A simple standardized protocol to evaluate the reliability of seed rain estimates

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Running title: Seed rain in grasslands
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How have we studied seed rain in grasslands and what
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do we need to improve for better restoration?
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André J. Arruda1,2,3, Elise Buisson3, Peter Poschlod4 and Fernando A. O.
Silveira1
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1. Departamento de Botânica, Universidade Federal de Minas Gerais. 30161-970 Belo
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Horizonte, Brazil.
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2. Author for correspondence to A. J. Arruda: [email protected]
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3. Université d’Avignon et des Pays de Vaucluse, IMBE – Institut Méditerranéen de
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Biodiversité et d’Ecologie, CNRS, IRD, Aix Marseille Université, IUT d’Avignon,
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AGROPARC BP61207, 84911 Avignon, France
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4. Institute of Plant Sciences, Faculty of Biology and Preclinical Medicine, University
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of Regensburg, D-93040 Regensburg, Germany
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Author contributions
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AJA, EB, FAOS, PP conceived and designed the research; AJA performed the review
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and analyzed the data; AJA, FAOS wrote the manuscript; EB, PP edited the manuscript.
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Abstract
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Seed rain, the number of seeds reaching an area, is a process that plays a key role in
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recruitment and regeneration in plant communities. A better understanding of seed rain
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dynamics is therefore a critical step for restoration practices. A wide variety of methods
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to study seed rain in grasslands are available, but there is little agreement to which is the
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most appropriate one. Here we: 1) assessed where, how and why research on seed rain
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has been carried out; 2) examined how methodological design and results have been
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reported and 3) provide guidelines for future research on seed rain in grasslands. We
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built a database of 185 papers from a systematic literature survey between 1980 and
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November 2016 and we found a remarkable unbalance of the numbers of studies
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between grassland types, which becomes even more dissimilar across global climatic
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ranges when the area covered by each grassland type is addressed. We also found a
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great disparity of methods and data being reported across studies. Despite recent
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progress in understanding seed rain dynamics, large knowledge gaps in important
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issues, such as the role of native dispersers, method efficiency and application of
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mechanistic models still persist. Finally, we propose guidelines for the implementation
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of minimum standardized methodology and data reporting, which will foster higher
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quality, transparency, reproducibility and value of seed rain studies and grassland
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restoration.
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Key-words: meadow, prairie, rangeland, seed limitation, seed trap, steppe
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Conceptual Implications
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• An unbalanced distribution of seed rain studies among grassland types calls for
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additional research efforts on non-temperate grasslands to better support restoration
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• We identified significant knowledge gaps in grassland seed rain research,
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which should now be tackled: the role of (1) native animals as seed dispersers, (2) pre-
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dispersal and post-dispersal seed predation, (3) non-native species, (4) method
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efficiency, (5) application of mechanistic models, (6) active restoration standards
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prevents a critical appraisal of the role of seed rain in restoration of grasslands
• We recommend the implementation of guidelines for methodology and data
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• The lack of standardization of methodology, terminology and data reporting
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reporting, which will depend on future collaborative efforts
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Introduction
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Restoration Ecology
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Seed rain is the number of seeds reaching an area, and it usually is quantified
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and qualified by placing traps in the plant community to catch seeds that then are
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identified and counted (Baskin & Baskin 2014). Seed rain is a critical step in plant life
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cycle, as it represents a demographic bridge between the adult and seedling stage
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(Harper 1977). Seed rain reflects species dispersal potential, and therefore the
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persistence or potential for change of the standing vegetation (Page et al. 2002).
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Additionally, it allows the arrival of seeds into suitable uncolonized microsites (Baker
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1974), with major implications for biological invasions and restoration ecology by
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revealing relevant information about how target species can reach a restored site, and
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whether seed rain is effective and efficient to restore a given site (Turnbull et al. 2000).
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Many plant communities are seed limited, meaning that microsites where seeds can
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arrive and germinate, remain vacant, which can be related to limited seed production
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and/or limited dispersal of available seeds among sites (Clark et al. 1998). Hence, seed
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rain estimates can provide a hint of successional direction by predicting the probabilities
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of propagule arrival (D'Angela et al. 1988).
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Over the last decades, seed rain has been analyzed both i) indirectly, by studies
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of plant reproductive potential (Boughton et al. 2016) and seed bank dynamics (Bertiller
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& Aloia 1997), and ii) directly, by collecting either seeds visible on the ground, by
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observing the movements of granivore animals (Izhaki et al. 1991) or from diaspore
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traps (Kollmann & Goetze 1998). The great diversity of methodologies reported for
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seed rain studies may have a close relation with the wide range of biological processes
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that may be involved, which makes the delimitations of this biological process often
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unclear (Fig. S1).
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In essence, an ideal method for studying seed rain is the one that can assess what
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seed, how many seeds and when that seed arrives in the seed bank (Schott 1995).
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Despite this, few seed rain studies use standardized methods that would allow cross-
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vegetation comparisons. As an example, numerous types of seed traps have been used in
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ecological studies with different characteristics, such as shape, size, height above soil
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surface and trap inclination, all of which can affect their effectiveness (Bakker et al.
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1996, Chabrerie & Alard 2005). A wide variety of seed rain measuring methods is
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available in the literature. However, there is little agreement to which is the most
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appropriate method taking into account a wide range of possible variables. This is
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especially true for grassy biomes, for which knowledge on natural regeneration
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following disturbance lags behind that of forest ecosystems (Meli et al. 2017).
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Grassy ecosystems cover around 52 million km², ca. 40% of the global land
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surface (White et al. 2000; Gibson 2009). Over the last decades huge areas of native,
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old-growth grasslands have been lost to agricultural expansion, desertification, mining,
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urbanization and other changes or have been degraded by changes in fire regimes,
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exotic species introduction, fertilization, drainage, liming, overgrazing, etc. (White et al.
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2000; Veldman et al 2015). In the face of increasing land-use pressures and increasing
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biodiversity loss in grasslands, biogeographical studies of spatial and temporal patterns
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of seed rain are essential to restoration and management practices (Bakker et al. 1996).
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While seed rain patterns in grasslands are very difficult to assess and to predict, a better
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understanding about their influence on the resilience and succession in these
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environments is urgently needed, aiming to achieve biodiversity conservation goals,
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secure ecosystem services (Parr et al. 2014) and provide basis for better restoration
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practices.
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Given that seed rain plays a pivotal role in restoration ecology, we explore the
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interplay between seed rain research and restoration in grasslands 20 years after Bakker
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et al. (1996) stressed the role of seed rain and seed banks in restoration ecology. Our
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goals were: 1) to assess where, how and why research on seed rain was carried out; 2) to
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examine methodological design and results reported; and 3) to provide guidelines for
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future research in seed rain, aiming to standardize and foster higher quality,
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transparency, reproducibility and value to seed rain studies in grasslands.
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Material and Methods
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Literature survey and grassland classification
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We surveyed papers in the Web of Science which have been published from
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1950 to 30th November 2016, by searching the following terms in the title, abstract, and
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key words of papers: “seed rain” plus “grassy biome”, “grassland”, “meadow”,
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“prairie”, “rangeland”, “savanna”, or “steppe”. We removed papers dealing only with
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seed production or seed bank, and included only studies that addressed the releasing
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process of diaspores from the parent plant and their movements until reaching the soil.
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After removing redundant papers, our survey comprised 185 papers published between
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1980 and 2016. From those, we removed the papers not related to grasslands (those
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addressing seed rain in forest ecosystems), and papers that did not study seed rain in
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detail, represented by studies that did not present any qualitative or quantitative data on
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seed rain over space or time. We were left with 98 papers that matched our criteria for
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this review.
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For each study, we classified the grassland type according to Dixon et al. (2014).
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We considered seven grassland types: alpine grassland; boreal grassland; cool semi-
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desert grassland; temperate grassland; Mediterranean grassland; tropical grassland and
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warm semi-desert grassland. Using ArcGIS software, we built a map plotting the
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geographic distribution of seed rain studies together with the global grassland
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distribution through the geographical coordinates available in Dixon et al. (2014).
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Relevance of seed rain studies to restoration ecology
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We considered studies with direct relevance to restoration ecology, such as those
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that addressed any of the following processes: recolonization, succession and
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predictions after degradation, endangered species conservation, spread of non-native
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species and natural plant communities or species dynamics. We classified degradation
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types reported in each study as endogenous or exogenous disturbances (sensu McIntyre
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and Hobbs 1999). The endogenous category refers to disturbances to which ecosystems
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were repeatedly exposed through evolutionary time and which, with an appropriate
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regime, allow ecosystems to maintain biodiversity. On the other hand, the exogenous
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category refers to novel, mainly anthropogenic disturbances, which may be
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incompatible with the maintenance of grassland biodiversity. We classified the
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ecological restoration processes, whenever mentioned, as passive or active restoration.
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Passive restoration stands for cases when only natural regeneration processes were
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evaluated, whereas active restoration refers to the implementation of restoration
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techniques, such as hay spreading or seed sowing (Rey Benayas et al. 2008).
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Methodological design
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We classified the studies depending on the methodologies used for seed rain
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studies according to the nature and scope of the experimental design into two
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categories: i) direct measurements and ii) mathematical or mechanistic models and
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simulations. The direct measurements included the use of seed traps (Bakker et al.
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1996) and focal or seed tracking observations (e.g. Ferguson & Drake 1999; Piazzon et
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al. 2012). Mathematical or mechanistic models and simulations used numerical methods
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for seed rain dynamics predictions and simulations (e.g. Doisy et al. 2014).
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In order to obtain additional information about the dispersal dynamics, we
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searched for studies that used methods to evaluate the effect of abiotic (such as water
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and wind) and biotic vectors of seed dispersal. Additionally, we recorded seed dispersal
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distance whenever provided in the original study.
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Owing to the fact that seed trap characteristics may strongly influence results
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(Bakker et al. 1996; Chabrerie & Alard 2005), we evaluated the following aspects for
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studies that employed seed traps as a method to estimate seed rain: trap type, total
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number of traps, trap efficiency in collecting seeds, trap protection against granivores,
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trap position on the ground, height categories for traps lodged above ground, trap
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position in relation to the main wind direction, and sticky traps slope angle. We
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classified the traps in the following categories: funnel trap, sticky trap, tray or gap trap
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and other traps.
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Methodologies and data reporting
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To evaluate standardization in methodologies and data reporting, we analyzed
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seed trap size and total surface measurements for the two most common trap types,
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funnels and sticky traps. Considering that traps with equivalent areas can have very
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different formats, which together with the total trap area, can affect the study outcome,
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we assessed how these measurements were reported in different ways, sorting them into
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three possible categories: i) trap area only; ii) format measures (width and length or
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diameter), iii) not informed. Secondly, we evaluated how many studies calculated the
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total area sampled by the traps. Thirdly, we evaluated how the data collected or
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estimated were reported. We created four categories of data reporting: seed density
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only, total number and density, total number only, not informed. Finally, we examined
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what seed traits (Jiménez-Alfaro et al. 2016) were reported in each study.
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Results
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We found an increase in the number of seed rain studies in grasslands over the
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two last decades, with the maximum number of studies/year of 10 in 2005. We found
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relative increases in the number of studies coinciding with the publication of review
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papers (Fig. S2).
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We found seed rain studies in grasslands across all vegetated continents, in
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tropical (N=7), temperate (N=82) and boreal (N=3) ranges (Fig. 1). However, the
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geographic distribution of studies was strikingly uneven, with most studies concentrated
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in Europe (N=46) and in North America (N=21). More than half (57%) of the seed rain
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studies were conducted in temperate grasslands, while the rest was spread among warm
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semi-desert grasslands (14%), alpine grasslands (10%), Mediterranean grasslands (8%),
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tropical grasslands (6%), boreal grasslands (3%) and cool semi-desert grasslands (1%).
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Only three studies were done in flooded grasslands, all belonging to the temperate
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grassland type.
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Figure 1: Geographic distribution of seed rain studies (black dots) in grasslands. Red
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dashed lines depict tropical areas and blue dashed lines depict boreal areas. Native
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grasslands distribution in yellow follows Dixon et al. (2014).
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Eighty-four papers (85%) of the selected studies were directly or indirectly
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related to ecological restoration. Among the studies related to ecological restoration, 80
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papers (95%) mentioned some type of disturbance, from which 73 (91%) reported
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exogenous disturbances, such as cultivation and mining and only seven (8%) of them
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addressed endogenous disturbance events. Regarding the latter, five studies addressed
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fire regimes, one mentioned drought regimes and fire and one simulated small soil
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disturbances naturally created by a native small mammal from a temperate grassland
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(Supplementary material I). Additionally, from the eighty-four studies applied to
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ecological restoration, 64% addressed passive restoration aspects only and 36% active
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restoration processes. From the 30 studies that addressed active restoration, only 11%
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tested seed sowing techniques.
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From the ninety-eight selected studies, 97% used direct measurements and 3%
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mathematical or mechanistic models and simulations. Additionally, across all selected
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studies, 21 mentioned or surveyed biotic dispersal. Within these 21 studies, birds were
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the main dispersers studied (42% of the studies), followed by livestock (29%), such as
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sheep, cattle and donkeys, ants (29%), other mammals not including bats (14%), bats
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(10%) and lizards (5%). Only 9 studies mentioned the influence of abiotic factors, such
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as wind (8 studies) and water (1 study). From the eight studies that provide some
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information about the main wind direction, five only mentioned and three measured this
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variable. Additionally, we checked how many studies estimated seed dispersal distance
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and found that only 24 studies took seed dispersal distance into account, from which
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less than a quarter presented seed dispersal distance estimates or measurements.
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Fifty-nine percent of seed rain studies were conducted at the community-level
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and 37% only at species-level. From the 37 studies that evaluated the seed rain at
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species-level, 51% included only one species. Additionally, from all studies, 20
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mentioned or evaluated the impact of non-native species, of which 70% reported non-
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woody species and 30% woody species.
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Only 46 studies provided information on complementary physical and
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physiological seed traits, such as size, weight, dormancy and viability. From those, 54%
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provided information on a single seed trait and less than 5% on more than three traits.
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Among the seed traits reported in these 46 studies, seed morphological adaptations for
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dispersal (other than size and weight) were the most common (39% of the studies),
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followed by seed size (33%), seed weight (30%), seed viability (24%), seed dormancy
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(15%), releasing height (11%), seed longevity (4%) and moisture content (2%).
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Sampling length for the 79 studies that provided this kind of information ranged
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from less than 1 month up to 60 months. Additionally, 76 studies provided information
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on sampling frequency, which ranged from weekly to 24 months intervals. Regarding
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the methods for seed identification, 89 studies dealt with this aspect. From those, 50%
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used visual identification through reference collections, 33% did not mentioned any
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seed identification method and 15% used seedlings emerging from seeds to identify
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species.
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From the 76 studies (77%) that used seed traps, 88% used only one type of seed
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traps, 8% used two types, 3% used three types and only one study used five types. The
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most common seed trap type was the funnel trap (34%), followed by the sticky trap
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(18%) and tray or gap trap (17%). Additionally, 18% of the studies used other types of
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traps. Surprisingly, we found information on the total number of traps only for 56 out of
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the 76 studies. Among these, the number of traps per study ranged from 14 to 576, with
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nearly half of the studies using less than 90 traps.
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Among the 76 studies that used seed traps, 62 (82%) did not provide any
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information about the seed trap efficiency in collecting seeds. Only eight studies (10%)
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mentioned trap efficiency and only six studies (8%) tested seed traps for efficiency.
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Only 18 studies (24%) provided information on trap protection against granivores.
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Information on seed trap position related to the ground was found for 56 studies only.
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Among these 56 studies, 52% placed traps aboveground, 50% at ground level and only
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4% underground (some studies included more than one type). For aboveground traps,
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we found a minimum height value of 0.5 cm and maximum of 90 cm. We also found
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that 32% of aboveground traps were positioned at a height of 50 cm or more, followed
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by those at 15 to less than 30 cm (28%), at one to less than 5 cm (25%) and at less than
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1 cm (21%).
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Additionally, we analyzed separately some specific aspects of trap types. We
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evaluated the sloping angle for sticky traps in the 17 studies (22%) that used this kind of
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trap. From these, 76% did not report this variable. Among those which reported this
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information, the angle of 0° (parallel to soil surface) was the most common (3 studies),
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followed by the angles of 45° and 90°, each one present in one study.
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We evaluated seed trap measurements for the most common traps, funnel and
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sticky traps. For the funnel and sticky traps, respectively 30% and 6% of the studies
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provided the seed trap surface area only. Subsequently, we evaluated trap area
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separately for each type of traps. For the funnel and sticky traps, most studies used
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particular trap area sizes. Additionally, only 14% of the studies calculated the total area
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covered by the funnel or sticky traps.
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We also evaluated how the total number of seeds collected or estimated was
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reported for the 82 studies that reported these data. Half of the studies presented seed
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density only (50%), followed by total seed number and seed density (28%) and total
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seed number only (22%).
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Discussion
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Our data clearly shows a lack of standardization in approaches, methods and
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data being reported in seed rain studies across global grasslands. We found unbalanced
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distribution of seed rain studies among hemispheres, different grassland types and, more
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importantly, that even basic aspects of a study (experimental design and number of
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species/seeds sampled), were not properly reported in many cases. Seed rain studies
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have different goals, and one should expect a wide diversity of methods in the literature.
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However, the lack of justification for the employment of different methods, and
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incomplete data reporting strongly hamper our ability to compare results among studies,
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hence preventing a better appreciation of the role played by seed rain in restoration
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ecology.
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General and biogeographical information
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The large proportion of seed rain studies related to ecological restoration
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underlines the great relevance of seed rain studies in restoration ecology (Bakker et al.
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1996; Freund et al. 2015). The small number of studies evaluating the effect of
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endogenous disturbances points out that this issue still needs to be better explored:
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endogenous disturbances usually have to be re-established as a means of or after
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restoration. For example, fire-stimulated flowering (Keeley et al. 2000) and seed release
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(Holmes & Richardson 1999) may affect natural regeneration patterns. However,
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natural recovery of some ecosystems may be quite slow if important drivers of recovery,
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such as the availability of propagules or dispersers are limited (Hubbell et al. 1999; Le
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Stradic et al. 2014).
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The geographical distribution of studies can substantially influence conclusions
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reached by ecologists, being therefore critical to know which biomes, regions, and
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landscapes remain understudied and undervalued (Martin et al. 2012). The remarkable
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unbalance between the numbers of studies worldwide indicates knowledge gaps,
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especially in old-growth tropical grasslands in the southern hemisphere (Veldman et al.
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2015). Considering the total area per grassland type (Dixon et al. 2014), alpine
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grasslands showed the second lowest area among the formations, but had more seed rain
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studies than tropical grasslands, which have an approximately 27 times higher total area
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(Table 1).
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High diversity of estimates of seed rain
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The considerable dominance of direct measurements to evaluate seed rain
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patterns reflects the sampling effort carried out in field experiments with use of seed
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traps or focal observations over the last few decades. Despite the potential usefulness of
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mechanistic models in providing reliable estimates of plant dispersal distances, they are
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still little explored by ecologists (Bullock et al. 2017). The development of dispersal
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mechanistic models is crucial to improve our understanding about relevant topics on
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restoration ecology, such as population dynamics in fragmented landscapes (Gilbert et
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al. 2014) and the arrival of non-native species (Hastings et al. 2005). Meanwhile, there
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is still a long way to go from mechanistic models to processes applicable to seed
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dispersal, in order to reduce the effort required to measure dispersal directly in the field
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(Bullock et al. 2006).
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Animals play important roles in dispersing seeds of native and non-native
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species. Most studies surveyed explored the role of frugivorous passerines or livestock
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as dispersers of grassland species. However, we found a large knowledge gap on the
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ecological role played by other native animals, such as lizards (Piazzon et al. 2012),
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beetles or ants (Nicolai & Boeken 2012; Lima et al. 2013) and non-volant mammals
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(Genrich et al. 2017) in dispersing seeds of native grassland species. Additionally,
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future research should focus on the roles of seed dispersers in dispersing seeds of
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invasive species, which will provide relevant information for restoration actions and
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post-restoration management (Buisson et al. 2017).
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Spatial patterns of seed deposition and issues related to seed sourcing, seed
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quality, availability and dormancy-breaking are of great interest for evaluating the
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effectiveness of dispersal and relevant hurdles for plant community reassembly after
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degradation (Dayrell et al. 2016). However, assessing the contribution of local versus
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distant diaspore sources can be a great challenge (Bullock et al. 2017), which may
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explain how estimating seed dispersal distance has been mostly overlooked by seed rain
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studies in grasslands.
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Sampling length, sampling frequency and seed identification techniques can
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have a great influence on the results. Thus, whenever possible, studies should prioritize
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longer collection periods and short collection frequencies. Short-term studies may imply
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non-overlapping patterns of dispersal period of some species. Furthermore, results are
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likely to be affected by the frequency of checking, mainly when traps are insufficiently
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or not at all protected against seed predation (Gorchov et al. 1993).
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Sampling effort and lack of standardization in the use of seed traps
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Measurements of seed rain in the field can be carried out using seed traps with
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different shapes, sizes, heights and inclinations (Chabrerie & Alard 2005). However,
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trap effectiveness at capturing seeds can vary not only among trap types and
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characteristics, but also over different vegetation or plant species and environmental
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conditions (Kollmann & Goetze 1998). Funnel traps have often been described in the
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literature as the best trapping method by catching the highest number of seeds
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(Kollmann & Goetze 1998). However, funnel trap efficiency may also retain diaspores
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belonging to seed banks through water run-off, and therefore ignoring secondary
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dispersal may result in overestimates of seed rain. Sticky traps, which are especially
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suitable for studying seed rain of anemochorous species, can be easily adapted to the
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Restoration Ecology
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local aerodynamic environment by the control of height, orientation and inclination
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(Chabrerie & Alard 2005). However, sticky traps can catch large amount of insects,
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drastically reducing their efficiency and making it difficult to identify the sampled seeds
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(Poschlod 1990). Alternatively, the use of soil gaps or pots with sterile soil have been
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often attributed as a more realistic method by the integration of seed arrival with other
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field natural conditions, such as secondary removal and predation (Kollmann and
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Goetze 1998), despite the recommendation for the avoidance of these variables for other
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trap types (Debussche & Isenmann 1994). Considering that trapping success can be very
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variable not only between trap types, but across environments and plant communities,
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comparisons between studies should always be made with caution (Kollmann & Goetze
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1998).
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Despite the fact that effects of seed trap area and height on sampling
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effectiveness have been debated since the seminal publications of Fischer (1987) and
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Jackel & Poschlod (1994), we still need to better explore how seed traits, such as size,
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weight and releasing height (Fischer et al. 1996; Jackel & Poschlod 1994; Tackenberg
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et al. 2003) can influence seed trap efficiency. Recommendations about the number of
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traps for seed rain studies have already been reported (Fischer 1987, Kollmann &
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Goetze 1998), but the number of traps needed greatly vary depending on the goals and
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background of the studies.
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Seed trap effectiveness tests are fundamental in seed rain research and should be
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conducted prior to field experiments (Debussche & Isenmann 1994), but we found they
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are rarely carried out. Ignoring such issues may have serious consequences in the
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reliability of seed rain estimates. Standardization of sampling efforts (Jackel &
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Poschlod 1994) and in tests of trap efficiency in collecting, storing and protecting seeds
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against granivores will be fundamental for a better understanding of the operation of
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different seed traps along distinct plant communities and geoclimatic conditions.
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Methodologies and data reporting
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Basic information about methods and results must be thoroughly, clearly and
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transparently reported to enable comparisons and facilitate inclusion in meta-analyses
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(Gerstner et al. 2017). Seed trap format measures, area and the total number of seeds
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collected or estimated reported by the studies evaluated here are remarkably
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unstandardized, sometimes unclear or sometimes data were even not provided. We also
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found a great variety of sizes for both sticky and funnel traps, which were rarely
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accompanied by a clear methodological justification. Finally, only few studies provided
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information on the proportional seed trap area (seed trap area over total plot area).
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Altogether, the lack of standardized methodologies in seed rain studies undermine the
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reliability of studies and prevent comparisons among sites, thereby preventing the
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evolution of the scientific knowledge on a key ecological process underpinning
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ecological restoration.
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Implications and guidelines for future seed rain studies
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When reporting data, researchers should have in mind that their data can be
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readily used by the scientific community to build-up knowledge from single studies
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(Gerstner et al. 2017). Therefore, it is imperative that not only experimental designs are
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clear and justified, but that data reporting adheres to minimum standards. Here, we
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propose guidelines for future research on seed rain studies in grasslands with the hope
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that standardized methodology, or at least better justified methods, will provide the
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scientific community with better conditions for the critical assessment of publications,
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fostering scientific knowledge.
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First, we propose the standardization for the number of seeds collected over time
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and space, according to the minimum parameters: total number of seeds per species
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sampled at each sampling interval; total number of species sampled at each interval;
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total number of seeds/species per trap over the total sampling time and total number of
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seeds/m² per day. Second, given the disparity of methods and data reporting across
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studies that used seed traps, we propose that the following minimum standard is
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reported: trap format measurements (width and length or diameter); total trap area per
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unit (cm²); number of traps per plot; total area covered by traps per plot (cm²); and
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percentage (%) of plot area covered by the traps. We recognize that our modest proposal
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will not be enough to standardize research at global scale, but this is the first step
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towards common and shared vocabulary, methods and data reporting.
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Prior to restoration, seed rain can be evaluated in order to assess the potential for
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regeneration and passive restoration. Restoration assessments should include seed rain
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data in post-restoration monitoring programs (Jacquemyn et al. 2011) and increasing
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knowledge on pre- and post-dispersal seed predation (Pardini et al. 2017) are to play an
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increasing role in determining restoration success and should be integrated into seed
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rain studies whenever possible. Despite considerable progress in recent decades, we still
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face great challenges to improve our knowledge and increase the use of seed rain studies
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to better support grassland restoration (Table 2). More research on restoration of
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tropical and sub-tropical grasslands is required due to the fact that techniques used for
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temperate grassland restoration are not successful in restoring tropical ones (Le Stradic
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et al. 2014). Additionally, understanding to what extent anthropogenic modifications are
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relevant to seed limitation will be fundamental to predict the capacity of grasslands to
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respond to these changes.
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Future successful restoration may also depend on seed addition, on which we
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still need to advance in the practical and theoretical framework (Bakker et al. 2003). We
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must also recognize the importance of considering several characteristics of seed rain,
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besides species composition and seed abundance. Spatial patterns of dispersal and seed
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traits, such as dormancy, longevity, releasing time and duration are fundamental for a
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better understanding on the formation of seed banks and the dynamics of community re-
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assembly following disturbances (Jiménez-Alfaro et al. 2016).
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Lastly, we need to critically stress the fact that cross-vegetation comparisons of
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seed rain data are prevented due to lack of standardized research protocols. We believe
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that the lack of standardization in methodology and data reporting creates a unique
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opportunity for the scientific community to put efforts on a global protocol of seed rain
450
methods. An increased implementation of guidelines for methodology and data
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reporting will foster higher quality, transparency, reproducibility and value to seed rain
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studies in grasslands. Future collaborative, international efforts are paramount for a
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global assessment of the role played by seed rain in restoration ecology.
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Acknowledgments
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We thank RS Oliveira, QS Garcia, NPU Barbosa and LF Fuzessy for criticism during
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early stages of the manuscript. NPU Barbosa and RLC Dayrell also assisted with the
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construction of the map and figures. We thank the reviewers for their comments which
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significantly increased manuscript quality. AJA receives a PhD scholarship from
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CAPES and FAOS receives grants from CNPq and FAPEMIG.
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biomes: misunderstood, neglected, and under threat. Trends in Ecology & Evolution
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29:205-213
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Piazzon M, Larrinaga AR, Pérez JR, Latorre L, Navarro L, Santamaría L (2012) Seed
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dispersal by lizards on a continental-shelf island: predicting interspecific variation in
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seed rain based on plant distribution and lizard movement patterns. Journal of
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Biogeography 39:1984-1995
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Poschlod P (1990) Vegetationsentwicklung in abgetorften Hochmooren des bayerischen
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Alpenvorlandes
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populationsbiologischer Faktoren. Diss. Bot. 152: 331 S. Stuttgart: Bornträger
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Rey Benayas JM, Bullock JM, Newton AC (2008) Creating woodland islets to reconcile
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ecological restoration, conservation, and agricultural land use. Frontiers in Ecology and
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the Environment 6:329-336
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Schott GW (1995) A seed trap for monitoring the seed rain in terrestrial communities.
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Canadian Journal of Botany 73:794-796
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Tackenberg O, Poschlod P, Bonn S (2003) Assessment of wind dispersal potential in
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plant species. Ecological Monographs 73:191-205
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Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? a review
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of seed sowing experiments. Oikos 88:225-238
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Veldman JW, Overbeck GE, Negreiros D, Mahy G, Le Stradic S, Fernandes GW, et al.
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et al. (2015) Where tree planting and forest expansion are bad for biodiversity and
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ecosystem services. BioScience 65:1011-1018
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White R, Murray S, Rohweder M (2000) Pilot analysis of global ecosystems: grassland
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ecosystems. Washington, DC: World Resources Institute
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Restoration Ecology
Table 1. Comparison between the number of seed rain studies with the total area for
each grassland type according to Dixon et al. 2014 (=98 studies).
Grassland type
Boreal Grassland
Alpine Grassland
Mediterranean
Grassland
Warm Semi-Desert
Grassland
Cool Semi-Desert
Grassland
Temperate Grassland
Tropical Grassland
Total area
(Km²)
246.322
591.357
1.594.750
N° of seed rain
studies
3
10
8
Studies/100.000
km²
1.21
1.69
0.50
3.030.720
13
0.43
5.661.110
1
0.02
8.104.830
16.156.620
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0.68
0.04
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Restoration Ecology
Table 2. Future challenges and proposed solutions to improve our knowledge and increase the use of seed rain studies to support grassland
restoration.
Challenges
Solutions
Seed rain spatial patterns,
heterogeneity and limitation
Seed trap efficiency and lack
of standardization in the use
of seed traps
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Increase periods of observation and reduce sampling intervals
Predict latitudinal and climate variations effects on seed rain
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Incorporate landscape metrics and estimate the relative importance of different dispersal modes
Discuss how the number of traps should vary according to study goals
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Consider the main direction of seed import
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Consider vegetation growing height and dispersal syndromes
Provide justification for the choice of seed traps (position on the ground, format, area, etc.)
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Test trap efficiency and protect seeds against granivory
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Critically evaluate and report negative aspects of each trap
Access
seed
collection
identity and quality
Increment reference seed collections
X-ray analyses
Reduce the seed supply of undesirable species
Introduce target species via seed addition
Success
of
restoration
practices and monitoring
Evaluate the effect of endogenous disturbances
Understand the boundaries and interactions between direct and indirect methods
Create opportunities to increase seed input from native seed dispersers
Increase
practicality
and
Restoration Ecology
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applicability of methods to
Page 28 of 79
Development of dispersal mechanistic models for undersampled vegetation
study seed rain
Avoid indirect estimates and forecasts by indirect methods
Assess the influence of wind, flooding and relief on seed dispersal
Unbalance
between
the
numbers of studies across
grasslands types
Biotic dispersers
Hurdles for plant community
reassembly after degradation
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Address the role of overlooked vectors in the dispersal of non-woody species
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Understand how issues related to seed sourcing, seed quality, availability and dormancy-breaking mechanisms
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Unstandardized or unclear
Methods and results must be thoroughly, clearly and transparently stated
methodology and lack of data
Standardization for the number of seeds collected over time and space
reporting
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Standardization for the trap format measurements and area within the sample area per plot
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Running title: Seed rain in grasslands
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How have we studied seed rain in grasslands and what
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do we need to improve for better restoration?
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André J. Arruda1,2,3, Elise Buisson3, Peter Poschlod4 and Fernando A. O.
Silveira1
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1. Departamento de Botânica, Universidade Federal de Minas Gerais. 30161-970 Belo
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Horizonte, Brazil.
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2. Author for correspondence to A. J. Arruda: [email protected]
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3. Université d’Avignon et des Pays de Vaucluse, IMBE – Institut Méditerranéen de
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Biodiversité et d’Ecologie, CNRS, IRD, Aix Marseille Université, IUT d’Avignon,
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AGROPARC BP61207, 84911 Avignon, France
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4. Institute of Plant Sciences, Faculty of Biology and Preclinical Medicine, University
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of Regensburg, D-93040 Regensburg, Germany
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Author contributions
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AJA, EB, FAOS, PP conceived and designed the research; AJA performed the review
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and analyzed the data; AJA, FAOS wrote the manuscript; EB, PP edited the manuscript.
Restoration Ecology
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Abstract
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Seed rain, the number of seeds reaching an area, is a process that plays a key role in
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recruitment and regeneration in plant communities. A better understanding of seed rain
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dynamics is therefore a critical step for restoration practices. A wide variety of methods
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to study seed rain in grasslands are available, but there is little agreement to which is the
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most appropriate one. Here we: 1) assessed where, how and why research on seed rain
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has been carried out; 2) examined how methodological design and results have been
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reported and 3) provide guidelines for future research on seed rain in grasslands. We
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built a database of 185 papers from a systematic literature survey between 1980 and
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November 2016 and we found a remarkable unbalance of the numbers of studies
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between grassland types, which becomes even more dissimilar across global climatic
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ranges when the area covered by each grassland type is addressed. We also found a
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great disparity of methods and data being reported across studies. Despite recent
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progress in understanding seed rain dynamics, large knowledge gaps in important
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issues, such as the role of native dispersers, method efficiency and application of
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mechanistic models still persist. Finally, we propose guidelines for the implementation
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of minimum standardized methodology and data reporting, which will foster higher
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quality, transparency, reproducibility and value of seed rain studies and grassland
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restoration.
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Key-words: meadow, prairie, rangeland, seed limitation, seed trap, steppe
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Conceptual Implications
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• An unbalanced distribution of seed rain studies among grassland types calls for
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additional research efforts on non-temperate grasslands to better support restoration
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• We identified significant knowledge gaps in grassland seed rain research,
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which should now be tackled: the role of (1) native animals as seed dispersers, (2) pre-
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dispersal and post-dispersal seed predation, (3) non-native species, (4) method
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efficiency, (5) application of mechanistic models, (6) active restoration standards
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prevents a critical appraisal of the role of seed rain in restoration of grasslands
• We recommend the implementation of guidelines for methodology and data
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• The lack of standardization of methodology, terminology and data reporting
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reporting, which will depend on future collaborative efforts
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Introduction
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Seed rain is the number of seeds reaching an area, and it usually is quantified
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and qualified by placing traps in the plant community to catch seeds that then are
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identified and counted (Baskin & Baskin 2014). Seed rain is a critical step in plant life
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cycle, as it represents a demographic bridge between the adult and seedling stage
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(Harper 1977). Seed rain reflects species dispersal potential, and therefore the
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persistence or potential for change of the standing vegetation (Page et al. 2002).
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Additionally, it allows the arrival of seeds into suitable uncolonized microsites (Baker
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1974), with major implications for biological invasions and restoration ecology by
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revealing relevant information about how target species can reach a restored site, and
Restoration Ecology
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whether seed rain is effective and efficient to restore a given site (Turnbull et al. 2000).
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Many plant communities are seed limited, meaning that microsites where seeds can
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arrive and germinate, remain vacant, which can be related to limited seed production
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and/or limited dispersal of available seeds among sites (Clark et al. 1998). Hence, seed
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rain estimates can provide a hint of successional direction by predicting the probabilities
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of propagule arrival (D'Angela et al. 1988).
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Over the last decades, seed rain has been analyzed both i) indirectly, by studies
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of plant reproductive potential (Boughton et al. 2016) and seed bank dynamics (Bertiller
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& Aloia 1997), and ii) directly, by collecting either seeds visible on the ground, by
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observing the movements of granivore animals (Izhaki et al. 1991) or from diaspore
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traps (Kollmann & Goetze 1998). The great diversity of methodologies reported for
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seed rain studies may have a close relation with the wide range of biological processes
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that may be involved, which makes the delimitations of this biological process often
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unclear (Fig. S1).
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In essence, an ideal method for studying seed rain is the one that can assess what
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seed, how many seeds and when that seed arrives in the seed bank (Schott 1995).
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Despite this, few seed rain studies use standardized methods that would allow cross-
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vegetation comparisons. As an example, numerous types of seed traps have been used in
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ecological studies with different characteristics, such as shape, size, height above soil
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surface and trap inclination, all of which can affect their effectiveness (Bakker et al.
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1996, Chabrerie & Alard 2005). A wide variety of seed rain measuring methods is
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available in the literature. However, there is little agreement to which is the most
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appropriate method taking into account a wide range of possible variables. This is
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especially true for grassy biomes, for which knowledge on natural regeneration
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following disturbance lags behind that of forest ecosystems (Meli et al. 2017).
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Grassy ecosystems cover around 52 million km², ca. 40% of the global land
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surface (White et al. 2000; Gibson 2009). Over the last decades huge areas of native,
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old-growth grasslands have been lost to agricultural expansion, desertification, mining,
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urbanization and other changes or have been degraded by changes in fire regimes,
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exotic species introduction, fertilization, drainage, liming, overgrazing, etc. (White et al.
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2000; Veldman et al 2015). In the face of increasing land-use pressures and increasing
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biodiversity loss in grasslands, biogeographical studies of spatial and temporal patterns
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of seed rain are essential to restoration and management practices (Bakker et al. 1996).
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While seed rain patterns in grasslands are very difficult to assess and to predict, a better
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understanding about their influence on the resilience and succession in these
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environments is urgently needed, aiming to achieve biodiversity conservation goals,
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secure ecosystem services (Parr et al. 2014) and provide basis for better restoration
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practices.
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Given that seed rain plays a pivotal role in restoration ecology, we explore the
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interplay between seed rain research and restoration in grasslands 20 years after Bakker
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et al. (1996) stressed the role of seed rain and seed banks in restoration ecology. Our
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goals were: 1) to assess where, how and why research on seed rain was carried out; 2) to
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examine methodological design and results reported; and 3) to provide guidelines for
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future research in seed rain, aiming to standardize and foster higher quality,
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transparency, reproducibility and value to seed rain studies in grasslands.
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Material and Methods
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Literature survey and grassland classification
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We surveyed papers in the Web of Science which have been published from
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1950 to 30th November 2016, by searching the following terms in the title, abstract, and
Restoration Ecology
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key words of papers: “seed rain” plus “grassy biome”, “grassland”, “meadow”,
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“prairie”, “rangeland”, “savanna”, or “steppe”. We removed papers dealing only with
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seed production or seed bank, and included only studies that addressed the releasing
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process of diaspores from the parent plant and their movements until reaching the soil.
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After removing redundant papers, our survey comprised 185 papers published between
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1980 and 2016. From those, we removed the papers not related to grasslands (those
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addressing seed rain in forest ecosystems), and papers that did not study seed rain in
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detail, represented by studies that did not present any qualitative or quantitative data on
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seed rain over space or time. We were left with 98 papers that matched our criteria for
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this review.
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For each study, we classified the grassland type according to Dixon et al. (2014).
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We considered seven grassland types: alpine grassland; boreal grassland; cool semi-
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desert grassland; temperate grassland; Mediterranean grassland; tropical grassland and
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warm semi-desert grassland. Using ArcGIS software, we built a map plotting the
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geographic distribution of seed rain studies together with the global grassland
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distribution through the geographical coordinates available in Dixon et al. (2014).
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Relevance of seed rain studies to restoration ecology
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We considered studies with direct relevance to restoration ecology, such as those
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that addressed any of the following processes: recolonization, succession and
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predictions after degradation, endangered species conservation, spread of non-native
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species and natural plant communities or species dynamics. We classified degradation
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types reported in each study as endogenous or exogenous disturbances (sensu McIntyre
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and Hobbs 1999). The endogenous category refers to disturbances to which ecosystems
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were repeatedly exposed through evolutionary time and which, with an appropriate
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regime, allows ecosystems to maintain biodiversity. On the other hand, the exogenous
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category refers to novel, mainly anthropogenic disturbances, which may be
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incompatible with the maintenance of grassland biodiversity. We classified the
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ecological restoration processes, whenever mentioned, as passive or active restoration.
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Passive restoration stands for cases when only natural regeneration processes were
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evaluated, whereas active restoration refers to the implementation of restoration
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techniques, such as hay spreading or seed sowing (Rey Benayas et al. 2008).
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studies according to the nature and scope of the experimental design into two
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categories: i) direct measurements and ii) mathematical or mechanistic models and
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simulations. The direct measurements included the use of seed traps (Bakker et al.
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1996) and focal or seed tracking observations (e.g. Ferguson & Drake 1999; Piazzon et
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al. 2012). Mathematical or mechanistic models and simulations used numerical methods
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for seed rain dynamics predictions and simulations (e.g. Doisy et al. 2014).
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Restoration Ecology
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In order to obtain additional information about the dispersal dynamics, we
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searched for studies that used methods to evaluate the effect of abiotic (such as water
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and wind) and biotic vectors of seed dispersal. Additionally, we recorded seed dispersal
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distance whenever provided in the original study.
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Owing to the fact that seed trap characteristics may strongly influence results
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(Bakker et al. 1996; Chabrerie & Alard 2005), we evaluated the following aspects for
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studies that employed seed traps as a method to estimate seed rain: trap type, total
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number of traps, trap efficiency in collecting seeds, trap protection against granivores,
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trap position on the ground, height categories for traps lodged above ground, trap
Restoration Ecology
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position in relation to the main wind direction, and sticky traps slope angle. We
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classified the traps in the following categories: funnel trap, sticky trap, tray or gap trap
177
and other traps.
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Methodologies and data reporting
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To evaluate standardization in methodologies and data reporting, we analyzed
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seed trap size and total surface measurements for the two most common trap types,
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funnels and sticky traps. Considering that traps with equivalent areas can have very
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different formats, which together with the total trap area, can affect the study outcome,
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we assessed how these measurements were reported in different ways, sorting them into
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three possible categories: i) trap area only; ii) format measures (width and length or
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diameter), iii) not informed. Secondly, we evaluated how many studies calculated the
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total area sampled by the traps. Thirdly, we evaluated how the data collected or
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estimated were reported. We created four categories of data reporting: seed density
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only, total number and density, total number only, not informed. Finally, we examined
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what seed traits (Jiménez-Alfaro et al. 2016) were reported in each study.
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Results
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We found an increase in the number of seed rain studies in grasslands over the
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two last decades, with the maximum number of studies/year of 10 in 2005. We found
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relative increases in the number of studies coinciding with the publication of review
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papers (Fig. S2).
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We found seed rain studies in grasslands across all vegetated continents, in
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tropical (N=7), temperate (N=82) and boreal (N=3) ranges (Fig. 1). However, the
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geographic distribution of studies was strikingly uneven, with most studies concentrated
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in Europe (N=46) and in North America (N=21). More than half (57%) of the seed rain
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studies were conducted in temperate grasslands, while the rest was spread among warm
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semi-desert grasslands (14%), alpine grasslands (10%), Mediterranean grasslands (8%),
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tropical grasslands (6%), boreal grasslands (3%) and cool semi-desert grasslands (1%).
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Only three studies were done in flooded grasslands, all belonging to the temperate
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grassland type.
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Figure 1: Geographic distribution of seed rain studies (black dots) in grasslands. Red
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dashed lines depict tropical areas and blue dashed lines depict boreal areas. Native
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gGrasslands distribution in yellow follows Dixon et al. (2014).
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Eighty-four papers (85%) of the selected studies were directly or indirectly
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related to ecological restoration. Among the studies related to ecological restoration, 80
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papers (95%) mentioned some type of disturbance, from which 73 (91%) reported
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exogenous disturbances, such as cultivation and mining and only seven (8%) of them
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addressed endogenous disturbance events. Regarding the latter, five studies addressed
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fire regimes, one mentioned drought regimes and fire and one simulated small soil
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disturbances naturally created by a native small mammal from a temperate grassland
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(Supplementary material I). Additionally, from the eighty-four studies applied to
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ecological restoration, 64% addressed passive restoration aspects only and 36% active
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restoration processes. From the 30 studies that addressed active restoration, only 11%
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tested seed sowing techniques.
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From the ninety-eight selected studies, 97% used direct measurements and 3%
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mathematical or mechanistic models and simulations. Additionally, across all selected
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studies, 21 mentioned or surveyed biotic dispersal. Within these 21 studies, birds were
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the main dispersers studied (42% of the studies), followed by livestock (29%), such as
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sheep, cattle and donkeys, ants (29%), other mammals not including bats (14%), bats
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(10%) and lizards (5%). Only 9 studies mentioned the influence of abiotic factors, such
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as wind (8 studies) and water (1 study). From the eight studies that provide some
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information about the main wind direction, five only mentioned and three measured this
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variable. Additionally, we checked how many studies estimated seed dispersal distance
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and found that only 24 studies took seed dispersal distance into account, from which
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less than a quarter presented seed dispersal distance estimates or measurements.
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Fifty-nine percent of seed rain studies were conducted at the community-level
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and 37% only at species-level. From the 37 studies that evaluated the seed rain at
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species-level, 51% included only one species. Additionally, from all studies, 20
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mentioned or evaluated the impact of non-native species, of which 70% reported non-
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woody species and 30% woody species.
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Only 46 studies provided information on complementary physical and
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physiological seed traits, such as size, weight, dormancy and viability. From those, 54%
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provided information on a single seed trait and less than 5% on more than three traits.
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Among the seed traits reported in these 46 studies, seed morphological adaptations for
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dispersal (other than size and weight) were the most common (39% of the studies),
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followed by seed size (33%), seed weight (30%), seed viability (24%), seed dormancy
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(15%), releasing height (11%), seed longevity (4%) and moisture content (2%).
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Sampling length for the 79 studies that provided this kind of information ranged
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from less than 1 month up to 60 months. Additionally, 76 studies provided information
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on sampling frequency, which ranged from weekly to 24 months intervals. Regarding
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the methods for seed identification, 89 studies dealt with this aspect. From those, 50%
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used visual identification through reference collections, 33% did not mentioned any
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seed identification method and 15% used seedlings emerging from seeds to identify
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species.
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From the 76 studies (77%) that used seed traps, 88% used only one type of seed
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traps, 8% used two types, 3% used three types and only one study used five types. The
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most common seed trap type was the funnel trap (34%), followed by the sticky trap
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(18%) and tray or gap trap (17%). Additionally, 18% of the studies used other types of
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traps. Surprisingly, we found information on the total number of traps only for 56 out of
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the 76 studies. Among these, the number of traps per study ranged from 14 to 576, with
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nearly half of the studies using less than 90 traps.
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Among the 76 studies that used seed traps, 62 (82%) did not provide any
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information about the seed trap efficiency in collecting seeds. Only eight studies (10%)
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mentioned trap efficiency and only six studies (8%) tested seed traps for efficiency.
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Only 18 studies (24%) provided information on trap protection against granivores.
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Information on seed trap position related to the ground was found for 56 studies only.
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Among these 56 studies, 52% placed traps aboveground, 50% at ground level and only
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4% underground (some studies included more than one type). For aboveground traps,
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we found a minimum height value of 0.5 cm and maximum of 90 cm. We also found
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that 32% of aboveground traps were positioned at a height of 50 cm or more, followed
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by those at 15 to less than 30 cm (28%), at one to less than 5 cm (25%) and at less than
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1 cm (21%).
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Additionally, we analyzed separately some specific aspects of trap types. We
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evaluated the sloping angle for sticky traps in the 17 studies (22%) that used this kind of
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trap. From these, 76% did not report this variable. Among those which reported this
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information, the angle of 0° (parallel to soil surface) was the most common (3 studies),
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followed by the angles of 45° and 90°, each one present in one study.
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We evaluated seed trap measurements for the most common traps, funnel and
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sticky traps. For the funnel and sticky traps, respectively 30% and 6% of the studies
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respectively provided the seed trap surface area only. Subsequently, we evaluated trap
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area separately for each type of traps. For the funnel and sticky traps, most studies used
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particular trap area sizes. Additionally, only 14% of the studies calculated the total area
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covered by the funnel or sticky traps.
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We also evaluated how the total number of seeds collected or estimated was
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reported for the 82 studies that reported these data. Half of the studies presented seed
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density only (50%), followed by total seed number and seed density (28%) and total
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seed number only (22%).
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Discussion
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Our data clearly shows a lack of standardization in approaches, methods and
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data being reported in seed rain studies across global grasslands. We found unbalanced
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distribution of seed rain studies among hemispheres, different grassland types and, more
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importantly, that even basic aspects of a study (experimental design and number of
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species/seeds sampled), were not properly reported in many cases. Seed rain studies
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have different goals, and one should expect a wide diversity of methods in the literature.
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However, the lack of justification for the employment of different methods, and
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incomplete data reporting strongly hamper our ability to compare results among studies,
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hence preventing a better appreciation of the role played by seed rain in restoration
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ecology.
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General and biogeographical information
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The large proportion of seed rain studies related to ecological restoration
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underlines the great relevance of seed rain studies in restoration ecology (Bakker et al.
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1996; Freund et al. 2015). The small number of studies evaluating the effect of
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endogenous disturbances points out that this issue still needs to be better explored:
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endogenous disturbances usually have to be re-established as a means of or after
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restoration. For example, fire-stimulated flowering (Keeley et al. 2000) and seed release
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(Holmes & Richardson 1999) may affect natural regeneration patterns. However,
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natural recovery of some ecosystems may be quite slow if important drivers of recovery,
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such as the availability of propagules or dispersers are limited (Hubbell et al. 1999; Le
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Stradic et al. 2014).
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The geographical distribution of studies can substantially influence conclusions
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reached by ecologists, being therefore critical to know which biomes, regions, and
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landscapes remain understudied and undervalued (Martin et al. 2012). The remarkable
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unbalance between the numbers of studies worldwide indicates knowledge gaps,
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especially in old-growth tropical grasslands in the southern hemisphere (Veldman et al.
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2015). Considering the total area per grassland type (Dixon et al. 2014), alpine
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grasslands showed the second lowest area among the formations, but had more seed rain
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studies than tropical grasslands, which have an approximately 27 times higher total area
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(Table 1).
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High diversity of estimates of seed rain
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The considerable dominance of direct measurements to evaluate seed rain
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patterns reflects the sampling effort carried out in field experiments with use of seed
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traps or focal observations over the last few decades. Despite the potential usefulness of
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mechanistic models in providing reliable estimates of plant dispersal distances, they are
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still little explored by ecologists (Bullock et al. 2017). The development of dispersal
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mechanistic models is crucial to improve our understanding about relevant topics on
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restoration ecology, such as population dynamics in fragmented landscapes (Gilbert et
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al. 2014) and the arrival of non-native species (Hastings et al. 2005). Meanwhile, there
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is still a long way to go from mechanistic models to processes applicable to the seed
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dispersal, in order to reduce the effort required to measure dispersal directly in the field
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(Bullock et al. 2006).
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Animals play important roles in dispersing seeds of native and non-native
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species. Most studies surveyed explored the role of frugivorous passerines or livestock
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as dispersers of grassland species. However, we found a large knowledge gap on the
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ecological role played by other native animals, such as lizards (Piazzon et al. 2012),
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beetles or ants (Nicolai & Boeken 2012; Lima et al. 2013) and non-volant mammals
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(Genrich et al. 2017) in dispersing seeds of native grassland species. Additionally,
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future research should focus on the roles of seed dispersers in dispersing seeds of
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invasive species, which will provide relevant information for restoration actions and
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post-restoration management (Buisson et al. 2017).
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Spatial patterns of seed deposition and issues related to seed sourcing, seed
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quality, availability and dormancy-breaking are of great interest for evaluating the
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effectiveness of dispersal and relevant hurdles for plant community reassembly after
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degradation (Dayrell et al. 2016). However, assessing the contribution of local versus
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distant diaspore sources can be a great challenge (Bullock et al. 2017), which may
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explain how estimating seed dispersal distance has been mostly overlooked by seed rain
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studies in grasslands.
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Sampling length, sampling frequency and seed identification techniques can
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have a great influence on the results. Thus, whenever possible, studies should prioritize
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longer collection periods and short collection frequencies. Short-term studies may imply
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non-overlapping patterns of dispersal period of some species. Furthermore, results are
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likely to be affected by the frequency of checking, mainly when traps are insufficiently
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or not at all protected against seed predation (Gorchov et al. 1993).
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Sampling effort and lack of standardization in the use of seed traps
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Measurements of seed rain in the field can be carried out using seed traps with
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different shapes, sizes, heights and inclinations (Chabrerie & Alard 2005). However,
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trap effectiveness at capturing seeds can vary not only among trap types and
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characteristics, but also over different vegetation or plant species and environmental
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conditions (Kollmann & Goetze 1998). Funnel traps have often been described in the
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literature as the best trapping method by catching the highest number of seeds
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(Kollmann & Goetze 1998). However, funnel trap efficiency may also retain diaspores
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belonging to seed banks through water run-off, and therefore ignoring secondary
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dispersal may result in overestimates of seed rain. Sticky traps, which are especially
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suitable for studying seed rain of anemochorous species, can be easily adapted to the
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local aerodynamic environment by the control of height, orientation and inclination
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(Chabrerie & Alard 2005). However, sticky traps can catch large amount of insects,
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drastically reducing their efficiency and making it difficult to identify the sampled seeds
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(Poschlod 1990). Alternatively, the use of soil gaps or pots with sterile soil have been
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often attributed as a more realistic method by the integration of seed arrival with other
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field natural conditions, such as secondary removal and predation (Kollmann and
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Goetze 1998), despite the recommendation for the avoidance of these variables for other
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trap types (Debussche & Isenmann 1994). Considering that trapping success can be very
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variable not only between trap types, but across environments and plant communities,
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comparisons between studies should always be made with caution (Kollmann & Goetze
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1998).
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Despite the fact that effects of seed trap area and height on sampling
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effectiveness have been debated since the seminal publications of Fischer (1987) and
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Jackel & Poschlod (1994), we still need to better explore how seed traits, such as size,
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weight and releasing height (Fischer et al. 1996; Jackel & Poschlod 1994; Tackenberg
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et al. 2003) can influence seed trap efficiency. Recommendations about the number of
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traps for seed rain studies have already been reported (Fischer 1987, Kollmann &
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Goetze 1998), but the number of traps needed greatly vary depending on the goals and
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background of the studies.
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Seed trap effectiveness tests are fundamental in seed rain research and should be
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conducted prior to field experiments (Debussche & Isenmann 1994), but we found they
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are rarely carried out. Ignoring such issues may have serious consequences in the
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reliability of seed rain estimates. Standardization of sampling efforts (Jackel &
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Poschlod 1994) and in tests of trap efficiency in collecting, storing and protecting seeds
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against granivores will be fundamental for a better understanding of the operation of
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different seed traps along distinct plant communities and geoclimatic conditions.
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Methodologies and data reporting
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Basic information about methods and results must be thoroughly, clearly and
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transparently reported to enable comparisons and facilitate inclusion in meta-analyses
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(Gerstner et al. 2017). Seed trap format measures, area and the total number of seeds
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collected or estimated reported by the studies and categories evaluated here are
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remarkably unstandardized, sometimes unclear or sometimes data were even not
398
provided. We also found a great variety of sizes for both sticky and funnel traps, which
399
were rarely accompanied by a clear methodological justification. Finally, only few
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studies provided information on the proportional seed trap area (seed trap area over total
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plot area). Altogether, the lack of standardized methodologies in seed rain studies
402
undermine the reliability of studies and prevent comparisons among sites, thereby
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preventing the evolution of the scientific knowledge on a key ecological process
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underpinning ecological restoration.
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Restoration Ecology
Implications and guidelines for future seed rain studies
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When reporting data, researchers should have in mind that their data can be
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readily used by the scientific community to build-up knowledge from single studies
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(Gerstner et al. 2017). Therefore, it is imperative that not only experimental designs are
410
clear and justified, but that data reporting adheres to minimum standards. Here, we
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propose guidelines for future research on seed rain studies in grasslands with the hope
412
that standardized methodology, or at least better justified methods, will provide the
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scientific community with better conditions for the critical assessment of publications,
414
fostering scientific knowledge.
415
First, we propose the standardization for the number of seeds collected over time
416
and space, according to the minimum parameters: total number of seeds per species
417
sampled at each sampling interval; total number of species sampled at each interval;
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total number of seeds/species per trap over the total sampling time and total number of
419
seeds/m² per day. Second, given the disparity of methods and data reporting across
420
studies that used seed traps, we propose that the following minimum standard is
421
reported: trap format measurements (width and length or diameter); total trap area per
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unit (cm²); number of traps per plot; total area covered by traps per plot (cm²); and
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percentage (%) of plot area covered by the traps. We recognize that our modest proposal
424
will not be enough to standardize research at global scale, but this is the first step
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towards common and shared vocabulary, methods and data reporting.
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Prior to restoration, seed rain can be evaluated in order to assess the potential for
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regeneration and passive restoration. Restoration assessments should include seed rain
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data in post-restoration monitoring programs (Jacquemyn et al. 2011) and increasing
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knowledge on pre- and post-dispersal seed predation (Pardini et al. 2017) are to play an
430
increasing role in determining restoration success and should be integrated into seed
431
rain studies whenever possible. Despite considerable progress in recent decades, we still
432
face great challenges to improve our knowledge and increase the use of seed rain studies
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to better support grassland restoration (Table 2). More research on restoration of
434
tropical and sub-tropical grasslands is required due to the fact that techniques used for
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temperate grassland restoration are not successful in restoring tropical ones (Le Stradic
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et al. 2014). Additionally, understanding to what extent anthropogenic modifications are
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relevant to seed limitation will be fundamental to predict the capacity of grasslands to
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respond to these changes.
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Future successful restoration may also depend on seed addition, on which we
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still need to advance in the practical and theoretical framework (Bakker et al. 2003). We
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must also recognize the importance of considering several characteristics of seed rain,
442
besides species composition and seed abundance. Spatial patterns of dispersal and seed
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traits, such as dormancy, longevity, releasing time and duration are fundamental for a
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better understanding on the formation of seed banks and the dynamics of community re-
445
assembly following disturbances (Jiménez-Alfaro et al. 2016).
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Lastly, we need to critically stress the fact that cross-vegetation comparisons of
447
seed rain data are prevented due to lack of standardized research protocols. We believe
448
that the lack of standardization in methodology and data reporting creates a unique
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opportunity for the scientific community to put efforts on a global protocol of seed rain
450
methods. An increased implementation of guidelines for methodology and data
451
reporting will foster higher quality, transparency, reproducibility and value to seed rain
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studies in grasslands. Future collaborative, international efforts are paramount for a
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global assessment of the role played by seed rain in restoration ecology.
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Acknowledgments
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We thank R.S. Oliveira, Q. S. Garcia, N.P.U. Barbosa and L.F. Fuzessy for criticism
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during early stages of the manuscript. N.P.U. Barbosa and R.L.C. Dayrell also assisted
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with the construction of the map and figures. We thank the reviewers for their
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comments which significantly increased manuscript quality. A.J.A. receives a PhD
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scholarship from CAPES and F.A.O.S. receives grants from CNPq and FAPEMIG.
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native seeds for restoration of megadiverse resource-poor environments: a reply to
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Debussche M, Isenmann M (1994) Bird-dispersed seed rain and seedling establishment
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in patchy Mediterranean vegetation. Oikos 69:414-426
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Dixon AP, Faber-Langendoen D, Josse C, Morrison J, Loucks CJ (2014) Distribution
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plants and animals on sheep in calcareous grasslands. Journal of Applied Ecology
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dune complex as a model in practice: impact of substrate, minimized inoculation and
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interaction outcomes in a plant-frugivore multilayer network. Oikos 126:361-368
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dynamics, community structure, and ecosystem function: perspectives from South
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Izhaki I, Walton PB, Safriel UN (1991) Seed shadows generated by frugivorous birds in
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Jackel AK, Poschlod P (1994) Diaspore production and the influence of the size of
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diaspore traps on the quantitative result of seasonal diaspore rain in two calcareous
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grassland sites. Berichte des Institutes für Landschafts- und Pflanzenökologie der
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Universität Hohenheim 3:123-132
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Jacquemyn H, Van Mechelen C, Brys R, Honnay O (2011) Management effects on the
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vegetation and soil seed bank of calcareous grasslands: An 11-year review. Biological
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Kollmann J, Goetze D (1998) Notes on seed traps in terrestrial plant communities. Flora
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(2017) A global review of past land use, climate, and active vs. passive restoration
564
effects on forest recovery. PLoS ONE 12:e0171368
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unter
besonderer
Berücksichtigung
standortskundlicher
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Schott GW (1995) A seed trap for monitoring the seed rain in terrestrial communities.
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Canadian Journal of Botany 73:794-796
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588
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Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? a review
590
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ecosystems. Washington, DC: World Resources Institute
iew
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Restoration Ecology
Restoration Ecology
Table 1. Comparison between the number of seed rain studies with the total area for
each grassland type according to Dixon et al. 2014 (=98 studies).
Grassland type
Boreal Grassland
Alpine Grassland
Mediterranean
Grassland
Warm Semi-Desert
Grassland
Cool Semi-Desert
Grassland
Temperate Grassland
Tropical Grassland
Total area
(Km²)
246.322
591.357
1.594.750
N° of seed rain
studies
3
10
8
Studies/100.000
km²
1.21
1.69
0.50
3.030.720
13
0.43
5.661.110
1
0.02
8.104.830
16.156.620
55
6
0.68
0.04
iew
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Page 54 of 79
Page 55 of 79
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Restoration Ecology
Table 2. Future challenges and proposed solutions to improve our knowledge and increase the use of seed rain studies to support grassland
restoration.
Challenges
Solutions
Seed rain spatial patterns,
heterogeneity and limitation
Seed trap efficiency and lack
of standardization in the use
of seed traps
Fo
Increase periods of observation and reduce sampling intervals
Predict latitudinal and climate variations effects on seed rain
rP
Incorporate landscape metrics and estimate the relative importance of different dispersal modes
Discuss how the number of traps should vary according to study goals
ee
Consider the main direction of seed import
rR
Consider vegetation growing height and dispersal syndromes
Provide justification for the choice of seed traps (position on the ground, format, area, etc.)
ev
Test trap efficiency and protect seeds against granivory
iew
Critically evaluate and report negative aspects of each trap
Access
seed
collection
identity and quality
Increment reference seed collections
X-ray analyses
Reduce the seed supply of undesirable species
Introduce target species via seed addition
Success
of
restoration
practices and monitoring
Evaluate the effect of endogenous disturbances
Understand the boundaries and interactions between direct and indirect methods
Create opportunities to increase seed input from native seed dispersers
Increase
practicality
and
Restoration Ecology
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5
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39
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42
43
44
45
46
47
applicability of methods to
Page 56 of 79
Development of dispersal mechanistic models for undersampled vegetation
study seed rain
Avoid indirect estimates and forecasts by indirect methods
Assess the influence of wind, flooding and relief on seed dispersal
Unbalance
between
the
numbers of studies across
grasslands types
Biotic dispersers
Hurdles for plant community
reassembly after degradation
Fo
Direct efforts to overlooked regions and environments
rP
Address the role of overlooked vectors in the dispersal of non-woody species
ee
Understand how issues related to seed sourcing, seed quality, availability and dormancy-breaking mechanisms
rR
Unstandardized or unclear
Methods and results must be thoroughly, clearly and transparently stated
methodology and lack of data
Standardization for the number of seeds collected over time and space
reporting
ev
iew
Standardization for the trap format measurements and area within the sample area per plot
Page 57 of 79
Fo
Figure S1: Theoretical framework showing the boundaries between seed rain dynamics
rP
(direct measurements) and other indirectly related processes (indirect measurements),
represented by aspects of reproductive potential and seed bank dynamics.
iew
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Restoration Ecology
Figure S2: Cumulative number of seed rain studies in grasslands from 1980 to 2016
within climatic global ranges. The arrows indicate when the revisions on the topic of
seed rain of Bakker et al. and Kollmann & Goetze were published.
Restoration Ecology
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Page 58 of 79
Page 59 of 79
Keywords searched
Publication Year
prairie
grassland
grassland
grassland
grassland
grassland
1980
1987
1989
1990
1993
1993
Author(s)
Rabinowitz D. & Rapp J.K.
Huenneke L.F & Graham C.
Peart D.R.
Spence J.R.
Milberg P.
Milberg P.
Poschlod P. & Jackel A.K.
1994
1995
Grulke N.E.
1995
Kollmann J.
Schott G.W.
1995
1996
Bakker J.P., Poschlod P., Strykstra R.J., Bekker R.M. and Thompson K.
1996
Hutchings M.J. & Booth K.D.
Kotanen P.M.
1996
Scholl E.L. & Kinucan R.J.
1996
1996
Smith R.S., Pullan S. and Shiel R.S.
1997
Price M.V. & Joyner J.W.
1997
Schott G.W. & Hamburg S.P.
Jensen K.
1998
1998
Kollmann J. & Goetze D.
1998
Marone L., Rossi B.E. and De Casenave J.L.
1998
Urbanska K.M., Erdt S. and Fattorini M.
1998
Willems J.H. & Bik L.P.M.
iew
ev
rR
ee
rP
grassland
grassland
grassland
grassland
grassland
grassland
grassland
grassland
grassland
steppe
grassland
grassland
grassland
steppe
grassland
grassland
Fo
1
2
3
4
5
6
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Restoration Ecology
Edwards G.R. & Crawley M.J.
grassland
grassland
1999
1999
grassland
savanna
grassland
meadow
grassland
prairie
grassland
grassland
grassland
1999
2000 Ekeleme F., Akobundu I.O., Isichei, A.O. and Chikoye, D.
2000
Urbanska K. M. & Fattorini M.
2001
Garcia D.
Kirmer A. & Mahn E.G.
2001
2001
Owen N.W., Kent M. and Dale M.P.
2001
Rogers W.E. & Hartnett D.C.
2002
Calvino-Cancela M.
2002
Kalamees R. & Zobel M.
Page M.J., Newlands L. and Eales J.
2002
2002
Sanchez A.M. & Peco B.
Sheppard A.W., Hodge P., Paynter Q. and Rees, M.
2002
Stroh M., Storm C., Zehm A. and Schwabe A.
2002
grassland
grassland
grassland
grassland
Ferguson R.N. & Drake D.R.
Lyaruu H.V.M.
Restoration Ecology
grassland
grassland
meadow
grassland
grassland
Arrieta S. & Suarez F.
2005
2005
Chabrerie O. & Alard D.
2005
Dostal P.
2005
Dovciak M., Frelich L.E. and Reich P.B.
2005
Flores, S.; Dezzeo, N.
2005
Jacquemyn H., Brys R. and Neubert M.G.
2005
Leck M.A. & Schutz W.
2005
Luzuriaga A.L., Escudero A., Olano J.M. and Loidi J.
2005
Pakeman R.J. & Small J.L.
2005
Welling P., Tolvanen A. and Laine K.
2006Buisson E., Dutoit T., Torre F., Romermann C. and Poschlod P.
Jakobsson A., Eriksson O. and Bruun H.H.
2006
2007
Bonvissuto G.L. & Busso C.A.
DiVittorio C.T., Corbin J.D. and D'Antonio C.M.
2007
2008
Dovciak, M., Hrivnak R., Ujhazy K. and Goemoery D.
2008
Smith D.C., Meyer S.E. and Anderson V.J.
2009
Christianini A.V. and Oliveira P.S.
2009
Lanta V. & Leps J.
2010
Wu G., Hu T. and Liu Z.
Yelenik S.G. and Levine J.M.
2010
2011
Auffret A.G. & Cousins S.A.O.
Burmeier
S.,
Eckstein R.L., Otte A. and Donath T.W.
2011
2011
Erschbamer B. & Mayer R.
2011
Santos G., Marchesini M, Oliveira J.M., Mueller S.C. and Pillar V.D.
2011
Kettenring K.M. & Galatowitsch S.M.
2011 Salazar A., Goldstein G., Franco A.C. and Miralles-Wilhelm F.
2012 D'hondt B., D'hondt S., Bonte D., Brys R. and Hoffmann M.
2012
Faust C., Storm C. and Schwabe A.
2012
Kirmer A., Baasch A. and Tischew S.
2012
Muenzbergova Z.
Nicolai N. and Boeken B.R.
2012
Piazzon M.,
2012Larrinaga A.R., Rodriguez-Perez J., Latorre L., Navarro, L. and Santamaria L
2012Salazar A., Goldstein G., Franco A.C. and Miralles-Wilhelm F.
2012
Scott A.J. & Morgan J.W.
2013
Diacon-Bolli
J.C., EdwardsP.J., Bugmann H., Scheidegger C. and Wagner H.H.
Fibich P., Vitova A., Macek P. and Leps J.
2013
2013 Galindez G., Ortega-Baes P., Scopel A.L. and Hutchings, M.J.
iew
ev
rR
ee
grassland
grassland
grassland
prairie
savanna
grassland
grassland
grassland
grassland
grassland
grassland
grassland
grassland
grassland
grassland
savanna
Welling P. & Laine K.
Alexander H.M. & Schrag A.M.
Larsson E.L.
Montiel S. & Montana C.
Mouquet N., Leadley P., Meriguet J. and Loreau M.
rP
grassland
grassland
grassland
grassland
savanna
savanna
prairie
grassland
grassland
grassland
grassland
grassland
grassland
grassland
grassland
rangeland
savanna
grassland
grassland
grassland
grassland
2002
2003
2003
2003
2004
Fo
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Page 60 of 79
grassland
2013
Larios L., Aicher R.J. and Suding K.N.
grassland
2013
Shang Z., Yang S., Shi J., Wang Y. and Long R.
rangeland
2013
Snyman H.A.
Page 61 of 79
grassland
2013
Zeiter M., Preukschas J. and Stampfli A.
grassland
grassland
2014
2014
Carlo T.A. & Tewksbury J.J.
grassland
2014
steppe
grassland
2014
2014
grassland
grassland
grassland
steppe
savanna
prairie
meadow
2014
2015
2015
2015
2015
2015
2015
Johnston D.B & Chapman P.L.
Johnston, D.B. & Chapman P.L.
Martinkova Z. & Honek A.
Freund L., Carrillo J., Storm C. and Schwabe A.
Laborde J. & Thompson K.
Lucero J;E., Allen P.S. and McMillan B.R.
Ragusa-Netto J. & Santos A.A.
Willand J.E., Baer S.G. and Gibson D.J.
Wu G., Shang Z., Zhu Y., Ding L. and Wang D.
grassland
2016
Chaudron C., Chauvel B. and Isselin-Nondedeu F.
Doisy D., Colbach N., Roger-Estrade J. and Mediene S.
Freund L., Eichberg C., Retta I. and Schwabe A.
Pruchniewicz D., Donath T.W., Otte A., Zolnierz L. and Eckstein R.L.
2016
Zeiter M., Schaerrer S., Zweifel R., Newbery D.M. and Stampfli A.
2016
iew
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grassland
Fo
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Page 62 of 79
APPLIED to restoration or not
Restoration Ecology
LOCATION of study
REVIEW or not?
1
2
3
4
5
6
Journal
Title
7
8
9
10
11
12
Journal of Applied Ecology
Seed rain in a north-american tall grass
Tucker
case
prairie
study
Prairie Research
Yes Area, in Callaway County, Missou
13
Journal of Range Management
A new sticky trap for monitoring seed rain in
case
grasslands
study
No
NA
14
Species
Journal
interactions
of
Ecology
in
a
successional
at
Sea
grassland
Ranch,
Sonoma
.1.
Seed
County
rain
case
and
study
(38?40'N,
seedling
recruitment
123?24'W),
Yes
on the coast 200 km north of
15
Seed
rain
in
grassland,
New
Zealand
herbfield,
Journal
snowbank,
of
Botany
and
fellfield
in
the
alpine
zone,
Craigieburn
case
study
range,
No
South-island,
Craigiebu
New-zealand
16
Seed bank
Annales
andBotanici
seedlings
Fennici
emerging after soil disturbance
in ashore
wetcase
seminatural
studyFunbo
grassland
Yeskm east
in sweden
southwestern
of Lake
10
of Uppsala in central Sweden
17
18
ative diaspore bank of calcareous
grassland plants .1. Seasonal dynamics
SwabianofAlb
diaspore
(700m
elevation)
and diaspore
inNo
the district
bank inStuttgart
2 calcareous
(Baden-Wuerttem
grassland site
Flora
caserain
study
19
mental-study of the effects
grazing
on vegetation change in a species-poor
wittenham
grassland
nature
the reserve
role of seedlings
in OXFORDSHIRE,
recruitment
England
into g
Journalofofsheep
Applied
Ecology
case
study and
Yes
20
Distribution
Arctic
and
of
Alpine
Phippsia-algida
Research
and
autosuccession
in
the
polar
semidesert,
case
study
Canadian
No
high
arctic
King
Christian
Island
(77046'N,
100043'W)
in
the
Canadian
Arctic
A
21
Ecoscience
Regeneration
window
for
fleshy-fruited
plants
during
case
scrub
study
development
Yes
Kaiserstuhl, a small mountain range of volcanic origin in SW-Germany, that is surrounded by the upper Rh
22
A seedCanadienne
trap for monitoring
De Botanique
the seed rain in terrestrial
communities
case study
No
NA
23Canadian Journal of Botany-Revue
24
review
ecology
Yes
NA
Bekker
R.M. and Thompson K.Seed banks and seed dispersal: Important topics in restoration
es 25
on the feasibility ofActa
re-creating
Botanicachalk
Neerlandica
grassland vegetation
onNational
ex-arable
land .1.
case
Thestudy
potential
roles
Yes
the seed TQ
bank
and the6seed
rain
Castle Hill
Nature
Reserve
(National
gridofreference
370060),
km north26
White House
Meadowmeadow:
of the case
University
Northern California Coast Range
Revegetation
following sail disturbance
in a California
Thestudy
role of
of California's
propagule
supply
Oecologia
Yes
27
Grazing
effects onNaturalist
reproductive characteristics of common curlymesquite
(Hilaria
belangeri)
Texas, near sonora
Southwestern
case studyEdwards
YesPlateau,
28
making
of
hay
from
Journal
mesotrophic
of
Applied
grassland
Ecology
in
a
field
in
northern
England:
Effects
of
case
hay
study
cut
date,
grazing
Yes
and
fertilizer
in Reference
a split-split-plot
Gillet
farm,
Upper
Teesdale
(National
Grid
NY863e
29
Ecology What resources are available to desert granivores: Seed
eastern
case
rainstudy
or
Mojave
soil seed
Desert
Yes
bank?
of California, North American deser
30
Canadian Journal
The seed
ofrain
Botany-Revue
and seed
Rockefeller
bank
Canadienne
of an
Experimental
adjacent
De Botanique
native
Tract,tallgrass
which
caseisprairie
study
part ofand
theold
Yes
Kansas
field Ecological Reserves in Jefferson
31
32
Species
composition
and
SchleswigHolstein
their relation
(North-western
vegetation
Germany)
Flora of soil seed bank and seed rain of abandoned wet meadows
case
study
Yes to aboveground
33
Flora
Notes on seed traps in terrestrial plant communities
review
Yes Wasenweiler; ,
34
FunctionalGranivore
Ecology impact on soil-seed reserves in the central Monte
case study
desert, Argentina
Yes
Biospher
35
Restoration
Seed rain
Ecology
in natural grassland and adjacent
Jakobshorn
ski run in the
Mountain
Swiss
caseAlps:
(2500
study
Am
preliminary
elevation)
Yes report
in the Canton of Grisons in the no
36
Applied
Restoration
Vegetation
of
high
Science
species
density
Gerendal
in
calcareous
Nature
grassland:
Reserve,
the
Province
role
case
of
study
of
seed
Limburg,
rain
and
Yes
in
soil
the
seed
southeasternmost
bank
part of The Ne
37
38
Herbivores, seed banks and seedling recruitment
Nash's Field,
in Silwood
mesic
grassland
Park, Yes
Berkshire, UK (National Grid reference 4
Journal of Ecology
case
study
39
New Zealand
Influence
Journal
ofof
vegetation
Botany structure on spatial patterns of case
seedstudy
deposition Yes
by birds Mana
40
41
Seed Journal
rain andofitsEcology
role in the recolonization of degraded hill slopes
Kondoa
semi-arid
Irangi Hills
central
(hereafter
Tanzania
called KIH) in central Tanzan
African
caseinstudy
Yes
42
Influence
of fallow type and land-use intensity on weed
farm
seed
of the
rainInternational
in a forest/savanna
of Tropical
zone
Agriculture (IITA) in Ibad
Weed Science
case
study Institute
Yestransition
43
Restoration Ecology Seed rain in high-altitude restoration
Jakobshorn plots
Mountain
incase
Switzerland
(2500
study m elevation)
Yes
in the Canton of Grisons in the no
44
Journal
Effects
of Vegetation
of seed dispersal
Scienceon Juniperus communis recruitment case
on aCampos
study
Mediterranean
No mountain
de Otero
(Sierra Nevada, Granada, Spain)
45
46
Goitsche,
anApplied
abandoned
lignite-miningon
area
(60 km2), isslopes
part of
German
Lignite Mining
and isGermany
situated between th
Spontaneous
and initiated
succession
unvegetated
in the
the Central
abandoned
area District
of Goitsche,
Vegetation
Science
caselignite-mining
study
Yes
47 Spatial andJournal
temporal
of Biogeography
variability in seed dynamics of machair sand dune plantcase
communities,
study
the
YesOuter Outer
Hebrides, Scotland
48
TemporalAmerican
vegetation
Journal
dynamics
of Botany
and recolonization mechanisms on different-sized
case study
soil disturbances
Yes
Flint
in tallgrass
Hills prairie
49 of seed dispersal
erns
Journaland
of Ecology
seedling recruitment in Corema album (Empetraceae):
Figueiras
case
the study
importance
and Muxieiro
Yes
of unspecialized
sand dunes in
dispersers
the Cies for
Islands
regenera
Natu
50
Ecology The role of the seed bank in gap regeneration in a calcareous
Laelatu,
casewestern
grassland
study Estonia,
community
Yes on the eastern coast of the Baltic Se
51
52 of Primary Australian
ment
Industries Croxdale
Research of
Station,
three west–north-west
seed-trap designs
CharlevilleYes
(26°42′S, 146°22′E). And The secondary
Journal ofExperimental
Botany Effectiveness
case of
study
53
Dispersal
Seed Science
mechanisms
Research
in Lavandula
Pedrezuela,
stoechas asubsp
municipality
pedunculata:
50 kmautochory
north
case study
of Madrid
and endozoochory
on
Yes
the southern
by sheep
side of the Sierra de Gua
54
affecting
Southern
in Australia
Tablelands of New South Wales
Journal ofFactors
Applied
Ecologyinvasion and persistence of broom Cytisus
casescoparius
study
Yes
55
Restorative
grazing as a tool for directed succession with diaspore inoculation:
the model
Jugenhei
ecosystems
Phytocoenologia
case study
Yesof sand
56
57
58
59
60
iew
ev
rR
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Page 63 of 79
Restoration Ecology
iew
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1
2
Kilpisjärvi
in sub-arctic
Finland (69
seeds in alpine meadow and heath vegetation
in sub-arctic
Journal Regeneration
of Vegetation by
Science
case
study
YesFinland
3
seed banks
and newly dispersed seeds inKansas
population
Field Station
dynamics
and
ofEcological
thestudy
annualReserves
sunflower,
Helianthus
the
annuus
KSR site), in Jeffers
Journal
of Ecology
case
No (henceforth
4 Role of soil
ways of trapping seeds, in alpine environments,
Lapland,
re Field
Nordic Journal Two
of Botany
case
study Sweden
Yes
5
Seed
Plant
bank
Ecology
dynamics of the desert cactus Opuntia
Mapimi
rastrera
Bio sphere
in twoReserve
habitats
case study
located
from the
in Yes
the
Chihuahuan
southernDesert
Chihuahuan Desert, Mexico
6
7
Immigration
Oikos and local competition in herbaceous plant communities:
afield
three-year
study
Yes
experiment
biologicalcase
station seed-sowing
of Foljuif,
Saint-Pierre-les-Nemours,
France
8
9 Spatial dynamics
Ilex aquifolium populations seed dispersal and seed bank:case
understanding
the
province
steps of
of Soria,
regeneration
Spain
Plant of
Ecology
study Oncala,
Yes first
10
PlantComparison
Ecology
of three seed trap types in a chalk grassland:
Hénouville
toward
case
nature
study
a standardised
reserve, some
Yes protocol
15 km west of Rouen in north-west
11 Is the population
Ecography
turnover of patchy-distributed annuals determined by Borecˇ
dormancy
case study
Yesor dispersal
hill dynamics
in NW Czechia
(446 m processes?
a. s. l.; 50831?N, 13859?
12
Ecological
Pathways
Monographs
in old-field
succession
to white
pine:
SeedArea
rain,(hereafter
case
shade,
study
andBoot
climate
Yeseffects
Boot
Lake Scientific
and
Natural
Lake),
in east-central Minnesota (458209
13
TemporalInterciencia
variations in soil seed number and in seed rain in a forest-savanna
case
sequence
study
in the
Yes
GranSabana,
Sabana,Estado
Venezuela
sector
norte
de
la
Gran
Bolívar, Venezuela
14
Fire
Ecological
increases
Applications
invasive
spread
of
Molinia
caerulea
mainly
through
changes
case
study
in
demographic
Yes
parameters
Kalmthoutse
Heide,
situated
in
the
northern
part
of Belgium (near
15
Perspectives
Regeneration
in PlantofEcology
Cyperaceae,
Evolution
withand
particular
Systematics
reference to seed
Caseecology
study and Yes
seed banksNA
16
Acta Oecologica-International
Regenerative role
Journal
of seed
of Ecology
banks following
30 kman
east
intense
ofcase
Vitoria-Gasteiz
soil
study
disturbance
(Basque
Yes
Country) in Northern Spain (42°
17
18
JournalThe
of Vegetation
role of the seed
Science
bank, seed raineastern
and theScotland,
timing ofUK.
disturbance
Glensaugh
case study
in Research
gap regeneration
YesStation of the Macaulay Institute (56
19
Journal
Plant
oftraits:
Vegetation
Their role
Science
in the regeneration of alpine plant communities
case
studyinin
sub-arctic
Yes Finland
Kilpisjärvi
sub-arctic
Finland (69
20
e implications
ofAgriculture
seed rain and
Ecosystems
seed bank
& patterns
Environment
for plant succession at the edges
caseofstudy
abandonedYes
fields inLaMediterranean
Crau,
landscapes
21
45 km
south
Stockholm
(58858’N, 17835’E)
Canadian
Local seedJournal
rain and
of seed
Botany-Revue
bank in a Canadienne
species-rich De
grassland:
Botanique
effectscase
of plant
abundance
seed size
study
Noofand
22
Phyton-International
Seed
rain
Journal
in
and
Monte
of
between
Experimental
Austral
vegetation
Neuquino
Botany
patches
nearby
in
the
arid
town
case
Patagonia,
study
of
Picun
Argentina
Leufu,
No
Province
of
Neuquen. Argentina( 39
23
Tom’s Point
Preserve,
a private
grasslanddeterminant
preserve
located
adjacentinvasion
to Tomales Bay in Marin Count
Spatial and
temporal patterns
of seed
dispersal:
An important
of grassland
Ecological
Applications
case study
Yes
24
Plant Ecology
Seed rain
andBiosphere
environmental
controls
invasion
of Picea
caseabies
study
into grassland
Yes
25
Poľana
Reserve
in theon
Western
Carpathian
Mountains,
Slovakia, Central Europe (Príslopy Pass,
26
Rangeland Ecology
Factors
& affecting
Management
Bromus tectorum seed bank carryover
case in
study
western Utah
Yes
Tooele
27
The relevance
Oecologia of ants as seed rescuers of a primarily bird-dispersed tree
caseinstudy
the Neotropical
No cerrado
savanna
Itirapina,
southeast
Brazil
28
How
Journal
does
of farm
surrounding
Vegetation
Science
vegetation
affecta the
of succession:case
A five-year
study
container
Yes
experiment
Organic
at Benesˇov
nad Lipou,
site course
in the southeastern
part
of
the Czech
Republic,
in the Ceskomoravska´ vrchov
29 Trade-off of
Polish
sexual
Journal
and asexual
of Ecology
recruitment
Qinghai-Tibetan
in a dominant
Plateau,
weedNW
Ligularia
China virgaurea
/ eastern
case study
side
(maxim.)
of the
Yes
InTibetan
alpine grasslands
Plateau (33°45’N,
(China) 102°04’E, M
30
Processes
Limiting
Santa
Grasslands
Cruz Island,
after
CA
Non-Native
/ Central Valley
Herbivore
Removal
Cruz Island, CA (34.02065 N
Restoration
EcologyNative Shrub Recovery in Exotic
case
study
Yes of Santa
31
Journal
Past and
ofpresent
Appliedmanagement
Ecology
influences the seed bank and seed
case
rainstudy
in a rural landscape
Yes
southern
mosaic
32
Spatially-restricted
plant material application creates colonization
northern
initials
Upper
forRhine,
flood-meadow
approx.
30
restoration
km southwest of Frankfurt, G
Biological Conservation
case
study
Yes
33
an34
successionalPlant
species
Ecology
groups
& be
Diversity
discriminated based on Rotmoosferner
their life historyintraits?
case
A study
study
from a Alps
glacier
Yes (Ötztal
foreland
the Central
Alps
the central
Austrian
Alps,inTyrol;
46
35
ActaSeed
Botanica
rain
of
Brasilica
woody
species in
mosaics of Araucaria
forest
andcase
grasslands
study in
Southern
Yes município
Brazil de São Francisco de Paula
Centro
de Pesquisas
e Conservação
da Natureza
(CPCN)
Pró-Mata
PUCRS,
36
Wetlands
Seed Rain of Restored and Natural
Dickinson
Prairie
County,
case
Wetlands
northwest
study
Iowa,
Yes in the southern part of the prairie p
37
seed
dispersal and
rather than persistent soil seed-banks,
fieldcontrol
experimental
seedling
recruitment
located
of35
woody
km south
plants
ofinBrasilia,
Neotropical
Brazil savann
(15856
Seeddormancy,
Science Research
case station
study
Yes
38
Ecological
A
data-driven
Modelling
simulation
of
endozoochory
by
ungulates
illustrates
case
study
directed
No
dispersal
Westhoek-South
is
a
nature
reserve
located
in
the
westernmost
tip
39
t community
structure
Journal of
of aVegetation
threatened
Science
sandy
a 9-yr
period
under
case
experimentally
induced
Yes
nutrient regimes:
is there
a lag
p
Germany,
in thegrassland
northernover
upper
Rhine
valley,
about
30 study
km south of
Frankfurt/Main
(Hesse) within
the
Cont
40
41
Applied
Sowing
Vegetation
of low andScience
high diversity
Central
seedGerman
mixtures
Lignite
in ecological
Mining restoration
District.
case study
south-eastern
of surface
Yes mined-land
part of Saxony–Anhalt, Germany (51
42
Seed
PlosDensity
One Significantly Affects Species Richness and Compositioncase
in Experimental
study
Yes
Plant Communities
experime
43
Harvester
Park
ants
Shaked
modifyLong-term
seed rain Ecological
using nestResearch
vegetation
(LTER)
and granivory
Station,Yes
located in the northern Negev desert o
Ecological Entomology
case
study
44
al
ational
by
Park on
(north-western
aJournal
continental-shelf
Spain)island:
/ Figueiras-Muxieiro,
predicting interspecific
a 12-ha dune
variation
system
in seed
located
rainon
based
the east
on plant
coast
of Monteagudo
and lizard
Islandmovement
(2.5 km from
pa
of Biogeography
case
study
No distribution
45lizards
Plant Ecology
Seed limitation of woody plants in Neotropical
casesavannas
study 35 Yes
km south of Brasilia, Brazil
46
47
Oecologia
Dispersal and microsite limitation in Australian
Northern
caseold
Plains
study
fields
of southeastern
Yes
Australia, Victoria (36°4'S, 144
48
Journal ofQuantification
Vegetation Science
of plant dispersal ability within and
Schaffhauser
beyond
case
a calcareous
study
Randen, Switzerland
grassland
Yes
(51°15′18’’ N, 03°02′33’’ E, 765
49
15
km
southeast
of
Cˇ
eske´
Budeˇjovice,
in the Czech Repu
Establishment
in meadow
Journal of Vegetation
Science and spatial associations of recruitscase
study gapsYes
50
e dynamics
of three
Plantshrub
Ecology
species in a fire-prone temperate
interplay
case
study(318
the550
seed
YesS, bank,
seedW),
rainanand
fireha
regime
Entre RIos savanna:
province the
of Argentina
/between
EPNP
588 1700
8,500
area of p
51
52
Effectof
ofVegetation
propagule pressure
California
Ridge grassland
in Irvine,
California,
after
an extreme
within
disturbance
Irvine Ranch Land Reserve (33.75
Journal
Science on recovery of aLoma
case
study
Yes the
53
Seedofrain
headwater
andResearch
its relationship
area of the Yellow
with above-ground
river, Maqin County.
vegetation
Theof
station
degraded
is situated
Kobresia
between
meadows
34 270–34 310N and 100 020
Journal
Plant
case
study
Yes
54
55
Bloemfontein
(lat 288500S,
long 268150E,
altitudeYes
1 350 m above sea level), situated in th
Disturbances
on Longevity
of Grass
Seeds, Semi-Arid
South
African
Rangeland
Rangeland
Ecology &Impact
Management
case
study
56
57
58
59
60
Restoration Ecology
Page 64 of 79
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1
2
Seed availability
AgricultureinEcosystems
hay meadows:
& Environment
Land-use intensification promotes seed
but
Switzerland
not the
over 12 differente
seed bank regions
caserain
study
Yespersistent
3
Directness
and
tempo of avian seed dispersal increases emergence of
wild
Sonoran
chiltepins
Desert
ingrasslands
desert grasslands
of southern Arizona (USA)
Journal of
Ecology
case
study
No
4
NationalWeed
Institute
of Agricultural
Research
(INRA) Centre
of Lusignan
(Poitou-Charentes,
France)
5
Weed seed
rain interception
by grass
cover depends
seed traits
Research
caseon
study
Yes to evaluate the environmental im
6
Seed addition viaApplied
epizoochorous
dispersal
Uppercase
Rhine
mimicking
Valley, Germany.
theYes
colonization
Northern
of bare
Upper
soilRhine
patches
Valley, Ge
Vegetation
Sciencein restoration: an experimental approach
study
7
Invasive
RoughPlant
Surface
Science
and High-Forb
and Management
Seed Mix Promote Ecological Restoration
Piceance
of Simulated
BasinWell
of western
Pads Colorado, USA
case study
Yes
8
9
Seed Rain
Invasive
and Seed
Plant
Bank
Science
Reveal
andthat
Management
Seed Limitation Strongly Influencescase
PlantNyna¨
study
Community
s nature
Yes
Assembly
reserve, in
southeastern
Grasslands Sweden ()
10
Crop Research
plants
Institute
grasslandatYes
Praha-Ruzyne at 50°05’10.448
Weed Research The establishment of Taraxacum officinale
caseinstudy
11
Restoration
of
a
Tuexenia
newly
created
inland-dune
complex
as
a
model
in
northern
practice:
Upper
impact
case
Rhine
of
study
substrate,
Valley,
Germany.
minimized
Yes
Apfelbachdüne;
inoculation and20grazing
km south of
12
Plant Ecology
into
& Diversity
species-rich limestone grassland: recruitment,
herbivory
case study
andin
the
Yes
threat
incipient
scrub
Cressbrook
Dale
the
Peakfrom
District
National
Park, Derbyshire
13 Scrub encroachment
14
Increased Primary Production from an Exotic Invader Does Not
Valley,
Tooele County, Utah, USA
Plos One
caseSubsidize
studyRushNative
Yes Rodents
15
Brazilian
Seed
Santa
rain
Journal
Helena,
generated
of Biology
a ranch
by bats
(6000
under
ha) in
Cerrado's
the municipality
pasture remnant
of Três Lagoas,
case
treesstudy
in(State
a Neotropical
of Mato
No Grosso
savannado Sul, Brazil; 4 km northea
ule16abundance and
Journal
richness
of Vegetation
are equivalent
Science
or higher
Illinois,
in communities
USA. Southern
restored
Illinoiswith
University
case
local
study
ecotypes
Agronomy
Yes
relative
Center
to cultivars
in JacksonofCounty,
dominant
Illinois,
species
US
17
Species-abundance-seed-size
patterns within
Qinghai-Tibetan
a plant community
Plateau
affected
(China)
by grazing
Qinghai
disturbance
Province; (338430 to 358160 N,
Ecological
Applications
case
studyDawu,
Yes
18
19
Effects
Agriculture
of lateEcosystems
mowing on &
plant
Environment
species richness and seed rain
Central-western
in road
France,
and adjacent
in
the Région
arableCentre
fields (Indre-et-Loire depa
caseverges
study
Yes
20
21
22
Effect of expansive species on seed rain and soil
Polish
seedparts
bankofof
the
mountain
Central
Sudetes
(N 50°36’39’’–50°39’35’’; E 16°25’56
Tuexenia
case
study mesic
Yesmeadows
23
Timing
of extreme
drought modifiesNegrentino,
reproductive
Switzerland
outputcase
in semi-natural
/ study
Negrentino Yes
grassland
(820 m a.s.l., 46°27051
Journal of
Vegetation
Science
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If species level, how many?
INVASIVE species MENTIONED
BIOTIC dispersal MENTIONED OR STU
COMMUNITY or species level?
seed rain method
REGENERATION DYNAMICS
DEGRADATION
GRASSLAND type
LONgitude ( ° / ' )
38° 53' NENDOGENUS
91° 54'
Temperate
W (simulations-pocket
GrasslandPASSIVEgopher
RESTORATION
DIRECT
disturbances
MEASUREMENTS
COMMUNITY
)
NA
Mediterranean
NA
Grassland
NA
DIRECT
NA
MEASUREMENTS
SPECIES
38° 40' N 123° 24'
Temperate
W
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
46° 06' S 171° 42'
Alpine Grassland NA
DIRECT
NA
MEASUREMENTS
COMMUNITY
Boreal Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY
59°52'N 17°51'E
Temperate
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY
48° 39' N 90° 20'
E
NA
5
5
NA
NA
NA
NI
NI
NI
NI
NI
NI
NO
NO
NO
NO
NO
NO
51° 37' N 1° 10'Temperate
W
Grassland
EXOGENOUS
ACTIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
YES
Cool
Grassland
PASSIVE
(fire regimes)
RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
NO
77° 46' N 100°
43'Semi-Desert
W ENDOGENUS
Temperate
Grassland
EXOGENOUS
PASSIVE
RESTORATION
DIRECT
MEASUREMENTS
SPECIES
29
NI
YES
48° 06’ N 7° 40’ E
Temperate GrasslandNA
DIRECT
MEASUREMENTS
NA
NA
NA
NA
NA
NI
NO
NA
NA
NA
NA
DIRECT
NA
MEASUREMENTS
NA
NA
NA
NO
W
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
50° 50' N 0° 3'Temperate
37' Semi-Desert
W
39° 45' N 123°
Warm
EXOGENOUS
Grassland
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
NO
31° 0' N 101°
0' W
Warm
Semi-Desert EXOGENOUS
Grassland
ACTIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
NO
Grassland
EXOGENOUS
ACTIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
39
NI
NO
54° 39' N 2° 15'Temperate
W
35° 0' N 115°28'
Warm Semi-Desert
W
Grassland
NA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
39° 03'N 95° 12'
Temperate
W
Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
Temperate
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY
YES (NON
50° 55' N 12° 24'
E
NA WOODY AND WOODY)
NO
48° 03' N 7° 43'
Temperate
E
Grassland
EXOGENOUS DIRECT
NA
MEASUREMENTS
COMMUNITY NA
NI
NO
34° 02' S 67° 58'
Temperate
W
GrasslandNA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
46°46' N 9° 50'Alpine
E
Grassland
EXOGENOUS DIRECT
NA
MEASUREMENTS
COMMUNITY NA
NI
NO
50° 51' N 5° 54'
Temperate
E
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
ACTIVE
Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
COMMUNITY NA
51° 24' N 0° 38'Temperate
W
NI
NO
41°6'S 174°48'E
Temperate Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
COMMUNITY NA
NI
YES
iew
ev
rR
ee
rP
Fo
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2
3
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Restoration Ecology
LATitude ( ° / ' )
Page 65 of 79
4° 40' S
7° 30' N
46°46' N
37° 06' N
51° 26' N
57° 05' N
39° 05' N
42° 15′ N
58° 35' N
Warm
EXOGENOUS
Grassland
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
35°
40' Semi-Desert
E
NI
NO
3° 54'Tropical
E
Grassland
EXOGENOUS
ACTIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
YES (WOODY SPECIE)
NO
9° 50'Alpine
E
Grassland
EXOGENOUS DIRECT
NA
MEASUREMENTS
COMMUNITY NA
NI
NO
Temperate
GrasslandNA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
YES
3° 21'
W
12° 20'
W
Temperate
Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
2° 56' W
Boreal Grassland
EXOGENOUSPASSIVE
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
96° 35'
Temperate
W ENDOGENUS
GrasslandPASSIVE
(fire regimes)
RESTORATION
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
NO
8°
Warm
53' WSemi-Desert Grassland
NA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
YES
23°Mediterranean
33' E
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
27° 33′ S
40° 46' N
35° 48′ S
49° 45' N
Warm
Grassland
DIRECT
MEASUREMENTS
COMMUNITY NA
152°
20′Semi-Desert
E
NA
NA
NI
NO
30°Mediterranean
36' W
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
YES
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
149° Temperate
40' E
SPECIES YES1 (NON WOODY SPECIES)
NO
8° 40'
Temperate
E
Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
YES
Restoration Ecology
69° 01' N 20° 50'Alpine
E
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
38° 56' N95° 15'
Temperate
W
Grassland
EXOGENOUS DIRECT
MEASUREMENTS
NA
SPECIES
1
68”21’N 18’29‘EAlpine Grassland NA
DIRECT
MEASUREMENTS
COMMUNITY NA
NA
26° 40' N 103°
Warm
40' Semi-Desert
W
Grassland
NA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
48° 15' N 2° 39'
Temperate
Grassland
EXOGENOUS
ACTIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
8
E
NI
NI
NI
NI
NI
NO
NO
NO
NO
NO
41° 57' N 2°Mediterranean
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
20' W
SPECIES
1YES (WOODY SPECIE)
YES
49°29’N 0°56’E
Temperate Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
Temperate
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
5
NI
NO
50° 31' N 13° 59'
E
Temperate
MATHEMATICAL
Grassland
NPASSIVE
A
OR
RESTORATION
MECHANISTIC MODELS
SPECIES
AND SIMULATIONS
1YES (WOODY SPECIE)
NO
45° 20' N 93° 11'
W
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
5° 24' N 61° 43'Tropical
W
Temperate
ENDOGENUS
GrasslandPASSIVE
(fire regimes)
RESTORATION
DIRECT MEASUREMENTS
SPECIES YES1 (NON WOODY SPECIES)
NO
51° 23' N 4° 26'
E
NA
NA
NA
NA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
NA
NA
NA
YES
42° 51′N 2°Mediterranean
37′W
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
56° 53' N 2° 31''
Temperate
W
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
69° 01' N 20° 50'Alpine
E
4° 50' N 43° 33'
Temperate
E
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
YES
58° 58' N 17° 35'
E
Temperate
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
39°20' S 69° 19'
Temperate
W
GrasslandNA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
4
NI
NO
57 ' W
38° 13' N 122°Mediterranean
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES YES
58(NON WOODY SPECIES)
NO
Temperate
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
NO
48° 38′ N 19°25′
E
1YES (WOODY SPECIE)
40° 31' N 112°
Warm
59'Semi-Desert
ENDOGENUS
Grassland
(fire regimes)
ACTIVE
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
NO
GrasslandNA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
YES
22° 12' S 47° 51Tropical
W
Temperate
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
49° 92' N 15° 00'
E
33°45’N 102°04’E
Alpine Grassland NA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
NO
46' W
Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
34° 01 N 119°Mediterranean
SPECIES YES2 (NON WOODY SPECIES)
NO
58°54' N 17°00' Boreal
E
Grassland
EXOGENOUS
ACTIVE ACTIVE
RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
YES
(Flooded) RESTORA
DIRECT MEASUREMENTS
COMMUNITY NA
49° 51' N Temperate
8° 24' E GrasslandEXOGENOUS
NI
NO
Alpine Grassland NA
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
6◦45’N 11◦02’E
Temperate
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
YES (WOODY SPECIE)
YES
29° 25' S 50° 35'
W
43° 22' N Temperate
95° 03' W GrasslandEXOGENOUS
(Flooded)
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
15° 56' S 47° 63'Tropical
W
SPECIES
14
NI
NO
Temperate
MATHEMATICAL
Grassland
EXOGENOUS
PASSIVEOR
RESTORATION
MECHANISTIC MODELS
SPECIES
AND SIMULATIONS
25
NI
YES
51° 04' N 2° 33'
E
Temperate
Grassland
EXOGENOUS
ACTIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
50° 02' N 7° 54'
E
51°8′ N 12°9′
Temperate
E
Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
SPECIES
1
NI
NO
50°09' N 14°33''E
Temperate Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
SPECIES
44
NI
NO
Warm
EXOGENOUS
Grassland
ACTIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
31° 17' N 34°
37' Semi-Desert
E
NI
YES
43° 22' N 8° Mediterranean
56' W
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
SPECIES
1
NI
YES
15° 56' S 47° 63'Tropical
W
Grassland
EXOGENOUS DIRECT
NA
MEASUREMENTS
SPECIES
23
NI
NO
36° 4' S 144° Temperate
24' E
Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
NO
51° 15′ N 03° 02′
Temperate
E
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
48° 55′ N Temperate
14° 39′ E GrasslandEXOGENOUS
(Flooded)
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
NI
NO
Temperate
GrasslandPASSIVE
(fire regimes)
RESTORATION
DIRECT MEASUREMENTS
SPECIES
3
NI
NO
31° 55' S 58° 17'
W ENDOGENUS
iew
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rP
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2
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33
34
35
36
37
38
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40
41
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45
46
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Page 66 of 79
Warm
44'ENDOGENUS
Semi-Desert
W
(fire
Grassland
and
PASSIVE
extreme
RESTORATION
DIRECT
drought)
MEASUREMENTS
COMMUNITY NA
33° 43' N 117°
NI
NO
34° 27' N 100° 02'Alpine
E
Grassland
EXOGENOUS
PASSIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
29° 05' S 26° 04'
E
Temperate
Grassland
EXOGENOUS DIRECT
MEASUREMENTS
COMMUNITY NA
NA
NI
NO
NI
NO
Page 67 of 79
Temperate
Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
COMMUNITY NA
47° 04' N 7° 55'
E
NI
NO
31°33′ N 111°04′W
Warm Semi-Desert Grassland
PASSIVE RESTORATION
DIRECT MEASUREMENTS
NA
SPECIES
1
NI
46°24' N 0° 7'Temperate
E
MATHEMATICAL
Grassland
EXOGENOUS
PASSIVEOR
RESTORATION
MECHANISTIC
MODELS
AND
SIMULATIONS
SPECIES
12
NI
ACTIVE
49° 50′ N 8° 34′
E
Temperate
Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
SPECIES
10
NI
ACTIVE
YES
NO
YES
39° 78' N 108°
Warm
33' Semi-Desert
W
EXOGENOUS
Grassland RESTORA
DIRECT MEASUREMENTS
SPECIES YES1 (NON WOODY SPECIES)
NO
58° 49' N 17°24'E
Temperate Grassland
EXOGENOUS
PASSIVEACTIVE
RESTORATION
DIRECT MEASUREMENTS
cOMMUNITY
NI
NO
Temperate
Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
50° 05’ N 14°18’
E
SPECIES
1
NI
NO
49° 56' N 8° 35'
Temperate
E
Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
YES
Temperate
Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
SPECIES
9
NI
YES
53° 17′ N 1° 45′
W
Warm
26' Semi-Desert
W
EXOGENOUS
Grassland
ACTIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY YES
40° 21' N 112°
NA(NON WOODY SPECIES)
NO
20° 44’ S 51° 41’Tropical
O
Grassland
EXOGENOUS DIRECT
NA
MEASUREMENTS
SPECIES
4
NI
YES
37°41' N 89° 14'
Temperate
W
Grassland
EXOGENOUS ACTIVE
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
NO
Alpine Grassland
EXOGENOUSRESTORA
DIRECT MEASUREMENTS
COMMUNITY NA
33°84’N 100°85’E
NI
NO
47° 60' N
1° 70'
E
Temperate
Grassland
EXOGENOUS
ACTIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY YES
NA(NON WOODY SPECIES)
NO
Fo
50° 36’ N 16° 25’
E
Temperate
Grassland
EXOGENOUS
ACTIVE RESTORATION
DIRECT MEASUREMENTS
COMMUNITY NA
46°27' N 8°55'
E
Temperate
Grassland
EXOGENOUS DIRECT
MEASUREMENTS
COMMUNITY NA
NA
iew
ev
rR
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rP
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2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
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19
20
21
22
23
24
25
26
27
28
29
30
31
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34
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40
41
42
43
44
45
46
47
48
49
50
51
52
53
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Restoration Ecology
NI
NI
NO
NO
Restoration Ecology
Page 68 of 79
PITFALL TRAPS
STICKY TRAPS
type of TRAPS
SEEDS IDENTIFICATION
Collection FREQUENCY
number of months studied
Complementary
measurements on Seeds
(weight, size, viability...)
Seed SOWN
BIOTIC dispersal by...
BIOTIC dispersal ONLY
1
2
3
4
5
6
7
8
9
10
11
12
NO
NI
NO
NIEQUAL OR6LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
STICKY TRAPS YES
13
MORE THAN
NA 3 INFORMATION
NA
NA/ Dispersal traits, releasing
NA
height,
NA size and
NI weight
STICKY TRAPS YES
14
NO
NI
NO
NI
5
3
MONTHS
TO
NI
LEES
THAN 6TRAPS
MONTHS
YES
STICKY
15
NO
3
INFORMATION
NI
NO
/
Dispersal
EQUAL
traits,
OR
viability
7
LESS
and
THAN
VISUAL
weight
15
DAYS
IDENTIFICATION
INTERVALS
FUNNEL
16
NO
NI
NO
NI
3
3 MONTHS TONI
LEES GAPS
THANTRAPS
6 MONTHS
17
18
1 INFORMATION
EQUAL
/ Dormancy
OR13LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
NO
NI
NO
19
3 MONTHS TONI
LEESTRAYS
THAN TRAPS
6 MONTHS
NO HERD /sheep NO
NI
15
20
NO
NA
NO
NI
NA
OTHER
NA
METHODOLOGIES
NI
WITHOUT SEED TRAPS
21
neficial
to
colonization
NO
of
open
sites
than
NO
the
scrub-centred
NI
EQUAL
OR
seed
24
LESS
rain
THAN
due
VISUAL
to
15
birds;
DAYS
IDENTIFICATION
Bustamante,
INTERVALS
FUNNEL
TRAPS
Simonetti & Mella (1992) reported simila
22
1 INFORMATION
Size
EQUAL/ OR
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
NO
NA
NO
NALESS THAN
23
24
MORE
NATHAN 3NA
INFORMATION
NA / Dispersal traits,
NAlongevity,
NAsize and weight
NA
NA
25
NO
NA
1NO
INFORMATION
EQUAL
/ Viability
OR3LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
STICKY TRAPS YES
26
16 DAYS TO 1 MONTH
NO
NI
NO
NI
20
NI STICKY TRAPS YES
27
NO
NI
NO
NI
4
NI
NI STICKY TRAPS YES
28
NA
NA
NA
NI
NA
NA
VISUAL
IDENTIFICATION
FUNNEL
29
NO
NI 2 INFORMATION
NO
/ Size and17
weight3 MONTHS
VISUAL IDENTIFICATION
TO LEESFUNNEL
THAN 6TRAPS
MONTHS
30
NO
NI
NO
NIEQUAL OR6LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL
31
32
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
NO
NA
NO
NIEQUAL OR6LESS THAN
33
NO
NA
NO
NI
516 DAYS TO
VISUAL
1 MONTH
IDENTIFICATION
5 TYPES OF TRAPSYES
34
NO
NI
1NO
INFORMATION / Weight
616 DAYS TO
VISUAL
1 MONTH
IDENTIFICATION
OTHER TRAPS
35
NO
NI
NO
NIEQUAL OR7LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
36
NO
NI
1
NO
INFORMATION
/
Viability
4
1
6
DAYS
TO
VISUAL
1
MONTH
IDENTIFICATION
FUNNEL TRAPS
37
38
GERMINATION
OR MORE
INTERVALS
GAPS TRAPS
NO
NO
NO
NI 12 MONTHS
22
39
ONE
yes ANIMAL/ BIRDS ONLY
NO
NI
216 DAYS TO 1 MONTH
NI OTHER TRAPS
40
41
/ NO
Dispersal traits and weight
TRAYS TRAPS
NO2 INFORMATION
NI
8
NI GERMINATION
42
STICKY TRAPS YES
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
NO
NO
NO
NIEQUAL OR24LESS THAN
43
NO
NI
NO
NIEQUAL OR14LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
OTHER TRAPS
44
ONE
YES ANIMAL/ BIRDS 1ONLY
NO
INFORMATION / Viability
12
16 DAYSOTHER
TO 1 MONTH
METHODOLOGIES
NI
WITHOUT SEED TRAPS
45
46
16 DAYS TO 1 MONTH
NO
NA
NO
NI
12
NI FUNNEL TRAPS
47
NO
NI
1 INFORMATION
NO
MORE THAN 1/ Dormancy
MONTH
9 BUT LESS THAN
3 MONTHS
OTHERINTERVALS
TRAPS
GERMINATION
48
NO
NA
NO
NI
16
16 DAYS TO 1 MONTH
NI
NA
49
MORE
THAN ONEYES
ANIMAL / Ants, Birds,
1NO
INFORMATION
Gulls and Rabbits
/ Viability
12
16 DAYSOTHER
TO
VISUAL
1 MONTH
METHODOLOGIES
IDENTIFICATION WITHOUT SEED TRAPS
50
NO
NI 2 INFORMATION
NO
MONTHS
24
INTERVALS
GAPS TRAPS
/ Size12and
weightOR MORE
GERMINATION
51
52
/ Dispersal5 traits NI
NO
NI 1 INFORMATION
NO
NI 3 TYPES OF TRAPS
53
NO HERD / Sheep 1 NO
INFORMATION / Viability
0,3 16
to 3DAYS TO 1 MONTH
2 TYPES OF TRAPSYES
GERMINATION
54
OTHER
WITHOUT SEED TRAPS
NO
NI
NO
NI
NA
NA METHODOLOGIES
NI
55
ANIMAL/
ANTS ONLY/
probable for
NOdispersal by ants isNO
NI some species
716 DAYS TO 1 MONTH
NI FUNNEL TRAPS
56
57
58
59
60
iew
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Page 69 of 79
Restoration Ecology
iew
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1
2
3 INFORMATION
6 MONTHS
traits,12
sizeTO
and
LESS
weight
VISUAL
THANIDENTIFICATION
12 MONTHS
OTHER TRAPS
NO
NI
NO / Dispersal
3
3 MONTHS TONA
LEES THAN
NO
NI
YES
NI
48
NA6 MONTHS
4
/ Dispersal
NO
NI 1 INFORMATION
NO
VISUAL IDENTIFICATION
OR MORE
2 TYPES
INTERVALS
OF TRAPS
48traits12 MONTHS
5
NO
NI
NO
NI
NA
OTHER
NA METHODOLOGIES
NI
WITHOUT SEED TRAPS
6
7
NA
NA
YES
NI
NA
NA
NA
NA
8
9 MORE THAN ONE
3 MONTHS TONA
LEES THAN
YES ANIMAL/ bird or cattle
NO excrements
NI
24
NA6 MONTHS
10
NO
NI
NO
NI
12
16 DAYS TO
VISUAL
1 MONTH
IDENTIFICATION
3 TYPES OF TRAPSYES
11
NO
NI
1 INFORMATION
NO
/ Dormancy
3
3 MONTHS
TO LEESOTHER
THAN 6TRAPS
MONTHS
GERMINATION
12
NA
NA 1 INFORMATION
NA
/ Dispersal
NAtraits NA
NA
NA
13
NO
NI
NO
1 INFORMATION
EQUAL/ OR
Size
14LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
TRAYS TRAPS
14
NO
NA
NO
NI
5
12OTHER
monthsMETHODOLOGIES
NI
WITHOUT SEED TRAPS
15
N ONE
NO Birds, Ungulates,
1 INFORMATION
Sheeps,
NA
Rats,/ Humans,
Dispersal
NAWaterfowl
traits NA
NA
NA
16 ANIMAL / Ants,
NO
NI
NA
NI
NI
16 DAYS TO 1 MONTH
NI GAPS TRAPS
17
18
NO
NI
NO
NIEQUAL OR12LESS THAN 15GERMINATION
DAYS INTERVALS
FUNNEL
19
NO
2NIINFORMATION
NO / Dispersal
6 MONTHS
traits
12and
TOweight
LESS
VISUAL
THANIDENTIFICATION
12 MONTHS
OTHER TRAPS
20
ONE
NO ANIMAL / ANTS ONLY
NO
NIEQUAL OR6LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
2 TYPES OF TRAPSYES
21
GERMINATION
/ Dispersal
6 MONTHS
traits
TO LESS
size THAN
12 MONTHS
TRAYS TRAPS
NO
NI2 INFORMATION
NO
12 and
22
NO
NI
2
INFORMATION
NO
/
Dispersal
EQUAL
traits
OR
15
LESS
and
THAN
size
VISUAL
15
DAYS
IDENTIFICATION
INTERVALS
FUNNEL
TRAPS
23
GERMINATION
MORE THAN
3 MONTHS
TRAYSINTERVALS
TRAPS
NO
NI
NO
NI 1 MONTH
6 BUT LESS THAN
24
EQUAL
/ Releasing
OR3LESS
height
THAN 15 DAYSNI
INTERVALS
OTHER TRAPS
25
NO
NI 1 INFORMATIONS
NO
26
NO
NI
NO
NI
24
NI
NA
NA
27
MORE THAN
YES ONE ANIMAL/ Birds
1NO
INFORMATION
and
EQUAL
Ants OR LESS
/ Viability
THAN
6
15 DAYS INTERVALS
NI OR
TRAYS
MONTHLY
TRAPS
28
NO
NI
NO
NI 6 MONTHS
60 TO LESS THAN 12NI
MONTHS
TRAYS TRAPS
29
NO
NI
NO
NI
5
NI GERMINATION
STICKY TRAPS
30
/ Weight and
VISUAL IDENTIFICATION
TO LEESTRAYS
THAN TRAPS
6 MONTHS
NO
NI 2 INFORMATION
NO
2 to viability
5 3 MONTHS
31
YES
HERD /
NO
NI
6
3 MONTHS
TO
LEES
TRAYS
THAN
TRAPS
12 GERMINATION 6 MONTHS
32
NI
12
MONTHS
VISUAL IDENTIFICATION
2 TYPES OF TRAPS
NO
NI
NO
33
NO
NO
1NO
INFORMATION
EQUAL
/ Weight
OR24LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
34
35
MORE THAN
NO ONE ANIMAL1 /INFORMATION
Bats
NOand Birds / Dispersal816traits
DAYS TO
VISUAL
1 MONTH
IDENTIFICATION
OTHER TRAPS
36
NO
NA
NO
NI
8
3 MONTHS
VISUAL IDENTIFICATION
TO LEESSTICKY
THAN 6TRAPS
MONTHS
YES
37
/ Dormancy,
longevity and
16 DAYS
moisture
TO
VISUAL
1content
MONTH
IDENTIFICATION
FUNNEL TRAPS
NO3 INFORMATION
NI
NI
13
38
YES
HERD
/
cattle
1
NO
INFORMATION
/
Viability
NA
NA
NA
GERMINATION
39
NO
NO
1 INFORMATION
NO
EQUAL
/ Dormancy
OR13LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
40
41
NA
NA
YES
NI
NA
NA
NA
NA
42
NO
YES
2
NA
OTHER
NA METHODOLOGIES
NI
WITHOUT SEED TRAPS
43ONE ANIMAL/ ANTS
MORE THAN
removal
VISUAL
THANIDENTIFICATION
3 MONTHS
OTHERINTERVALS
TRAPS
NO ONLY _Ants posdispersal
NA
NI 1 MONTH
5 BUT LESS
44
ONE ANIMAL / Lizard
YES
NO
NI
NA
NA
NA
NA
45
NO
NI2 INFORMATION
NO
/ Dispersal traits
13
16 DAYS
and size
TO
VISUAL
1 MONTH
IDENTIFICATION
FUNNEL TRAPS
46
47
NO
NI
YES
MORE THAN
NI 1 MONTH
6 BUT LESS
VISUAL
THANIDENTIFICATION
3 MONTHS
OTHERINTERVALS
TRAPS
48
NO 2 INFORMATION
NI
NO/ Dispersal traits and816releasing
DAYS TO
VISUAL
height
1 MONTH
IDENTIFICATION
2 TYPES OF TRAPS
49
NO
NI
NO
NI
516 DAYS TO 1 MONTH
NI GAPS TRAPS
50
NO
NA
2
INFORMATION
NO
/
Dormancy
and
5
viability
3
MONTHS
TO
LEESTRAYS
THAN TRAPS
6 MONTHS
GERMINATION
51
52
STICKY TRAPS YES
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
NO
NI
NO
NIEQUAL OR6LESS THAN
53
NO
NI
NO
NI 1 MONTH
4 BUT LESS
MORE THAN
VISUAL
THANIDENTIFICATION
3 MONTHS
OTHERINTERVALS
TRAPS
54
55
VISUAL IDENTIFICATION
NO
NI
NO
NI
NA
NA
NA
56
57
58
59
60
Restoration Ecology
iew
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1
2
/ Size and viability
3 MONTHS TONI
LEESOTHER
THAN 6TRAPS
MONTHS
NO
NI 2 INFORMATION
NO
3
3
ONE
3 MONTHS TONI
LEESOTHER
THAN 6TRAPS
MONTHS
YES ANIMAL/ BIRDS ONLY
YES
NI
36
4
NI
5
3NA
INFORMATION
OTHER
traits
WITHOUT SEED TRAPS
NO
NO / Size, weight, dispersal
NA
NA METHODOLOGIES
6
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
YES HERD / sheep NO
NIEQUAL OR12LESS THAN
7
STICKY TRAPS YES
INTERVALS
NO
NI
YES
NIEQUAL OR5LESS THAN 15 DAYSNI
8
9
NO
NI
2 INFORMATION
NO
/ Releasing
6 MONTHS
height
12 TO
andLESS
sizeTHAN 12NI
MONTHS
OTHER TRAPS
10
1YES
INFORMATION / Viability
NO
NI
NA
NA
NI GAPS TRAPS
11
NOHERD
/
DONKEYS
NO
NI
EQUAL
OR
24
LESS
THAN
VISUAL
15
DAYS
IDENTIFICATION
INTERVALS
FUNNEL TRAPS
12
MORE THAN ONENO
ANIMAL / Birds andNO
Others
MORE vertebrates
THAN
NI 1 MONTH
31 BUT LESS
VISUAL
THANIDENTIFICATION
3 MONTHS
OTHERINTERVALS
TRAPS
13
14
1NO
INFORMATION / Weight
3 MONTHS
VISUAL IDENTIFICATION
TO LEESFUNNEL
THAN 6TRAPS
MONTHS
NO
NI
11
15
YESONE ANIMAL/
2 INFORMATION
BATSNO
/ Dispersal traits
12
16 DAYS
and size
OTHER
TO
VISUAL
1 MONTH
METHODOLOGIES
IDENTIFICATION WITHOUT SEED TRAPS
16
NO
NI
YES
NIEQUAL OR
6.5LESS THAN
VISUAL
15 DAYS
IDENTIFICATION
INTERVALS
STICKY TRAPS YES
17
1NO
INFORMATION / Weight
NO
NI
6
NI
NI STICKY TRAPS
18
19
LEES THAN /15Dispersal
DAYS 3OR
traits
3 MONTHS
VISUALTO
IDENTIFICATION
LESS
2 TYPES
THAN OF
6 MONTHS
TRAPSYES
NO
NI 1 INFORMATION
NO
20
21
GERMINATION
22
NO
NI
NO
NI
NA
NA
OTHER
METHODOLOGIES WITHOUT SEED TRAPS
23
TO 1 MONTH
NO
NI
NO
NI
0,5 16
to DAYS
1
NI STICKY TRAPS YES
24
25
26
27
28
29
30
31
32
33
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40
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Page 70 of 79
Meauseres standarization of the surfac
Traps above, at or under soil level
Restoration Ecology
Trap protection against GRANIVORES
Other methodologies without seed tra
Page 71 of 79
Traps Height ABOVE ground
Seed traps -Efficiency in
colecting seeds
Total number of traps
Other types of traps
TRAY AND GAP SOILS TRAPS
FUNNEL TRAPS
1
2
3
4
5
6
7
8
9
10
11
12
50
NI
NI
ABOVE
2 DIAMETER ONLY
13
COMPARASSION OF GROUND LEVEL AND ABOVE SOIL LEVEL
NA / Capture
2TESTED
to 60 success
(12 postions
NIwas strongly
- Aprox.influenced
2, 8, 13,
WIDTH
18,
by23,
the
AND
28,
height
LENGTH
34, 39,
from
44,which
49, 54,
see
6
14
252
TESTED
NI
NI
NI
WIDTH
AND
LENGTH
15
YES
Two categories: 40 to
TESTED
70
NI
ABOVE
1
NA
16
YES
NA
NI
NI GROUND LEVEL NA
NA
17
18
30
TESTED
NI GROUND LEVEL NA
NA
19
YES
80
NI
NI GROUND LEVEL NA
NA
20
FOCAL
OBSERVATION
NA
NA
NA
NA
NA
NA
21
85
TESTED
YES
ABOVE 20 to 40
NA
22
YES
ABOVE 1,5 to 2
NA
72
NI
23
24
NA
NA
NA
NA
NA
NA
25
NI
NI
NI
ABOVE
2DIAMETER AND AREA
26
NI
NIWIDTH AND LENGTH
40 MENTIONED YES
27
60
NI
NI
NI
NIWIDTH AND LENGTH
28
YES
20
NI
NI
NI
NI
NA
29
48 MENTIONED YES
ABOVE
0.5
NA
30
YES
NI
NI
NI GROUND LEVEL NA
NA
31
32
YES GROUND LEVEL NA
YES
42
NI
NA
33
YES
YES
NA MENTIONED NI
ABOVE 40 toWIDTH
45
AND LENGTH
34
YES
84
NI
NI
ABOVE
0.5
NA
35
YES
50
NI
NI
ABOVE
0.5
NA
36
YES
125
NI
NI
GROUND
LEVEL
NA
NA
37
38
YES
NI
NI
YES GROUND LEVEL NA
WIDTH AND LENGTH
39
YES
45
NI
ABOVE
50
NA
NI
40
NO
41
YES
ACCESS MENTIONED NI GROUND LEVEL NA
NA
42
NI
NI
NI
NI
NIWIDTH AND LENGTH
43
YES
50
NI
NI
ABOVE
0.5
NA
44
FOCAL OBSERVATION
NA
NA
NA
NA
NA
NA
45
46
NI
YES
14
NI
ABOVE
20
NA
47
YES
126 MENTIONED NI GROUND LEVEL NA
NA
48
NA
NA
NA
NA
NA
NA
49
FOCAL OBSERVATION
NA
NA
NA
NA
NA
NA
50
YES
240
NI
NI
NA
NA
NA
51
52
YES
ABOVE AND
0,1UNDER
to 15
YES
YES
NA MENTIONEDGROUND,
NA
53
YES
124 MENTIONED YES GROUND LEVEL NA
WIDTH AND LENGTH
54
SEED PRODUCTION
POTENTIAL AND SEED BANK DYNAMICS
YES
NA
NA
NA
NA
NA
NA
55
90
YES
15
NI
NI
ABOVE
NA
56
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60
iew
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Restoration Ecology
YES
YES
YES
YES
SEED PRODUCTION POTENTIAL
YES
YES
YES
YES
SOIL SEED BANK GERMINATION
YES
YES
YES
YES
YES
YES
YES
NI
NA
TESTED
NA
NA
NA
120
NI
NA
30
NA
NA
40
90
NI
108
100
32
NI
50
NA
NA
80
30
108
NI
NA
NI
NI
NA
NI
NA
NA
NI
NI
NI
NI
NI
NI
NI
NI
NA
NI
NI
NI
NI
NI
ee
YES
YES
YES
YES
YES
YES
SEED PRODUCTION POTENTIAL
YES
YES
YES
YES
YES
YES
YES
NI
NA
NA
NA
NA
NA
NI
NI
NA
NI
NA
NA
NI
NI
NI
NI
NI
NI
NI
NI
NA
YES
NI
NI
YES
NI
NA
NA
25WIDTH AND LENGTH
NI
NA
NA
NA
20
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
NA
NI DIAMETER ONLY
NI
NA
NA
NA
NA
NA
NI
NA
NA
NA
20
NA
NA
NA
NIWIDTH AND LENGTH
NA
NA
NA
NA
NI
NI
NI
NI
NI
NA
NI
NA
NA
NI
NA
NI
NI
NI
NI
NI
YES
NI
NI
NI
YES
NA
NI
NA
NA
YES
NA
YES
NI
YES
NI
NI
NA
ABOVE
NI
NA
ABOVE
NA
NA
GROUND LEVEL
GROUND LEVEL
NI
NI
NI
GROUND LEVEL
GROUND LEVEL
NI
NA
ABOVE
UNDER
NI
GROUND LEVEL
GROUND LEVEL
NA
NA
NA
NA
NA
GROUND LEVEL NA
NA
GROUND LEVEL NA
NA
ABOVE
50
NA
GROUND LEVEL NA
WIDTH AND LENGTH
ABOVE
50
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
ABOVE
0 to 4
NA
NA
NA
NA
ABOVE
50
NA
NI
NI
NA
ABOVE 20 to 70
NA
GROUND LEVEL NA
NA
NI
NI
NA
iew
YES
NA
60
216
50
108
NA
50
NA
NA
120
NA
108
NA
230
200
240
NI
NI
NA
NA
NI GROUND LEVEL
NA
NA
NA
NA
ev
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YES
YES
YES
NI
NA
24
NA
NA
rP
YES
Fo
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2
3
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Page 72 of 79
NI
NI
NI GROUND LEVEL NA DIAMETER ONLY
139
NI
NI
NI
NI
NA
NA
NA
NA
NA
NA
NA
Page 73 of 79
YES
NI
576
NI GROUND LEVEL NA
YEScategories: 182 to 265
Two
NI
NA
seed interception by different plant species
NA
NI
YES
30
24
240
YES
YES
YES
YES
YES
FOCAL OBSERVATION
YES
Fo
SEED BANK SURFACE
NI
NI
NA
YES
NA
NI
NA
NI
NA
NA
NA
NI
ABOVE
90
NA
NI
NI
NI
NI GROUND LEVEL NA
AREA ONLY
NA
NA
NI
YES
NI
NI
NA
64
NI
NI
ABOVE
90
NA
102 MENTIONED NI
ABOVE
2
NA
144
NI
NI
ABOVE 0,3 to 0,5
NA
NA
NA
NA
NA
NA
NA
36
NI
NI GROUND LEVEL NADIAMETER ONLY
90
NI
NI
NI
NIWIDTH AND LENGTH
NO
NI
ACCESS
NI
NI
NA DIAMETER ONLY
NA
84
NA
NI
NA
YES
NA
ABOVE
iew
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Restoration Ecology
NA
NA
5 DIAMETER ONLY
DIAMETER SURFACE of other traps
NA
NA
NA
NA
NA
NI
WIDTH AND LENGTH SURFACE of othe
NA
NA
NA
NA
NA
NI
MEAUSERES STANDARIZATION OF the
Meauseres standarization of the funne
NA
NA
NA
NA
NA
AREA ONLY
total area (m²) SURFACE of funnel trap
total area (m²) surface of sticky
NI
NI
NI
NA
NA
NA
DIAMETER SURFACE of funnel traps
Diameter surface of sticky traps
9 cm
NI
NI
NA
NA
NA
WIDTH AND LENGTH SURFACE of funn
Witdth and Length surface of sticky tr
NI
5x4
10x10
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
DIAMETER AND AREA
NI
8.5 cm
NA
WIDTH AND LENGTH
0.5 m x 0.5 m
79cm²
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
10 cm
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
WIDTH-LENGTH
NA
AND5.5x5.5
AREA
NI
0.30 m2
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
10 cm
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
14 cm 0,8624 m²
NA
NA
NA
NA
NA
NA
NA
5 cm x 1 cm NA
NA
NA
NA
NA
NA
NA
9X1.5
NI
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
AREA
NI
NI
40.7 cm2
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
6.3 cm
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
314.15 cm²
cm2 per plot
NA
NA
NA AREA ONLY
NI
NIper trap and 1885 NA
NA
NA
30x30
NI
NI
DIAMETER AND AREA
NI
23 cm 416 cm2
NI
NA
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
3.2 cm
NA
NA
NA AREA
ONLY
NI cm² per plot or 0.21%
NA of theNA
NA
104
cm² perNItrap and 520
total surface
NA
NA
NA
DIAMETER AND AREA
NI
10 cm
0.2 m2
NA
NA
NA
15x15
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
9.5X9.5
NA
NA
NA
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
5x100
NA
NA
NI
NI
NA
NA
NI DIAMETER ONLY NI
NI DIAMENTER ONLY NI
NA
NA
NA
NA
DIAMETER AND AREA
NI
NA
NA
iew
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Restoration Ecology
NA
NA
NA
NA
24 cm
NA
NA
NA
NA
NA
NA
NA
AREA ONLY
NA
NI
NA
NI
NA
NA
NA
NA
NA
WIDTH AND LENGTH
9.5 X 9.5 cm
NA DIAMETER ONLY NI
11.5 cm
NA
NA
NA
NA
NI
NA
NA
NA
NA DIAMETER ONLY NI
11 cm
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
15 to 10 cm NI
2.2 cm
NI
NA
NA
24 cm 452 cm2
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
Page 74 of 79
Page 75 of 79
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
15x15
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
10×6
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
14 cm
NA
NA
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NI DIAMETER ONLY NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
AREA
NI
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
20X30
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
NA
NA
NA
NI
NA
NA
DIAMETER AND AREA
NA
NI
NA
NA
NA
NA AREA ONLY
NI
NA
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
DIAMETER AND AREA
NI
NA
NA
NA
NA AREA ONLY
NI
NA
NA
NA
NA
NA
NA
NA
8.5 cm
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
WIDTH AND LENGTH
10 x 6 cm
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
NA
AREA ONLY
NA
NA
NI
NA
NI
NA
NA
NI
NA
NI
NA
NA
NA
NA
NA
NA
NA
10 cm
NI DIAMETER ONLY NI
10 cm
NA
NA DIAMETER ONLY NI
9 cm
NA
NA
NA
NA
NA
NA
WIDTH,
NA LENGTH 3,6m2
AND
90×40cm
AREA
TOTAL AREA COVERED IN EACH V
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA AREA ONLY
NI
NI
NA
NA DIAMETER ONLY NI
10 cm
NA
NA
NI
NI
NI
NA
NA DIAMETER ONLY NI
5 cm
NA
NA AREA ONLY
NI
NI
10 cm
NI
NA
NA
NA
NA DIAMETER
NA AND OTHER MEASURES 0.3 cm
NA
NA
WIDTH AND LENGTH
30 x 30 x 8 cm
NA
NA
NA
NA
NA
NI
0.14 m²
NA
NA
NA
NA
NA DIAMETER ONLY NI
55 cm
NA
NA
NA
NA
NA
AND 53
OTHER
× 27 MEASURES
× 10–cm3
NAWIDHT LENGHT
NA
NA
NA
WIDTH AND
8 x LENGTH
8 cm by 7 cm depth
NI
ev
rR
ee
rP
Fo
10 cm
NA
NA
22 cm
NA
NI
NA
NA
DIAMETER ONLY NI
NI
NA
NA
NA AREA ONLY
NI
NA
NA
NA
0.038 m2
NA
NA
NA
NA
NA
0.452 m²
NA
NA
NA
NA
NA
NA
NA
NA
DIAMETER ONLY
iew
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Restoration Ecology
10 cm
NA
NI
NA
NA
NA
NA
NA
NA
13 cm
NA
NA
NA
NA
NA
NA
22 cm 0.038 m2
NA
NA
NA
NA
WIDTH AND LENGTH
20 x 20 cm
NI
254 cm² and 1385 cm²
NI
DIAMETER
AND
OTHER
MEASURES 26 cm
NA
NA
NA
NA
NA
NI
NI
NA
NA
NI
NA
NA
Restoration Ecology
NA
NA
NA
NA
NA
NA DIAMETER ONLY NI
3.6 cm
NA
NA
NA
NA
NA
NA
NA
NA
44 cm
NA
NA
NA
NA
AREA ONLY
NA
NA
NA
DIAMETER AND AREA
NI
NA
NA
NA
NA
NA
m² per plotNA
NI0,0452 m²NIper trap and 0.452 NA
NI
NA
NI
NA
0.1 m2
NA
NA
NA
NA
NA
NA
NA
NA
NI
10×6
NA
NA
NA
NA
NA
18 cm
NI
WIDTH AND20LENGTH
x 20 cm quadrat
NA
NA
NA
NA
NA
NA AREA ONLY
NI 0,011 m²NIper trap or 0.362 m²
NAper plotNA
NA
NA
NA
NA
NA
NA
DIAMETER AND AREA
NI
15 cm
NA DIAMETER ONLY NI
6.7 cm
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NI
NA
NA
NA
NA
NA
NA
NA
NI
14 cm
NI
NA
NA
NA
NA DIAMETER ONLY NI
NA
NI
NA
3,8 cm
NA
NI
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NI
NA
WIDTH AND LENGTH
8x8x10 cm
NA
NA
NA
iew
ev
rR
ee
rP
Fo
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 76 of 79
NA
NA
NI
14 cm
NA
Seeds dispersed by
granivore
NI
NI
NI
NI
NI
NA
TOTAL
NI NUMBER AND DENSITY
NI DENSITY ONLY
MENTIONED
TOTAL NUMBER AND DENSITY
MENTIONED
TOTAL NUMBER AND DENSITY
NI DENSITY ONLY
MENTIONED NA
NA
NI
NI
NI
NA
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NA
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NA
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
TOTAL NUMBER ONLY
TOTAL
NI NUMBER AND DENSITY
NI
TOTAL NUMBER ONLY
NI
NA
NI
NA
MENTIONED
DENSITY ONLY
NI DENSITY ONLY
NI DENSITY ONLY
NI
NA
NI
TOTAL
TOTAL
NI NUMBER AND DENSITY
MENTIONED
TOTAL NUMBER AND DENSITY
NI DENSITY ONLY
NI DENSITY ONLY
MENTIONED
TOTAL NUMBER AND DENSITY
TOTAL
NI NUMBER AND DENSITY
NI
NI
NI
NA
NI
NI
NI
NA
NI
NI
NI
NA
NI
ev
rR
ee
NI
NA
Average distance of
dispersal
Seeds dispersed by
frugivore
Seeds dispersed by wind
MAIN WIND direction
NI
NI
NI
NI
NI
NA
rP
Fo
NI
NI
NI
NI
NI
NA
iew
1
2
3
4
5
6
7
8
9
10
11
12
MENTIONED
NA
OR CONSIDERED
NI
NI
13
NA
NI
NI
NI
14
NA
NI
NI
NI
15
a total
surface
area
in
each
MEASUR
plot
of
283.5
cm²
NI
to
567
NI
cm²
16
NI
NI
NA
17
18
NA
NA
NI
NI
19
NI
NI
NA
NI
20
NA
NA
NA
NI
21
NA
NI
NA
NI
22
NA
NA
NI
NI
23
24
NA
NA
NA
NA
25
NA
NI
0°
NI
26
NI
NI
NI
27
NA
NI
NI
NI
28
NA
NI
NI
NA
29
NA
NI
NI
NA
30
NA
NI
NI
NA
31
32
NA
NI
NA
NI
33
NI 0° AND 90°
NI
34
NI
NI
NI
NA
35
NA
NI
NI
NA
36
NA
NI
NI
0°
37
38
NA
NI
NA
NI
39
0.25-m2
NI
NA
NI
40
41
NA
NI
NA MENTIONED
42
NI
NI
NI
43
NI
NI
NI
NA
44
NA
NA
NA
NI
45
46
NA
NI
NA MENTIONED
47
NI
NI
NI
NA
48
NA
NI
NI
NI
49
NA
NA
NA
NI
50
NA
NI
NA
NI
51
52
NA
NI
45° MENTIONED
53
NA
NI
NI
NI
54
NA
NA
NA
NI
55
NA
NA
NI
NI
56
57
58
59
60
Number of seeds or
seedlings counted in seed
rain
Restoration Ecology
Seeds dispersed by water
SLOPING at aN ANGLE (only for sticky t
total area (m²) SURFACE of other traps
Page 77 of 79
NI
NI
NI DENSITY ONLY
MENTIONED
MENTIONEDTOTAL
NI NUMBER AND DENSITY
NI
NI
NI DENSITY ONLY
NI
NI
NI DENSITY ONLY
NI
NI
NI DENSITY ONLY
MENTIO
NA
NI DENSITY ONLY
NI
NI
NI DENSITY ONLY
NI
NI
TOTAL
NI NUMBER AND DENSITY
NI
NI
NI
NA
MENTIONED
MENTIONEDTOTAL
NI NUMBER AND DENSITY
NI
NI MENTIONED
TOTAL NUMBER ONLY
MENTIO
NED
NI
NA
NI
NI
NI
NA
NI
TOTAL NUMBER ONLY
NI
MENTIONED
TOTAL NUMBER AND DENSITY
NI
NA
NI DENSITY ONLY
Restoration Ecology
iew
ev
rR
ee
rP
Fo
1
2
NA
NI
NI
NI
NI
NI
NI
NI DENSITY ONLY
3
NA
NA
NA
NI
NA
NA
NA ESTIMATED NA
4
DENSITY ONLY
1.5MENTIONED
to 2.0 m2 OR CONSIDERED
NI
NI
NI
NI
NI MENTIONED
5
NA
NA
NA
NI
NI
NI
NI
NI DENSITY ONLY
6
7
NA
NA
NA
NI
NA
NA
NA
NI DENSITY ONLY
8
9
NA
NA
NA
NI
NA
NA
NA
NI
NA
10
MENTIONED
NI
OR CONSIDERED
45°
NI
NI
NI
NI MENTIONED
TOTAL NUMBER AND DENSITY
11
NI
NA
NI
NA
NA
NA MENTIONED
TOTAL NUMBER ONLY
MENTIONED
OR CONSIDERED
12
NA
NA
NA
NI
NA
NA
NA
NI
NA
13
OTAL AREA COVERED IN EACHNIVEGETATION
NA TYPE NI
NI
NI
NI
TOTAL
NI NUMBER AND DENSITY
14
NA
NA
NA
NI
NI
NI
NI MENTIONED
DENSITY ONLY
15
NA
NA
NA
NA MENTIONED NA
NA
NI DENSITY ONLY
16
0.25 m2
NI
NI
NI
NI
NI
NI DENSITY ONLY
NA
17
18
NI
NI
NI_ possibly surface run-off
NI MENTIONED NI DENSITY ONLY
NA MENTIONED
19
NI
NI
NI
NI
NI
NI
NI
NI
NA
20
NI
NI
0°
NI
NI
NI
NI
NI
TOTAL
21
0.5 dm2
NI
NA
NI
NI
NI
NI
NI DENSITY ONLY
22
NA
MEASURED
NA
MENTIONED
NI
NI
NI
MENTIONED
TOTAL NUMBER ONLY
23
TOTAL NUMBER AND DENSITY
NI
NA MENTIONED NI
NI
NI ESTIMATED
24
25
NI
NA
NI
NI
NI
NI MENTIONED
DENSITY ONLY
26
NA
NI
NI
NI
NI
NI
NI
NI DENSITY ONLY
27
NA
NI
NA
NI
NA MENTIONED
MENTIONED NI
NA
28
NI
NI
NA
NI
NI
NI
NI
NI DENSITY ONLY
29
NA
NI
NI
NI
NI
NI
NI DENSITY ONLY
NA
30
NA
NI
NI
NI
NI
NI
NI DENSITY ONLY
31
NI
NI
NA
NI
NI
NI
NI
NI
TOTAL NUMBER
TOTAL ONLY
32
MENTIONED
OR CONSIDERED
NI
NI
NI
NI MENTIONEDNUMBER
NI
NA
33
NA
NI
NI
NI
NI DENSITY ONLY
34
NA MENTIONED NI
35
m2 per trap and 1,128m2 to 2,256m2
NI
per
NAplot
NI
NA
MENTIO
NA
TOTAL
NI NUMBER AND DENSITY
36
NA
NI
NI
NI
NI
NI
NI
NI DENSITY ONLY
37
NA
NA
NI
NI
NI
NI
NI
NI DENSITY ONLY
38
NA
NA
NA
MENTIONED
NA
NA
NA
MENTIONED
NA
39
NA
NI
NA
NI
NI
NI
NI
TOTAL
NI NUMBER AND DENSITY
40
41
NA
NA
NA
NI
NA
NI
NI
TOTAL
NI NUMBER AND DENSITY
42
NA
NA
NA
NI
NI
NI
NI
TOTAL
NI NUMBER AND DENSITY
43
NA
TOTAL NUMBER ONLY
NI
NI
NI
NI
NI
NI
44
NA
NA
NA
NI
NA
NA
NA
NI
NA
45
NA
NI
NI
NI
TOTAL
NI NUMBER AND DENSITY
NA MENTIONED NI
46
47
NI
NI
NI
NI
NI MENTIONED
TOTAL NUMBER ONLY
NA
48
MEASURED NI MENTIONED NI
NI
NI ESTIMATED
TOTAL NUMBER ONLY
49
NI
NA
NI
NI
NI
NI
NI DENSITY ONLY
50
NI
NI
NA
NI
NI
NI
NI
NI
DENSITY ONLY
51
52
NI
NI
NI
NI
NI
NI
NI
NI DENSITY ONLY
53
NA
TOTAL
NI
NI
NI
NI
NI
NI NUMBER AND DENSITY
54
55
NA
NI
NI
NI
NI
NI
NI
NI
NA
56
57
58
59
60
Page 78 of 79
Page 79 of 79
NA
NI
NI
NA
NA
NI
NI
NA
NI
TOTAL NUMBER ONLY
NI
NA
NA
NI
MENTIO
NED
NA
NA
NA
NI
NI
NI
NI
TOTAL NUMBER ONLY
NI
NI
NA
NI DENSITY ONLY
NI
NA
NI
NI
NI
NI
NI
NI
NI
NI
NI DENSITY ONLY
MENTIONED
TOTAL NUMBER AND DENSITY
NA
NA
NA
NA
NI
NI
NA
MENTIONED
NI
MENTIONED
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
MENTIONED
NI
NI
NI
ESTIMATED
TOTAL NUMBER ONLY
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
TOTAL NUMBER ONLY
NI
NI DENSITY ONLY
NI
NI
NI DENSITY ONLY
NI
NI MENTIONED
DENSITY ONLY
MENTIONED
MENTIONED
ESTIMATED
DENSITY ONLY
NI
NI
NI DENSITY ONLY
NI
NI
NI
TOTAL NUMBER ONLY
NI
NI
NI
TOTAL NUMBER ONLY
NI
NI
NI
NI
iew
ev
rR
ee
rP
Fo
1
2
NI
NI
3
0.15 m2
NI
4
5
NA
NA
6
NA
NI
7
NI
NI
8
9
NI
10
NI
11
NA
NI
12
1.8 m2 FOR ALL TRAPS (102NITRAPS)
13
14
NA
NI
15
NA
NI
16
NA
NI
17
NA
NI
18
19
NI
NI
20
21
22
NI
23
NA
NI
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Restoration Ecology