How have we studied seed rain in grasslands and what do we need to improve for better restoration?

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Ecology of seed dispersal

Seed dispersal

Plants are sessile organisms, and apart from a small number of species that are able to disperse via vegetative fragmentation (particularly aquatic species), plants depend mostly on seeds to disperse (Kraft & Ackerly 2014). Seeds are the products of sexual reproduction in most vascular plants and are the means by which plants produce offspring capable of disperse (Vander Wall et al. 2005). We can simply define seed dispersal as movement of seeds with potential consequences for gene flow across space (Vellend 2010; Kraft & Ackerly 2014). On the other hand, seed dispersal can be seen as a complex process, represented by multiple stages (departure, transfer and settlement) and influenced by a wide variety of mechanisms and factors (Burgess et al. 2016). Consequently, distinguishing the effects of diverse mechanisms and factors influencing seed dispersal in plant communities, and analyzing their implications in plant assembly and recruitment, is a challenging task in seed ecology (Schupp et al. 2010; Arnan et al. 2012; Török et al. 2018).
Seed dispersal represents the first step for recruitment in plant communities, influencing plant demography and spatial distribution (Jordano et al. 2007; Schupp et al. 2010). A successful seed dispersal event consists of a displacement from a source into a site (the seed shadow) where a seed can than germinate and establish (Jordano et al. 2007). On the other hand, dispersal may be a risky choice for the plants considering that the elevated investment in reproduction may not always result in dispersal success (Ronce 2007). Seed mortality may be high in some plant communities due to non-favorable habitat conditions and to predation (Ims & Andreassen 2000; Hanski et al. 2000), and may greatly vary between species, ecosystems and habitats (Matter 2006; Schtickzelle et al. 2006). Because seed fate is potentially influenced by many factors and mechanisms that shape plant community assembly, methods to quantify and qualify the spatial and temporal seed dispersal dynamics are of extreme relevance (Russo et al. 2006).

Studying seed dispersal

To quantify the spatial distribution of seed dispersal (seed shadow) and summarize the consequences of dispersal movements two metrics are often used: dispersal rate and dispersal kernel (Bowler & Benton 2005; Ronce 2007). Dispersal rate describes the expected proportion of seed arrival in an area over the time (Robledo-Arnuncio et al. 2014). On the other hand, dispersal kernel represents the probability for a seed to disperse to any position relative to the maternal plant and its consequences on seed fate (Klein et al. 2013). We can estimate these dispersal metrics by direct observation of diaspores deposition or by tracking individual diaspores (Cousens et al. 2008; Jones & Muller-Landau 2008). However, as seed dispersal is expected to be influenced by a vast diversity intrinsic (e.g. phenotype) and extrinsic variables (e.g. human disturbance), direct measurements is notoriously challenging (Russo et al. 2006; Ronce 2007).
Studying seed dispersal dynamics in plant communities does not simply imply quantifying dispersal rates and kernels of single species, but also assessing how seed dispersal metrics can vary across plant species, environmental conditions and time (Ronce 2007). Consequently, the measurement of dispersal dynamics in plant communities can demand great methodological efforts and be challenging to interpret (Clobert et al. 2001; Ronce 2007). For example, diaspore-animal interactions (e.g. secondary seed removal and seed predation) and abiotic factors (e.g. wind and water dynamics in the landscape), may greatly vary across time and space between and within ecosystems and plant species (Levin & Muller-Landau 2000; Westcott et al. 2005; Nathan 2007; Jordano et al. 2007; Burgess et al. 2016), challenging our ability to measure, estimate and compare seed dispersal dynamics (Robledo-Arnuncio et al. 2014).

Dispersal over time and space

Dispersal can greatly vary over time and space due to variation in mechanism and factors influencing seed dispersal across these scales (Robledo-Arnuncio et al. 2014). Thus, assimilate comprehensive temporal and spatial scales, may be a critical step to obtain accurately estimates and ecological inferences about seed dispersal in plant communities (Kraft & Ackerly 2014). Temporal issues, such as dispersal fluctuations across seasons, can be crucial in predicting plant community assembly and recruitment success, but have received much less attention than spatial aspects in seed dispersal (Robledo-Arnuncio et al. 2014).
The spatial pattern of seed deposition may mediate the probability of success of dispersal through its outcomes on deposition in a favorable site (e.g. germination gaps) and on post-dispersal interactions with ground foraging animals (Rico-Gray & Oliveira 2007; Christianini & Oliveira 2009). The predominance of short distance dispersal events in plant communities may affect plant persistence, migration and seedling recruitment in disturbed areas (Thomson et al. 2011; Török et al 2018). On the other hand, despite the fact that most seeds travel only a short distance, some seeds can present remarkable ability to achieve long-distance dispersal events (Kraft & Ackerly 2014). Spatial and temporal aspects, such as environmental conditions (e.g. disturbance) and seasons (e.g. rainy season) may greatly influence qualitative and quantitative aspects of seed dispersal (Robledo-Arnuncio et al. 2014). Hence, taking into account both spatial and temporal dispersal patterns between plant species can be a crucial step on studies about seed dispersal (Thomson et al. 2011; Tamme et al. 2014).

Dispersal across plant species

Variation in dispersal potential across plant species can be substantial (Dalling et al. 2002; McEuen & Curran 2004), resulting in potentially large differences in recruitment capacity (Vittoz & Engler 2007; Thomson et al. 2010; Tamme et al. 2014). Variation in dispersal potential may be a result of how physical (e.g. ballistic mechanisms and floatability) and biological (e.g. diaspore-animal interactions) components of seed dispersal may vary between plant species (Burgess et al. 2016). For example, wind-dispersed species normally presents small seeds and/or dispersal structures (e.g. wings) to travel long distances in the wind (Ganeshaiah & Shaanker, 1991). Additionally, diaspores from different species may greatly differ in their interactions dynamics with animals, directly influencing the quantitative and qualitative outcomes for seed dispersal success (Jordano et al. 2007; Schupp et al. 2010).
In the case of animal-diaspore interactions, dispersal dynamics may be a result of animals’ preferences for habitats and diaspores (Vander Wall 1997; Rodríguez-Pérez et al. 2012). Seed predators may target specific species (Roselli 2014), influencing in different ways the role of seed limitation in natural recovery across species. On the other hand, seed dispersers may increase seed survival and germination by foraging on fruit and cleaning seeds (Christianini et al. 2007) or depositing seeds in favorable locations (Sternberg et al. 2007, Arnan et al. 2012).
Directed dispersal represents the arrival of seeds in a particular location and can direct influence seed dispersal success (Wenny 2001; Christianini et al. 2007). Directed dispersal can be partially explained by the way in which seed movement is affected by disperser behavior (e.g. ants carrying seeds to dump-piles) and habitat conditions (e.g. wind dynamics) (Schurr et al. 2005; Trakhtenbrot et al. 2014) and is a common process in seeds dispersed by wind, water run-off or animals (Robledo-Arnuncio et al. 2014; Chabrerie & Alard, 2005; de Rouw et al. 2018). However, less evident is the relative influence of habitat conditions (e.g. disturbance) on directed dispersal by wind and water run-off (Chabrerie & Alard, 2005; de Rouw et al. 2018).

Seed rain

Seed rain is the number of seeds reaching an area, and it usually is quantified and qualified by placing traps in the plant community to catch seeds that then are identified and counted (Baskin & Baskin 2014). Seed rain is thus a measurement of seed dispersal rates, representing species dispersal potential in time and space (Page et al. 2002). As an important component of seed dispersal, seed rain measurements can provide crucial information on successional trajectories, thereby being a useful tool to assess recovery potential in disturbed areas (Turnbull et al. 2000; Török et al. 2018). Seed rain can been analyzed both (1) indirectly, by studies of plant reproductive potential (Boughton et al. 2016) and seed bank dynamics (Bertiller & Aloia 1997), and (2) directly, by collecting either seeds visible on the ground, by observing the movements of granivore animals (Izhaki et al. 1991), or from diaspore traps (Kollmann & Goetze 1998).

Secondary seed dispersal

Secondary seed dispersal can be defined as the relocation of a diaspore dispersed to a given area by a different factor responsible for the primary seed dispersal and which may reshape seed shadows and strongly influence plant community assembly (Christianini & Oliveira 2009; Robledo-Arnuncio et al. 2014). Empirical studies examining secondary seed dispersal showed important variability among diaspores and sites (Schupp et al. 2010). Abiotic (e.g. water run-off) and biotic (animal-diaspore removal) factors may provide by secondary dispersal an increase in seed dispersal success expanding seed shadow and survival or hampering seed dispersal success (e.g. seed predation) (Rico-Gray & Oliveira 2007; Sternberg et al. 2007, Arnan et al. 2012).
As diaspores constitute a highly nutritive food resource for animals (Thorsen at al. 2011; Schowalter 2016), secondary dispersal by animals is of great relevance on plant community assembly and plant recruitment in disturbed systems (Martinson & Fagan 2014). The ways in which vertebrates and invertebrates interact with diaspores have been crucial to the development of theoretical models about seed dispersal and predation (Nathan & Casagrandi 2004). By moving seeds, ground foraging animal seed predators can accidentally work as seed dispersers and even facilitate seed germination (Rico-Gray & Oliveira 2007; Gómez et al. 2019), thus promoting regeneration (Schupp 1988).

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Seed dispersal and restoration

Dispersion is the first mechanism to act when colonizing a new biotope (Török et al. 2018). From the moment that only a fraction of the total species pool is able to reach a particular site (i.e. available species), a better understanding about the biotic and abiotic drivers and filters that are governing or limiting plant recovery is crucial (Prach & Pyšek 2001; Török et al. 2018). Understanding to what extent anthropogenic modifications are relevant to seed limitation is fundamental to predict the capacity of ecosystems to respond to anthropic changes (Török et al. 2018). For example, prior to restoration, seed rain and secondary seed dispersal can be evaluated in order i) to assess the potential for regeneration or passive restoration and ii) to plan restoration actions (Jacquemyn et al. 2011; Pardini et al. 2017; Török et al. 2017), because they allow i) better understanding of ecological processes and ii) therefore adjustment of management.
The effects of dispersal on vegetation recovery dynamics still need to be better explored (Török et al. 2018). For that, the development of studies about seed rain dynamics, dispersal vectors and seed disperser networks are crucial to a better understand of the consequences of human disturbance on dispersal dynamics (Robledo-Arnuncio et al. 2014). In seed-limited ecosystems, any reduction in seed quantity (e.g., seed predation) may compromises plant recruitment, while processes that increase seed dispersal success may prompt plant recruitment (Calviño-Cancela 2007). Thus, better understanding the mechanisms controlling seed dispersal (e.g. dispersal agents) and those outcomes (e.g. benefits and costs) is crucial for restoration practices in seed-limited ecosystems (Arnan et al. 2012; Dayrell et al. 2016; Török et al. 2018).

Seed dispersal in campo rupestre

Campo rupestre

The Brazilian campo rupestre is an OCBIL – Old Climatically-Buffered Infertile Landscape (sensu Hopper et al. 2016), that encompasses old-growth fire-prone tropical grasslands associated to extremely poor soils on ancient mountaintops (Fig. 3) (Silveira et al. 2016). Campo rupestre vegetation harbors a highly diversified flora with remarkable levels of plant endemism (Echternacht et. al. 2011; Colli-Silva et al. 2019) and is characterized by a predominantly herbaceous stratum, with shrubs and herbs associated to rocky outcrops and shallow soils with low nutrient contents (Giulietti et al. 1997; Oliveira et al. 2015). Despite campo rupestre be geologically and floristically associated to the Cerrado and Caatinga biomes (Moro et al., 2015; Neves et al., 2018), several authors highlight the singularities of campo rupestre vegetation and indicate it as a unique bioregion (Prance 1994; Zappi et al., 2017; Colli-Silva et al. 2019).
Campo rupestre vegetation occurs between 800 and 2,000m altitude and is especially found along the Espinhaço Range (Fernandes 2016), a mountain range that extends almost continuously for over 1,200 km2 from southeast to northeast Brazil and represents an enclave between the Atlantic Forest, Cerrado and Caatinga biomes (Conceição et al. 2016). The Espinhaço Range is mostly composed by Precambrian quartzite outcrops originating from ancient sea floor and desert deposits, and that evolved under tectonic and climatic stability, representing one of the most ancient landscapes on earth (Conceição et al. 2007; Barbosa et al. 2015).
The extreme weathering dynamics combined with the nature of the nutrient-poor parent rocks from the Espinhaço Range, results in shallow, acidic, excessively drained and nutrient impoverished soils (Benites et al. 2007; Oliveira et al. 2015). In this bioregion, the combination of ample altitudinal and latitudinal ranges, topographic aspects (e.g. isolation among vegetation islands), historical climatic and biogeographic stability, high habitat heterogeneity and strong soil nutrient limitations are recognized as the main reason for the extraordinary floristic richness and endemism of campo rupestre (Silveira et al. 2016; Colli-Silva et al. 2019).
Campo rupestre vegetation is amongst the most biologically diverse and unique in the world, harbouring more than 6,000 plant species with some families reaching up to 80−90 % of endemism (Echternacht et al. 2011; Silveira et al. 2016). Despite its high richness and plant heterogeneity, some plant families and genera confer a certain unicity to this bioregion, such as: Velloziaceae (e.g. Vellozia), Xyridaceae (Xyris) and Asteracae (Lychnophora) (Mello-Silva et al. 2011; Colli-Silva et al. 2019). While some plant families in campo rupestre are extremely rich (e.g. the ten richest families account for more than a half of the flora in campo rupestre), almost 1/4 of the plant families are represented by a single species (Colli-Silva et al. 2019). The families Eriocaulaceae, Velloziaceae and Xyridaceae have their centre of diversity in the campo rupestre, presenting high levels of endemism and many narrowly endemic species (e.g. species occurring in single location or population) extremely threatened by human-caused disturbance (Costa et al. 2008; Echternacht et al. 2011).

Campo rupestre resilience to human-caused disturbance

The vulnerability of mountain ecosystems to human-caused disturbance is well recognized (Jacobi et al. 2007; Foggin 2016), posing great challenges for conservation and restoration attempts (Buisson et al. 2019; Le Stradic et al. 2018b). The Espinhaço Range harbors not only a biological treasure but huge reserves of gold, diamonds and iron (Fernandes et al. 2016), which are the main reasons for the fact that more than 20% of campo rupestre natural areas have been impacted by human activities since the 18th century (Magnanini, 1961; Fernandes et al. 2016). Human-caused disturbances in campo rupestre have intensified along the past decades, especially by urban expansion, quarrying and mining activities, and drastically hampering plant communities’ dynamics in these disturbed sites (Barbosa et al. 2010; Fernandes et al. 2018).
Plant communities from campo rupestre, although highly resilient to endogenous disturbances (e.g. fire), are extremely vulnerable to human-caused exogenous soil disturbances (Le Stradic et al. 2018b; Buisson et al. 2019). Le Stradic et al. (2018b) showed that plant communities colonizing quarrying (inducing the destruction of vegetation and upper soil horizons) remained very different from reference sites even eight years after degradation, with almost no recovery of the natural vegetation. Generally speaking, for grasslands, after topsoil disturbance, the internal species pool (i.e. remaining vegetation, seed bank) is often reduced or even absent and natural recovery depends mainly on seed dispersal from surrounding sites via the seed rain (Bakker et al. 1996; Campbell et al. 2003; Shu et al. 2005; Buisson et al. 2006; Török et al. 2018).
Growing evidences suggest that the low resilience of campo rupestre vegetation to soil disturbance can be closely linked to seed dispersal limitation and environmental filter related to the extreme harshness in disturbed sites, which may hinder seed germination and plant establishment (Coelho et al. 2008; Garcia et al. 2012, 2014; Silveira et al. 2012a). However, we still have a lot to advance to understand what mechanisms and factors hamper recovery in campo rupestre, especially those related to seed dispersal limitation (Le Stradic et al. 2018b).

Table of contents :

1. Grassland resilience
1.1 Resilience
1.2 Old-grow grasslands resilience
2. Vegetation dynamics
2.1 Plant community assembly
2.2 Dispersal filter
3. Ecology of seed dispersal
3.1 Seed dispersal
3.2 Studying seed dispersal
3.3 Dispersal over time and space
3.4 Dispersal across plant species
3.5 Seed rain
3.6 Secondary seed dispersal
3.7 Seed dispersal and restoration
4. Seed dispersal in campo rupestre
4.1 Campo rupestre
4.2 Campo rupestre resilience to human-caused disturbance
4.3 Seed dispersal dynamics in campo rupestre
4.4 Seed dispersal limitation in campo rupestre
5. Study area
6. Objectives
CHAPTER 1 – How have we studied seed rain in grasslands and what do we need to improve for better restoration?
1. Abstract
2. Conceptual implications
3. Introduction
4. Material and methods
4.1. Literature Survey and Grassland Classification
4.2. Relevance of Seed Rain Studies to Restoration Ecology
4.3. Methodological Design
4.4. Methodologies and Data Reporting
5. Results
6. Discussion
6.1. General and Biogeographical Information
6.2. High Diversity of Estimates of Seed Rain
6.3. Sampling Effort and Lack of Standardization in the Use of Seed Traps
6.4. Methodologies and Data Reporting
6.5. Implications and Guidelines for Future Seed Rain Studies
CHAPTER 2 – A simple standard test to evaluate the efficiency of seed traps and of a seed sorting method to assess seed rain in a tropical grassland
1. Abstract
2. Introduction
3. Description and implementation
3.1. Seed traps
3.2. Standardized protocol
3.3. Proof of control
4. Results
5. Discussion
6. Conclusions
CHAPTER 3 – How can seed rain dynamics in disturbed and preserved areas help to understand the resilience of a megadiverse tropical grassland?
1. Abstract
2. Introduction
3. Material and methods
3.1. Study region
3.2. Sampling design
3.3. Statistical analyses
4. Results
4.1. Seed rain richness and diversity
4.2. Seed rain according to plot and seed trap
4.3. Temporal patterns of seed rain
4.4. Seed rain and floristic similarity between plot types
5. Discussion
6. Conclusions
CHAPTER 4 – Topsoil removal compromises campo rupestre regeneration by reshaping diaspore fate and interactions with potential ground-dwelling dispersers
1. Abstract
2. Introduction
3. Material and methods
3.1. Study area
3.2. Diaspores from native species
3.3. Sampling design
3.4. Statistical analyses
4. Results
4.1. 48-hour removal trial experiment
4.2. Diaspore observation experiment
4.3. Ant diaspore interactions
5. Discussion
6. Conclusions


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