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Plant functional diversity in agricultural margins and fallow fields varies with landscape complexity level: Conservation implications
Accepted Manuscript Title: Plant functional diversity in agricultural margins and fallow fields varies with landscape complexity level: Conservation implications Author: Maohua Ma Irina Herzon PII: DOI: Reference:
S1617-1381(14)00090-9 http://dx.doi.org/doi:10.1016/j.jnc.2014.08.006 JNC 25375
To appear in: Received date: Revised date: Accepted date:
27-1-2014 5-8-2014 5-8-2014
Please cite this article as: Ma, M., and Herzon, I.,Plant functional diversity in agricultural margins and fallow fields varies with landscape complexity level: conservation implications, Journal for Nature Conservation (2014), http://dx.doi.org/10.1016/j.jnc.2014.08.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Plant functional diversity in agricultural margins and fallow fields varies with
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landscape complexity level: conservation implications
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Maohua Ma*,Irina Herzon
Department of Agricultural Sciences, P.O. Box 27, FI-00014 University of Helsinki, Finland
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*Corresponding author. Tel.: +358919158451; fax: + 358919158582. E-mail address:
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References: 52
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Word count of main text: 3655
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[email protected]
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Abstract A consensus has been established that functional traits rather than taxonomic diversity play a
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fundamental role in linking biodiversity with ecosystem processes and associated services. This study from Finland addressed an issue of relative values of fallow and field margin
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biotopes in conservation of plant functional diversity (based on six functional traits of
relevance to ecosystem services, and diversity of multiple traits) in agricultural landscapes
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differing in their structural complexity. Relative covers of plant species were surveyed in sampling plots located in perennial fallow fields and three types of perennial margins
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(margins between crop fields, along forest edges and by river) in three types of landscape context (simple, intermediate and complex). Fallow fields significantly contributed to the
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total functional diversity only in simple landscapes. The river margins provided the greatest functional diversity, especially in reproduction and regeneration traits while crop margins
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were consistently characterised by the lowest functional diversity. Substantial functional diversity of fallow patches in simple landscapes was due to high abundance of functional
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species, while that of river margins stemmed from presence of unique species. The plant functional diversity progressively declined with agricultural landscapes becoming simplified. The study indicates non-cropped biotopes having complementary roles in ensuring multifunctionality of agro-landscapes and confirms importance of biotope mosaic for functional diversity.
Keywords: agricultural landscapes; agri-environmental policy; ecosystem services; noncropped biotopes; functional traits.
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Highlights •
Fallow fields had the highest contribution to the total functional diversity in simple
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landscapes. River margins supported the greatest functional diversity.
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Fallows and margins displayed differences in diversity of individual functional traits.
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Fallows had few unique species but supported high species abundances per sample.
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Introduction The economy-driven progression of agricultural production into more intensive and
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specialised forms leads to the deterioration in the ecological state of agricultural ecosystems
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(Stoate et al. 2009). Among other impacts, this drives homogenisation of the agricultural
landscapes (Benton et al. 2003). One of the commonest counteractive options is preservation,
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establishment and management of field margin biotopes, which, in the EU, is mainly done through the agri-environmental contracts and cross-compliance baseline (IEEP 2008).
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Ecological benefits of linear habitats as reservoirs of beneficial invertebrates, predators of pest species or crop pollinators have been widely appreciated (Marshall et al.1994; Cole et al.
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2012). Another common agri-environment option at farm scale is fallowing, that is, removal of whole field parcels from production. Fallowing of a certain portion of a field area had been
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an obligation across the EU until 2008, when it was abolished (i.e. CAP set-aside; Hart &
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Baldock 2011). Many countries, including Finland, offer payments for voluntary fallowing of
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fields with an objective of enhancing biodiversity (Kovács-Hostyánszki et al. 2011; Toivonen et al. 2013).
A hypothesis considering the relationship between effectiveness of agri-environment schemes and landscape complexity (Tscharntke et al. 2005) sets local farm management into a landscape perspective. Accordingly, efficiency of agri-environmental allocations depends on level of landscape complexity, which is defined at three levels based on cover of semi-natural areas: cleared (< 1% of semi-natural habitats, lowest diversity); simple (1-20%); and, complex (>20%, highest diversity). The intermediate level, that is simple landscape, is predicted to be optimal to agri-environmental management, which has generally been
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corroborated in a meta-analysis (Batáry et al. 2011). Most recently, the framework has been extended to consider provisioning of ecosystem services (Tscharntke et al. 2011).
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A consensus has been established that species functional traits play a fundamental role in linking biodiversity with ecosystem processes and services (Díaz & Cabido 2001; Hooper et
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al. 2005; Reiss et al. 2009). For instance, there are well-established links between plant leaf traits (e.g. LDMC) and nutrient cycling providing ecosystem supporting service (Reich et
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al.1992; Poorter & Garnier 1999; Garnier et al. 2004); diversity in plant life forms is a strong
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surrogate to assess variation in plant net primary productivity delivering regulating service (Lieth & Whittaker 1975; Saugier et al. 2001). However, studies on impacts of agri-
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environment management on biodiversity still focus mainly on taxonomic species diversity rather than species’ functional properties. Yet, it has been suggested that in production
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systems, landscape-moderated conservation of total species richness or abundance of red-data
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listed species will not necessarily optimize ecosystem services (Kleijn et al. 2011).
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Functional diversity can be measured by functional composition of multiple traits using functional diversity indices (e.g. functional richness, functional evenness). Indices that mix richness and evenness, such as RAO’s index (Botta-Dukát 2005), have also been used extensively (Díaz et al. 2007; Flynn et al. 2009; Mason et al. 2012). Assessment of landuse effects on indices composed by functional traits relevant for key ecosystem functions can therefore provide insight on how to optimise land management for maintaining multiple ecosystem services.
This study focused on functional diversity of vascular plants in fallow and margin biotopes along a spatial gradient from simple to complex landscape context. The key research 5
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questions were: 1) How does functional biodiversity compare among different biotopes of margins and fallows? More specifically: i) How do relative roles of margins and fallows change with increased landscape complexity? and ii) Do relative contributions of two biotope
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types to functional diversity differ from those to taxonomic diversity? 2) How does the
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overall landscape-level functional diversity change under different landscape context?
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Since large habitats generally contain more species than small habitats (species-arearelationships, MacArthur & Wilson, 1967) we hypothesized that whole-field patches (fallows)
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are more effective in promoting taxonomic diversity than narrow biotopes of linear type (margins). Furthermore, since in environments with low biodiversity plant communities are
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likely to be unsaturated, a positive linear relationship between taxonomic and functional diversities can be expected. Therefore, we foresaw that simple landscape biotopes of high
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taxonomic diversity would also contribute to greater functional diversity. In landscapes
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favoring high levels of taxonomic diversity, functional diversity reaches an asymptote (Sasaki
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et al. 2009). Therefore in complex landscapes, we expected fallows to contribute more to taxonomic diversity than functional: additional species would likely be functionally redundant.
Methods
Study area
The study area is located in Lepsämänjoki watershed in Nurmijärvi commune, 30 km north of Helsinki (60° 23' – 60° 28' N, 24° 31' – 24° 43' E) in southern Finland (Fig. 1). This flat drainage area is 214 km². Soil types are mostly sandy clay and fine sand. The area belongs to the southern boreal zone with a mean annual temperature of 4.4 °C (-7.6 °C – 16.7 °C), mean precipitation is 65 mm (48 mm – 70 mm) and the average duration of snow cover is 132 days. 6
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Main crops are spring cereals, row crops and silage (Tike 2011). All of these require intensive management making the study area a production-intensive landscape by Finnish
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standards.
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Sampling design
a spatial gradient from simple to complex landscape:
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Based on the main landuse types, we selected three landscape types typical for the area along
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1) Simple landscape dominated by fields and with only crop margins (no river and very small forest patches);
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2) Intermediate landscape with a high cover of forest, and margins represented by crop margins and forest margins (no river);
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3) Complex landscape with a high cover of forest and a river, margins included crop
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margins, forest margins and river margins.
We surveyed fallow fields and three types of perennial margins: margins between crop fields; along forest edges; and, by the only river in the study area. Since neighbouring crop types, slopes, and shading varied along the river, we treat the river samples as independent. All fallow fields were represented by grassland fallow type (Toivonen et al. 2013) established within the past 10 years (average age 5.4, range 4-9). All have been managed by annual mowing without biomass removal, chemical applications or grazing. We did not survey fallows younger than four years (typical rotation period for grassland in Finland) as well as the only grazed parcel. We digitized land-cover of the major types (field, forest, river, ditch, road and building) in the landscape squares in ArcGIS 9.3 (ESRI 2008) and calculated landscape metrics (Table 1) in Fragstats 3.3 for ArcGIS 9 (McGarigal et al. 2002). Digitized 7
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data on land use (including presence of fallow fields) came from the Land Use Register and the Information Centre of the Ministry of Agriculture and Forestry (Tike 2011). We deducted
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the age of the fallows from the same register for years 2001 – 2011.
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For each landscape type, we sampled three landscape squares of 1x1 km (nine in total). In each landscape square, we chose at random three margin strips as sampling sites for each
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margin types. Accordingly, there were only crop margins in the simple landscape, crop and forest margins in the intermediate landscape, and crop, forest and river types in the complex
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landscape. The majority of margins were beside cereal fields (spring barley). Two crop margins and one river margin in the complex landscape were beside root vegetable fields.
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These and forest margins were about 0.5-2 m wide and river margins were about 3-8 m wide. In each sampling site, six or seven 1-m2 plots were sampled at systematic intervals. Five
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fallow sampling sites, corresponding to age and management restriction, were chosen
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randomly in each landscape type. There was a non-directional difference in average ages (in
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the simple landscape: mean 5.2, range 4-7; intermediate: 4.8, 4-9; and complex: 6.2, 4-8). In each fallow site, four to eight 1-m2 plots were sampled depending on field size so that the field area was covered systematically.
Not all species of vascular plants were fully (binomially) identified but some were placed within a genus and subsequently treated as a pseudo-species (e.g. Taraxacum, Alchemilla). Relative covers of species were estimated in each plot according to the logarithmic scale (1 ≤0.125%, 2 ≤0.5 %, 3 ≤2%, 4 ≤4%, 5 ≤8%, 6 ≤16%, 7 ≤32%, 8 ≤64%, 9 >64%). Species nomenclature followed Hämet-Ahti et al. (1998). All field workers undertook training in field methods. 8
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Functional traits and diversity index We calculated species richness per each site and landscape (taxonomic diversity). For
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functional diversity, we used six types of functional traits (Table 2) on the basis of their
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potential importance for ecosystem functions and associated ecosystem services (Díaz et al.
2005; Swinton et al. 2006), and following the recommendations of Cornelissen et al. (2003).
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Measurement of leaf dry matter content (LDMC) followed the method proposed by
Vendramini et al. (2002). After cutting, leaf samples were stored in sealed plastic bags, which
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were slightly moistened, kept in cold boxes with ice bags and brought back to lab usually within 3 – 8 h. In the laboratory, the leaf samples were blotted dry to remove any surface
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water, weighed as fresh weight and then oven-dried in paper bags at 60 °C for two days, after which their dry mass was measured as: LDMC=dry weight/fresh weight. We collected
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information on other traits from the literature (Hämet-Ahti et al. 1998), online trait data-base
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Biolflor (Biolflor, 2004) (http://www2.ufz.de/biolflor/index.jsp), Seed Information Database
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(SID, 2008) (http://data.kew.org/sid/sidsearch.html), and Nature Gate of Finland (http://www.luontoportti.com/suomi/fi/kasvit/).
We used RAO’s index as a measure of functional diversity (Botta-Dukát 2005). It is based on the quadratic entropy of Rao (1982) that incorporates both the relative abundances of species and a measure of the pairwise functional differences between species by measuring species distance in functional trait space (Mason et al. 2005; Lepš et al. 2006). The index is a generalized form of the Simpson index of diversity (Lepš et al. 2006) and measures both functional richness and divergence of communities (Mouchet et al. 2010). Since the RAO’s functional diversity index is produced by distance of paired species in trait space and 9
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weighted by species relative abundances, variability of species composition and abundances are the two keys in determining the index.
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We first measured RAO’s index for single traits and then calculated a compound RAO’s index of multiple functional traits as a mean over the RAO’s indices for single traits in each
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sampling site (Lepš et al. 2006). We used a macro tool for MS Excel 2010 (available freely
at:http://botanika.bf.jcu.cz/suspa/FunctDiv.php).In order to estimate gamma-level diversity at
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landscape scale, we pooled data over all biotopes for each landscape type.
Statistical analysis
Because not all biotope types were present in each landscape type (i.e. only crop margins in
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simple landscapes), we tested the differences in diversity between biotope types separately for each landscape type using generalized linear modeling (GLM) with Poisson distribution
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for species richness. None of the models with alternative link functions in GLM performed satisfactory for the individual traits or the mean over them, therefore we used non-parametric
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Kruskal-Wallis test or Mann-Whitney test (in simple landscapes with two samples). To ascertain the differences among the types of biotopes in intermediate and complex landscapes (more than two types), we used Tukey test with ranked sums (Sokal and Rolf 1995). We used the same non-parametric tests for differences in parameters in fallows across the landscapes. All analysis was run in R 2.13.0 (R Development Core Team, 2014). No statistical test was possible on data pooled on landscape level here because of the sample size of three. We also identified unique species in the margins (i.e. not found in the fallows) and fallows (i.e. not found in the margins) for each landscape type.
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Relative roles of margins and fallows in supporting functional diversity Fallow fields significantly contributed to the total functional diversity only in simple landscapes. In both simple and intermediate landscapes, fallow biotope was characterized by
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significantly higher diversity than the margins for life forms and LDMC (Table 3). Diversity in these traits, but not in the others, was the highest in fallows in complex landscapes
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(Kruskal-Wallis test; P = 0.048 and 0.009, respectively). In complex landscapes with river
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margins, levels of functional diversity in fallow did not differ significantly from those in crop and forest margins. River margin biotope had the highest diversity for LDMC, dispersal
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modes and seed mass. Crop margins were consistently characterized by the lowest functional diversity. There were no significant differences in pollination types and flowering phenology
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among biotope types. Functional diversity of fallows did not change across landscape
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gradient (Fig. 2b).
Functional diversity in different biotope types showed a different pattern from that of species
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richness along the gradient of landscape context (Fig. 2). In complex landscapes, fallows supported the greatest species diversity (Fig. 2a) while river margins became the biotope supporting the greatest functional diversity (Fig. 2b). Species richness in fallow biotopes was similar to that in the most taxonomically diverse margin type of a corresponding landscape type: forest margin in the intermediate and river margin in the complex landscape (Table 3; Fig. 2a). However, there was no statistically significant difference in species diversity in fallows among the landscape types (Kruskal-Wallis test; P = 0.156). Margins between crop fields were also taxonomically least diverse across all landscape types. Species richness in crop or forest margins did not change across the landscape gradient, while in fallow fields it increased steadily but non-significantly (Fig. 2a).
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Functional diversity on landscape level When the data in each landscape square were pooled and the margins were treated as one
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biotope type, the RAO’s diversity index of fallows was very similar to the total RAO’s index
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in simple landscapes, and they contributed most to the total functional diversity (Fig. 3). In complex landscapes, contribution of margins was higher than that of fallows. While
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functional diversity in the fallows did not change considerably from simple to complex landscape context, it increased in the margins, also driving an increase in the total functional
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diversity (Fig. 3). Fallows always had a lower number of unique species than the margins
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Discussion
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than those in the margins (Fig. 4b).
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(Fig. 4a) while the relative abundances of each species in fallows were significantly higher
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Functional value of fallow and margin biotopes Fallow and margin biotopes demonstrated different and complementary roles in conserving functional diversity. Although taxonomic diversity in fallows equaled that of the most species-rich margin type, contribution of fallows to the overall functional diversity exceeded that of only crop margins. Fallows and margins displayed apparent differences in individual functional traits. Fallows and river margins had the highest variation of life forms and LDMC-traits related to supporting services. LDMC is one of the most important effect traits on determining nutrient cycling and efficiency of carbon acquisition by plants being a key in delivering ecosystem supporting services (Chapin et al. 2002; Garnier et al. 2004). Therefore, fallows may support a greater variety of fundamental properties of plants relevant to 12
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ecosystem supporting services than crop and forest margins do. Fallow vegetation represented a relatively low variation for such reproduction and regeneration traits as dispersal, seed mass, pollination and flowering phenology. These traits reflect plant strategies
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in responding to environmental changes and relate to regulating ecosystem services (Grime
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1997; Díaz et al. 2005).
River margins were functionally the most diverse biotope type. According to the national
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agri-environmental policy, the required minimum width of margins along watercourses is 3 m.
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The margins along crop and forest edges are mostly < 1 m (Ma, unpublished data). A greater width, and hence a broader gradient of soil conditions from river-side to field-side, is likely to
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explain enhanced diversity in the river margins (Ma et al. 2002). Wide riparian river margins also have potential to promote survival of functional species with poor dispersal capability
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(Cole et al. 2012). Crop margins had consistently the lowest functional diversity of the
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biotope types, most probably due to their narrow character, disturbance and restricted species
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pool of the neighbouring crops.
Different values of fallows and margins in functional and taxonomic diversity indicate that biotopes of greater taxonomic diversity do not always support greater functional diversity, and different types of biotopes may not have the same roles in maintaining ecosystem services.
Landscape context modifies functional value of fallows While margins are an obligatory feature of agricultural landscapes, fallowing of whole fields is voluntary and can be seen as an additional management tool. For the objective of sustaining and enhancing functional diversity of plan communities, fallowing seems to be 13
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more efficient if carried out in simple landscapes without high quality biotopes, as was expected. In this study, since most of the species in fallows can also be found in margins, the highest contribution to fallow functional diversity comes from high species abundances in
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fallows. Species pool size and competition operate simultaneously in determining a local species composition (Weiher & Keddy 1999). In simple landscapes with a relatively small
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species pool, an unsaturated local community leads to lower competition and allows for
higher averaged species abundance than would be expected for a complex landscape with a
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saturated local community. Difference of species turnover over a relatively large area can
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influence local species coexistence by varying resource ratios (Fargione & Tilman 2002), which leads to a very different abundance patterns in communities (fallows vs. margins).
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Increasing relative abundances of species of important functional roles by fallowing can be
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seen as insurance for ecosystem processes they contribute to.
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Contrary to the pattern of functional diversity, adding a fallow patch to a simple landscape in this study did not result in a significantly enhanced level of taxonomic diversity. Most species
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registered in fallows already occur in margins, especially in complex landscapes. Tscharntke et al. (2005) argued that a high efficiency of local allocation of habitat for species diversity in landscape of intermediate complexity is due to a small species pool, to which a new patch can add considerably. Here there was a tendency for species diversity in fallows to increase across landscape complexity but it was not statistically significant. It is plausible that the history of management may further confound the landscape influence. In simple landscapes, agricultural management tends to be intensive, which depletes the seed bank of fallows and slows down community development. In complex landscapes, fallows are more likely to continue from extensively utilised grasslands; this and proximity of dispersal sources (Wilson 1992) may lead to a rapid enrichment of fallows in complex landscapes. Yet, we could not
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detect this pattern in our data. A more rigorous experimental study is necessary to test the patterns.
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Total functional diversity progressively declined with agricultural landscapes becoming simplified. Similarly, Tscharntke et al. (2008) found that functional diversity of birds and
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insects and their beta diversity declined with agricultural transformation from diversified to uniformed landscapes. In complex landscapes, presence of varied biotopes enhances plant
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species turnover (beta-level diversity) at landscape level. Community composition
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differentiates through varied resources availability and disturbance types, their frequency and strength, resulting in establishment of functionally unique plant species at any particular site
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across a landscape (O’Gorman et al. 2010).
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Conservation implications
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Since whole-field parcels and linear elements with non-cropped vegetation appear to perform
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differently in terms of functional diversity, a policy that promotes only one type and neglects the other may fail on the objective of an ecologically sustainable agro-landscape. However, in promoting more demanding management options, such as fallowing, the policy might consider conservation efficiencies according to landscape complexity. In a highly productive simplified landscape, delivery of ecosystem services by species capable of persisting in it could be a more attainable goal of management since species of conservation value are rarely found in either semi-natural or established biotopes (Kleijn et al. 2011). In such landscapes, fallows seem to be more effective in maintaining functional diversity of plants. Their potential can be enhanced by sowing of specific species with “missing” traits. In complex landscapes, where fallow fields are more likely to attain high species diversity and therefore contribute to intrinsic biodiversity objective, long-term retention of fallows and management 15
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aimed at their diversity should be a primary objective. Introducing an Ecological Focus Area obligation that includes fallow patches into the requirements of the Common Agricultural Policy is justified. While they could be established across a variety of landscapes, their
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objectives and management might be tailored by agricultural landscape character.
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Acknowledgements
We thank Anni Kiviranta, Marjaana Toivonen, Hanna Seitapuro, Mariel Delasalle and
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Catherine Le Barh for help with fieldwork and landscape analysis. Miia Jauni provided some of the trait data. Vegetation sampling was kindly allowed by the farm owners. This work was
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funded by the Academy of Finland (project number 132092) to M.M. and by Finnish
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Ministry of Agriculture and Forestry (project number 2589/311/2009) to I.H. Riho Marja helped in statistical analysis. Feedback of David Kleijn and two anonymous reviewers
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considerably improved the manuscript.
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Mason, N. W. H., Mouillot, D., Lee,W. G., & Wilson, J. B. (2005). Functional richness, functional evenness and functional divergence: the primary components of functional
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Reich, P.B., Walters, M.B., & Ellsworth, D.S. (1992). Leaf lifespan in relation to leaf, plant and stand characteristics among diverse ecosystems. Ecological Monographs, 62, 356–392.
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Rakosy, L., & Ramwell, C. (2009). Ecological impacts of early 21st century agricultural
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Toivonen, M., Herzon, I., & Helenius, J. (2013). Environmental Fallows as a new policy tool to safeguard farmland biodiversity in Finland. Biological Conservation, 159, 355–366.
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Captions Figure 1. Location and land cover of the study area, the Lepsämänjoki watershed in
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Nurmijärvi commune, southern Finland.
Figure 2. Species richness a) and RAO’s functional diversity index b) by habitat type of
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fallow, field margin, forest margin and river margin along a landscape gradient (mean and
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95% CI). N = 32
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Figure 3. RAO’s index for pooled functional diversity in margins, fallows and all biotopes in
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landscape squares.
Figure 4. Number of unique species a) and mean of relative abundance of each species b) in
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fallows and margins of the landscape squares (mean and 95% CI).
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Table 1. Landcover/landuse of three types of landscape context. SHDI refers to ShannonWiever diversity index of landcover, and NA - not available. Simple
Intermediate
Complex
landscape
landscape
landscape
0.2326
0.4617
crop margin
0.93
0.56
forest margin
0.02
0.27
028
river margin
NA
NA
0.12
Forest area (%) †
7.32
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90.32
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Field area (%) †
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Margin density *
0.6845
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SHDI of landcover diversity
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Landcover
0.32
69.43
52.56
24.38
37.24
* Total margin length/ area of landscape square (1 km2)
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te
d
† Area of landcover / area of landscape square
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Biotope types
P
Simple landscape
Crop < Fallow
0.001
Intermediate landscape
Crop < Forest = Fallow
0.002
Complex landscape
Crop = Forest = Fallow <
0.000
us
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Mean of RAO’s indices for traits
River Life form Crop < Fallow
Intermediate landscape
Crop < Forest < Fallow
0.02
Complex landscape
Crop = Fallow < Forest =
0.003
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Crop < Fallow
0.001
Intermediate landscape
Crop < Forest < Fallow
0.000
Crop = Forest = Fallow <
0.012
Complex landscape
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Simple landscape
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LDMC
0.002
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Simple landscape
River
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Table 3. Differences in the RAO’s indices for functional traits, their mean and total species number of vascular plants among biotope type (fallow and margins of field, forest and river types) in three landscapes of simple, intermediate and complex type. Kruskal-Wallis and Mann-Whitney (for simple landscape) non-parametric test used everywhere except for species richness, where Poisson GLM was used. Ns stands for non-significant differences.
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River
Dispersal
Simple landscape
Ns
Intermediate landscape
Ns
Complex landscape
Crop = Forest = Fallow <
0.02
River
Seed mass
Simple landscape
Ns
Intermediate landscape
Ns
Complex landscape
Crop = Forest = Fallow <
0.015
River Pollination
Ns for all landscapes
Flowering phenology
Ns for all landscapes 28
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Species number Simple landscape
Ns
Intermediate landscape
Crop < Forest = Fallow
0.028
Complex landscape
Crop = Forest < River =
0.025
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d
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an
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Fallow
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Table2
Ecosystem processes
Ecosystem services
Life form
Nominal *
-
Primary productivity
Supporting service
Leaf dry matter content
Continuous
mg g-1
Nutrient cycling
Supporting service
Pollinating type
Nominal †
-
Plant-pollinator interactions
Regulating service
Seed mass
Continuous
mg
Regeneration strategies
Regulating service
Flowering phenology
Nominal ‡
-
Reproduction strategies, climate response
Regulating service, possible cultural service
Dispersal type
Nominal ¶
-
Regeneration strategies
Regulating service
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Unit
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Type
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ep te
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Functional traits
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Table 2. Plant functional traits and ecosystem processes and services to which they contribute (Díaz et al. 2005)
* Life forms: annual forb, perennial forb, annual graminoid, perennial graminoid, legume, fern, and shrub. † Pollination types: bee, Lepidoptera, Diptera, Coleoptera, wasp, wind, self, and apomictic. ‡ Flowering phenology: early spring, spring, summer, autumn, and late autumn. ¶ Dispersal types: birds, ants, human, wind, and self.
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Figure 1
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Figure2
Figure 2
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Figure3
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Figure 3
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Figure4
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a)
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b)
Figure 4
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S1617-1381(14)00090-9 http://dx.doi.org/doi:10.1016/j.jnc.2014.08.006 JNC 25375
To appear in: Received date: Revised date: Accepted date:
27-1-2014 5-8-2014 5-8-2014
Please cite this article as: Ma, M., and Herzon, I.,Plant functional diversity in agricultural margins and fallow fields varies with landscape complexity level: conservation implications, Journal for Nature Conservation (2014), http://dx.doi.org/10.1016/j.jnc.2014.08.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Plant functional diversity in agricultural margins and fallow fields varies with
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landscape complexity level: conservation implications
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Maohua Ma*,Irina Herzon
Department of Agricultural Sciences, P.O. Box 27, FI-00014 University of Helsinki, Finland
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*Corresponding author. Tel.: +358919158451; fax: + 358919158582. E-mail address:
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References: 52
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Word count of main text: 3655
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[email protected]
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Abstract A consensus has been established that functional traits rather than taxonomic diversity play a
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fundamental role in linking biodiversity with ecosystem processes and associated services. This study from Finland addressed an issue of relative values of fallow and field margin
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biotopes in conservation of plant functional diversity (based on six functional traits of
relevance to ecosystem services, and diversity of multiple traits) in agricultural landscapes
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differing in their structural complexity. Relative covers of plant species were surveyed in sampling plots located in perennial fallow fields and three types of perennial margins
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(margins between crop fields, along forest edges and by river) in three types of landscape context (simple, intermediate and complex). Fallow fields significantly contributed to the
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total functional diversity only in simple landscapes. The river margins provided the greatest functional diversity, especially in reproduction and regeneration traits while crop margins
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were consistently characterised by the lowest functional diversity. Substantial functional diversity of fallow patches in simple landscapes was due to high abundance of functional
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species, while that of river margins stemmed from presence of unique species. The plant functional diversity progressively declined with agricultural landscapes becoming simplified. The study indicates non-cropped biotopes having complementary roles in ensuring multifunctionality of agro-landscapes and confirms importance of biotope mosaic for functional diversity.
Keywords: agricultural landscapes; agri-environmental policy; ecosystem services; noncropped biotopes; functional traits.
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Highlights •
Fallow fields had the highest contribution to the total functional diversity in simple
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landscapes. River margins supported the greatest functional diversity.
•
Fallows and margins displayed differences in diversity of individual functional traits.
•
Fallows had few unique species but supported high species abundances per sample.
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•
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Introduction The economy-driven progression of agricultural production into more intensive and
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specialised forms leads to the deterioration in the ecological state of agricultural ecosystems
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(Stoate et al. 2009). Among other impacts, this drives homogenisation of the agricultural
landscapes (Benton et al. 2003). One of the commonest counteractive options is preservation,
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establishment and management of field margin biotopes, which, in the EU, is mainly done through the agri-environmental contracts and cross-compliance baseline (IEEP 2008).
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Ecological benefits of linear habitats as reservoirs of beneficial invertebrates, predators of pest species or crop pollinators have been widely appreciated (Marshall et al.1994; Cole et al.
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2012). Another common agri-environment option at farm scale is fallowing, that is, removal of whole field parcels from production. Fallowing of a certain portion of a field area had been
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an obligation across the EU until 2008, when it was abolished (i.e. CAP set-aside; Hart &
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Baldock 2011). Many countries, including Finland, offer payments for voluntary fallowing of
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fields with an objective of enhancing biodiversity (Kovács-Hostyánszki et al. 2011; Toivonen et al. 2013).
A hypothesis considering the relationship between effectiveness of agri-environment schemes and landscape complexity (Tscharntke et al. 2005) sets local farm management into a landscape perspective. Accordingly, efficiency of agri-environmental allocations depends on level of landscape complexity, which is defined at three levels based on cover of semi-natural areas: cleared (< 1% of semi-natural habitats, lowest diversity); simple (1-20%); and, complex (>20%, highest diversity). The intermediate level, that is simple landscape, is predicted to be optimal to agri-environmental management, which has generally been
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corroborated in a meta-analysis (Batáry et al. 2011). Most recently, the framework has been extended to consider provisioning of ecosystem services (Tscharntke et al. 2011).
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A consensus has been established that species functional traits play a fundamental role in linking biodiversity with ecosystem processes and services (Díaz & Cabido 2001; Hooper et
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al. 2005; Reiss et al. 2009). For instance, there are well-established links between plant leaf traits (e.g. LDMC) and nutrient cycling providing ecosystem supporting service (Reich et
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al.1992; Poorter & Garnier 1999; Garnier et al. 2004); diversity in plant life forms is a strong
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surrogate to assess variation in plant net primary productivity delivering regulating service (Lieth & Whittaker 1975; Saugier et al. 2001). However, studies on impacts of agri-
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environment management on biodiversity still focus mainly on taxonomic species diversity rather than species’ functional properties. Yet, it has been suggested that in production
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systems, landscape-moderated conservation of total species richness or abundance of red-data
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listed species will not necessarily optimize ecosystem services (Kleijn et al. 2011).
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Functional diversity can be measured by functional composition of multiple traits using functional diversity indices (e.g. functional richness, functional evenness). Indices that mix richness and evenness, such as RAO’s index (Botta-Dukát 2005), have also been used extensively (Díaz et al. 2007; Flynn et al. 2009; Mason et al. 2012). Assessment of landuse effects on indices composed by functional traits relevant for key ecosystem functions can therefore provide insight on how to optimise land management for maintaining multiple ecosystem services.
This study focused on functional diversity of vascular plants in fallow and margin biotopes along a spatial gradient from simple to complex landscape context. The key research 5
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questions were: 1) How does functional biodiversity compare among different biotopes of margins and fallows? More specifically: i) How do relative roles of margins and fallows change with increased landscape complexity? and ii) Do relative contributions of two biotope
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types to functional diversity differ from those to taxonomic diversity? 2) How does the
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overall landscape-level functional diversity change under different landscape context?
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Since large habitats generally contain more species than small habitats (species-arearelationships, MacArthur & Wilson, 1967) we hypothesized that whole-field patches (fallows)
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are more effective in promoting taxonomic diversity than narrow biotopes of linear type (margins). Furthermore, since in environments with low biodiversity plant communities are
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likely to be unsaturated, a positive linear relationship between taxonomic and functional diversities can be expected. Therefore, we foresaw that simple landscape biotopes of high
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taxonomic diversity would also contribute to greater functional diversity. In landscapes
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favoring high levels of taxonomic diversity, functional diversity reaches an asymptote (Sasaki
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et al. 2009). Therefore in complex landscapes, we expected fallows to contribute more to taxonomic diversity than functional: additional species would likely be functionally redundant.
Methods
Study area
The study area is located in Lepsämänjoki watershed in Nurmijärvi commune, 30 km north of Helsinki (60° 23' – 60° 28' N, 24° 31' – 24° 43' E) in southern Finland (Fig. 1). This flat drainage area is 214 km². Soil types are mostly sandy clay and fine sand. The area belongs to the southern boreal zone with a mean annual temperature of 4.4 °C (-7.6 °C – 16.7 °C), mean precipitation is 65 mm (48 mm – 70 mm) and the average duration of snow cover is 132 days. 6
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Main crops are spring cereals, row crops and silage (Tike 2011). All of these require intensive management making the study area a production-intensive landscape by Finnish
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standards.
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Sampling design
a spatial gradient from simple to complex landscape:
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Based on the main landuse types, we selected three landscape types typical for the area along
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1) Simple landscape dominated by fields and with only crop margins (no river and very small forest patches);
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2) Intermediate landscape with a high cover of forest, and margins represented by crop margins and forest margins (no river);
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3) Complex landscape with a high cover of forest and a river, margins included crop
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margins, forest margins and river margins.
We surveyed fallow fields and three types of perennial margins: margins between crop fields; along forest edges; and, by the only river in the study area. Since neighbouring crop types, slopes, and shading varied along the river, we treat the river samples as independent. All fallow fields were represented by grassland fallow type (Toivonen et al. 2013) established within the past 10 years (average age 5.4, range 4-9). All have been managed by annual mowing without biomass removal, chemical applications or grazing. We did not survey fallows younger than four years (typical rotation period for grassland in Finland) as well as the only grazed parcel. We digitized land-cover of the major types (field, forest, river, ditch, road and building) in the landscape squares in ArcGIS 9.3 (ESRI 2008) and calculated landscape metrics (Table 1) in Fragstats 3.3 for ArcGIS 9 (McGarigal et al. 2002). Digitized 7
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data on land use (including presence of fallow fields) came from the Land Use Register and the Information Centre of the Ministry of Agriculture and Forestry (Tike 2011). We deducted
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the age of the fallows from the same register for years 2001 – 2011.
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For each landscape type, we sampled three landscape squares of 1x1 km (nine in total). In each landscape square, we chose at random three margin strips as sampling sites for each
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margin types. Accordingly, there were only crop margins in the simple landscape, crop and forest margins in the intermediate landscape, and crop, forest and river types in the complex
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landscape. The majority of margins were beside cereal fields (spring barley). Two crop margins and one river margin in the complex landscape were beside root vegetable fields.
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These and forest margins were about 0.5-2 m wide and river margins were about 3-8 m wide. In each sampling site, six or seven 1-m2 plots were sampled at systematic intervals. Five
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fallow sampling sites, corresponding to age and management restriction, were chosen
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randomly in each landscape type. There was a non-directional difference in average ages (in
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the simple landscape: mean 5.2, range 4-7; intermediate: 4.8, 4-9; and complex: 6.2, 4-8). In each fallow site, four to eight 1-m2 plots were sampled depending on field size so that the field area was covered systematically.
Not all species of vascular plants were fully (binomially) identified but some were placed within a genus and subsequently treated as a pseudo-species (e.g. Taraxacum, Alchemilla). Relative covers of species were estimated in each plot according to the logarithmic scale (1 ≤0.125%, 2 ≤0.5 %, 3 ≤2%, 4 ≤4%, 5 ≤8%, 6 ≤16%, 7 ≤32%, 8 ≤64%, 9 >64%). Species nomenclature followed Hämet-Ahti et al. (1998). All field workers undertook training in field methods. 8
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Functional traits and diversity index We calculated species richness per each site and landscape (taxonomic diversity). For
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functional diversity, we used six types of functional traits (Table 2) on the basis of their
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potential importance for ecosystem functions and associated ecosystem services (Díaz et al.
2005; Swinton et al. 2006), and following the recommendations of Cornelissen et al. (2003).
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Measurement of leaf dry matter content (LDMC) followed the method proposed by
Vendramini et al. (2002). After cutting, leaf samples were stored in sealed plastic bags, which
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were slightly moistened, kept in cold boxes with ice bags and brought back to lab usually within 3 – 8 h. In the laboratory, the leaf samples were blotted dry to remove any surface
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water, weighed as fresh weight and then oven-dried in paper bags at 60 °C for two days, after which their dry mass was measured as: LDMC=dry weight/fresh weight. We collected
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information on other traits from the literature (Hämet-Ahti et al. 1998), online trait data-base
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Biolflor (Biolflor, 2004) (http://www2.ufz.de/biolflor/index.jsp), Seed Information Database
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(SID, 2008) (http://data.kew.org/sid/sidsearch.html), and Nature Gate of Finland (http://www.luontoportti.com/suomi/fi/kasvit/).
We used RAO’s index as a measure of functional diversity (Botta-Dukát 2005). It is based on the quadratic entropy of Rao (1982) that incorporates both the relative abundances of species and a measure of the pairwise functional differences between species by measuring species distance in functional trait space (Mason et al. 2005; Lepš et al. 2006). The index is a generalized form of the Simpson index of diversity (Lepš et al. 2006) and measures both functional richness and divergence of communities (Mouchet et al. 2010). Since the RAO’s functional diversity index is produced by distance of paired species in trait space and 9
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weighted by species relative abundances, variability of species composition and abundances are the two keys in determining the index.
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We first measured RAO’s index for single traits and then calculated a compound RAO’s index of multiple functional traits as a mean over the RAO’s indices for single traits in each
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sampling site (Lepš et al. 2006). We used a macro tool for MS Excel 2010 (available freely
at:http://botanika.bf.jcu.cz/suspa/FunctDiv.php).In order to estimate gamma-level diversity at
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landscape scale, we pooled data over all biotopes for each landscape type.
Statistical analysis
Because not all biotope types were present in each landscape type (i.e. only crop margins in
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simple landscapes), we tested the differences in diversity between biotope types separately for each landscape type using generalized linear modeling (GLM) with Poisson distribution
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for species richness. None of the models with alternative link functions in GLM performed satisfactory for the individual traits or the mean over them, therefore we used non-parametric
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Kruskal-Wallis test or Mann-Whitney test (in simple landscapes with two samples). To ascertain the differences among the types of biotopes in intermediate and complex landscapes (more than two types), we used Tukey test with ranked sums (Sokal and Rolf 1995). We used the same non-parametric tests for differences in parameters in fallows across the landscapes. All analysis was run in R 2.13.0 (R Development Core Team, 2014). No statistical test was possible on data pooled on landscape level here because of the sample size of three. We also identified unique species in the margins (i.e. not found in the fallows) and fallows (i.e. not found in the margins) for each landscape type.
Results 10
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Relative roles of margins and fallows in supporting functional diversity Fallow fields significantly contributed to the total functional diversity only in simple landscapes. In both simple and intermediate landscapes, fallow biotope was characterized by
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significantly higher diversity than the margins for life forms and LDMC (Table 3). Diversity in these traits, but not in the others, was the highest in fallows in complex landscapes
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(Kruskal-Wallis test; P = 0.048 and 0.009, respectively). In complex landscapes with river
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margins, levels of functional diversity in fallow did not differ significantly from those in crop and forest margins. River margin biotope had the highest diversity for LDMC, dispersal
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modes and seed mass. Crop margins were consistently characterized by the lowest functional diversity. There were no significant differences in pollination types and flowering phenology
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among biotope types. Functional diversity of fallows did not change across landscape
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gradient (Fig. 2b).
Functional diversity in different biotope types showed a different pattern from that of species
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richness along the gradient of landscape context (Fig. 2). In complex landscapes, fallows supported the greatest species diversity (Fig. 2a) while river margins became the biotope supporting the greatest functional diversity (Fig. 2b). Species richness in fallow biotopes was similar to that in the most taxonomically diverse margin type of a corresponding landscape type: forest margin in the intermediate and river margin in the complex landscape (Table 3; Fig. 2a). However, there was no statistically significant difference in species diversity in fallows among the landscape types (Kruskal-Wallis test; P = 0.156). Margins between crop fields were also taxonomically least diverse across all landscape types. Species richness in crop or forest margins did not change across the landscape gradient, while in fallow fields it increased steadily but non-significantly (Fig. 2a).
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Functional diversity on landscape level When the data in each landscape square were pooled and the margins were treated as one
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biotope type, the RAO’s diversity index of fallows was very similar to the total RAO’s index
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in simple landscapes, and they contributed most to the total functional diversity (Fig. 3). In complex landscapes, contribution of margins was higher than that of fallows. While
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functional diversity in the fallows did not change considerably from simple to complex landscape context, it increased in the margins, also driving an increase in the total functional
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diversity (Fig. 3). Fallows always had a lower number of unique species than the margins
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Discussion
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than those in the margins (Fig. 4b).
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(Fig. 4a) while the relative abundances of each species in fallows were significantly higher
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Functional value of fallow and margin biotopes Fallow and margin biotopes demonstrated different and complementary roles in conserving functional diversity. Although taxonomic diversity in fallows equaled that of the most species-rich margin type, contribution of fallows to the overall functional diversity exceeded that of only crop margins. Fallows and margins displayed apparent differences in individual functional traits. Fallows and river margins had the highest variation of life forms and LDMC-traits related to supporting services. LDMC is one of the most important effect traits on determining nutrient cycling and efficiency of carbon acquisition by plants being a key in delivering ecosystem supporting services (Chapin et al. 2002; Garnier et al. 2004). Therefore, fallows may support a greater variety of fundamental properties of plants relevant to 12
Page 12 of 33
ecosystem supporting services than crop and forest margins do. Fallow vegetation represented a relatively low variation for such reproduction and regeneration traits as dispersal, seed mass, pollination and flowering phenology. These traits reflect plant strategies
ip t
in responding to environmental changes and relate to regulating ecosystem services (Grime
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1997; Díaz et al. 2005).
River margins were functionally the most diverse biotope type. According to the national
us
agri-environmental policy, the required minimum width of margins along watercourses is 3 m.
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The margins along crop and forest edges are mostly < 1 m (Ma, unpublished data). A greater width, and hence a broader gradient of soil conditions from river-side to field-side, is likely to
M
explain enhanced diversity in the river margins (Ma et al. 2002). Wide riparian river margins also have potential to promote survival of functional species with poor dispersal capability
d
(Cole et al. 2012). Crop margins had consistently the lowest functional diversity of the
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biotope types, most probably due to their narrow character, disturbance and restricted species
Ac ce p
pool of the neighbouring crops.
Different values of fallows and margins in functional and taxonomic diversity indicate that biotopes of greater taxonomic diversity do not always support greater functional diversity, and different types of biotopes may not have the same roles in maintaining ecosystem services.
Landscape context modifies functional value of fallows While margins are an obligatory feature of agricultural landscapes, fallowing of whole fields is voluntary and can be seen as an additional management tool. For the objective of sustaining and enhancing functional diversity of plan communities, fallowing seems to be 13
Page 13 of 33
more efficient if carried out in simple landscapes without high quality biotopes, as was expected. In this study, since most of the species in fallows can also be found in margins, the highest contribution to fallow functional diversity comes from high species abundances in
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fallows. Species pool size and competition operate simultaneously in determining a local species composition (Weiher & Keddy 1999). In simple landscapes with a relatively small
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species pool, an unsaturated local community leads to lower competition and allows for
higher averaged species abundance than would be expected for a complex landscape with a
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saturated local community. Difference of species turnover over a relatively large area can
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influence local species coexistence by varying resource ratios (Fargione & Tilman 2002), which leads to a very different abundance patterns in communities (fallows vs. margins).
M
Increasing relative abundances of species of important functional roles by fallowing can be
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seen as insurance for ecosystem processes they contribute to.
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Contrary to the pattern of functional diversity, adding a fallow patch to a simple landscape in this study did not result in a significantly enhanced level of taxonomic diversity. Most species
Ac ce p
registered in fallows already occur in margins, especially in complex landscapes. Tscharntke et al. (2005) argued that a high efficiency of local allocation of habitat for species diversity in landscape of intermediate complexity is due to a small species pool, to which a new patch can add considerably. Here there was a tendency for species diversity in fallows to increase across landscape complexity but it was not statistically significant. It is plausible that the history of management may further confound the landscape influence. In simple landscapes, agricultural management tends to be intensive, which depletes the seed bank of fallows and slows down community development. In complex landscapes, fallows are more likely to continue from extensively utilised grasslands; this and proximity of dispersal sources (Wilson 1992) may lead to a rapid enrichment of fallows in complex landscapes. Yet, we could not
14
Page 14 of 33
detect this pattern in our data. A more rigorous experimental study is necessary to test the patterns.
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Total functional diversity progressively declined with agricultural landscapes becoming simplified. Similarly, Tscharntke et al. (2008) found that functional diversity of birds and
cr
insects and their beta diversity declined with agricultural transformation from diversified to uniformed landscapes. In complex landscapes, presence of varied biotopes enhances plant
us
species turnover (beta-level diversity) at landscape level. Community composition
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differentiates through varied resources availability and disturbance types, their frequency and strength, resulting in establishment of functionally unique plant species at any particular site
M
across a landscape (O’Gorman et al. 2010).
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Conservation implications
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Since whole-field parcels and linear elements with non-cropped vegetation appear to perform
Ac ce p
differently in terms of functional diversity, a policy that promotes only one type and neglects the other may fail on the objective of an ecologically sustainable agro-landscape. However, in promoting more demanding management options, such as fallowing, the policy might consider conservation efficiencies according to landscape complexity. In a highly productive simplified landscape, delivery of ecosystem services by species capable of persisting in it could be a more attainable goal of management since species of conservation value are rarely found in either semi-natural or established biotopes (Kleijn et al. 2011). In such landscapes, fallows seem to be more effective in maintaining functional diversity of plants. Their potential can be enhanced by sowing of specific species with “missing” traits. In complex landscapes, where fallow fields are more likely to attain high species diversity and therefore contribute to intrinsic biodiversity objective, long-term retention of fallows and management 15
Page 15 of 33
aimed at their diversity should be a primary objective. Introducing an Ecological Focus Area obligation that includes fallow patches into the requirements of the Common Agricultural Policy is justified. While they could be established across a variety of landscapes, their
us
cr
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objectives and management might be tailored by agricultural landscape character.
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Acknowledgements
We thank Anni Kiviranta, Marjaana Toivonen, Hanna Seitapuro, Mariel Delasalle and
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Catherine Le Barh for help with fieldwork and landscape analysis. Miia Jauni provided some of the trait data. Vegetation sampling was kindly allowed by the farm owners. This work was
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funded by the Academy of Finland (project number 132092) to M.M. and by Finnish
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Ministry of Agriculture and Forestry (project number 2589/311/2009) to I.H. Riho Marja helped in statistical analysis. Feedback of David Kleijn and two anonymous reviewers
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considerably improved the manuscript.
16
Page 16 of 33
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Captions Figure 1. Location and land cover of the study area, the Lepsämänjoki watershed in
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Nurmijärvi commune, southern Finland.
Figure 2. Species richness a) and RAO’s functional diversity index b) by habitat type of
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fallow, field margin, forest margin and river margin along a landscape gradient (mean and
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95% CI). N = 32
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Figure 3. RAO’s index for pooled functional diversity in margins, fallows and all biotopes in
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landscape squares.
Figure 4. Number of unique species a) and mean of relative abundance of each species b) in
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fallows and margins of the landscape squares (mean and 95% CI).
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Table 1. Landcover/landuse of three types of landscape context. SHDI refers to ShannonWiever diversity index of landcover, and NA - not available. Simple
Intermediate
Complex
landscape
landscape
landscape
0.2326
0.4617
crop margin
0.93
0.56
forest margin
0.02
0.27
028
river margin
NA
NA
0.12
Forest area (%) †
7.32
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90.32
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Field area (%) †
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Margin density *
0.6845
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SHDI of landcover diversity
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Landcover
0.32
69.43
52.56
24.38
37.24
* Total margin length/ area of landscape square (1 km2)
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te
d
† Area of landcover / area of landscape square
26
Page 26 of 33
Biotope types
P
Simple landscape
Crop < Fallow
0.001
Intermediate landscape
Crop < Forest = Fallow
0.002
Complex landscape
Crop = Forest = Fallow <
0.000
us
cr
Mean of RAO’s indices for traits
River Life form Crop < Fallow
Intermediate landscape
Crop < Forest < Fallow
0.02
Complex landscape
Crop = Fallow < Forest =
0.003
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Crop < Fallow
0.001
Intermediate landscape
Crop < Forest < Fallow
0.000
Crop = Forest = Fallow <
0.012
Complex landscape
te
Simple landscape
d
LDMC
0.002
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Simple landscape
River
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Table 3. Differences in the RAO’s indices for functional traits, their mean and total species number of vascular plants among biotope type (fallow and margins of field, forest and river types) in three landscapes of simple, intermediate and complex type. Kruskal-Wallis and Mann-Whitney (for simple landscape) non-parametric test used everywhere except for species richness, where Poisson GLM was used. Ns stands for non-significant differences.
Ac ce p
River
Dispersal
Simple landscape
Ns
Intermediate landscape
Ns
Complex landscape
Crop = Forest = Fallow <
0.02
River
Seed mass
Simple landscape
Ns
Intermediate landscape
Ns
Complex landscape
Crop = Forest = Fallow <
0.015
River Pollination
Ns for all landscapes
Flowering phenology
Ns for all landscapes 28
Page 27 of 33
Species number Simple landscape
Ns
Intermediate landscape
Crop < Forest = Fallow
0.028
Complex landscape
Crop = Forest < River =
0.025
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te
d
M
an
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cr
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Fallow
29
Page 28 of 33
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Table2
Ecosystem processes
Ecosystem services
Life form
Nominal *
-
Primary productivity
Supporting service
Leaf dry matter content
Continuous
mg g-1
Nutrient cycling
Supporting service
Pollinating type
Nominal †
-
Plant-pollinator interactions
Regulating service
Seed mass
Continuous
mg
Regeneration strategies
Regulating service
Flowering phenology
Nominal ‡
-
Reproduction strategies, climate response
Regulating service, possible cultural service
Dispersal type
Nominal ¶
-
Regeneration strategies
Regulating service
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Unit
M
Type
Ac c
ep te
d
Functional traits
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Table 2. Plant functional traits and ecosystem processes and services to which they contribute (Díaz et al. 2005)
* Life forms: annual forb, perennial forb, annual graminoid, perennial graminoid, legume, fern, and shrub. † Pollination types: bee, Lepidoptera, Diptera, Coleoptera, wasp, wind, self, and apomictic. ‡ Flowering phenology: early spring, spring, summer, autumn, and late autumn. ¶ Dispersal types: birds, ants, human, wind, and self.
Page 29 of 33
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Figure 2
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Figure3
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Figure 3
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Figure4
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a)
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b)
Figure 4
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