Download The role of past and present management in the rural landscape

Institutionen för naturgeografi
och kvartärgeologi
The role of past and present management
in the seed dispersal of grassland plants
in the rural landscape
Alistair G. Auffret
Licentiatavhandling i naturgeografi
2010
Cover illustration: Richard Swan
www.themoonunderground.com
Abstract
The destruction and fragmentation of semi-natural grasslands due to
agricultural industrialisation during the past 150 years has had serious
consequences for biodiversity in the rural landscape. Currently, plant
communities are usually better explained by historical than by present
day landscape configurations, and the ability for plant species to
disperse in space and in time, within and between remaining habitat
fragments or to restoration sites will be an important factor in the
future diversity in the landscape. Here, I present a landscape scale
seed bank and seed rain experiment covering semi-natural grasslands,
pastures on former arable fields, abandoned grasslands and small
remnant habitats. The results suggest that in addition to grassland
specialists remaining in the field layer of abandoned grasslands,
remnant seed banks have the potential to be important contributors to
the future diversity of the rural landscape. However, unsuitable
grazing intensities in current pastures are limiting the potential for
dispersal of target species across the landscape. Despite large changes
in agricultural practice, there still exists the opportunity for humanmediated seed dispersal to increase functional connectivity in
fragmented landscapes, and I also present a review article in which I
assess past and present human-mediated seed dispersal vectors, and
give recommendations for management and further research.
List of papers.
I. Auffret, A. G., Cousins, S. A. O, Seed bank and seed rain as sources of future diversity in
the rural landscape, Manuscript
II. Auffret, A. G., Human mediated seed dispersal for conservation in the European rural
landscape, Manuscript submitted to Applied Vegetation Science
Introduction
Habitat destruction and land use change are currently the most serious threat to terrestrial species
worldwide (Sala et al. 2000; Baillie et al. 2004), and the associated fragmentation of remaining
habitats results in the biological impoverishment of what is left (Harrison & Bruna 1999). The
species-area relationship is a long known ecological theory which states that smaller areas of habitat
support fewer species and vice versa (Arrhenius 1921), mediated by the effect of distance from a
larger species source (MacArthur & Wilson 1967). After habitat loss, there often exists a time-lag
before a reduction in the number of species, the 'extinction debt' (Tilman et al. 1994). The extinction
debt is an example of how land use history can affect current and future ecological patterns, and
indeed, site history is embedded in the structure and function of all ecosystems (Foster et al. 2003).
In Europe, species-rich semi-natural grasslands have been created and maintained by the long
history of grazing by wild animals and livestock (Vera 2000), but agricultural industrialisation in the
nineteenth and twentieth century has resulted in the widespread and severe loss of semi-natural
grassland habitat. Investigations comparing maps pre- and post-industrialisation have found that
between around 70% up to almost 100% of grasslands have been either converted to arable land or
abandoned to become deciduous woodland (Fuller 1987; Pärtel, Mandla & Zobel 1999; Cousins
2001; Luoto et al. 2003; Bender et al. 2005; Adriaens, Honnay & Hermy 2006). The high species
richness of remaining fragments (Kull & Zobel 1991; Klimeš et al. 2001; Eriksson et al. 2006) has
contributed to the extinction debt in European rural landscapes, where present-day biodiversity
patterns are better explained by former land-use (Lindborg & Eriksson 2004; Helm, Hanski & Pärtel
2006; Gustavsson, Lennartsson & Emanuelsson 2007; Chýlová & Münzbergová 2008; Krauss et al.
2010). The existence of grassland plant populations in abandoned grasslands and small and linear
habitats, such as mid-field islets, road verges and field boundaries (Smart et al. 2002; Cousins 2006;
Johansson, Cousins & Eriksson 2010) adds further to the diversity of the rural landscape. The
severity of the habitat loss, in addition to the high biodiversity value of remaining fragments
highlights the importance of conserving and restoring semi-natural grasslands, at broad spatial
scales incorporating present day, abandoned and converted grasslands habitats.
The maintenance and re-creation of species-rich grasslands have both been key goals in agrienvironmental schemes in the EU, of which the effects for biodiversity are largely unknown (Kleijn
& Sutherland 2003). In order for existing grassland populations to persist, and for the recolonisation
of abandoned or former arable sites after restoration, it is essential that plant species can disperse to
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these target areas. The dispersal failure associated with the loss of structural habitat connectivity
resulting from the fragmentation of semi-natural grasslands has already contributed to species loss
(Ozinga et al. 2009). Functional connectivity, when the movement of organisms through the
landscape is facilitated by landscape structure and other factors (Taylor, Fahrig & With 2006), is
increased when a dispersal vector can move seeds between fragmented plant communities. In
addition to dispersal in space, plant species are also able to disperse in time, through the longevity
of seeds in the soil, the combination of which is often seen as a trade-off (Venable & Brown 1988;
Rees 1993; Thompson et al. 2002).
A general lack of dispersal in space to target sites on former arable fields means that the formation
of species-rich grassland communities is expected to take several decades (Gibson & Brown 1992;
Smith et al. 2000). These sites are dispersal limited, and require seed sowing in order to enhance
recruitment of desirable species (Pywell et al. 2002; Lindborg 2006; Kardol et al. 2008). Such
investigations, however, take place on very small experimental scales, which may reduce the
likelihood of spontaneous recolonisation, which has in fact been recorded on former arable fields
(Ruprecht 2006; Cousins & Aggemyr 2008; Dahlström, Rydin & Borgegård 2010).
Evidence of dispersal in time, of grassland species in the seed banks of abandoned grasslands has
regularly been found (Falińska 1999; Mitlacher et al. 2002; Wagner, Poschlod & Setchfield 2003;
Bisteau & Mahy 2005; Bossuyt & Honnay 2008). Restoration of grassland communities relying
upon the seed bank is however generally thought to be unfeasable (Bossuyt & Honnay 2008). The
re-creation of species-rich grassland from abandoned sites with only cutting and mowing
management, and therefore relying heavily on the contribution of the seed bank, has had mixed
results (Pärtel et al. 1998; Stampfli & Zeiter 1999; Klimeš, Jongepierová & Jongepier 2000;
Hellström et al. 2006). Again, these investigations focus on small scale species richness for short
periods, and further research into how remnant populations in seed banks can contribute to species
richness after restoration is required.
It is clear that dispersal in space is important for populations of grassland plants in the rural
landscape today. Dispersal is still general poorly studied (Bullock et al. 2002), and measuring
dispersal is difficult, especially between patches and at large spatial scales (Eriksson 1996; Nathan
et al. 2003). It is this rare long-distance dispersal, however, which has a disproportionately large
impact upon species distributions and dynamics (Nathan 2006; Ozinga et al. 2009), and it may often
occur via non-standard means, i.e with a different dispersal vector to which the seed has evoloved to
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disperse (Higgins, Nathan & Cain 2003). Humans have long influenced the dispersal of plant
species through their actions (Hodkinson & Thompson 1997), and this human-mediated dispersal
can be seeds dispersed directly by humans, as well as by human associated vectors, such as
transport and livestock (Wichmann et al. 2009). In rural Europe, past agricultural practices have
provided several dispersal vectors, such as the free roaming of livestock throughout the landscape
and fertilising with manure (Poschlod & Bonn 1998). It is these vectors which have contributed to
the seed dispersal for hundreds of years, and should also be considered in the modern context.
Land use, history and dispersal are all important factors for the conservation and restoration of
species-rich grassland communities in the landscape today, but all are relatively poorly studied. In
this licentiate thesis I assess how seed dispersal in time and space is affected by past and present
land use, and how this affects the grassland plant communities in the rural landscape.
In Paper I, I present a a landscape scale seed bank and seed rain experiment in a rural area in
southern Sweden, where I:
[1] Determine whether or not seed bank and seed rain patterns can be distinguished at large
spatial scales.
[2] Assess whether seed bank and seed rain can be predicted by current surrounding
vegetation, or if are they more similar to past or intended future plant communities.
Paper II is the first review paper summarising the recent research into human-mediated seed
dispersal in the Eurean rural landscape, assessing the potential of different vectors for the
conservation and restoration management of species-rich grasslands.
Methods
Study area
The empirical part of this thesis (Paper I) was carried out in a 36 km 2 agricultural landscape in the
county of Södermanland in southern Sweden (58°54’N, 17°00’E, see Fig. 1). The region has a long
history of anthropogenic influence, containing several runestones and burial sites dating from the
Bronze Age, and has been managed for agriculture since at least the Iron Age. Like much of rural
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Europe, the landscape consists of a mosaic of arable fields, semi-natural and old field pastures,
managed and unmanaged woodland, small and linear habitats and settlements (Fig. 1).
Sampling and analysis
In Paper I, seed bank, seed rain and above-ground vegetation was investigated in ten replicates of
four habitat types in the landscape described above: abandoned semi-natural grasslands, former
arable fields, mid-field islets and semi-natural fields (Fig. 1, Table 1), covering a spectrum of
habitat types and sizes in the rural landscape. Sites were chosen after examining historical maps and
aerial photographs (1600s, 1901, 1950s, present day) of the area, consulting land managers, and
visiting the landscape. In each site, thirty plots were created (total 1200). In each plot, seed bank
samples were taken, and a seed trap was left in the field during the summer of 2008. Vegetation
inventories were carried out during 2008 and 2009, identifying all plant species present in the 1 m 2
surrounding each plot, and by walking around the site to find additional species. Sites were
unfenced, allowing the free movement of people and animals through them, resulting in the loss of
some samples during the investigation.
Abandoned grassland
Semi-natural grassland
Grazed former arable field
Mid-field islet
Figure 1. Aerial photograph showing part of the study landscape from Paper I, highlighting the different habitat types
sampled. Photo: Sara Cousins, November 2008.
After the collection of seed traps from the field, seed bank and seed rain samples were grown in an
unheated greenhouse for seven months. Emerging seedlings were identified, counted and removed,
and those not immediately identifiable were grown separately until identification was possible.
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Table 1. Short descriptions of the habitat types investigated in Paper I.
Abandoned semi-natural
grassland (ABA)
Deciduous forest/scrub, historically grazed or cut for hay, but subsequently abandoned
and subject to secondary succession.
Mid-field islet (MFI)
Small, rocky habitats, formerly managed as part of larger pasture or meadow, but
surrounded by crop fields during agricultural industrialisation.
Former arable field
(FAF)
Relatively flat, ditched pastures, which have previously been cultivated and treated with
chemical herbicides and fertilisers.
Semi-natural grassland
(SNG)
Open species-rich grassland which has never been cultivated, and has been managed as
pasture or meadow for much of the last 300 years or more. May have been briefly
abandoned and subsequently re-cleared.
In total, 1190 seed bank, 797 seed rain, and 1026 vegetation samples were analysed. All analyses
were performed using R 2.11.0 (R Core Development Team 2009). Chao similarity (Chao et al.
2005), a method which accounts for differences in sample sizes caused by the loss of seed traps,
was used as a basis for a permutation test comparing seed bank, seed rain and above-ground
vegetation communities at the site level, as well as for assessing the similarity of the seed bank and
seed rain with above-ground vegetation between habitat types. Characteristic species of seminatural grassland above-ground vegetation were determined using IndVal analysis (Dufrêne &
Legendre 1997), modified by Roberts (2010).
The predictive capacity for the above ground vegetation community to predict the species
composition of the seed bank and seed rain was examined using co-correspondence analysis
(CoCA- see ter Braak & Schaffers (2004); Simpson (2009) for a full description of the method).
First, a predictive CoCA related the species compositions of the two communities (vegetation and
bank, vegetation and rain), before leave-one-out cross-validation was used to determine the
predictive accuracy of the model. Models were created at three scales (Fig. 2): [1] prediction of the
plot level seed bank and rain communities by the presence/absence of plant species in the
vegetation in the plot (plot vs plot), [2] prediction of plot level seed bank and seed rain by
vegetation in the site (site vs plot), and [3] prediction of the site level seed bank and seed rain
communities by the site vegetation (site vs site). Models were made at each scale for all habitat
types, where data were available for both sources (bank, rain, vegetation) considered. In all cases,
models were chosen with the number of axes corresponding to the highest prediction ability (%
cross-validatory fit). Significance (p= 0.05) of pairwise differences between models was tested
using a one sample permutation t-test of the mean prediction error sum of squares for each site
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between all models within each source and scale, between sources at the same scale, and
corresponding models between scales.
[1] Plot Vegetation v Plot Bank/Rain
Plot
Plot
Site
[2] Site Vegetation v Plot Bank/Rain
Plot
Plot
Plot
Site
[3] Site Vegetation v Site Bank/Rain
Figure 2. Visualisation of the three scales used for the co-correpondence analysis in Paper I.
In Paper II, a thorough literature search was conducted using the ISI Web of Science®, plus studies
referenced within relevant search results, of seeds dispersed via human-mediated vectors under
natural conditions (i.e. samples taken from vector without any seed addition) in Europe. Studies
relevant to the subject of human-mediated dispersal in the rural landscape through time were also
retrieved for discussion with regard to the conservation and restoration of semi-natural grasslands.
Results and Discussion
Paper I
A total of 54 357 seedlings of 188 species were counted and identified from the seed bank and seed
rain samples. The inventory of the vegetation found 277 species, with a total of 296 species
identified in the whole investigation. Table 2 shows a summary of the results broken down by
source and habitat.
The permutation test revealed significant differences in community composition between habitats
for the seed bank (F = 7.013, R2 = 0.369, P = 0.001), seed rain (F = 4.538, R2 = 0.286, P = 0.002)
and above-ground vegetation (F = 14.749, R2 = 0.558, P = 0.001). This shows that through taking a
number of samples in several replicate sites, broad patterns in the seed bank, seed rain and above6
ground vegetation at the landscape scale can be picked up. This allows the discussion of dispersal
patterns at a larger spatial scale, and relate the habitats making up the mosaic of past, present and
future species-rich grasslands.
Table 2. Number of seeds, species and recovered samples from the seed bank and seed rain experiment, and the above
ground vegetation inventory. ABA = Abandoned semi-natural grasslands, FAF = Former arable fields, MFI = Mid-field
islets and SNG = Semi-natural grasslands.
Seed bank
Seed rain
Vegetation
Seedlings
Species
Samples
Seedlings
Species
Samples
Species
ABA
7704
130
299
3461
91
242
133
FAF
13 336
116
299
2581
79
183
82
MFI
9937
139
296
2542
104
255
142
SNG
13 419
129
296
1396
74
116
151
Total
44 396
177
1190
9980
144
797
239
All but one (ABA seed rain, site vs site) of predictive CoCA cross-validations gave results higher
than zero (Fig. 3), meaning that the predictive ability of the model was better than by chance.
Predictive ability was, however, generally quite low, with at most 11.55% of the semi-natural
grassland seed bank plots predicted by the plot vegetation. The site level vegetation was not able to
predict the composition of the seed bank or seed rain better than the plot level vegetation, nor were
the site level bank and rain communities ever as accurately predicted by the surrounding vegetation
as were the plot level communities.
The vegetation of the ABA, MFI and SNG habitats predicted the seed bank better than it did the
seed rain, whereas the reverse was true for former arable fields, and the plot level seed rain
communities were significantly better predicted by surrounding vegetation in FAF than in SNG
habitats. Seed banks can be seen as the accumulation of several years of seed rain, and therefore it
should be expected that the seed bank better represents the community feeding it. Jakobsson,
Eriksson & Bruun (2006) found a strong positive relationship between abundance of reproductive
ramets and abundance in the seed bank and seed rain, indicating that it is not the species present in
the vegetation which are important, but those which are able to set seed. In the investigated
landscape, the former arable field sites were characterised by a low grazing intensity, and
communities were therefore able to complete their reproductive cycle and set seed, probably
explaining the relatively high predictability of the seed rain by the above-ground vegetation in this
habitat.
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Figure 3. Prediction (% cross-validatory fit) of seed bank and seed rain communities by surrounding vegetation in four
habitat types at three scales: [1] plot bank/rain by plot vegetation (plot vs plot), [2] plot bank/rain by site vegetation (site
vs plot), and [3] site bank/rain by site vegetation (site vs site). Significance (p=0.05) of pairwise differences shown,
where letters in common indicate no difference between habitats at the same source and same scale. Significant
differences between source and within scale are denoted by an asterix. Models predicting communities at the plot scale
were always significantly different to corresponding models predicting site communities, while corresponding models
predicting at the plot vs Plot and site vs plot scales were never significantly different (not denoted).
The plot level seed bank communities were significantly better predicted by surrounding vegetation
in SNG than in ABA and MFI habitats. This is probably due to the continuous history of
management, whereas the seed banks of the other habitat types appear out of synchrony with
current vegetation, which has developed relatively recently due to abandonment. Given longer time
without management, abandoned grasslands eventually become more similar to the above-ground
vegetation, forming characteristic forest seed banks (Plue et al. 2010).
Twenty-two characteristic (specialist) semi-natural grassland species were identified by the IndVal
analysis. Table 3 shows that many of these species are present in the bank, rain and vegetation of
the other habitats. Ajuga pyramidalis, Alchemilla spp., Erophila verna, Lotus corniculatus and
Primula veris remained in the seed banks of the former grassland, despite having disappeared
completely from the above-ground vegetation. The Chao similarity analysis indicated that the seed
bank and rain communities of most habitats were most similar to the above-ground vegetation of
the same habitat (Fig. 4), with the exception that seed banks of the MFI and ABA habitats were
more similar to the SNG above-ground vegetation, and the SNG seed rain were most similar to the
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vegetation of the FAF sites. These results support the conclusion drawn from the CoCA analysis,
that semi-natural grasslands subjected to abandonment are out of synchrony with the above
vegetation, as the ABA and MFI sites contained populations of grassland specialists in their seed
banks, and the whole seed bank communities were more similar to the above-ground vegetation in
existing grasslands than to their own. Furthermore, the presence of specialists in the vegetation and
seed rain indicates reproducing populations and/or dispersal from nearby populations. The results
imply that in addition to grassland specialists remaining in the vegetative layer, remnant seed banks
have the potential to be important contributors to the future diversity of the rural landscape.
0.17
0.29
0.24
0.25
Seed Rain
ABA
FAF
MFI
SNG
Vegetation
ABA
FAF
MFI
SNG
Seed Bank
ABA
FAF
MFI
SNG
0.29
0.37
0.28
0.39
Figure 4. Similarity of seed bank and seed rain communities to the habitat type vegetation to which they are most
similar. Arrows connect seed bank and seed rain communities to the vegetation community to which they are most
similar. Values are Chao similarity (0-1) between the connected habitat types. where ABA = Abandoned semi-natural
grasslands, FAF = Former arable fields, MFI = Mid-field islets and SNG = Semi-natural grasslands.
The poor predictive power of the CoCA models for the SNG seed rain, and the correspondence
between the SNG seed rain and the FAF vegetation (Figs. 3 and 4) suggests that in contrast to
former arable fields, few species in semi-natural grasslands are currently setting seed, and those that
are are probably common throughout the landscape. Semi-natural grasslands in the study landscape
are heavily grazed, and a high grazing intensity can could be limiting the number of propagules to
contribute to the existing population, create a seed bank, or to disperse to other areas in the seed
rain.
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Table 3. Number of sites for each habitat where local grassland specialists were found in the seed bank, seed rain and
above-ground vegetation. ABA = Abandoned semi-natural grasslands, FAF = Former arable fields, MFI = Mid-field
islets and SNG = Semi-natural grasslands.
Species
IndVal
ABA
Bank
n=10
Rain
n=10
Veg
n=9
FAF
MFI
SNG
Bank Rain Veg
n=10 n=10 n=10
Bank Rain Veg
n=10 n=10 n=10
Bank Rain Veg
n=10 n=8 n=10
Plantago lanceolata
0.8000
0
0
0
0
0
0
0
0
0
5
1
8
Lotus corniculatus
0.7800
4
4
0
1
0
1
2
0
0
3
0
8
Filipendula vulgaris
0.6440
0
0
3
0
1
1
0
0
1
0
0
8
Campanula rotundifolia
0.6344
7
7
8
0
1
1
8
4
5
7
2
9
Pimpinella saxifraga
0.6009
0
0
4
0
0
2
0
1
6
1
1
10
Trifolium arvense
0.5455
0
0
0
1
1
0
0
0
1
6
0
6
Rumex acetosa
0.5020
2
2
6
3
2
6
2
1
5
4
2
9
Viola canina
0.4777
6
6
2
0
0
0
3
1
1
4
0
6
Veronica chamaedrys
0.4600
9
9
9
8
3
8
8
6
5
10
5
10
Trifolium pratense
0.4410
3
3
1
5
4
7
3
0
5
9
1
9
Anthoxanthum odoratum
0.4361
2
2
3
0
1
1
2
1
2
5
0
8
Alchemilla spp
0.4286
2
2
0
4
1
2
3
0
0
2
0
5
Ranunculus auricomus/bulbosus
0.4233
1
1
4
4
0
5
1
0
3
2
0
8
Arabidopsis thaliana
0.4000
4
4
0
6
0
0
7
0
0
6
3
4
Scleranthus annuus
0.4000
0
0
0
0
0
0
0
0
0
1
1
4
Festuca ovina
0.3862
3
3
4
1
1
1
5
2
4
8
2
6
Carex spicata
0.3667
0
0
0
0
0
1
0
0
0
0
0
4
Primula veris
0.3429
1
1
0
0
0
1
1
0
0
1
1
4
Potentilla argentea
0.3415
6
6
1
7
3
0
10
4
3
10
2
4
Veronica officinalis
0.3390
10
10
2
1
0
2
6
0
2
8
3
6
Ajuga pyramidalis
0.3000
4
4
0
0
0
0
2
0
0
4
1
3
Erophila verna
0.3000
Total species per site/source
1
1
0
2
0
0
3
1
0
9
1
3
16
16
12
12
10
14
16
9
13
20
14
22
Paper II
The literature search yielded 23 articles investigating seed dispersal via human mediated vectors
(Table 4).
Grazing animals
Most of the articles found (16) are concerned with seed dispersal via grazing animals, both epi
(outside)- and endozoochorously (inside the animal), and show the large amount of seeds and
species which can be dispersed in this manner. It is not only seeds with appendages designed for
attachment which can be dispersed epizoochorously, as unappendaged, small and smooth seeds can
all attach to the fur of different grazing animals (Fischer, Poschlod & Beinlich 1996; Couvreur et al.
2004; Römermann, Tackenberg & Poschlod 2005; de Pablos & Peco 2007).
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Table 4. Human-mediated seed transport in natural conditions in the European rural landscape. Methods vary widely between studies.
Reference
Country
Vector
Number of replicates*
Epizoochory
Endozoochory
Couvreur et al. 2004
Belgium
Couvreur et al. 2005
Fischer, Poschlod & Beinlich 1996
Wessels et al. 2008
Belgium
Germany
Germany
Bakker & Olff 2003
Bruun and Poschlod 2006
Cosyns et al. 2005
Cosyns et al. 2006
Netherlands
Germany
Belgium
Belgium
Cosyns & Hoffmann 2005
Couvreur et al. 2005
Dai 2000
Eichberg, Storm & Schwabe 2007
Kuiters & Huiskes 2010
Malo & Suárez 1995
Pakeman, Digneffe & Small 2002
France/Belgium
Belgium
Sweden
Germany
Belgium/Netherlands
Spain
Spain
Sweden
Netherlands
Netherlands
Netherlands
Netherlands
Netherlands
UK
Hodkinson and Thompson 1997
Mayer 2000
UK
Germany
Schmidt 1989
Strykstra, Verweij & Bakker 1997
Zwaenepoel, Roovers & Hermy 2006
Germany
Mitlacher et al. 2002
Mouissie et al. 2005
11
Motor Vehicles
Humans
Belgium
Total seeds*
Cattle
Donkey
Horse
Donkey
Sheep
Sheep
125
46
30
41
16
41-63
3692
2483
210
NA
8511
9420
Number of identified
species*
63
33
20
29
85
56
Cattle
Cattle
Cattle and Horse
Cattle
Horse
Horse
Donkey
Cattle
Sheep
Sheep
Cattle (Spring)
Cattle (Winter)
Cattle and Sheep
Cattle
Cattle
Cattle
Horse
Sheep
Sheep
30
48
51
12
12
56
14
30
32
24
8
8
29
50
10
15
10
10
12
6124
14703
59049
18974
10808
53493
NA
393
2669
11130
1373
17
1504
1161 (kg-1)
4605 (kg-1)
1095 (kg-1)
661(kg-1)
527 (kg-1)
359 (kg-1)
35
56
117
50
49
106
53
26
28
72
46
5
44
51
34
39
35
31
21
Car
Tractor†
Plough†
Heavy cultivator†
Rotary tiller†
Rotary harrow†
Curry comb†
Car
Mowing machinery
Car
201
1
1
1
1
1
1
4
7
240
367
6
1945
844
320
658
460
3926
NA
690
37
4
35
28
30
25
11
124
27
33
Clifford 1956
Ireland
Boots
Unknown (22.1g)
65
11
Wooderuffe-Peacock 1918
UK
Clothes
3
NA
19
* As far as can be deduced from the text. This includes both replication and pseudoreplication, i.e. 75 could mean either 75 individuals, or one individual sampled 75 times. Epizoochorous units are
animals, endozoochorous are “samples”.
† In this study, machinery was driven through mud of varying soil dry matter, but species lists are not given. Displayed here are the individual runs that yielded the most seeds and species.
Endozoochory also has the potential to disperse seeds with a range of other dispersal adaptations
(Couvreur et al. 2005; Bruun & Poschlod 2006). Large grazers have a remarkable capacity for
endzoochorous seed dispersal, with approximately 1 200 000 seeds per individual per summer
calculated for both cattle and horses in a coastal dune landscape in Belgium (Cosyns et al. 2005), up
to 2 600 000 seeds per year for cattle in the Netherlands (Mouissie et al. 2005), and an estimated
1510 seeds per square metre per year deposited by grazing cattle in a Mediterranean wooded
pasture (Malo, Jiménez & Suarez 2000).
Both epi- and endozoochory are important for the diversity of the rural landscape, and are known to
disperse specialist and red-listed species (Fischer, Poschlod & Beinlich 1996; Eichberg, Storm &
Schwabe 2007; Wessels et al. 2008). The two vectors have been found to complement one another
with regards to species dispersed (Couvreur et al. 2005), and the contents of Table 4 indicate a
complementarity between different grazing animals, with the larger mammals transporting a large
number of seeds internally, and sheep transporting far more on their coats than other animals.
Investigations have shown that each studied herbivore species transport the diaspores of plant
species not transported by any other herbivore study species (Couvreur et al. 2004; Cosyns et al.
2005).
Despite the obvious potential of zoochorous seed dispersal in the rural landscape, very little is now
realised. Where mixed grazing animals were once allowed to roam almost freely throughout the
landscape (Clout 1998; Dahlström 2006), this is now a less common practice, and single species are
often kept in the same small pastures for the whole grazing season. Even longer distance dispersal
was possible via transhumance, which is the seasonal movement of livestock between pastures. This
practice was widespread for centuries (Whyte 1998), facilitating the movement of seeds between
landscapes and even countries, but has been progressively abandoned as a result of economic
development (Manzano & Malo 2006). Experimentally attached seedlings were found to travel
hundreds of kilometres in two of Europe's last remaining transhumance drives (Fischer, Poschlod &
Beinlich 1996; Manzano & Malo 2006). In today's landscape, long distance dispersal via grazing
animals can occur via management practices such as the movement of transportation of grazing
animals between isolated nature reserves (Couvreur et al. 2004; Wessels et al. 2008), or by the recreation of extensive forest-pasture mosaics (Kumm 2004).
12
Motor Vehicles
Whereas movement of grazing animals within and between landscapes has reduced through time,
the invention of motor vehicles and agricultural machinery has introduced a new potential for seed
dispersal in the rural landscape (see Table 4). Not surprisingly other published motor vehicle
dispersal studies state that most species transported are typical of local roadsides and ruderal land
(Clifford 1959; Wace 1977; Schmidt 1989; Hodkinson & Thompson 1997; Schmidt et al. 2004;
Zwaenepoel, Roovers & Hermy 2006; Von der Lippe & Kowarik 2007) and regularly managed road
verges can act as remnant habitats for grassland specialists (Milberg & Persson 1994; Cousins
2006). No plant species have evolved to be dispersed via motor vehicles, but Zwaenepoel, Roovers
& Hermy (2006) found a significantly higher proportion of seeds with persistent seed banks were
dispersed this way. Furthermore, the seed banks of verges can be important repositories for
grassland species (Milberg & Persson 1994; Berge & Hestmark 1997), and therefore motor vehcles
could be an important, non-standard long distance dispersal vector of the grassland plant species
which are traditionally dispersed through time.
Mowing machinery operating in species-rich meadows has also been found to be an effective
dispersal agent, where small subsamples of material collected post-mowing contained 27 of 52
species found in the meadow system (Strykstra, Verweij & Bakker 1997). Larger agricultural
machinery has been shown to transport seeds between arable fields (Mayer 2000), but this has not
been studied in semi-natural grasslands. These vehicles are used on pastures, and in addition to the
potential seeds dispersed, the physical disturbance can promote the generation of new seedlings, an
effect documented on grassland with other heavy vehicles (Hirst et al. 2003). Road verges should
have the same mowing regimes as ancient meadows. This would maintain species richness and
allow plants to reach the reproductive stage (Jantunen et al. 2007), in turn allowing the effectiveness
of motor vehicles to disperse grassland species to aid in grassland connectivity.
Humans
Humans themselves can also be non-standard, long-distance dispersers of seeds through the
landscape . Recently, two species of Brassica were regularly found to remain attached to the mud on
boots after 5 km walking, which was almost fifty times further than the maximum value calculated
for wind dispersal, which is their primary vector (Wichmann et al. 2009). A study from Australia
(Mount & Pickering 2009) has shown the capacity for clothing to disperse seeds of both native and
13
alien plants, where 207 clothing samples yielded almost 25 000 seeds of 70 taxa. The paper also
contains a useful summary of the few published clothing dispersal studies, which is dominated by
work from the Southern Hemisphere focussing on alien species (Healy 1943; Whinam, Chilcott &
Bergstrom 2005). There is a clear absence of recent work from Europe quantifying the number of
seeds and species dispersed with humans, which is limited to Clifford (1956), where material
attached to shoes were found to contain seeds of 44 species representing a range of dispersal
adaptations, and Woodruffe-Peacock (1918), who identified mud from boots, as well as clothing and
hair as the sources of seeds for a number of species colonising a newly created fox covert.
Figure 5. Human-mediated seed dispersal vectors in the modern rural landscape.
Mechanisation of agriculture has meant there are fewer humans working in the landscape, but the
potential for dispersal by recreational walkers (and ecologists) remains. Many people walking
through the modern landscape are accompanied by dogs, and these can also be effective dispersers
of seeds (Heinken 2000; Graae 2002). Seeds transported on humans and their pets will also travel in
cars and other modes of transport, increasing dispersal distances further.
The studies summarised in Table 4 show that human-mediated dispersal can be important in terms
of both number of seeds and species. It is clear, however, that modern land-use change and
agricultural intensification has negatively affected this potential. In order to preserve, conserve and
restore high species richness in semi-natural grassland landscapes, it is therefore important to draw
inspiration from past land use and its dispersal vectors, to increase functional connectivity where
structural connectivity has been lost. It is equally important is not to overlook the potential of those
dispersal vectors that modern life and agriculture has introduced. A great deal of research into
14
human-mediated seed dispersal has been done during the past decade, but there is still more to be
done, and in the case of semi-natural grasslands, it is vital that both agricultural history and the
landscape scale are considered.
Conclusions and future directions
Paper I shows how past land use has left an imprint on the dispersal of grassland plant species in
time and space. The seed banks of abandoned semi-natural grasslands and mid-field islets can give
an important contribution to the future biodiversity of the rural landscape. The high degree of
fragmentation, as well as the intense grazing on existing species-rich grasslands, however, appears
to be limiting the dispersal through space within and between semi-natural grassland fragments. It is
clear from Paper II that agricultural change in the twentieth century has not only negatively affected
diversity in the rural landscape, but also the potential dispersal of plants across it. There is, however,
a potential for successful dispersal of grassland plants, both by drawing inspiration from past
practices, as well as by facilitating dispersal by more non-standard means in the modern landscape
(Fig. 5). Such dispersal vectors certainly warrant further research, and during the rest of my PhD
studies, I will investigate endozoochorous seed dispersal in both an island nature reserve in the
Stockholm archipelago, as well as in the study landscape from Paper I, where I will also evaluate
dispersal via motor vehicles. I also plan to publish the first investigation into seed dispersal via
humans in the northern hemisphere for several decades. The results of these empirical studies will
be used to model dispersal in time and space in fragmented landscape, and provide
recommendations for management
Acknowledgements
First I will thank my supervisor Sara Cousins for the opportunity to start this exciting research project, and for being
just the kind of supervisor I need. Thanks also to my other supervisors Ove Eriksson and Johan Berg for attending
meetings, reading manuscripts and answering emails extremely promptly. The various members of the Landscape
Ecology group at INK have all helped me in their various ways, and along with the PhD student group, the academic
and non-academic staff, they have made the department a very nice place to work. The seed bank and seed rain project
would have been a total disaster were it not for the sterling efforts in dreadful conditions of Nils Hedberg, Ewa
Hedberg, Hedvig Nenzen, Alexander Norberg and Isabell Wärmé. Finally, Tyresö Handelsträdgård kindly allowed us to
use their greenhouse, and the landowners of Ludgo and Spelvik past and present must be thanked for providing a
beautiful study landscape.
15
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