, it is of interest to explore the
interplay between historical and present-day land use
and management, and their effects on the dispersal
of plant species in these important habitats.
5
A.G. AUFFRET
The aim of this thesis
The work described in this thesis studies how human
activity and seed dispersal are linked in the rural
landscape. Specifically, I investigate the ecological,
geographical and historical influences on seed dispersal in fragmented semi-natural grasslands today.
Concentrating mainly on the different seed dispersal
vectors in the rural landscape, I focus on how mobile
seeds are in time and space, using this to evaluate
the potential for seeds to disperse successfully and
effectively. In these valuable historical landscapes, I
look at how seed mobility can be directly and indirectly influenced by past land use and management,
exploring the changing roles of historical dispersal
vectors, and the roles that new dispersal vectors
can have in the landscape today. Specifically, I aim
to identify the main seed dispersal vectors in the
rural landscape, understand which types of plants
and seeds they disperse, and evaluate their role in
seed dispersal in the context of the conservation
and restoration of semi-natural grasslands. Another
important goal is to give concrete examples for how
any findings can be applied in the conservation of
semi-natural grasslands, with regards to improving
structural and functional connectivity at the landscape scale.
The thesis is broadly laid out in three stages:
1. Assessment of current knowledge. Paper I is the
result of an extensive literature search with the
aim of collating what is known about how humans can mediate the dispersal of seeds in the
rural landscape with a focus on the conservation
and restoration of European semi-natural grasslands. Important dispersal vectors are identified,
along with gaps in the knowledge and the need
for more research.
6
2. Empirical investigation. Forming the main part
of the thesis, Papers II–IV are the result of three
investigations studying different aspects of seed
dispersal in rural landscapes. Paper II describes
an investigation of the mobility of seeds in time
(through the soil seed bank) and in space (in
seed rain), and how they relate to current or former land use, without directly considering the
vector by which the seed arrived at the site. Papers III and IV consider three different dispersal vectors, with the aim of identifying which
species can be dispersed long distances with the
help of humans, and what attributes (life-history
traits) of the seeds and plants of these species
have. Paper III compares the potential role of
a traditional long-distance seed dispersal vector
(free-ranging livestock) with that of a modern
one (motor vehicles). The structural connectivity of grasslands provided by present-day road
networks is also investigated. Paper IV evaluates
the role of humans themselves as seed dispersal
vectors. Seeds dispersed from species-rich meadows are compared to the available species pools,
and the past and present roles of humans in the
dispersal of plant species in the rural landscape
are discussed.
3. Future directions. Using the knowledge gained
from the previous stages, Paper V looks forward
by suggesting a way to broadly include dispersal in conservation planning. Here it is suggested
that a knowledge of the landscape and its main
seed dispersal vectors can form a basis for understanding the potential for seeds to cross between
fragmented habitats.
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
Assessment of the
current knowledge
(Paper I)
With the aim of capturing the state of the art
with regard to how humans can affect seed dispersal in rural landscapes, a literature search
was conducted for human-mediated dispersal studies in European grasslands. The following broad
search terms were used in the ISI Web of Science
(http://www.isiknowledge.com): anthropochor*, dispers* cloth*, dispers* footwear, human mediated dispersal, endozoochor*, epizoochor*, exozoochor*, motor vehicle* dispers*, zoochor* (see Table 1 for different types of dispersal and their names). Relevant
publications found in the reference lists of resulting
articles were also considered.
Three main vectors of human-mediated seed dispersal for European grassland plants were identified:
grazing livestock, motor vehicles and human clothing
(Box 3). Livestock had unsurprisingly received the
most attention in the literature. Cattle can disperse
a great deal of seeds and species in their manure,
accumulating to over a million or more seeds per individual and year (Cosyns et al., 2005a; Mouissie et
al., 2005), while seeds are also transported in their
coats (Couvreur et al., 2004b). Sheep are also good
at moving seeds, especially in their coat (Fischer et
al., 1996; Wessels et al., 2008), and horses and donkeys complete the set of livestock studied (Cosyns
and Hoffmann, 2005; Couvreur et al., 2005). Dispersal on the outside (epi-) and through the inside
(endozoochory) of grazers are reported to be complementary with regards to the species transported
(Couvreur et al., 2005). Different livestock can also
complement one another, with sheep more successful epizoochorous and larger animals endozoochorous
dispersers. With regards to dispersal distances, endozoochory can disperse seeds as far as the animal can
move within two to three days (Cosyns et al., 2005b),
while sheep can disperse seeds more than 400 km in
their coats (Manzano and Malo, 2006).
Motor vehicles have also been found to disperse
a lot of seeds. Private vehicles disperse seeds representative of the local roadside flora, but studies
are concentrated in urban and suburban environments with a focus on ruderal and invasive species
(Hodkinson and Thompson, 1997; Zwaenepoel et al.,
2006; von der Lippe and Kowarik, 2007). In rural
areas, where roadsides contain grassland species in
the vegetation and seed bank (Milberg and Persson, 1994; Cousins, 2006), the dispersal of grassland
species across the landscape might be more common.
Agricultural machines are more concentrated in rural environments, and the limited research regarding
their ability to disperse seeds indicates they are also
quite capable of transporting available seeds (Strykstra et al., 1997; Mayer, 2000).
Humans can also disperse seeds of many species
on their clothes and shoes (Mount and Pickering, 2009). Investigations into this type of humanmediated dispersal have mainly been concerned with
the spread of invasive species to sensitive areas
(Healy, 1943; Whinam et al., 2005), and a study from
Europe investigating which seeds and species are dispersed on clothing is lacking. Long distances are also
possible using this vector, with seeds able to remain
attached to footwear for the duration of a 5 km walk
(Wichmann et al., 2009; Pickering et al., 2011).
Based on the literature search, it appears that
along with the fragmentation of grassland habitat,
a decline in dispersal has also occurred with agricultural change during the 20th century. Less movement
of livestock, along with a declining rural population
is likely to have reduced dispersal opportunities for
grassland plants. It is, however, important that modern seed dispersal vectors such as motor vehicles are
also considered, and that views of human-mediated
dispersal in general are not biased towards the spread
of invasive species. The review resulted in management recommendations, namely the need for more
mixed grazing, and the increased movement of livestock across the landscape, both between pastures
and to targets for restoration. The gaps in the knowledge which would manifest in the following section
of this thesis were the need to study the potential
of the three main human-mediated dispersal vectors
(livestock, motor vehicles and humans) to provide
connectivity in the modern rural landscape.
7
A.G. AUFFRET
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Empirical
investigation
(Papers II–IV)
Methods
Studying and measuring seed dispersal is very difficult (Nathan et al., 2003; Bullock et al., 2006). Different methods can be employed according to the goals
of the study. Unless a dispersal event is slow enough,
or the distance short enough to be observed during
the whole movement stage from parent plant to settled location, natural dispersal distances cannot realistically be measured. Instead, seeds generally have
to be artificially attached to a vector, such as animals
(e.g. Kiviniemi and Eriksson, 1999) and relocated
8
after deposition. This can mean that seeds do not
become attached to the vector as they might do in
’real life’, and that for logistical reasons only one or a
handful of species can be studied. Another approach
is – depending on the studied vector(s) – to manually remove seeds from the vector (e.g. Couvreur
et al., 2004b), collect deposited seeds (e.g. Cosyns
and Hoffmann, 2005) or use seed traps to collect dispersed seeds (e.g. Jakobsson et al., 2006). This means
that the source location of the seeds is not usually
known, and therefore distances cannot be measured.
However, this approach does allow for the identification of the species which can be dispersed in a certain
way, and equally importantly, which species cannot.
Both the described approaches (attaching and removing/collecting) yield different information, and
both are useful in contributing to the understanding
of long-distance seed dispersal. The empirical investigations in this thesis (Papers II–IV) use the latter
method of sample collection, as the aim of the work
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
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was to broadly understand the impacts of human activity and management on dispersal processes at the
community and landscape level. Therefore, understanding which species and what kinds of species are
dispersed was prioritised over how far seeds could
disperse through human activity.
Study area
The main study area for this work (Papers II–III)
was the rural landscape around the parishes of Ludgo
and Spelvik in the county of Södermanland, southern Sweden (58 ◦ 54’ N, 17 ◦ 00’ E; Figure 1; Box 4).
Like much of southern Sweden, the region has a long
history of anthropogenic influence. Historical maps
from the 17th century show that at that time, most
of the landscape was covered in open or semi-open
pasture or meadow. By the beginning of the 20th century, a lot of grassland close to the settlements had
been turned into arable fields as technology had progressed to allow heavier soils to be ploughed. Another
period of agricultural change took place during the
20th century. Farming shifted from being sustenancebased to commercial, resulting in a more rationalised
and intensive agriculture. In the 1950s many wooded
grasslands were planted with coniferous forest. Surplus arable land was converted to improved grassland or planted spruce forest, while a lot of the lessproductive semi-natural grassland pasture was abandoned to become secondary forest. In addition to the
main land uses, small and remnant habitats exist on
mid-field islets, road verges and field strips. There
are around 15 farms in the area, and just over 200
other houses, many of which are summer cottages,
and mostly concentrated in the village of Aspa.
Paper III also uses semi-natural grasslands from
the whole of the south of Sweden for a structural
connectivity study, while data collection for Paper
IV takes place in hay meadows from across a large
area of Sweden (Figure 1).
Historical and present-day maps and GIS
tools
Sweden has an excellent archive of detailed historical maps dating back through the past few centuries, which has given researchers the opportunity
to analyse land use and related ecological change
(e.g. Cousins, 2001; Gustavsson et al., 2007). In this
thesis, historical map data were used to select sites
for Papers II and III, by following land-use trajectories in order to find habitats with different landuse histories for Paper II, and historical semi-natural
grasslands for Paper III. Historical maps were georeferenced, interpreted and digitised to create digital maps over the main study area. Present-day
! "
! Figure 1. Map showing study areas and sites for Papers
II-V.
land-use data were extracted from Sweden’s general land-use map (Översiktskartan) and the property map (Fastighetskartan). The freely available
map data over Swedish Board of Agriculture’s (Jordbruksverket) database of valuable grasslands (TUVA,
http://www.sjv.se/tuva) was also used in the classification of today’s semi-natural grassland.
In Paper III, the structural connectivity of remaining semi-natural grasslands by road verges in
southern Sweden was assessed. First, the number
of grasslands from the TUVA valuable grassland
database lying adjacent to a public road were identified, before the distances between nearby grasslands
along the road network and Euclidean distances were
compared. In Paper IV, approximate potential dispersal distances between meadows and the postal areas of participants’ home addresses were calculated.
Throughout the thesis, data visualisation, manipulation and map creation was done using either ArcGIS 9.3–10.1 or Quantum GIS 1.6–1.7. Geographical analyses were carried out with PostGIS 1.5.3
(Holl and Plum, 2009), with the additional package
PgRouting 1.03.
9
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Seed dispersal
Seed bank (dispersal in time - Paper II)
To assess the impact of agricultural land use on the
seeds which are found buried in the soil, ten replicates of the following four habitat types were used:
10
[i] semi-natural grassland pasture, [ii] pasture which
has previously been cultivated (former arable field),
[iii] secondary woodland on abandoned semi-natural
grassland and [iv] mid-field islets (see Box 4). In each
of these ten replicates, 30 1 × 1 m plots were laid out
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
randomly in a 10 × 10 m grid (total 1200 plots). One
8 × 8 × 10 cm soil sample was taken from the centre of each plot, with the top layer of vegetation and
soil removed to leave only seeds forming part of the
permanent seed bank.
Samples were dried and cold stored, before the
soil was concentrated according to Ter Heerdt et
al. (1996). Concentrated samples were then spread
thinly on a layer of potting soil and grown in a greenhouse until germination was judged to have finished.
Emerging seedlings were identified and counted, with
unidentified seedlings replanted and grown until
identifiable.
Seed rain (Paper II)
In each of the seed bank plots described above, a seed
trap filled with potting soil, measuring 8 × 8 × 10 cm
was placed in the ground in the early summer 2008
and left out until early winter. After collection, the
contents of the seed trap were spread onto a layer
of compost and greenhouse grown according to the
method described above for the seed bank samples.
Grazing livestock (Paper III)
Seven semi-natural grasslands in the study area were
used to investigate endozoochorous dispersal by grazing livestock. Each month between May and September 2009 (five occasions), the pastures were visited,
and manure samples collected from each of the livestock types present. Two litres were collected for cattle and horses, while 1 L was collected for sheep. In
total, 31 samples were collected, of which 24 were
from cattle, four from horses and three from sheep.
These samples were dried, chilled and concentrated
similarly to the seed bank samples, before being
grown in a greenhouse, and emerging seedlings identified and counted.
Motor vehicles (Paper III)
The five farms which owned and managed the seminatural grasslands from the manure study were also
used to investigate seed dispersal by motor vehicles.
On the same sampling days as the livestock investigation, plus once in April before the livestock were let
outside, mud was collected from vehicles in the farm
yard. This generally involved one car and one allround tractor from each farm, but all vehicles present
in the farmyard which had been used between sampling periods were sampled. In total, 17 samples from
cars and 31 samples from tractors were collected. After collection, samples were processed and grown using the same method as were used for the grazing
livestock samples.
Clothing and footwear (Paper IV)
In July–September 2010, members of 38 groups of the
Swedish Society for Nature Conservation (Naturskyddsföreningen) managing 48 species-rich meadows
across Sweden took part in an investigation of seed
dispersal by humans on their clothing. Each participant was asked that on returning home after the
hay-cutting, they should remove their outer clothes,
shaking them and brushing them down, emptying
pockets, picking visible plant material and emptying
and banging together footwear. All resulting material was placed in one plastic bag and posted to me
before being examined under a microscope and any
seeds in the sample were identified and counted. A
total of 214 samples were received.
Species available for dispersal
In order that the seeds dispersed could be put into
the context of which species were available and which
did not disperse, and which life-history traits (plant
and seed attributes) might contribute to dispersal,
the local species pool was identified. This was collected in different ways for the different investigations. To assess how the established vegetation affected the seed bank and seed rain (Paper II), an
inventory of each of the 1200 1 m2 plots was undertaken to identify which plant species were available
at the plot level. The plot data were then pooled for
each of the 40 sites to identify the species pool at the
site level.
In Paper III, seeds were dispersed by livestock,
motor vehicles and farming machinery with access
to several habitats in large areas of the landscape.
Therefore the available species pool for this study
was taken from the local plant atlas (Rydberg and
Wanntorp, 2001), where all species present in the two
5 × 5 km grid squares covering the study area were
included.
A mixture of sources provided the species pools
for 36 of the 48 meadows from Paper IV. Species lists
came mostly from the groups managing the meadows, but when these were not available, data were
either extracted from the Swedish Species Gateway
(Artportalen, http://www.artportalen.se/), or from
local or regional plant atlases. Meadows in the vicinity of Stockholm where species lists were not otherwise available were inventoried especially for the
investigation.
Data analysis
A mixture of statistical techniques was used to analyse the dispersal data at both the species and community level. Lists of dispersed species were compared to lists of grassland specialists, nationally pro11
A.G. AUFFRET
Table 2. Descriptions of the different categories of species used in this thesis to evaluate positive vs negative effects of
human-mediated seed dispersal.
Definition
Over-represented
in
semi-natural
grassland vegetation compared to
abandoned grasslands, mid-field islets
and grazed former arable fields in
Ludgo-Spelvik.
Source
Paper II
Protected species
Protected by Swedish law. There are
different levels of protection, covering
some or all of the following restrictions:
picking flowers, uprooting the plant,
removing seeds and doing any of the
above for commercial reasons.
Species Protection
Statute 2007:845
Red-listed species
Plant species judged to be at risk of
extinction, according to the following
scale: LC = least concern, NT = near
threatened, VU = vulnerable, EN =
endangered, CE = critically endangered, RE = regionally extinct.
Gärdenfors (2010)
Paper II
Paper III
Paper IV
Nationally invasive species
Non-native species in Sweden whose
introduction or spread threatens local
biodiversity.
European Network on Invasive
Alien
Species
http://www.nobanis.org
Paper III
Paper IV
Internationally invasive species
Non-native species worldwide whose
introduction or spread threatens biodiversity in a country other than Sweden.
Centre
for
Agricultural
Bioscience International –
http://www.cabi.org/isc
Paper IV
Grassland specialist species
tected, red-listed (Gärdenfors, 2010) and/or nationally or internationally invasive species (Table 2).
In Paper II, the capacity for the available established species to predict dispersal in time or space
was assessed using co-correspondence analysis (Ter
Braak and Schaffers, 2004). This method involves
taking a predictor and response community from the
same set of plots. A model is created relating the
communities from all but one plot, which is then used
to try to predict the response community from the
predictor community in that remaining plot. This
is carried out for each plot in turn to assess how
well the response community can be predicted. The
method was used to evaluate how well the species
dispersed in the seed bank and seed rain were predicted by the available species in the surrounding
vegetation. Ecological community similarity of dispersed species was calculated between each habitat
type to assess if species available in the seed bank or
seed rain were more related to the established vegetation in the habitat from which they were collected,
or to another habitat. At the species level, indicator
species analysis (Dufrêne and Legendre, 1997) was
used for the vegetation data to identify characteristic species of the semi-natural grassland habitats
which could then be used to see if these ’specialists’
12
Used in
Paper II
Paper III
Act
–
Paper II
Paper III
Paper IV
were present in the seed bank or seed rain of the four
habitats.
Comparison of the dispersed and available species
communities was carried out at the trait level in Papers III–IV, as well as being discussed in terms of
percentage of the available species which were dispersed. Data regarding seed number, seed mass (mg)
and seed releasing height (m), along with those relating to the ability to form a seed bank (persistent
or transient), attach to animals (seed morphology,
hooked, otherwise appendaged or not appendaged)
or disperse in the wind (terminal velocity m s-1 ) were
extracted from the LEDA trait database (Kleyer et
al., 2008). These traits were then used to compare
dispersed and available species, to see which traits
could explain whether a seed was dispersed by livestock, manure, both or neither (multinomial logistic
regression, Venables and Ripley, 2002; Paper III), or
by humans or not (quasibinomial logistic regression,
Paper IV). Community similarity of dispersed and
available species was calculated for the meadows in
Paper IV, with linear regression used to assess how
the number of samples received from a meadow affected how well the dispersed species represented the
available species.
Differences between the species dispersed by manure and motor vehicles in Paper III were further
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
compared using permutational multivariate analysis of variance, while the individual species responsible for any differences were identified using indicator species analysis. Differences in the number of
seeds and species dispersed by the vectors through
the season were compared using Monte-Carlo random sampling. All numerical analyses in this thesis were carried out in the statistical environment R
2.11.0–2.14.1 (R Development Core Team, 2011).
Results and discussion
Dispersal in relation to available species
Across all three empirical investigations, 123 122
seeds or emerging seedlings were counted. Threehundred and seven species were positively identified
as being mobile in time or space, while many more
were grouped into aggregates or to the genus level.
From now on, all such groups are counted as species.
Figure 2. Similarity of seed bank and seed rain communities to the habitat-type vegetation to which they were
most similar, where ABA, abandoned semi-natural grasslands; FAF, former arable fields; MFI, mid-field islets;
SNG, Semi-natural grasslands. Different line formats are
used for the different habitat types to facilitate the following of arrows between the boxes.
A total of 54 357 seedlings emerged from the
seed bank and seed rain samples (Paper II), representing 188 species. The inventory of the established vegetation found 277 species, with a total of
296 species identified in the whole investigation. The
co-correspondence analysis revealed that seed bank
and seed rain communities were generally not very
well predicted by the surrounding vegetation. The
best prediction was provided for the seed bank of the
semi-natural grassland, but seed bank and vegetation
appeared to be out of synchrony in the other habitat
types. This was supported by the similarity analysis,
which showed that seed banks in the former grassland habitats (mid-field islets and abandoned grass-
lands) were more similar to the established seminatural grassland communities (Figure 2). The existence of semi-natural grassland communities in the
seed banks of abandoned habitats is not in line with
the common assertion that semi-natural grasslands
do not form permanent seed banks (Bossuyt and
Honnay, 2008), but instead indicate that as well as
current diversity patterns in the vegetation (Lindborg and Eriksson, 2004), seed bank communities
are also largely influenced by their past management.
The strength of this influence has since been found
to relate to the time since the grassland was abandoned (Plue and Cousins, 2013). The results from
the seed rain experiment showed how current management influences seed availability in the landscape,
as the seed rain in lightly-grazed former arable fields
and ungrazed abandoned habitats were most similar to the surrounding established vegetation (Figure 2). Seed rain in semi-natural grasslands was actually most similar to vegetation in former arable
fields, possibly because the intensive grazing in these
species-rich habitats only allows the most common
and widespread species to grow and produce a detectable seed rain.
The 31 samples (total volume 57.6 L) of manure
collected from livestock grazing semi-natural grassland pasture produced 31 793 seedlings of 108 species
(Figure 3). A similar number of species emerged from
mud attached motor vehicles, where 12 618 seedlings
of 110 species emerged from 48 samples (35.1 L).
Sixty-nine species were shared between the two vec-
Figure 3. Visualisation of emerging species identified
from samples of manure from livestock grazing seminatural grassland and cars and tractors driving around
the rural landscape. For simplicity, invasive and protected
species available in the plant communities are not considered.
13
A.G. AUFFRET
Figure 4. Density (boxplots) and total species richness per month (line) of [a] manure samples and [b]
motor vehicle samples throughout the grazing season. Boxes represent the upper and lower quartiles, thick
lines show the median, and the whiskers indicate the range of the dataset without outliers. Outliers (open
circles) are where an observation falls outside the quartiles +/ − (1.5× the interquartile range). Letters in
common represent no significant difference of species density (a-b) and seedling density (x-z) within vector,
while * shows significant differences between vectors for a particular month from the monte-carlo analysis.
tors, and the total of 149 species identified represented a noteworthy 25% of the landscape’s available
species pool (approximately 18% by each vector).
That such a relatively high percentage of species was
dispersed by these vectors indicates both the importance of the studied semi-natural grasslands for the
total biodiversity of the landscape, while also highlighting the potential for motor vehicles to disperse
seeds from a range of habitats in the landscape. Seed
and species density of samples were generally quite
comparable between the two vectors (Figure 4), but
despite these similarities and the number of shared
species, the composition of the samples was significantly different. Both total seed content and species
presence differed by vector according to the permutational multivariate analysis of variance (F = 29.6,
R2 = 0.28, P = 0.001, and F = 59.3, R2 = 0.44, P
= 0.001 respectively), and indicator species analysis
showed that where dispersed species did not overlap,
they were often what would be considered typical
grassland species in the case of the manure samples,
and common ruderals in the case of motor vehicles.
The clothes and shoes of humans were also found
to disperse a considerable fraction of the available
species. A total of 24 354 seeds of 197 species were
14
identified, 34% of the 514 species from the meadow
inventories (Figure 5). Of the 214 samples received,
211 (99%) contained seeds, indicating the ubiquity
Figure 5. Visualisation of seed species identified from
samples of human-dispersed seeds from 48 Swedish meadows. For simplicity, invasive and protected species available in the plant communities are not considered.
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
30
10
F = 57.83
R2= 0.62
P = <0.001
2
4
6
8
10
12
Number of samples
0.1
0.2
0.3
0.4
(b) Similarity to source community
Similarity
The indicator species analysis identified 22 grassland
specialist species in the study area for Papers II and
III (Box 5). Seeds of many these specialists were
found to be mobile in time and space. All but two
specialists were found in the seed bank samples, five
of which were found in the seed banks of the former grassland habitats despite not being available in
the established vegetation. This, along with the similarity of the abandoned seed bank communities to
the semi-natural grassland vegetation provides further evidence that semi-natural grassland plants are
able to disperse in time.
Fifteen specialists were found to be dispersed by
livestock grazing semi-natural pastures in the study
area. It is perhaps not surprising that animals grazing grasslands disperse grassland specialist species,
but specialists were also found to be mobile in other
parts of the landscape. Four specialists not present
in the vegetation of former arable fields were nevertheless found in the seed bank or seed rain in these
pastures, while eight were found in the motor vehicle samples. Although seeds of specialist species
were present in smaller concentrations compared to
the manure samples, the dispersal of more than onethird of the area’s specialist species by motor vehicles
is quite remarkable. Dispersal by motor vehicles is
generally considered in the context of invasive species
(von der Lippe and Kowarik, 2007; Taylor et al.,
2012), but only four invasive species emerged from
the samples, and these were introduced to the study
area before the invention of motor vehicles (Rydberg
and Wanntorp, 2001).
Plant species protected by Swedish law (Species
Protection Act: Statute 2007:845), and those on the
national red list of threatened species (Gärdenfors,
2010) were also found to be mobile. Three protected
or red-listed species were found in the seed bank or
seed rain, although this seemed to be quite an underrepresentation compared with what was available in
the vegetation. Seven such species were found on the
20
Specialist, protected, red-listed and invasive
species
40
50
60
(a) Species richness
Number of species
of seed dispersal on clothing and footwear. The more
samples which were received from a meadow resulted
in a higher number of species and a better representation of the community in the source meadow (Figure
6). Potential dispersal distances with humans were
found to be very long, ranging from 1.3 km to 110
km, with an average distance of 13.4 km. This shows
how modern transportation methods can greatly increase the dispersal distances previously measured
on humans walking in the landscape (Pickering et
al., 2011; Wichmann et al., 2009).
F = 16.4
R2= 0.31
P = <0.001
2
4
6
8
10
12
Number of samples
Figure 6. Effect of increasing sample size on humanmediated dispersal. Total species richness (a) and BrayCurtis similarity to source community (b) of seeds dispersed with clothing and footwear of different numbers
of volunteers cutting valuable meadows throughout Sweden.
footwear and clothing of volunteers cutting speciesrich meadows, and the fact that 34% of all the species
recorded in the sites (many of which are designated
protected areas) were dispersed by humans indicates
15
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that many typical grassland species can be dispersed
in this way. Only three invasive species were found in
the clothing and footwear samples, but 71 (36%) of
species found are considered invasive in other countries, highlighting the risk of invasions associated
with long-distance travel to sensitive areas (Ware et
al., 2011; Chown et al., 2012).
16
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Dispersal traits
The plant trait analyses revealed that life-history
and dispersal traits can to some extent determine
how species can be moved around the landscape by
different human-mediated dispersal vectors (Table
3). Both motor vehicles and livestock manure were
found to disperse small and persistent seeds. This has
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
Table 3. Species life history and dispersal traits significantly (P=<0.05) associated with dispersal via manure, motor
vehicles and clothing and footwear. A plus indicates an increased likelihood for a species having a particular trait to
be dispersed via a given vector compared to the available species pool, a minus indicates a negative effect. Brackets
means a near-significant tendency. A multinomial logistic regression of the dispersed species compared to the available
landscape species pool used the analysis for manure and motor vehicles, whereas a quasibinomial logistic regression of
dispersed seeds compared to available species in the studied meadow habitats was used for analysis of the clothing and
footwear.
Manure
Motor vehicles
Manure & Motor vehicles
Clothing & footwear
Seed bank
persistence
+
+
+
+
Seed
mass
−
−
−
Hooked
seeds
Appendaged
seeds
+
+
been previously reported for both vectors separately
(Pakeman et al., 2002; Bruun and Poschlod, 2006;
Zwaenepoel et al., 2006; von der Lippe and Kowarik,
2012). In addition, both vectors were found to disperse relatively low growing (seed releasing) species,
which probably reflects the short vegetation in the
pastures and road verges of the rural landscape. In
another study, seeds adapted to dispersal by wind
have been found to disperse in the slipstream of
cars without becoming attached (von der Lippe et
al., 2013). Comparing traits between vectors, it was
found that motor vehicles were more likely to disperse species which produce many seeds. Together
with the findings that the two vectors generally disperse species with quite similar traits, this indicates
that dispersal by motor vehicles merely requires that
the seeds are available to be dispersed. Unlike grazing
animals who consume and defecate vast quantities of
seeds every day (Cosyns et al., 2005a), attachment to
motor vehicles more stochastic, and therefore species
producing more seeds can reasonably be expected to
attach more regularly.
Species that are able to form persistent seed
banks were also found to be dispersed in clothing
and on footwear. Along with the results from grazing
livestock and motor vehicles, it shows how humanmediated dispersal can move seeds through space
which also have the ability to disperse in time. Motor
vehicles and humans might be expected to disperse
seeds with persistent seed banks as the mud attaching to vehicles and shoes will contain seeds in the
seed bank. With grazing livestock, the persistence required to form seed banks is also required to survive
gut passage, while seed-containing mud can also attach to the hooves of large herbivores (Heinken and
Raudnitschka, 2002; Picard and Baltzinger, 2012).
The tendency of seeds from lower growing plants to
disperse with humans indicates that even in relatively open habitats, smaller herbs are probably more
Seed
number
Seed
release height
−
−
−
(−)
Seed
terminal velocity
likely to be dispersed. Additionally, seeds with hooks
and other appendages were more likely to disperse on
the clothing of volunteers. In this respect, humans
can act just like other animals with regards to seed
dispersal by attachment (Römermann et al., 2005;
Hovstad et al., 2009), although a lack of humans in
the modern rural landscape compared to in the past
means that this kind of dispersal is relatively rare.
Management of structural, functional
and temporal connectivity
The results from the empirical investigations indicate
that seeds in the rural landscape have the potential
to be mobile in both time and space. Both seminatural grassland communities and local specialists
were found in the soil of abandoned grasslands and
mid-field islets. In addition, seeds were found in all
manure samples, 99% of clothing and footwear samples, and all but the very smallest of samples of mud
from motor vehicles. Around a quarter to one-third
of available species were found to be potentially dispersed by the studied vectors, including species with
a range of dispersal traits. Several grassland specialist, protected and red-listed species were present, and
relatively few invasives.
As the investigations were concerned with
human-mediated dispersal vectors, the potential for
this mobility to be realised lies to some extent in
the hands of humans managing the landscape. The
need for better connectivity and dispersal is clear,
as it was found that only 3.4% of the more than
thirty-thousand valuable grasslands in southern Sweden have another grassland less than 100 m away,
which is the distance reasonably covered by wind dispersed species (Schleicher et al., 2011). Around 40%
of valuable grasslands are structurally connected to
each other via road verges on the public road net17
A.G. AUFFRET
work, which provides a great potential for improving dispersal between fragmented grasslands. Despite
containing grassland species (Cousins, 2006), road
verges are by no means strips of semi-natural grassland, and they must be managed effectively to promote opportunities for colonisation of– and seed production by grassland species for long-distance dispersal via motor vehicles (Kiviniemi and Eriksson, 1999;
Jantunen et al., 2007).
Despite the potential for dispersal via motor
vehicles, any successful dispersal events would be
quite rare and unpredictable. Livestock were found
to disperse more grassland specialists, and at much
higher concentrations than motor vehicles. Therefore, to ensure a more dependable supply of seeds,
the potential of livestock for long-distance dispersal should be managed through the increased movement of livestock around the landscape. This could
be achieved both by moving livestock between fragmented species-rich habitats (Auffret et al., 2012), or
by opening up boundaries between species-rich pastures and restoration areas (Kumm, 2004). Movement should be concentrated in the late summer,
around the time of highest seed availability (Figure
4), and the risk of spread of unwanted species back
into the species-rich pasture must be weighed up
against the dispersal benefits (Mouissie et al., 2005).
Human-mediated dispersal of seeds on people’s
footwear and clothing can hardly be managed for
conservation purposes. However, the good representation of the available flora dispersed on clothes,
along with the increase in potential dispersal with
more samples (Figure 6) indicates how humans might
have once been regular and effective seed dispersal
vectors in the rural landscape when rural populations were larger. I have only focussed on the passive
dispersal by humans, but historical farming practices
also included the active spread of grassland seeds,
for example via the spreading of hay (Poschlod and
Bonn, 1998; Edwards et al., 2007). Since the modernisation of agriculture resulted in a rural-urban
migration (Satterthwaite et al., 2010), the reduction of humans working in the landscape might have
contributed to the dispersal failure evident in fragmented rural landscapes today (Ozinga et al., 2009).
On the other hand, the number of species identified
which are invasive in other countries shows how effective measures are needed to reduce the unintentional
dispersal of invasive species into sensitive areas by
increasingly mobile humans.
The work in this section of the thesis has generally been concerned with the movement stage of
dispersal, the mobility of seeds in time and space.
The results from Paper II also gave some implicit indications of how human management can benefit the
18
other stages of effective dispersal. The incongruence
between the established vegetation and the seed rain
in semi-natural grasslands indicates that the grazing
intensity in these pastures was too high to allow the
species present to set enough seed for future dispersal in the landscape or for seed bank replenishment.
In former arable fields, the grazing intensity was apparently too low, as several grassland specialists were
found in the seed bank and seed rain, but were never
present in the established vegetation. A lack of microsites for colonisation has previously been identified as a further limitation for restoration of these
habitats (Öster et al., 2009), to which a low grazing
intensity could be a contributing factor. In addition
to increasing seed dispersal by livestock, the removal
of boundaries between species-rich and restored pastures might also result in a more heterogeneous disturbance regime which could benefit both seed production and colonisation. Further, the strategic selection of sites for conservation and restoration management should be considered with regard to abandoned
and remnant habitats which can contain populations
of grassland communities in both the vegetation and
the seed bank. More recently abandoned sites contain
more diversity in the seed bank (Plue and Cousins,
2013), and these remnants can act as sources of diversity for the relatively seed-poor former arable fields.
Managing habitats to facilitate seed production and
colonisation is an important complement to other
measures which might improve the dispersal of seeds
in the landscape which have been found here to be
highly mobile.
Future directions
(Paper V)
Seed mobility and movement ecology
The previous sections of this thesis have presented
evidence that human-mediated seed dispersal vectors
are potentially very capable dispersers, and providing they are present, should allow ample opportunity
for the movement of plant species through the rural
landscape. Papers I–IV and the references therein
have shown how human-mediated dispersal vectors
can disperse seeds of target species and communities
long distances, representing a range of life-history
traits. While recommendations can and have been
made which might improve the potential of humanmediated seed dispersal, connections between dispersal and conservation practice are generally lacking
(Trakhtenbrot et al., 2005; McConkey et al., 2012).
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
The uncertainties regarding where seeds actually end up is an obstacle to fully understanding
how human-mediated dispersal vectors can provide
connectivity between fragmented grassland habitats.
The movement ecology paradigm (Nathan et al.,
2008) identifies the importance of knowing how seeds
are moved by their vectors, and recent work has indeed found that the behaviour of animals results in a
directional dispersal of seeds to suitable areas for establishment (Carlo et al., 2013; Perea et al., in press).
The interaction between different seed dispersal vectors and their environment is clearly an important
factor when considering long distance seed dispersal,
but a broad approach is needed if practitioners are to
be able to identify dispersal processes in a landscape
with a focus on conservation. A useful step forward
could be to redirect the focus away from species and
seeds, and onto the landscape and the dispersal vectors which inhabit it.
Paper V describes a new approach to broadly deal
with dispersal in conservation management. It involves a combination of movement ecology (Nathan
et al., 2008) and time geography (Hägerstrand,
1970). Time geography is a theoretical framework
developed in the field of human geography to describe human movement and the spread of information, based around the fact that people can only be in
one place at one time, and that they follow relatively
predictable and repetitive patterns of movement constrained by external factors. Applying the concept
of time geography to human-mediated dispersal vectors and how geographical features of the landscape
can explain or constrain their movement (Figure 7),
might allow for the broad identification of dispersal patterns in a landscape, and how structural and
functional connectivity can be managed to improve
dispersal between fragmented habitats patches.
Dispersal geography
Figure 7. Maps showing the an area of Ludgo parish, southern Sweden in 1900 and today. The geographical
features of the landscape which can influence the movement of dispersal vectors can broadly be split
into two groups. Polygons can represent areas of habitat, matrix or former/potential habitat, while their
boundaries can limit movement between landscape features. Linear features such as paths, roads and
field boundaries can provide structural connectivity between habitats, while governing the movement of
dispersal vectors such as motor vehicles, humans and livestock. A clear reduction of semi-natural habitat
has occurred between time steps, although the amount of roads has increased. Linear features other than
roads and rivers which might influence dispersal are not shown on the available maps, and such limitations
of available data should always be noted.
19
A.G. AUFFRET
Daily prism
Present
590
Cars 26 724
Cattle 1354
Horses 55
Sheep 108
Cattle 360
Tractors 1793
Sheep 197
Fallow deer 504
Elk 70
Horses 139
None
1473
1900
Wild animals have largely the same freedom to move
through the landscape as previously, but were hunted
close to extinction in the 19th century, and are present
at much higher concentrations today.
Previously, livestock were vital for both labour and food
production, and their manure was an important
fertiliser. Animals had much more freedom to roam the
landscape, and in principle all available land was grazed,
including arable fields post-harvest. Today, livestock are
much more constrained to their pastures and individual
farms.
At the turn of the 20th century, motor vehicles were
very rare. Horse-drawn carts existed, but more dispersal
was probably provided by the livestock pulling the cart
(below). Today, cars travel long distances, but are
constrained at the landscape scale by roads. On the
other hand, tractors have more freedom to move in
different areas of the landscape.
Not only was there a higher population density in rural
areas compared to today, but all households were
involved in agriculture, and people covered long
distances moving across the landscape. Today, most
people leave the landscape to go to work, and are only
active for short periods of the day at smaller scales,
constrained by time and land use.
Explanation
Öster-Malma hunting area (ca 155 km2 ).
Source
1900: Swedish Association for Hunting and Wildlife
Management.
Present: Swedish Association for Hunting and Wildlife
Management and Södermanland county board (number
of animals shot during the 2011/12 hunting season).
Scale
Parishes of Ludgo and Spelvik (ca 92 km2 ).
Source
1900: Swedish Board of Agriculture.
Present: Swedish Board of Agriculture (data for 2010).
Scale
Nyköping municipality (ca 1554 km2 ).
Source
Present: Statistics Sweden (data for 2011).
Scale
Parishes of Ludgo and Spelvik (ca 92 km2 ).
Source
1900: Södermanland county board.
Present: Nyköping municipality (data for 2013).
Scale
Source
Table 4: Shifts in the mobility and numbers of seed dispersal vectors in the rural landscape between 1900 and today. Daily prisms show relative
movement ranges of four dispersal vectors in the landscape, where darker shading indicates the relative populations of vectors based on real data.
Vector
Humans
Motor vehicles
Livestock
Wild animals
Negligible
Roe deer 84
Red deer 63
Wild boar 201
20
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
The dispersal geography of a case
landscape
To illustrate this idea, the study area from Papers II–III was used, with two time layers (today
and the beginning of the 20th century) used to
compare polygon and linear features in contrasting
landscapes (Figure 7). Like most of Europe, there
has been a huge reduction in semi-natural grassland habitat during the past 100 years. Linear landscape features (roads) have increased according to
the map, although there has actually been a general trend in Sweden, and probably much of Europe
for the reduction in linear features such as footpaths,
hedgerows, ditches and field boundaries in rural landscapes (Ihse, 1995). Table 4 illustrates the changing
movement patterns and populations of four dispersal vectors at the two time steps. The time geography framework’s daily prisms of movement give an
indication of when and how far the different vectors
move in the landscape, and data regarding the populations of the vectors were collated. This allows for
an assessment of the main dispersal vectors which are
active in the landscape, and the changes of dispersal
potential provided by different vectors between two
landscapes or two time periods can be broadly identified. Along with the main dispersal vectors iden-
tified in Paper I (humans, livestock and motor vehicles), free-ranging wild herbivores were also considered, as they have also been identified as longdistance dispersal vectors in the landscape, often dispersing species of open grassland habitats in their
fur, hooves and dung (Heinken and Raudnitschka,
2002; Eycott et al., 2007; Jaroszewicz et al., 2009).
Although not strictly human-mediated vectors, their
movements can be influenced by land use and populations are controlled by hunting.
The landscape and the movement of its dispersal
vectors were then combined to visualise the landscape in terms of dispersal potential and limitation (Figure 8). While the historical map shows a
well-connected landscape with much dispersal potential, the physical and human geographical constraints mean that dispersal in today’s landscape is
much more limited. However, the exercise facilitates
the identification of areas where management to improve dispersal through increasing structural and
functional connectivity can be implemented. Recommendations for management from the earlier studies
in this thesis, such as the management of road verges
to improve seed production and dispersal (Paper
III), the rotational grazing of livestock between seminatural pastures (Paper III) and the opening up of
boundaries between semi-natural grassland and for-
Figure 8. Visualisation of dispersal patterns in a rural landscape in southern Sweden in two time steps
based on livestock movement in semi-natural grasslands, wind dispersal (100 m) and linear features. Letters
indicate areas where dispersal is constrained and/or management could be altered to improve dispersal. (A)
shows how much dispersal is largely limited to within-habitat movement of livestock. Linear features such
as road verges (B) can connect fragmented grasslands, while boundaries exist between adjacent habitat
and potential habitat (C) which limit movement of vectors between them. Purely functional connectivity
could be achieved by moving livestock between fragmented pastures (D).
21
A.G. AUFFRET
mer arable field (Paper II) can now be clearly identified geographically. Comparing two different landscapes, be it in time or space, can also be useful with
regard to the populations and movement of dispersal vectors in the landscape. In this case study, there
have been increases in some dispersal vectors, but
decreases in others, while their mobility through the
landscape has also changed (Table 4). It can be valuable to identify these differences, and where possible
manage landscapes and vectors accordingly. Not all
vectors can be managed for dispersal, but populations of wild animals can be maintained at healthy
levels as well as allowing areas of shelter to grow on
existing habitat may facilitate some semi-directed,
rare long-distance dispersal events. Humans can also
not be managed to facilitate dispersal today, but
in other areas such tourist hotspots where invasive
species can be a threat, the number and mobility of
humans in the landscape can be a very important
factor for conservation.
are managed to translate seed mobility into effective
dispersal and functional connectivity.
I believe that looking at the movement ecology
of seed dispersal vectors is an important forward
step in the ecology of plant dispersal. The dispersal geography concept presented here may not be
the definitive path, but identifying the importance of
the interaction of dispersal vectors and the landscape
is certainly something to consider alongside gaining
further understanding of different stages of humanmediated seed dispersal, from attachment to detachment and colonisation. Looking at the movement and
behaviour of human-mediated seed dispersal vectors
in relation to their environment should aid the understanding of their contribution to the build-up of
biodiversity in historical landscapes, as well as the
important role they may play in facing current and
future ecological challenges.
Concluding remarks
Many thanks to Sara Cousins, Ove Eriksson and Jan
Plue for reading and commenting upon earlier versions of this summary. Louise Tränk helped with the
Swedish sections.
The work presented in this thesis has provided evidence that seeds in the rural landscape are highly
mobile, in both space and time. Three main humanmediated dispersal vectors, livestock, humans and
motor vehicles, were identified and found to move
many seeds of many species, potentially long distances. Seed dispersal by human-mediated vectors
was near ubiquitous, with very few samples from
motor vehicles and human clothing not containing
any seeds at all. The human-mediated vectors investigated were generally found to disperse more
grassland specialists and/or protected and red-listed
species than invasive species. Seeds were found to
attach to humans just as they would to any other
animal, and motor vehicles have the potential to disperse the same kinds of species as livestock disperse
in their manure. Especially with regard to dispersal
by motor vehicles and directly by humans, I hope
that this work will help to remove any bias with
regards to human-mediated dispersal, which is often studied in the context of invasive alien species.
There has certainly been a shift in dispersal patterns in the rural landscape, from the well-connected
former landscapes with a free movement of vectors,
to today’s landscape of small and isolated habitat
patches, with reduced numbers of historical vectors
more confined in their movements. New vectors have
arrived, but in landscapes where structural connectivity has been lost, it is important that all humanmediated seed dispersal vectors, both old and new,
22
Acknowledgements
Financial support
Funding for this PhD project was provided by grant
number 2006-2130 from the Swedish Research Council for Environment, Agricultural Sciences and Spatial planning (FORMAS) to Sara Cousins. Many
thanks also go to the Department of Physical Geography and Quaternary Geology for providing my
salary for the second half of my studies. Generous
financial help from AEW Smitt’s scholarship and
the cross-disciplinary project EkoKlim at Stockholm
University allowed Paper IV to become a reality.
Help from K A Wallenberg’s fund, and the International Association for Landscape Ecology allowed me
to travel to Beijing in 2011 to present my work, while
the Bert Bolin Centre for Climate Research funded
my trip to a rewarding summer school in Copenhagen
in 2010.
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SEED MOBILITY AND LANDSCAPE CONNECTIVITY
Summary of papers
Paper I
Paper II
Can seed dispersal by human activity play a
useful role for the conservation of European
grasslands?
Past and present management influences the
seed bank and seed rain in a rural landscape
mosaic
A.G. Auffret
Humans have influenced the dispersal of plant species
throughout history. In the European rural landscape,
where species-rich semi-natural grasslands have resulted from a long history of management, dispersal is now thought to be a limiting factor for the
conservation and restoration of grasslands which
have become fragmented due to agricultural change.
This paper reviews the recent research into humanmediated dispersal in the European rural landscape,
and explores the potential positive aspect of humanmediated dispersal for grassland conservation, in
contrast to its common association with the spread
of invasive species. A literature search was undertaken to identify the different human-mediated dispersal vectors operating in rural landscapes, and for
the assessment of their dispersal potential in the historical and modern landscape. Grazing animals are
important dispersers, transporting a high percentage
of available species pools on their fur and in their manure. However, the reduced movement of livestock
through the landscape has also meant a reduction in
seeds dispersed in this way. To address this problem,
there should be a greater movement of grazing animals throughout the landscape, either within larger
grazing areas or between existing grasslands. Where
this is not possible, other, more directed dispersal of
seeds from species-rich communities to target sites
should be considered. Other, non-standard humanmediated dispersal vectors can also transport seeds of
many species. Both private vehicles and agricultural
machinery have been found to disperse seeds with a
variety of dispersal specialisations, but further investigation is required to understand their role in rural
landscapes where road verges can host grassland specialist communities. Humans and their pets are also
identified as capable seed dispersers, but Europeanbased research into the topic is severely lacking. The
potential of non-standard human-mediated seed dispersal vectors to make a positive contribution to biodiversity should be considered, but more research
into all types of human-mediated vectors is important if we are to fully understand their role in the
dispersal of plant species in fragmented landscapes.
A.G. Auffret, S.A.O. Cousins
Seed banks represent a plant’s ability to disperse in
time, while seed rain represents dispersal in space.
Both have the potential to be important sources of
diversity in the rural landscape, where fragmented
habitats are linked by their historical land uses. In
this paper, seed bank, seed rain and established vegetation were sampled in four habitat types: abandoned semi-natural grassland, grazed former arable
field, mid-field islets and grazed semi-natural grassland in a rural landscape in southern Sweden. The
results from this large-scale experiment then examine
whether community patterns can be distinguished
at large spatial scales and whether seed bank and
seed rain are best explained by current, past or intended future vegetation communities. We counted
54 357 seedlings of 188 species from 1190 seed bank
and 797 seed rain samples. Seed bank, seed rain and
established vegetation communities all differed according to the habitat they were sampled in, but
despite these differences, several species characteristic of managed grassland vegetation were present
in the seed bank, seed rain and vegetation of the
other three habitats. The seed banks of semi-natural
grassland and the seed rain of the former arable fields
were generally better predicted by their surrounding
established vegetation than were the other habitat
types. The seed rain was generally most similar to the
surrounding vegetation, except for the semi-natural
grasslands where the seed rain most resembled the
vegetation in the former arable fields. On the other
hand, seed banks were most similar to the vegetation in semi-natural grassland in all habitats except
for the former arable fields, and grassland specialist
species remained in the seed banks of the abandoned
grasslands and mid-field islets even after they had
disappeared above-ground. This indicates that seminatural grassland communities are able to form seed
banks which survive land-use change and abandonment, but today’s grasslands are not setting enough
seed for dispersal at the local and landscape scale.
Despite today’s grazing management, gap availability and seed input could be limiting the colonisation
of target species in former arable fields, which were
sometimes present in the seed bank and seed rain
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A.G. AUFFRET
but were not in the established vegetation. Meanwhile, remnant populations in the seed banks indicate that abandoned grasslands and mid-field islets
could be valuable sources of future diversity in the
landscape after restoration. By connecting existing
grasslands with restoration targets, increased disturbance in the target habitats would allow for colonisation via the seed bank or seed rain, while decreased grazing intensity would benefit seed production in the source grasslands. Otherwise, landscapewide propagule availability might increase with a
more varied timing and intensity of management.
Paper III
Grassland connectivity by motor vehicles
and grazing livestock
A.G. Auffret, S.A.O. Cousins
In addition to habitat loss and fragmentation, agricultural change has led to a change in seed dispersal
processes in the rural landscape through a loss of
structural and functional connectivity. In rural landscapes, human-mediated dispersal vectors are prevalent, and in this paper, we explored whether the loss
of connectivity via free-ranging livestock could be
mitigated by the increase in roads and motor vehicles. We found that 39% of all valuable semi-natural
grassland habitats in southern Sweden are adjacent
to public road verges, with a typical distance of
around 1 km between grasslands along verges. In
the rural landscape, where road verges are often considered to be suitable habitat for grassland species,
this could provide useful structural connectivity between grassland patches. Additionally, by collecting
mud attached to cars and farming machinery and
manure from livestock (cattle, horse, sheep) grazing
semi-natural grassland pasture, we found that motor
vehicles are also capable seed dispersers. A similar
number of species were dispersed by both livestock
and motor vehicles, although the composition of samples was quite different. Motor vehicles dispersed
more grassland specialists than invasive species, although in much lower abundances than did grazing
livestock. Despite these differences, motor vehicles
were found to be able to disperse species with the
same kinds of dispersal traits as livestock, with lowgrowing plants, as well as those with small seeds and
persistent seeds over-represented in the samples. A
high number of seeds, species and specialists in manure samples means that greater movement of livestock is desirable to increase functional grassland
connectivity. However, effective management could
improve the suitability of roadsides as grassland cor28
ridors and increase the availability of seeds for longdistance human-mediated dispersal via cars and tractors. Our results suggest that in many rural landscapes, connectivity by road networks could help mediate habitat loss and fragmentation of grasslands.
However, such effects can be context dependent, and
the connectivity provided by roads could have serious negative consequences in other regions where
invasive species are more of a threat.
Paper IV
Humans as long-distance dispersers of rural
plant communities
A.G. Auffret, S.A.O. Cousins
Humans are known for their capacity to disperse organisms long distances. Long-distance dispersal can
be important for species threatened by habitat destruction, but research into human-mediated dispersal is often focussed to few and/or invasive species. In
this paper, we use citizen science to identify the capacity for humans to disperse seeds on their clothes
and footwear from a known species pool in a valuable habitat, allowing for an assessment of the fraction and types of species dispersed by humans in
an alternative context. We collected material from
volunteers cutting 48 species-rich meadows throughout Sweden. Almost all (99%) of the 214 samples
contained seeds, with a total of 24 354 seeds of 197
species counted. This represented 34% of the available species pool including several rare and protected
species. However, 71 species (36%) are considered invasive elsewhere in the world, highlighting the risk of
human-mediated dispersal in sensitive areas. Trait
analysis showed that as with other animals, seeds
with hooks or other appendages were more likely to
be dispersed by humans, while seeds with a persistent seed bank were also over-represented. The more
samples received from a meadow resulted in more dispersal, both in terms of the total number of species
and representation of the meadow’s source community. The use of motor vehicles by participants resulted in longer dispersal distances than previously
recorded for clothing and footwear, with an average distance of 13 km. We consider humans capable
seed dispersers, transporting a significant proportion
of the plant communities in which they are active,
just like more traditional vectors such as livestock.
When rural populations were larger, people might
have been regular and effective seed dispersers, and
the urbanisation resulting in a reduction in humans
in the landscape may have exacerbated the dispersal
failure evident in declining plant populations today.
SEED MOBILITY AND LANDSCAPE CONNECTIVITY
With the fragmentation of habitat and changes in
land use resulting from agricultural change, and the
increased mobility of humans worldwide, the dispersal role of humans may have shifted from providers
of regular local and landscape dispersal to providers
of much rarer long-distance and regional dispersal,
and international invasion.
Paper V
Dispersal geography: a new concept for
managing seed dispersal in rural landscapes
A.G. Auffret, J. Berg, S.A.O. Cousins
The difficulties of understanding the mechanics of
seed dispersal with regards to attachment, detachment, distance and direction means that dispersal is
not often taken into account in conservation planning. Recently, the movement and behaviour of seed
dispersal vectors in combination with the landscape
they inhabit have been found to aid the prediction
of where seeds disperse to. In human-dominated
landscapes however, seed dispersal is largely humanmediated and often occurs by non-standard vectors.
Human-mediated vectors are very capable of dispersing seeds of a wide range of plants long distances,
and despite uncertainties in the whole dispersal process, their movements follow fairly predictable patterns. Here we present a method of visualising seed
dispersal processes, where geographical features are
used in combination with knowledge of dispersal vectors to identify dispersal potential and limitations in
real landscapes, using data which should be readily available to practitioners. To illustrate the approach, we compare dispersal between two time periods in a rural landscape in southern Sweden. As
habitat patches have become smaller and more isolated, there has also been a shift in the available seed
dispersal vectors, their populations and their movement patterns. Visualising these changes has allowed
us to identify concrete management recommendations in specific areas of the landscape. Although
our focus was conservation in traditional landscapes,
the method could also be used to compare different landscapes, and in the identification of dispersal
pathways of invasive species. The need for including dispersal in conservation measures is clear, and
we believe it is timely to consider a more general
approach, shifting the focus from individual seeds
to dispersal vectors, and their interactions with the
landscape which surrounds them.
29
A.G. AUFFRET
Thank you
I really love my work, and the help and company of others plays a big part in that.
My supervisor Sara Cousins has been just the right kind of supervisor. Thank you for giving me the
freedom to pursue my own interests, while always being there to provide ideas, insight and reassurance.
Thanks for putting your project in my hands. My co-supervisors have also done all that was asked of
them. Ove Eriksson at the Department of Botany was a great source of advice at the start of an
investigation and a valuable friendly reviewer of manuscripts at the end. Johan Berg at the Human
Geography Department waited patiently until the final paper to enrich the thesis with a real sense of history.
Bente Graae at NTNU Trondheim was my supervisor for my undergraduate dissertation. Thank you for introducing me to the world of seed dispersal, and for my time at Abisko which enriched my life in so many ways.
It’s been a real pleasure to watch the Landscape Ecology Group grow up around me, surrounding
me with fantastic colleagues. I particularly thank Reto Schmucki for abundances of dedicated help,
encouragement, ecological inspiration and good cheese. Good beer was usually provided by Jan Plue, who
also contributed with calm advice and wisdom on all manner of things. Thank you to everyone else in the
group for and allowing me to storm unannounced into your offices for spontaneous complaining, rejoicing and
general chit-chat. I’ve had a lot of practical help from field assistants and colleagues during data collection,
and the help of Nils Hedberg, Isabell Wärmé, Alex Norberg, Hedvig Nenzén, Josefin Reimark,
Peter Litfors, Ingela Lundwall, Mats Regnell and Jessica Lindgren has been both invaluable and
enjoyable. Thanks to the extremely open and helpful landowners and managers in Ludgo-Spelvik, the
Department of Botany and Tyresö Handelsträdgård for greenhouse space, and all the members of
Naturskyddsföreningen who contributed to Paper IV. I am also grateful to the open-source computing
community for providing me with the toolbox needed to analyse my data.
Our research group is only a small part of our large department at INK. Thanks to the administrative
staff for making things run smoothly, especially Susanna Blåndman, Carina Henricksson and Yanduy
Cabrera who all do a great job with smiles on their faces. A lack of direct contact with other administrative
staff is almost certainly because they are doing a great job too. Thanks also to all my fellow PhD students,
especially my lovely lovely corridor mates past and present for good company and sterling but futile
efforts to win the pub quiz. Fellow innebandy players have helped make Wednesdays the best days, and in
general the department is filled with friendly and interesting people who contribute to the good atmosphere
we have here. Lastly, I am truly grateful for everyone for putting up with the smell of drying cow manure
which emerged from my room, your labs and your ovens every now and then.
To my parents: I’ve never opened either of your doctoral theses, but I hope you at least read this part
of mine. Thanks for all kinds of support over the years, especially helping me through my university years
and supporting and encouraging my move across the North Sea. Thank you to the Tränks for welcoming
me into your family and for great times on Öland and elsewhere. Thanks to friends, family and football
players for good times and welcome distractions outside of work.
Louise, you sent me the job advert, taught me Swedish, helped me talk to scary farmers, collected soil
samples in frosty fields in the middle of a moose hunt, and at five-months pregnant you cleared a meadow-full
of hay while everyone else just stood and watched. Thank you for opinions, discussions, a helping hand and
a shoulder to cry on. You are a part of this thesis even if your name isn’t on the cover. You and Hille make
my life wonderful and I’m very lucky to have you.
Finally, I thank everyone everywhere who has ever been interested in my work and reminded me that this
is a subject that people care about. I hope it can be of some use.
30

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