Restoration of campos rupestres: species and turf translocation as techniques for restoring highly degraded areas.

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Main processes controlling savannas

At the beginning of the 20th century, the climatic theory (i.e. the presence of a dry season during winter as a driver for savanna formation) was a popular explanation for the origin of savannas (Beard 1953). More recently, various alternative hypotheses have been proposed, with current debate seeming fall under two main schools of thought: one favoring a bottom-up model (formation and regulation by, e.g., water and soil nutrients); and the other, top-down (formation and regulation principally through fire and herbivory) (Bourlière et Hadley 1970, Sarmiento 1984, Collinson 1988, Mistry 2000, Van Langevelde et al. 2003, Bond & Keeley 2005, Scanlon et al. 2005, Bond 2008, Midgley et al. 2010) (Figure 8). The details of, and some of the problems with, the main competing hypothesis can be summarized as follows:
1) Climate: Savannas only occur in climates characterized by the alternation of wet and dry seasons. On the contrary, we now know that savannas are found in climates capable of supporting forests.
2) Edaphic factors (i.e. nutrient and water availability): savannas occur on soils too nutrient-poor to allow forest establishment.
3) Fires and herbivory: fires prevent forest re-establishment and grazing activity by large herbivores serves to maintain open vegetation.
4) Human activity: savannas are an anthropogenic artifact created by clearing and burning forests. This particular point is controversial because there is now evidence that savannas are ancient and actually pre-date the earliest human populations.

The controversial Cerrado

Like the definition of savanna, the definition of Cerrado is also controversial: Is Cerrado a savanna? Is Cerrado a biome? Indeed, the cerrado has been variously referred to as a biome (Oliveira-Filho & Ratter 2002), as the Brazilian savanna vegetation (Ratter et al 1997), as a complex of biomes (Coutinho 2006, Batalha 2011), or as a unique entity (Eiten 1972) (Figure 10). Eiten (1968, 1972), who has published several influential articles about the Cerrado, points out that the Cerrado is a unique entity, and cannot be considered a true savanna because its floristic richness greatly differentiates it from typical tropical savannas. He defines the Cerrado as a mix of xeromorphic woodland, scrub, savannah, and grassland vegetation in central Brazil (Eiten 1968). The cerrado forms a vegetational and floristic province in an intermediate-rainfall region with a definite dry season (Eiten 1972). The Cerrado cannot be uniquely classified as savanna because of its rich variety of physiognomies (Coutinho 1978). Coutinho (1978), in his “forest-ecotone-grassland” concept, states that the Cerrado is a complex of oreadic2 formations, representing savanna-intermediary formations (campo sujo, campo cerrado, cerrado sensu stricto) and two extreme formations: a forest formation (cerradão) and a grassland formation (campo limpo). He concludes that the Cerrado is a mosaic of three biomes (see also Walter (2006) and Batalha (2011)). Coutinho (2006) later reviews the  concept of the biome, strengthening his prior definition (Coutinho 1978) while noting that all tropical savannas have a physiognomic complexity, which leads to a kind of mosaic that manifests as a gradient of communities. At the same time, he also acknowledges the fact that savannas are considered biomes by the majority of authors. Olson et al. (2001) include the Cerrado in the ecoregion3 of “tropical & subtropical grasslands, savannas and shrublands,” underlining a certain unicity between the Cerrado and other savanna formations.
Recent work, by such authors as Ratter et al. (1997), Silva & Bates (2002) and Oliveira & Marquis (2002), considers the entire Cerrado, in which the cerradão is explicitly included (Figure 10), a savanna. On the other hand, Coutinho (2006) concludes that the Cerrado is a savanna biome, and because the Cerradão is actually a distinct seasonal forest, he considers it separately (see also Rizzini 1997 and Walter 2006) (Figure 10). Finally Batalha (2011) corroborates the “forest-ecotone-grassland” concept of Coutinho (1978) and emphasizes that Cerrado is not a biome but a complex of biomes (Figure 10).

Brief history of the evolution of the Cerrado

During the Cretaceous epoch, angiosperm was spread, creating a (Crane & Lidgard 1989, Lupia et al. 1999, McElwain et al. 2006) new fire regime by increasing fuel availability (Bond & Scott 2010). The savanna’s origin, marked by the expansion and the predominance of C4 grasses, is estimated to have occurred during the Miocene epoch some 8 million years ago, and is thought to have been the result of environmental pressures associated with intense light levels, high temperature, low CO2, and fire (Keeley & Rundel 2005, Bond et al. 2005, Beerling & Osborne 2006, Edward et al. 2010). Fire played an important role in promoting the spread of grasslands and savannas at that time, accelerating forest loss (by slowing the recovery rates of tree species following destruction by fire), and generating positive feedback loops which promoted drought and more fire (Bond et al. 2003, Beerling & Osborne 2006). Neotropical vegetation was structured by four major events (Burnham & Graham 1999, Safford 1999, Fiaschi & Pirani 2009): (1) isolation (break-up of West Gondwana and separation of South America from Africa), (2) the uplift of the Andes and changing drainage systems, (3) the closure of the Isthmus of Panama, and (4) quaternary climate fluctuations. Vuilleumier (1971) highlights the evidence for climatic events that occurred during the last million or so years and have affected the biota of South America. The last glacial period was wetter than the Holocene epoch (90 000 to 21 000 Years Before Present) (Van Der Hammen 1974). However, during the Last Glacial Maximum (LGM) (20,000 to 18,000 YBP, late Pleistocene) there was a decrease in precipitation and a very dry period (drier than the Holocene), associated with lower temperatures and lower atmospheric humidity (due to the slight recession of glaciers) (Van Der Hammen 1974, Ledru 2002). Werneck et al. (2012) demonstrates that the LGM and LIG (Last Interglacial, 120 000 YBP) were the periods of narrowest and widest Cerrado distributions, respectively. During the LMG, climatic conditions did not allow for the development of the Cerrado (Ledru 2002, Werneck 2012). The late Pleistocene was marked by the extinction of the South American megafauna, and the mid-Holocene, by the loss of other large-mammal lineages due to the reduction of open formations in South America (De Vivo & Carmignotto 2004). The increase in seasonality beginning ca. 7 000 YBP was necessary for Cerrado vegetation to grow on the Central Plateau and to eventually result in the physiognomy of the Cerrado we know today (Ledru 2002, Ledru et al. 2006).

Characteristics of the campos rupestres

The presence of quartzitic rocky outcrops is a fundamental property of campos rupestres as well as the associated coarse texture and shallow sandy soil, with high Al3+ and low nutrient contents (Benites et al. 2003, 2007). In contrast to the Cerrado, campos rupestres are almost all well-drained dry grasslands (with the notable exception of the peat bog physiognomy) (Eiten 1978). The local drainage systems, together with the heterogeneity of the topography, create humid and arid sites that are often separatedfrom each other by just a few centimeters (Vitta 1995, Alves & Kolbek 2010). Campos rupestres are subjected to stressful climatic conditions, such as high daily temperature oscillations, intense irradiation (UV), strong winds, and a marked dry season.

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Current Threats on Mountains ecosystems: focus on the campos rupestres

In 2002, the Parties of the Convention on Biological Diversity (CBD) adopted a work program on mountain biological diversity (1) in order to reduce the loss of global and regional mountain biodiversity and (2) to help foster increased knowledge of ecosystem functioning and community composition, because, as it is often the case in tropical regions, there is insufficient understanding of critical processes (Escudero 1996, Romdal & Grytnes 2007), and this presents a serious barrier to implementing effective conservation or restoration programs. Indeed, the CBD has recognized the fragility of mountain ecosystems and species, as well as their vulnerability to man-made and natural disturbances, particularly in the current context of land-use and climate changes (CBD 2012). Mountain ecosystems are hot spots of biodiversity with many endemic species (Giulietti et al. 1997, Price 1998, Chaverri-Polini 1998, Porembski & Barthlott 2000, Barthlott et al. 2005, 2007, Kier et al. 2005, Martinelli 2007), most of which play an essential role in ensuring the regional and global diversity (Burke 2003). One of the great intrinsic values of mountains lies in their being the source of many of the world’s rivers (FAO 1998). Mountain degradation has thus become a worldwide concern because of the consequences it has in terms of ecosystem service losses (FAO 1998), including degradation of water-quality, increasing soil erosion, and biodiversity loss. There is current evidence of adverse human impact on mountains worldwide (Burke 2003), and Brazil is no exception (Jacobi et al. 2007, Ribeiro & Freitas 2010). Pending changes in Brazilian environmental legislation (Law n°12.651, May 25th 2012) will further complicate the conservation of mountain ecosystems because it eliminates hilltops as e nvironments that can be considered Permanent Preservation Areas (PPA) (Ribeiro and Freitas 2010, Codigo florestal 2012). Mountain ecosystems are also known to be poorly resilient to disturbances and therefore require restoration once they have been degraded (Urbanska & Chambers 2002). Though well-adapted to constrained environmentalconditions, such as shallow and nutrient-poor soils and endogenous disturbances (sensu White & Jentsch 2001) such as fire, campos rupestres seem highly sensitive to land conversions, mainly because of their precise adaptation to their original environments (Ribeiro & Freitas 2010).

Table of contents :

Acknowledgements, Agradecimentos & Remerciements
List of Tables
List of figures
1. Context
2. Objectives
3. Restoration ecology
3.1. Definitions
3.2. Goals & Reference Ecosystem
3.3. Type of intervention
3.4. Legislation
3.5. Restoration Ecology & Community Ecology
4. Community Theory
4.1. Ecological community
4.2. Community ecology
4.3. Disturbance & Resilience
4.4. Succession: How do ecosystems change following a disturbance?
4.5. Assembly rules: How do species assemble into communities?
5. Biological model
5.1. Savanna ecosystems
5.1.1. Definition
5.1.2. Geographic distribution
5.1.3. Main processes controlling savannas
5.2. Cerrado
5.2.1. What is the Cerrado?
5.2.2. The controversial Cerrado
5.2.3. Brief history of the evolution of the Cerrado
5.3. Campos rupestres
5.3.1. Definition
5.3.2. Espinhaço range
5.3.3. Characteristics of the campos rupestres
5.3.4. What about the terminology?
5.3.5. Are campos rupestres included in the Cerrado?
5.4. Current Threats on Mountains ecosystems: focus on the campos rupestres .
6. Study areas: Serra do Cipó campos rupestres
6.1. Geographic situation
6.2. Climate
6.3. Study sites
Chapter 1 – Baseline data for the conservation of campos rupestres: Vegetation heterogeneity and diversity.
1. Introduction
2. Material and Methods
2.1. Study area and sites
2.2. Soil analyses
2.3. Plant survey
2.4. Statistical analyses
3. Results
3.1. Soil analyses
3.2. Plant survey
4. Discussion
4.1. Soils
4.2. Similarities between the two grassland types
4.3. Differences between the two grassland types
5. Conclusions
Transition to Chapter 2
Chapter 2 – Reproductive phenological patterns of two Neotropical mountain grasslands
1. Introduction
2. Material & Methods
2.1. Study area
2.2. Plant survey
2.3. Statistical analyses
3. Results
3.1. Flowering, fruiting and dissemination patterns in sandy and stony grasslands. .
3.2. Flower and fruit production among grassland types and among families
3.1. Phenology and fruit production of species co-occurring in both grassland types.
4. Discussion
4.1. Flowering, fruiting and dissemination patterns in sandy and stony grasslands. .
4.2. Flower and fruit production in sandy and stony grasslands.
4.3. Comparison between sandy and stony grasslands.
5. Conclusion
Transition to Chapter 3
Chapter 3 – Degradation of campos rupestres by quarrying: impact, resilience & restoration using hay transfer
1. Introduction
2. Material and Methods
2.1. Study area
2.2. Resilience of the campos rupestres
2.2.1. Vegetation
2.2.2. Soils
2.2.3. Seed banks
2.3. Restoration using hay transfer
2.4. Statistical analysis
2.4.1. Resilience
2.4.2. Restoration using hay transfer
3. Results
3.1. Resilience of the campos rupestres
3.2. Vegetation establishment limitation
3.2.1. Site limitation
3.2.2. Few viable seeds in the soils
3.3. Restoration using campo rupestre hay transfer
3.3.1. Vegetation cover
3.3.2. Effect of substrate on the number of seedlings
3.3.3. Effect of the type of hay on the number of seedlings
3.3.4. Limitation
4. Discussion
4.1. Resilience of campos rupestres
4.2. Restoration using campo rupestre hay transfer
5. Conclusion
Transition to Chapter 4
Chapter 4 – Diversity of germination strategies and dormancy of graminoid and forb species of campos rupestres.
1. Introduction
2. Material and methods
2.1. Seed collection
2.2. Germination experiments
2.3. Pre-fire vs. post-fire germination
2.4. Evolutionary ecology of seed dormancy
2.5. Statistical analyses
3. Results
3.1. Intraspecific patterns of seed germination requirements
3.2. Effects of fire-related cues
3.3. Viability
3.4. Pre-fire vs. post-fire germination
3.5. Evolutionary ecology of seed dormancy
4. Discussion
5. Conclusion
Transition to Chapter 5
Chapter 5 – Restoration of campos rupestres: species and turf translocation as techniques for restoring highly degraded areas.
1. Introduction
2. Material and Methods
2.1. Study area
2.2. Translocation of individuals
2.3. Turf transfer
2.4. Statistical analysis
2.4.1. Individual translocation
2.4.2. Turf translocation
3. Results
3.1. Individual translocation
3.1.1. Effect of substrate type (natural VS. degraded substrate) and nutrient supply ..
3.1.2. Effect of the translocation period
3.1.3. At the species level: cases of Paspalum erianthum and Tatianyx arnacites.
3.2. Turf transplantation
3.2.1. Effects of the turf size
3.2.2. Effects of the turf origin
3.2.3. Effects of the substrate of the degraded area.
3.2.4. Reference grassland regeneration
4. Discussion
5. Conclusion
General Discussion
1. What do we want to restore?
1.1. Composition and structure of herbaceous communities of campos rupestres
1.2. From the regional species pool to the external species pool: patterns of reproduction in campos rupestres
2. Plant community dynamics after disturbance
2.1. Regeneration after a natural disturbance
2.2. Campos rupestres are not resilient to a strong disturbance
2.3. Drivers of plant community recovery
2.3.1. Dispersal filter
2.3.2. Environmental filter
2.3.3. Biotic factors
3. Can we restore campos rupestres?
4. From restoration ecology to community ecology
Main considerations of this thesis
1. To increase studies at large scale and use functional traits
2. Effect of fire on reproductive phenology
3. Understanding regeneration after natural disturbance
4. Germination
5. Looking for new restoration techniques


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